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Chapter VI

Contents

CHAPTER VI

Hemothorax and Hemothoracic Empyema

Thomas H. Burford, M.D.

GENERAL CONSIDERATIONS

At the beginning of World War II, there was little or no realization of the fact that hemothorax was the most frequent, and probably the most important, complication of wounds of the chest. A brief experience with these wounds, however, compelled the recognition of both its frequency and its importance. The principles and techniques by which hemothorax was managed influenced the entire scheme of the treatment of chest wounds from forward hospitals through chest centers.

In view of these facts, it is surprising to find that hemothorax had attracted very little attention before World War II. Surgeons who dealt with it at all were divided into two schools. One group maintained that absorption of the sanguineous intrapleural material would invariably take place, and with reasonable promptness. The other group advocated the prompt evacuation of the pleural cavity, on the premise that blood, by its mere presence, was harmful. Even those who did not accept the theory that all hemothoraces were absorbed by natural processes believed that this occurred in 90 to 95 percent of all thoracic wounds.

When the literature of the prewar period is examined, one cannot fail to be impressed with the small number of observers who concerned themselves with the fate of the 5 or 10 percent of patients whose hemothoraces were not absorbed. This lack of concern was evident in the military manual on thoracic surgery issued in 1943 under the auspices of the American Association for Thoracic Surgery and the National Research Council (1). Blood in the chest, according to this manual, tends to remain fluid, probably because it is defibrinated by the motions of the lungs and the heart. A section was devoted to the management of infected hemothorax, but no recommendations were made for dealing with the exceedingly important complication of clotted hemothorax. The omission was typical. It was also unfortunate. The casualties whose hemothoraces clotted or did not absorb for other reasons constituted the group who developed empyemas that tended toward chronicity and who presented encased lungs or contracted hemithoraces, with resulting impairment of respiratory function.

Until articles on unabsorbed hemothorax began to be published from the Mediterranean Theater of Operations, U.S. Army, in World War II, not many observers even mentioned the possible clotting of blood in the pleural cavity.


238

It is also startling, in retrospect, to find in the prewar literature almost no effort to distinguish postpneumonic and metapneumonic empyema from posttraumatic empyema, although the latter variety, if not correctly managed, gives rise to a far higher incidence of chronicity. Both varieties were discussed as if they were of the same origin and had the same characteristics. Studies on hemothorax as an antecedent to empyema were remarkable for their paucity.

The recognition of hemothorax as perhaps the most important complication of wounds of the chest was a development of World War II. Had the prewar laissez-faire approach to it been carried over into military surgery, it would have resulted in an intolerably high rate of pleural sepsis in World War II.

Nomenclature-Before proceeding with the discussion of hemothorax and its sequelae, it is necessary to define the meaning and implications of the terms used for this condition in World War II:

The term "simple hemothorax" implied the presence of blood in the pleural cavity, without complicating features. This term was used whether the blood was the result of injury to the chest wall alone or was the result of a penetrating or a perforating wound.

The term "infected hemothorax" implied the presence of bacteria in the pleural fluid, plus the clinical manifestations of their presence.

The term "chronic hemothorax" or "chronic traumatic hemothorax" was used to indicate any collection of blood in the pleural cavity that could not be reduced by thoracentesis. The term implied that fresh blood had ceased to enter the pleural space, that hemostasis had been achieved, and that the collection of blood was therefore residual. A chronic hemothorax was usually an organizing hemothorax. It was the clotting of the blood plus its inevitable sequela, organization, that made aspiration no longer possible. A neglected accumulation of intrapleural blood that could be satisfactorily aspirated was not considered chronic because it could be evacuated at will by proper treatment.

There was general agreement that the term "chronic hemothorax" was both inadequate and misleading. It did not indicate, or even suggest, the really important element in the pathologic process. This element was the presence of fibrin, whether it was derived from blood spilled into the pleura, or from exudate formed by the pleura, or had been deposited in some other manner. Some such term as "fibrothorax" would have been more expressive and more correct, but the term "chronic traumatic hemothorax" began to be used, and semantic changes were not practical in wartime.

INCIDENCE OF HEMOTHORAX AND ITS COMPLICATIONS

Hemothorax-Statements concerning the incidence of hemothorax in combat-incurred wounds of the chest are necessarily imprecise. Probably every casualty with a perforating or a penetrating thoracic wound had a hemo-


239

thorax of some degree. In a certain proportion of injuries, perhaps 15 or 20 percent, the collection of blood was so small as to cause no clinical manifestations, and it was rapidly absorbed by natural processes.

Various studies from the hospitals in the Mediterranean theater, including the chest centers, show the incidence of hemothorax to range from 80 to 84 percent. Well over half of the casualties received in field hospitals after wounding already had enough blood in the pleural cavity to make its removal an urgent part of the effort to restore the cardiorespiratory equilibrium. More significant than the high initial incidence is the fact that about three-quarters of the casualties received in base hospitals arrived with sufficient intrapleural blood to require treatment.

In the great majority of hemothoraces, once the policy of early and complete thoracentesis had been established, recovery was prompt and uncomplicated in the absence of complications from other components of the thoracic injury. In 752 hemothoraces treated at the 300th General Hospital chest center in the Mediterranean theater, between 1 April and 20 December 1944, by Maj. Thomas H. Burford, MC, and Maj. (later Lt. Col.) Edward F. Parker, MC, there were no complications in 603 of 678 cases in which the blood could be removed by aspiration. The average time required for complete clearing of the chest was from 10 to 14 days, and the average number of thoracenteses required was from 3 to 4.

Clotting and organization-The hemothoraces that gave rise to difficulties were those in which clotting occurred. Exactly how often this happened, it is not possible to say. During the Italian campaign, some forward hospitals reported incidences of clotting ranging to 25 and 30 percent. These levels are exceptionally high. In one or two later studies, the incidence was 9 or 10 percent, which is rather low. Clotting probably occurred in about 15 percent of all hemothoraces, even when thoracentesis was undertaken early and was repeated as necessary.

The incidence of clotting naturally varied with circumstances. It was more frequent in severe wounds. It was also more frequent the longer thoracentesis was delayed. A casualty who was brought promptly to a hospital near the frontline and whose chest was evacuated as part of the regimen of resuscitation seldom developed an organizing hemothorax.

In nearly all instances of extensive clotting, some degree of organization of the clot followed. Infection, with its clinical manifestations, could and did occur in many unclotted hemothoraces, but it was much more likely to occur in large clotted collections. Two other consequences of clotting were also serious:

1. If an organizing hemothorax was of any size, simple removal of the clots at thoracotomy or attempted evacuation of the pleural cavity by water-seal intercostal drainage practically always proved inadequate, and the resulting pulmonary reexpansion was entirely unsatisfactory.


240

2. If expectant treatment was employed in organizing hemothorax, the period required for resolution was always prolonged. In one group of 13 patients observed late in the war, the total time for clearing ranged from 41 to 125 days and averaged 78 days. Clotting of a hemothorax was therefore an important cause of prolonged morbidity.

Infection and hemothoracic empyema-Most infected hemothoraces were preceded by clotting, and most posttraumatic empyemas were preceded by infected hemothoraces. There was seldom any doubt of the sequence of events. In a small number of cases, even uninfected organizing hemothoraces produced extreme degrees of respiratory crippling, though the worst of these cases did not compare in severity with the crippling observed in patients in whom infection of a hemothorax had been permitted to become chronic. During World War I, chronic empyema was the most frequent complication of chest wounds (2). Almost a quarter of the thoracic casualties died, and from 25 to 30 percent developed empyema. If these same proportions had prevailed during World War II, the results of chest wounds would have been disastrous.

In the early months of fighting in North Africa, before the management of hemothorax had been standardized, the incidence of empyema was high, running to 25 or 30 percent in some hospitals. Even in the chest center at the 53d Station Hospital, Bizerte, which was equipped and staffed for the specialized care of chest injuries, it was 22.6 percent. By the end of the war, the general incidence in the theater did not exceed 10 or 11 percent, and more than one hospital had achieved an incidence as low as 7 percent. In the European Theater of Operations, U.S. Army, which had the early experience of the Mediterranean theater to guide it, chronic hemothoracic empyema was also infrequent.

An incidence of even 7 percent is much higher than the incidence of empyema after chest wounds in civilian practice. The explanation of the difference is simple: In civilian life, the agents of wounding are usually ice picks and bullets, which have a limited and localized destructive capacity. In combat-incurred injuries, on the other hand, while bullets were frequently as innocuous from this standpoint as they are in civilian life, most wounds were large wounds, and tissue destruction was extensive. Moreover, in combat-incurred wounds, the missiles often carried with them into the chest fragments of fractured ribs, bits of clothing, and other debris. Retained metallic foreign bodies, unless they were very large, played no significant role in most intrapleural infections (p. 327).

In World War II, the factors most frequently responsible for posttraumatic empyema were delayed and inadequate evacuation of the pleural cavity, inadequate debridement, inadequate drainage of the pleural cavity, and excessively prolonged treatment by aspiration and instillation of penicillin when it was obvious that radical therapy was required. The necessary interruption of professional supervision of casualties in the chain of evacuation was probably responsible for a small number of cases early in the war. How serious a part


241

inadequate early treatment plays in the development of empyema is evident in figures reported by d'Abreu (3): When the British evacuated 88 soldiers of all nationalities who had been engaged in guerrilla warfare in Yugoslavia and who had had no early surgical treatment for their chest wounds, they found that 48 of them had empyema.

The reduction in the incidence of posttraumatic empyema as the war progressed was the result of several factors, the most important of which was the increasing emphasis put upon early, complete evacuation of the pleural cavity, which was followed by prompt reexpansion of the lung. The advent of penicillin, with its beneficial effect on residual infection, also played a part. Penicillin represented an improvement over the sulfonamides, but it was not the major factor in the improvement. The most important single factor in the lowered incidence of posttraumatic empyema was the improvement in the surgery of chest wounds that came to pass with the increased experience of general and thoracic surgeons and of anesthesiologists.

Figures for empyema supplied by the Medical Statistics Division, Office of The Surgeon General, appear in tables 13 and 14. In connection with table 13, attention is called to the fact that data available only for 1944 and 1945

TABLE 13. -Admissions for empyema of the chest in the U.S. Army, by area and year, 1942-45

[Preliminary data based on sample tabulations of individual medical records]
[Rate expressed as number of admissions per annum per 1,000 average strength]

Area


1942-45

1942

1943

1944

1945

Num-
ber

Rate

Num-
ber

Rate

Num-
ber

Rate

Num-
ber

Rate

Num-
ber

Rate

Continental United States

406

0.03

121

0.05

175

0.03

75

0.02

35

0.01

Overseas:

 

 

 

 

 

 

 

 

 

 

    

Europe

100

0.02

2

0.02

13

0.05

20

0.01

65

0.03

     Mediterranean1

14

.01

---

---

5

.01

9

.01

---

---

    

Middle East

4

.03

---

---

4

.08

---

---

---

---

     China-Burma-India

1

.00

---

---

---

---

1

.01

---

---

    

Southwest Pacific

15

.01

1

.01

2

.01

7

.01

5

.00

     Central and South Pacific

25

.02

2

.01

11

.04

7

.02

5

.01

    

North America2

20

.04

5

.05

11

.06

4

.03

---

---

    

Latin America

4

.01

2

.02

2

.02

---

---

---

---


Total overseas3

201

0.02

12

0.02

48

0.03

51

0.01

90

0.02


Total Army

607

0.02

133

0.04

223

0.03

126

0.02

125

0.02

1Includes North Africa. 2
Includes Alaska and Iceland. 3
Includes admissions on transports.


242

show that the incidence of empyema during this period was nearly six times higher than the number of admissions due to the condition.1

For 1944 (table 13), preliminary tabulations of individual medical records showed 126 admissions and 805 secondary cases of empyema. The figure for the secondary cases was derived from a 20-percent sample, consisting of 161 punchcard records. One-third of the cases of empyema occurred among admissions in the Zone of Interior and two-thirds among admissions overseas. In the latter group, more than 70 percent of the cases were of battle origin. Three-fourths of the remaining cases originated in disease and the other quarter in nonbattle injuries. Nearly 90 percent of the empyemas secondary to battle in-

TABLE 14.-Distribution of a 20 percent sample1 of secondary cases of empyema of the chest in the U.S. Army, 1944,2 by area of admission, type of admission of primary condition, and evacuee status

[Preliminary data based on sample tabulations of individual medical records]

Type of admission

Continental United States


Overseas

Europe

Mediterranean

Middle East

China-Burma-
India

Southwest Pacific

Central and South Pacific

North America


EVACUATED

Battle injury and wound:

 

 

 

 

 

 

 

 

    

Thoracic

---

36

8

---

1

4

1

---

    

Thoracoabdominal

---

5

8

---

---

---

---

---

    

Other regions

---

8

1

---

---

---

---

---


Total


---


49


17


---


1


4


1


---

Nonbattle injury:

 

 

 

 

 

 

 

 

    

Thoracic

---

1

---

---

---

---

---

---

    

Thoracoabdominal

---

1

---

---

---

---

---

---

    

Other regions

---

1

---

---

---

---

---

---


Total


---


3


---


---


---


---


---


---

Disease:

 

 

 

 

 

 

 

 

    

Pneumonia

---

1

---

---

---

---

---

---

    

Bronchiectasis

---

1

---

---

1

---

---

---

    

Other diseases

---

5

1

---

---

1

1

1


Total


---


7


1


---


1


1


1


1


Grand total


---


59


18


---


2


5


2


1

1It should be pointed out again that the term "admissions" refers to patients admitted to medical treatment facilities for the specified condition as the primary cause of admission, while the term "incidence" includes not only these patients but also patients in whom the specified condition was reported as secondary to other admission diagnoses.

TABLE 14.-Distribution of a 20 percent sample1 of secondary cases of empyema of the chest in the U.S. Army, 1944,2 by area of admission, type of admission of primary condition, and evacuee status- Continued

[Preliminary data based on sample tabulations of individual medical records]

Type of admission

Continental United States


Overseas

Europe

Mediterranean

Middle East

China-Burma-
India

Southwest Pacific

Central and South Pacific

North America


 NOT EVACUATED

Battle injury and wound:

 

 

 

 

 

 

 

 

    

Thoracic

---

1

---

---

---

1

---

---

    

Thoracoabdominal

---

---

1

---

---

---

---

---

    

Other regions

---

---

---

---

---

---

---

---


Total

---

1

1

---

---

1

---

---

Nonbattle injury:

 

 

 

 

 

 

 

 

    

Thoracic

4

---

---

---

---

1

---

---

    

Thoracoabdominal

---

---

---

---

---

---

---

---

    

Other regions

1

1

---

---

1

1

---

---


Total


5


1


---


---


1


2


---


---

Disease:

 

 

 

 

 

 

 

 

    

Pneumonia

26

3

4

2

---

---

---

---

    

Bronchiectasis

2

---

---

---

---

---

---

---

    

Other diseases

21

---

2

---

---

---

---

---


Total


49


3


6


2


---


---


---


---


Grand total


54


5


7


2


1


3


---


---

1Two sample cases-one admission each in the European theater and in the Southwest Pacific Area-have been omitted from the table since they could not be located in the card file.
2
1944 refers to year in which primary cause of admission occurred. The empyema may have occurred in that year or subsequent on 1944.

jury followed injuries of the chest or thoracoabdominal region. There were 115 separations from service for empyema during the 1942-45 period.

PATHOGENESIS OF ORGANIZING HEMOTHORAX

Natural History of Simple Hemothorax

Origin of blood-Though it was not always possible to determine the exact origin of the blood in the pleural cavity, by far the most frequent source was wounds of the lung. Hemorrhage from the lung, however, tends to spontaneous arrest within a short time. Lacerations of intercostal vessels were the


244

FIGURE 71.-Hemothorax with recurrent pulmonary hemorrhage. A. Posteroanterior roentgenogram showing extensive right hemothorax, with retained foreign body, 7 days after wounding. B. Same, 7 days later, after secondary hemorrhage from lung.

second most frequent source; in many instances, bleeding from these injuries was combined with bleeding from wounds of the lung. In a much smaller number of injuries, the source of the bleeding was the internal mammary vessels; the vessels of the heart, the pericardium, or both; and the larger vessels, such as the innominate and subclavian arteries and the azygos vein. As has already been pointed out, casualties with injuries of the great vessels of the chest seldom survived to reach a field hospital.

Secondary hemorrhage into the pleural cavity was extremely uncommon. It was recorded only 3 times in 752 cases of hemothorax studied by Major Burford and Major Parker. In only one of the three cases did the hemorrhage recur from the lung (fig. 71), 2 weeks after wounding. In the second case, the recurrence was from a laceration of the intercostal artery. In the third case, an unsuspected traumatic aneurysm of the right subclavian artery ruptured, and the patient died almost at once (p. 45). The roentgenologic examination (fig. 72) did not arouse the suspicion that a lesion of such potential gravity could coexist with the characteristic picture of clotted hemothorax.

Effects of blood on pleural structures-In spite of the problem hemothorax has presented, at least in combat wounds, there have been remarkably few studies of the intrapleural changes associated with it. The fluoroscopic studies made by Edwards and Davies (4) in 1940 represent one of the first serious efforts to ascertain the nature of the pleural response to blood in the pleural cavity. Before the war, opinions differed concerning its irritative effects. The World War II experience was not conclusive, and final judgment must be reserved.


245

FIGURE 71.-Continued. C. Same, 2 days later, showing residual clotted hemothorax after two thoracenteses. D. Same, after thoracotomy for removal of foreign body and decortication of right lung. At operation, it was found that the secondary hemorrhage had occurred from a laceration of the lung at site of entry of missile.

Little evidence was produced in World War II to substantiate the theory that unaltered liquid blood acted as an inflammatory agent. This generalization held, however, only while the blood remained unaltered. There seemed no doubt that it underwent rather profound physiochemical changes as soon as it left its normal endothelial-lined habitat and that these changes were progressive in both kind and degree. The first fluid aspirated after wounding was pure blood or distinctly bloody, but its character changed as aspirations were continued. It became serosanguineous, and then, before the chest was entirely emptied, it became merely serous.

A fibrin layer was uniformly found on the pleural surface in all hemothoraces. It was always more pronounced in clotted than in unclotted cases. Since clotted blood not only binds fibrin but also represents a greater physiochemical departure from normal than a liquid hemothorax, in which fibrin is free, the inference was that the fibrin layer represented an inflammatory response rather than a passive deposition of fibrin or a salting-out phenomenon. As would be expected, the response was proportional to the degree of alteration of the blood; that is, whether it was (1) clotted or (2) clotted and contaminated.

In the hemothoraces controlled by thoracenteses, laboratory studies showed that the pleural fluid was low in protein and relatively free of red blood cells. Even in uncomplicated hemothoraces, as just pointed out, a certain amount of fibrin was deposited over the pleural surfaces, but the thin, shaggy coat was not demonstrable on roentgenologic examination, and the fibrin content of the intrapleural fluid was so small that total aspiration was entirely feasible (fig. 73).


246

FIGURE 72.-Posteroanterior roentgenogram showing clotted right hemothorax. There is nothing in the film to suggest the traumatic aneurysm of the first portion of right subclavian artery, rupture of which was immediately fatal.

Theories of Origin of Organizing Hemothorax

The pathogenesis of organizing hemothorax was no clearer at the end of the war than at the beginning. There were no facilities in a combat zone for experimental studies on why clotting occurred in some traumatic hemothoraces and did not occur in others. Clinical and pathologic observations in a large number of chest injuries do, however, permit a certain amount of legitimate speculation.

Certain causes could be eliminated at once. An analysis of the missiles that caused the wounds associated with clotted hemothorax revealed no common denominator to explain what occurred. The degree of pneumothorax present apparently played no part, as might have been expected; the presence or absence of air does not influence the clotting of blood. The relative severity of the wounds of the lungs and soft tissues played no decisive role; hemothorax was more frequent in severe injuries because severe injuries were more frequent. Organizing hemothorax occurred in some cases in which the injury was limited to the external chest wall and also occurred in some contusions and blast injuries.

With these obvious factors eliminated, it was necessary to turn to the mechanism of clotting for a possible explanation of clotted or organizing hemothorax. There were three theories:

1. The first hypothesis was that bacteria might be present in the pleural cavity and, in the presence of blood, might incite an exudative response, which


247

FIGURE 73.-Massive liquid hemothorax without infection. A. Posteroanterior roentgenogram made shortly after wounding and showing hemothrax. B. Same, 10 days later, after six thoracenteses, by which a total of 3,150 cc. of blood and other fluid was removed.

would favor the formation of fibrin deposits, rather than a transexudative response. If bacteria were seeded generously over the pleural surfaces, a frankly suppurative response would be expected, and a true suppurative pleuritis would develop. If, however, they were implanted in such small numbers as not to incite a widespread pleural response, their presence might still be sufficient to alter the response from transexudative to exudative, and the clinical picture would be dominated by the presence of fibrin deposits rather than by suppuration.

The sharp and often prolonged febrile responses seen in organizing hemothorax furnished clinical evidence of the exudative character of the pleural response to blood. In uninfected hemothoraces, a moderate febrile response often occurred, but it was practically always of short duration, usually no longer than from 10 to 14 days. In infected cases, the clinical manifestations continued, and if suppuration were impending, they became more pronounced.

Bacterial seeding probably explained some instances of organizing hemothorax, but it could not be accepted as a universal explanation. It was undoubtedly a factor in some hemothoraces which went on to empyema. The fact that nonhemolytic Staphylococcus aureus was the most frequent causative organism in empyema and that this organism does not produce fibrolysin lent some support to this theory. Clotted blood containing pathogenic bacteria served as an excellent culture medium, just as devitalized muscle served as a culture medium in all wounds. This was particularly true of anaerobes, which develop rapidly under low oxygen tension. Clot formation about bacteria in hemothorax also had the effect of preventing penicillin or the sulfonamides from reaching these entrenched organisms. They were not influenced by either local or systemic therapy.


248

2. The second hypothesis was that clotting in hemothorax might be the result of the simultaneous presence of blood and coagulative ferments in the pleural cavity. This theory was not considered acceptable. For one thing, the actual amount of blood present seemed of no importance; the preponderance of white clot present in some cases pointed to an excess of plasma. There was also no uniformity in the time at which clotting occurred. Clotted blood was sometimes found in the pleural cavity when thoracotomy was performed from 4 to 6 hours after wounding. Sometimes, the clot was so firm a few days after wounding that it defied needle aspiration. In other instances, the blood might remain liquid for many days, and all of it could be removed by thoracentesis.

There was no acceptable explanation for these variables. It might be that the churning movements of the diaphragm, heart, lungs, and chest wall had a defibrinating effect. Sellors (5) remarked that any surgeon who opened a recent hemothorax must have been impressed "by the tumultuous way in which the blood is flung about the pleural cavity." Fibrin and blood clots were often seen in the costophrenic sinus and the lower portion of the pleural cavity within a short time after wounding. Another consideration was that both the lungs and the muscles are ready sources of thromboplastin.

Even granting all of these facts, acceptance of the theory that the presence of whole blood and coagulative ferments was responsible for organizing hemothorax would leave many cases unexplained.

3. The most reasonable hypothesis was that, as the result of trauma, normal pleural fluid was so modified that it became exudative rather than serous. As has already been pointed out, a response by the pleura could be expected whenever blood was spilled into the pleural cavity as the result of wounding, even if the process went no further. Moreover, wounds of the lungs and pleura cannot be fundamentally different from wounds of other tissues. If this reasoning is sound, the so-called edema of wounding might be expected to occur in these tissues just as in other damaged tissues. The presence of edema, which reached its peak within 2 to 4 days after wounding, could reasonably be assumed to affect the character of the pleural effusion caused by trauma, in all probability making it richer in fibrin. There would then be present in the pleural cavity an excess of coagulative ferments from the wounded chest wall or lung or both, combined with an excessive fibrin from the pleural effusion. In other words, there would be added to the whole blood spilled into the pleural cavity, which might itself clot by natural physiologic processes, increments from the pleural response to wounding that would enhance the natural process of clotting.

It is easy to explain why early thoracotomy and evacuation of whatever intrapleural fluid was then present did not necessarily protect the patient against the development of a subsequent clotted intrapleural mass. Wounds of the thorax frequently resulted in the widespread changes known as wet


249

lung (p. 207). Wet lungs were heavy and soggy, and they expanded only sluggishly and never completely in the absence of vigorous corrective measures. For a few days after wounding, therefore, dead space2 in the pleural cavity permitted the accumulation of pleural exudate that eventually became a part of, or constituted, the clotted intrapleural mass. If all the blood in the pleural cavity had been evacuated at thoracotomy or otherwise, the pleural exudate that continued to accumulate under these circumstances was chiefly white. If all the blood had not been removed, the clot would be layered or marbled.

The hypothesis seems reasonable that a change in the character of the normal pleural fluid furnishes an explanation for the clinical vagaries observed in clotted hemothorax. It also seems to explain the sequential relation of this process to the original trauma.

PATHOLOGIC CHANGES IN CHRONIC TRAUMATIC HEMOTHORAX

The limited pathologic studies possible in a combat zone seldom warrant generalizations on any subject. A large enough number of hemothoraces were observed, however, to elucidate the pathologic changes in chronic traumatic hemothorax and to establish the rationale for its management.

Gross Pathology

All hemothoraces, as already pointed out, involved typical and definite changes within the pleural cavity, slight at first but more pronounced as the process went on to clotting and organization.

The process of hemo-organization began with the laying down of a thin, loosely adherent film of fibrin and blood cells over both pleural surfaces. Within 2 or 3 days of its formation, angioblastic and fibroblastic proliferation began to occur.3 As early as from 7 to 14 days after wounding (figs. 74 and 75), fibroblasts could be seen growing out from the older (pleural) side toward the younger portion. The transition to adult fibrous tissue was progressive and rapid (fig. 76). Capillaries grew in from the pleura, and within 8 to 10 weeks, complete cellular symphysis had occurred in most cases. Decortication, which would have been simple earlier, had now often become impossible (figs. 77 and 78).

2Dead space may be defined as any air or fluid or matter without the confines of a normal anatomic habitat and without a blood supply.
3These observations were made on specimens secured at operation for bronchopleural fistulas, removal of foreign bodies, and similar conditions. Small clotted hemothoraces were often found at these procedures, and, when interest in this complication of thoracic wounds had developed, sections were regularly taken for study.


250

FIGURE 74.-Photomicrograph showing organizing hemothorax with replacement of acute fibrinopurulent deposit by young vascular connective tissue at end of first week after wounding. The pleural aspect of the layer of exudate removed from the visceral pleura is toward left and periphery toward right.

The essential feature of chronic traumatic hemothorax was the formation of this fibroblastic and fibrinofibrous membrane or peel over the visceral and parietal pleurae. Once it had formed, the hemothorax was converted into an enclosed hematoma of the pleural space (fig. 79).

It should be emphasized that, in the beginning, the pleura itself took no part in the pathologic process. Until fusion between it and the rind occurred, it remained remarkably normal in appearance. The pleural thickening which was sometimes described on roentgenograms was never observed at operation. The practice of describing peripheral obscuration as thickened pleura was incorrect and misleading. In the early phases of an organizing hemothorax, examination of sections of the encasing sac never revealed elastic tissue, although elastic fibers were always found in sections from the lung or the soft


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FIGURE 75.-Photomicrograph showing fibroblastic membrane from clotted hemothorax 11 days after wounding. Note that, even at this early stage, the hemothorax has a definite capsulelike character. Capillaries have already begun to appear in older (pleural) side at bottom of specimen. Hematoxylin and eosin stain. (X 60)

tissue of the thoracic wall just beneath the pleural mesothelium. If, however, the process went on without interruption, the membrane eventually underwent complete fibrous and vascular union with the pleura, which then lost its identity as a delimiting membrane.

The facts just stated were of great importance in the selection of the time for decortication (p. 286). The ease with which a cleavage plane could be established between the two layers (the rind and the pleura) at operation was a direct function of the age of the limiting membrane (fig. 78). Experience showed that after 4 weeks from the date of injury the chances of performing satisfactory decortication dropped rapidly with each succeeding week.

The development of infection, even if it went on to suppuration, did not accelerate the process of organization of the hemothorax to any appreciable degree. There was also no evidence that the union between the peel and the underlying pleura was any firmer when infection was present.

The most prominent feature of the intrapleural mass was that it was always relatively or absolutely solid, because of the fibrin component. It was usually thickest in the basal thoracic gutter posteriorly. The distribution of


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FIGURE 76.-Photomicrograph showing section of peel of clottedhemothrax 4 weeks after wounding. Membrane has assumed a definitely fibrous character. Capillaries are visible at their point of entrance from visceral pleura (lower left of section). Hematoxylin and eosin stain. (X 100)

the fibrin thus followed the natural principles of gravity as they would operate in any recumbent subject with an accumulation of fluid in the pleura.

In the typical organizing hemothorax, the mass was made up of three layers (fig. 79):

1. The outer layer was a tough organized membrane (rind, peel), the thickness of which was related to the length of time that had elapsed since wounding. At the end of 4 or 5 weeks, the rind was usually from 2 to 4 mm. thick. Later, it might be from 5 to 8 mm. thick, or even thicker. If the mass was composed of solid fibrin, the rind was always very thick.

This rind completely surrounded the original hemothorax and was intimately attached to the visceral and parietal surfaces of the pleura, though usually, in spite of the intimacy of the adhesions, it could be separated without difficulty from the visceral pleura, at least in early stages of the process. The


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FIGURE 77.-Photomicrograph showing section from clotting hemothorax. Note fusion between dense layer of collagenous connective tissue and subjacent pleura and lung (lung is to left).

rind was resistant, did not tear readily, and had the gross appearance of fibrous tissue.

The rind usually passed directly from the visceral to the parietal pleura at all points at which these surfaces met, but attenuated projections frequently extended beyond these limits, along opposed pleural surfaces or into the interlobar fissures. The costophrenic gutter was almost consistently obliterated by the elevated diaphragm and was sealed off by the reflection of the peel. Beyond these points of symphysis, it was often surprising to find only a thin layer of filmy pleural adhesions. At a greater distance, entirely free pleural space might be encountered.

2. The middle layer of the chronic traumatic hemothorax was a soft, unorganized mass, with the consistency of fibrin. It differed from patient to patient in gross appearance, chiefly because of differences in color. Sometimes, it was almost white. Sometimes, it was the color of mahogany. Sometimes, it was


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FIGURE 78.-Photomicrograph of section through membrane, pleura, and lung (lung is at lower margin) in posttraumatic empyema 12 weeks after wounding. Note cellular intimacy. No line of demarcation can be seen, and surgically no line of cleavage could be established. This patient's chance for decortication was forfeited by delay in resorting to it. Van Gieson's stain. (X 100)

definitely bloody. A certain amount of marbling was not uncommon, but it was more frequent to find the middle layer the same color throughout. Differences in color seemed to depend upon the relative proportions of blood and plasma in the mass or upon the amount of pleural effusion or pleural exudate that had originally accumulated and that had been modified by whatever degenerative changes might have occurred with the passage of time.

3. The third layer (center) of the intrapleural mass was typically lobulated (fig. 79). It might consist of a single large space or of a network of spaces. Sometimes, it was a mushy core from whose interstices fluid could be squeezed. The fluid looked like what it was, supernatant fluid from a mass of retracting fibrin. It varied in color from yellow to red, brown, or mahogany.

The formation of the central fluid-filled space or spaces was clearly the result of retraction of the original clot. In fact, the whole pathologic process in organizing hemothorax did not seem to differ in any important way from the well-known process of organization in intravascular thrombi.

The foregoing description bears out what has already been said (p. 238), that the term "organizing hemothorax" or "chronic traumatic hemothorax"


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FIGURE 79.-Cross-sectional diagram showing pathologic process in clotting, organizing hemothorax. Membranous peel (rind), essentially a fibrinofibrous envelope, is shown investing visceral and perietal pleurae. In center is loculated purulent material. Loculation explains why in many infected hemothoraces infection could not be diagnosed by thoracentesis, because aspirating needle did not reach center of process, which was recognized only at operation.

carried no implication of the origin or gross appearance of the intrapleural mass. The nomenclature suggests that the mass might be the result of the presence of clotted blood alone, as in some instances it was. The gamut was run, however, from such cases through (1) those in which a considerable portion of blood was still present but in which there were also present increments of white clot (that is, plasma, fibrinous pleural effusion, or fibrinous exudate) to (2) those in which the entire mass seemed to consist of white clot. The variations seemed due not so much to the amount of whole blood originally spilled into the pleura as to the pleural response to its presence.

Histopathology

Histologic examination of sections from an organizing hemothorax confirmed the gross observations (figs. 74-78 and 80-85). As already pointed out, as early as 7 to 10 days after wounding, there was microscopic evidence of fibroblastic and angioblastic proliferation from the pleural surfaces to the clot. The peel or rind thus formed increased progressively in thickness as the fibroblastic invasion continued.


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FIGURE 80.-Photomicrograph showing later of fibrin 3 mm. thick removed from visceral pleura in uninfected clotted hemothorax 11 days after wounding. Note beginning organization in portion immediately adjacent to pleura (on left).

Within 3 or 4 weeks after wounding, adult fibrous tissue was demonstrable in the outer layer of the organizing hemothorax. The fibers and nuclei were arranged roughly parallel to the surface. The long axes of the capillaries were at right angles to the surface, and the capillaries were continuous through the pleura.

Within 4 to 7 weeks after wounding, small arterioles, with smooth muscle fibers in their walls, could be demonstrated at or near the outer surface of the peel. Active fibroplasia continued along the inner (younger) surface, with resulting increases in the thickness of the rind. In some instances, layers of fat cells developed in the peel. along the outer surface. It was speculated, but never proved, that this phenomenon might possibly represent a regressive process, heralding eventual degeneration and absorption of the peel. For reasons not clear, the membrane was always thicker, more vascular, and more adherent on the parietal than on the visceral pleura.


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FIGURE 81.-Fibrotic process in organizing hemothorax. A. Photomicrograph showing section of fibrofibrinous layer removed from visceral pleura in uninfected clotted hemothorax. Note fibrosis in portion of rind adjacent to pleura at top. B. Photomicrograph showing more pronounced fibrous changes at distal free margin of same section.


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FIGURE 82.-Photomicrograph showing calcium deposition in collagenous connective tissue layer of exudate on visceral pleura in organizing hemothorax.

Microscopically, the rind in hemothoracic empyema could not be differentiated from the rind in organizing hemothorax without infection. The only evidence of inflammation seen under the microscope was observed on the inner surface of the rind, along which fibrin or blood clot was in process of organization. It was limited to infiltration by varying numbers of polymorphonuclear leukocytes (fig. 85).

The second (middle) layer appeared on microscopic examination to be merely a mass of fibrin with scattered, formed blood elements trapped in its meshes.

Pulmonary Effects of Organizing Hemothorax

When the process of organization was complete, a dense fibrous membrane encased some portions of the lung, or the whole lung, thus limiting its mobility and preventing its complete expansion. A contraction of the hemithorax was sometimes present also. Even in the early stages of an organizing hemothorax, it was easy to see that the tough, resistant, inelastic rind that invested the visceral pleura effectively prevented pulmonary reexpansion. If the process were not terminated by surgical measures, fibrosis increased, and the rind and the pleura became intimately adherent. As time passed, tough scar tissue extended through the pleura into the interstitial pulmonary tissue. The degree of cel-


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FIGURE 83.-Photomicrograph showing biopsied section of lung and pleura after removal of overlying exudate. Note that pleura retains most of its normal characteristics.

lular intimacy made it difficult, and sometimes impossible, to develop a cleavage plane at operation, particularly if the pleura had been denuded or the lung wounded. In such cases, the results of surgery were not likely to be good: The lung, even when liberated by the procedure of decortication, could not expand because the fibrotic process had extended to it. When complete pulmonary reexpansion was impossible, the stage was set for the development of infection.

When the intrapleural mass was removed, it was frequently evident that the lung had not only been compressed by the intrapleural accumulation but had also been greatly displaced and had sometimes been infolded also (p. 183).

Resolution

Massive organizing hemothorax not treated by surgery could terminate in two ways: (1) by the formation of a fibrothorax or pleural calcification (fig. 82) or (2) by the development of a suppurative process. Spontaneous resorption of small and even moderate amounts of accumulated clotted blood or small amounts of fibrin was conceivable. If resorption of larger amounts occurred, which was not usual, recognizable sequelae were almost inevitable.

The rapidity and extent of clearance in any given hemothorax were impossible to predict. In some cases in which the initial observations gave promise of complete and prompt resolution, the process might suddenly become static, usually about the fourth week. Perhaps the chief reason for the dis-


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FIGURE 84.-Photomicrograph showing replacement of fibrinous exudate, pleura, and adjacent lung (lung is at extreme left) by collagenous connective tissue in organizing hemothorax.

cussion concerning the optimum timing of decortication (p. 286), which continued throughout the war, was the lack of agreement concerning the possibilities of resolution in an organizing hemothorax. The exact size and type of an intrapleural mass in which spontaneous resolution might be expected were never agreed upon, nor was the length of time in which expectant treatment should be practiced. Generally speaking, cavities involving less than 50 percent of the pleural space or less than 500 cc. in volume usually cleared spontaneously over a 6-week period, but this was a generalization to which there were multiple exceptions. No doubt, the most important consideration was the thickness of the intrapleural mass. It was repeatedly observed that roentgenologic clearing was confined to the inner portions of the clot. The thickest areas, notably the portion in the posterior thoracic gutter, were still clearly demonstrable on roentgenograms after almost complete clearing of other areas had occurred.


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FIGURE 85.-Photomicrograph showing infected organizing hemothorax with bacteria (Staphylococcus hemolyticus on culture) deep in unorganized portion of fibrin and growing in masses in its meshes. Note conspicuous absence of leukocytes.

BACTERIOLOGY OF ORGANIZING HEMOTHORAX

Hemothoraces represent the largest hematomas with which the body must deal. They are usually far too large to vascularize rapidly, which probably accounts for their tendency to infection, particularly when they are of the clotted type. This tendency was one of the many reasons why it was important that thoracentesis be performed promptly and repeated as necessary.

All types of bacteria were isolated from hemothoraces, including a surprisingly large proportion of anaerobic streptococci and staphylococci. Bacteriologic findings in 24 cases of hemothoracic empyema are shown in the following tabulation:


Bacteria

Number of cases

Proteolytic and saccharolytic clostridia

2

Micrococcus tetragenus

2

Hemolytic Staphylococcus aureus

1

Hemolytic Staphylococcus aureus, proteolytic Clostridium

1

Hemolytic Staphylococcus aureus, hemolytic Streptococcus, Pseudomonas aeruginosa

1

Hemolytic Staphylococcus aureus, Escherichia coli, Aerobacter aerogenes, nonhemolytic Streptococcus

1

Hemolytic Staphylococcus aureus, Escherichia coli, Aerobacter aerogenes, nonhemolytic Streptococcus

1

Streptococcus viridans

1

Hemolytic Streptococcus

1

Anaerobic Streptococcus

1

Nonhemolytic Streptococcus, Pseudomonas aeruginosa

1

Streptococcus viridans, proteolytic and saccharolytic clostridia, Bacillus proteus

1

Proteolytic Clostridium

1

Escherichia coli

1

Escherichia, type unidentified

1

Clostridium, unclassified

1

Cultures sterile

6

Pseudomonas aeruginosa

1


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Clostridial infections, which were not numerous, were nearly always caused by non-gas-forming bacteria. Remarkable combinations of bacteria were found in both the liquid and the unclotted hemothoraces. In the order of frequency, the offending organisms were streptococci, clostridia, staphylococci, Escherichia, and Pesudomonas. Regardless of the bacteriology, the clinical course was essentially the same, except that when Escherichia was present, the illness was usually more serious.

In some cases, bacteriologic confirmation was lacking in spite of clear-cut signs that infection had occurred. There were two explanations:

1. Bacteria might not be present in demonstrable numbers in the fluid portions of the mass.

2. The needle might, by chance, have been introduced into loculations (fig. 79) in which the fluid was still uninfected. If this was the explanation and infection had actually occurred, repeated efforts to find organisms would eventually be successful as the infection spread to the entire mass or as more rewarding sites were selected for aspiration.

In some patients, for whom no explanation was forthcoming, signs of sepsis were clear cut and organisms were found in fluid aspirated from the chest, but there was virtually no leukocytic response (fig. 85). In this group of cases, the fluid was thin and practically without sediment, even when organisms were present in large numbers.

In some cases, suppuration, as evidenced by purulent material on aspiration, did not manifest itself for 4 to 6 weeks. In a considerable number of these cases, it had been thought that resolution was occurring. The factor (or factors) which determined which cases would go on to prompt suppuration and in which suppuration would be delayed or would not be evident at all was never clearly demonstrated. Whatever the factor (factors) might be, the explanation was probably the balance or imbalance between (1) the rapidity and extent of the clotting that trapped the infecting bacteria in the fibrous mass


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and kept them from contact with the pleura and (2) the ability of the pleura to control or eliminate the bacteria that were originally in contact with it. If the organisms in an infected hemothorax were virulent and if seeding was heavy and early, a suppurative pleuritis was likely to occur promptly. Both the liquid and the clotted contents of the intrapleural space would be involved in the pathologic process. If, however, for one reason or another, the contaminating bacteria did not gain the ascendancy and instead became entrapped within the clotted intrapleural mass, then the mechanism of a delayed or latent infection was set up.

PHYSIOPATHOLOGY OF HEMOTHORAX

The bony thorax imposes definite limitations on the size of the thoracic cavity. This means that any space-occupying medium can seriously disrupt the normal function of the heart and the lungs. From this point of view, pneumothorax and hemothorax produced almost identical physiopathologic results. By impeding cardiac return and pulmonary expansion, they tended not only to reduce the volume of circulating blood but also to decrease the degree of oxygen saturation. The response was an increased cardiac and respiratory rate, both of which were almost invariably observed in any severe thoracic injury. The pain caused by damage to the thoracic cage and the voluntary restriction of motion to minimize the discomfort further added to the physiologic disturbances because the respiration was rapid and shallow and the pulse was fast. For these various reasons, it was necessary to empty the chest of blood and air as rapidly as possible.

CLINICAL PICTURE AND DIAGNOSIS

Simple hemothorax-The diagnosis of simple hemothorax almost never offered any difficulty. The history of wounding was clear cut. Hemothorax was known to be the most frequent complication of thoracic wounds. Finally, the pleural contents were readily aspirable. At first, the fluid was blood or bloody. Later, if resolution began to occur, the blood disappeared and the fluid became serous, as well as scantier, on successive aspirations.

Roentgenologic examination revealed intrapleural obscuration consistent with the presence of fluid (fig. 86). The lung margin was characteristically distinct and scalloped. This finding was particularly suggestive if the lateral view revealed the process localized to the posterior half of the involved hemithorax.

Organizing hemothorax-The diagnosis of organizing hemothorax was not always so simple. In the early stages, when clotting had occurred but fluid could still be obtained, it was sometimes impossible to distinguish the condition from a simple hemothorax. Later, it might be necessary to insert


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FIGURE 86.-Spontaneous resolution of clotted hemothorax. A. Posteroanterior roentgenogram showing clotted hemothorax on right. B. Same, showing spontaneous resolution after 6 weeks.

FIGURE 87.-Posteroanterior roentgenogram showing right clotted hemothorax. Note that border of partially collapsed lung is still fairly distinct. In liquid hemothoraces, borders of collection of blood were usually seen only as diffuse haze.


265

FIGURE 88.-Lateral roentgenogram showing clotted hemothorax over right lower and middle lobes. The sharp superior border seen in this view and not seen in posteroanterior roentgenograms came to be recognized as typical of clotted hemothorax.

the needle into many different areas of the chest to obtain any fluid. The aspirated material consisted of only small amounts of serum, which contained fragments of clot and fibrin threads. Efforts at drainage by insertion of an intercostal water-seal catheter were practically always unsuccessful.

If organization had gone on to fibrosis, the clinical picture was distinctive. A patient with fibrothorax was likely to show an overall contracture of the affected hemithorax; narrowing of the intercostal spaces; elevation and more or less immobility of the leaf of the diaphragm on the affected side; often considerable limitation of movement of the chest wall; and, not infrequently, an associated atrophy of the extracostal musculature, no doubt as the result of disuse.

Roentgenologic examination in organizing hemothorax (figs. 87 and 88) revealed a dense opacity corresponding to the area of the original hemothorax. Resorption and consequent improvement in the roentgenologic appearance (figs. 89 and 90) was observed in a few cases that had reached this stage, but, as a rule, narrowing of the interspaces, as well as contracture and relative immobility of the chest wall, was likely to remain unaltered.

Hemothoracic empyema-The clinical picture of hemothoracic empyema was that of typical empyema modified by the special considerations introduced


266

FIGURE 89.-Clotted hemothorax with spontaneous clearing. A. Posteroanterior roentgenogram showing clotted hemothorax 2 weeks after wounding. B. Same, 1 month later. Chest has almost completely cleared by natural processes. Neither thoracentesis nor surgery was used.

by the chest wound. Fever was usually high, and the patient was likely to become more toxic than he had been. There might be an associated pneumonitis with productive cough.

The sudden spillage of purulent pleural fluids in large amounts into the bronchial tree made the diagnosis of empyema with bronchopleural fistula simple. If there was leakage of only a small amount, the diagnosis was more difficult. The finding of a fluid level, otherwise unexplained, on the roentgenogram was almost certain evidence of a fistula.

The diagnosis of empyema was confirmed by the aspiration of fluid that was chocolate brown, foul smelling, or frankly purulent. In some cases, as just noted (p. 262), infection had been present for some time before purulent fluid appeared.

The degree of mediastinal immobility present in any given case depended upon the degree of organization that had occurred in the preexisting hemothorax. It was therefore roughly proportional to the length of time that had elapsed since injury rather than to the duration of the infection or the thickness of the purulent exudate.

Differential diagnosis-Large extracostal or intrapulmonary hematomas, as well as lobular or lobar atelectasis following bronchial obstruction, were usually readily distinguished from chronic traumatic hemothorax. Pneumonia was also readily distinguished. Infolded lung sometimes offered special difficulties (p. 183).


267

FIGURE 90.-Clotted hemothorax with spontaneous clearing. A. Posteroanterior roentgenogram showing right-sided massive clotted hemothorax, without infection, 2 days after wounding. B. Same, 3 weeks later. Complete spontaneous clearing occurred later in this case, in which evidences of resorption of fluid were noted from beginning.

MANAGEMENT OF SIMPLE HEMOTHORAX

Rationale of Thoracentesis

Thoracentesis was part of the routine of resuscitation for four reasons, all concerned with the restoration of normal cardiorespiratory physiology:

1. To relieve high intrapleural pressure.

2. To permit increased aeration of the pulmonary parenchyma and thus encourage prompt reexpansion of the lung.

3. To correct shock by relieving the hypoxia that was helping to cause it.

4. To relieve the shift of the heart and mediastinum and thus both improve the venous return to the heart and increase the volume flow of blood (fig. 91).

There were three additional reasons for continuing thoracentesis after resuscitation as part of the management of simple hemothorax in forward hospitals:

1. To decrease the possibility of later clotting.

2. To encourage apposition of the lung and the thoracic wall and thus limit the extent of infection if hemothoracic empyema should develop.

3. To prevent late fixation and contraction of the chest.

Failure to carry out aspiration of a simple hemothorax in forward hospitals often presented surgeons working in rear areas with complicated problems of organizing hemothorax and hemothoracic empyema, problems which could be solved only by radical surgery. The management of empyema was the responsi-


268

FIGURE 91.-Management of hemothorax by thoracentesis. A. Schematic showing of massive hemothorax with colapse of involved lung and shirt of mediastinum with partial collapse of uninvolved lung. B. Expansion of involved lung after removal of blood by simple aspiration of chest. This procedure, in addition to greatly increasing vital capacity, also indicates amount of intrapleural hemorrhage.


269

bility of surgeons in base hospitals and hospital centers, but its prevention was usually the responsibility of surgeons in forward hospitals.

Very early in the war, the practice of air replacement after thoracentesis was condemned, and all the attention was devoted to the policy of early, vigorous aspiration. Certain objections to thoracentesis that had been advanced before the war proved entirely theoretical:

1. The military experience showed that there was no risk of causing renewed bleeding by thoracentesis; no case is on record in which this happened. This might have been expected. The two chief sources of hemorrhage in chest wounds were extrapulmonary (from the chest wall or the mediastinum) and pulmonary. The existence of a hemothorax, however, had no effect on extrapulmonary bleeding, while the reason that pulmonary bleeding usually ceased spontaneously was not the effect of the hemothorax but the lowered pressure in the pulmonary artery and its branches (p. 153). Many more errors were made in World War II by not aspirating the chest than by aspirating it and taking the remote and theoretical risk of recurrent hemorrhage.

Only one case is on record in the Mediterranean theater in which there seemed to be any connection at all between aspiration of a hemothorax and secondary hemorrhage, and, in this case, the relation was entirely on a post-hoc-ergo-propter-hoc basis. Intrapleural bleeding occurred 10 days after closure of a sucking wound of the chest, after 2,850 cc. of bloody fluid had been aspirated over a 3-day period. Just as preparations were being made for exploratory thoracotomy to determine the source of the bleeding, the hemorrhage ceased as abruptly as it had begun, and recovery thereafter was entirely uneventful.

2. The risk of infection after a properly performed thoracentesis proved negligible.

3. The concept that only small amounts of fluid could be removed at one time proved completely false. Withdrawal of 1,000 to 1,500 cc. at one sitting usually caused no symptoms but, instead, produced relief of symptoms. Occasional patients complained of a tight feeling, pain in the chest, dyspnea, or dizziness after large amounts had been withdrawn, but these symptoms disappeared as soon as aspiration was discontinued and seldom recurred when the procedure was resumed 24 hours later.

If hemorrhage continued or recurred (fig. 92), thoracotomy was indicated. Reaccumulation of 1,000 to 1,500 cc. of blood within a short period after the first aspiration of the chest was likely to be associated with failure to maintain a satisfactory blood pressure and with a falling hematocrit. In these circumstances, simple aspiration could not be expected to be effective.

Technique of Thoracentesis

Since the purpose of the first aspirations of the chest was to relieve pressure and to aid in the restoration of normal cardiorespiratory physiology, it was not necessary to empty the chest completely. At the end of 48 or 72 hours,


270

FIGURE 92.-Schematic showing of recurrent hemothorax after thoracentesis.

aspiration was carried out at least once daily, in order to empty the pleural cavity as rapidly and as completely as possible. If thoracentesis had been instituted as soon as the casualty was seen, not more than three to five daily aspirations were usually necessary.

The patient was transferred to the base as soon as he was fever free and the chest had been completely or almost completely emptied. If he was received in a fixed hospital with clinical or roentgenologic signs of fluid, aspiration was resumed and was continued until the chest was empty or until it was clear that other measures would be necessary.

A single negative aspiration was not accepted as conclusive. Often three or four punctures had to be made before a loculated pocket was found. If several punctures produced no results, another surgeon attempted aspiration the next day. The effort was not abandoned in any case in which there was roentgenologic evidence of fluid or a suggestive pleural shadow until repeated attempts to locate and remove the fluid had been made. The fact that blood had clotted (fig. 93) did not necessarily interfere with its aspiration.

Results of Thoracentesis

The results of early, vigorous thoracentesis in hemothorax were excellent from the beginning. If this was the chief or the only complication of a thoracic wound, the great majority of casualties who were treated by this method could be returned to duty within 6 to 8 weeks after wounding.


271

FIGURE 93.-Schematic showing of massive clotted hemothorax. Aspiration of blood is still possible when process of organization is still incomplete, but when physical signs and roentgenologic findings point to a large accumulation of intrapleural fluid and only small amounts of blood can be aspirated, further attempts at evacuating chest are unlikely to be successful. If patient is dyspneic or shows signs of early infection, thoracotomy and evacuation of clots must be undertaken promptly. Usually, however, it is safe to wait for surgery (decortication) at the base.

Results improved as time passed. In August 1943, it was estimated that about 6 percent of casualties with uninfected hemothorax observed at the chest center at the 21st General Hospital, located near Naples, required decortication. By the end of the war, the only casualties in this group who required decortication were those in whom massive clotting had begun shortly after wounding. At this time, the operation was chiefly used in complicated cases of hemothorax and in hemothoracic empyema. The most reasonable explanation of the improvement was the excellent treatment of hemothorax in forward areas, including prompt, vigorous thoracentesis; measures to promote early pulmonary reexpansion; and a material reduction in the number of thoracotomies performed at initial wound surgery for the evacuation of hemothoraces.

While a hemothorax could become infected and empyema could develop early enough to require treatment in an evacuation hospital or even, occasionally, in a field hospital, these complications did not usually ensue until the patient had reached the base section. Both complications are therefore discussed elsewhere (p. 275).


272

CLINICAL PICTURE AND DIAGNOSIS OF HEMOTHORACIC EMPYEMA

Hemothoraces, as already pointed out, represented the largest hematomas with which the body had to deal in combat-incurred wounds. The fact that they were far too large to vascularize rapidly might very well have played a part in their pronounced tendency to infection.

When infection supervened in either the liquid or the clotted variety of hemothorax, it was not always easy to make a distinction between infected hemothorax and hemothoracic empyema,. The precise differentiation depended on changes in the visible characteristics of the pleural fluid. These changes did not always occur immediately (p. 266). The infection was classified as hemothoracic empyema as soon as gross pus or purulent exudate was observed in the aspirated material.

There were distinct differences between the hemothoracic empyema of combat-incurred wounds and the postpneumonic or metapneumonic variety of empyema. In the latter variety, two features were prominent:

1. Infection of the pleural space was initiated upon essentially normal pleural surfaces.

2. The preexistent pathologic changes were in the lung.

Hemothoracic empyema had the following characteristics:

1. The pleural space was seldom normal. It had been altered in varying degrees by the fibrinous deposit that resulted from the presence of blood in the pleural cavity. Posttraumatic empyema was therefore not primarily an infection of the pleura per se but an infection originating in pleural dead space occupied by a hematoma enclosed in a fibrinous capsule.

The antecedent status of the pleural space was a point of great importance. Infection developing within a pleural cavity which has not been the site of a significant hemothorax is always a more favorable type than hemothoracic empyema which develops in a preexisting pleural clot or a neglected liquid hemothorax. In the former type, the restraining membrane or peel commonly observed in all pleural irritative phenomena dates from the onset of the infection. In the hemothoracic type, the peel antedates the clinical evidence of infection and may be well on to maturity before treatment is started.

2. The lung was collapsed and compressed because of the presence of intrapleural blood. There were no changes caused by disease in it, and by the time empyema developed, healing had usually occurred in any pulmonary wound. It was repeatedly observed at decortication that the lung had returned to normal, as evidenced by its ability to expand, even when it had sustained extensive lacerations and contusions. There had been time for this recovery to ensue. When empyema developed in a liquid hemothorax, the average time between wounding and demonstration of pus by thoracentesis or at operation was 15 days. In the clotted variety it was 18 days.


273

3. The constrictive pulmonary investment-that is, the rind which enclosed the hemothorax-was responsible for failure of the lung to reexpand.

4. The purulent exudate thickened more slowly in the hemothoracic than in the postpneumonic or the metapneumonic variety of empyema.

5. Loculation was more frequent in the hemothoracic variety of empyema, and total empyema occurred more readily.

6. Even in patients with extensive hemothoracic empyema of several weeks' duration, there was no reaction in the costal periosteum, the ribs were never triangular, and the fingers were never clubbed as in the variety of empyema in which there was no antecedent trauma.

All of the circumstances associated with a combat wound are favorable for the development of empyema. They include the wound itself and the tissue destruction that accompanies it; the contamination introduced by the missile and the debris brought into the wounds with it; in many instances, the presence of pathogenic bacteria; tissue necrosis; the presence of an intrathoracic foreign body; pneumothorax or hemothorax, with resulting dead space in the pleural cavity; and the ideal culture medium furnished by a clotted or an organizing hemothorax. Neither chemotherapy nor antibiotic therapy could in themselves overcome these circumstances. Only good surgery could meet the situation.

EMPYEMA IN THE WORLD WARS

There was a vigorous discussion of empyema at the 1946 meeting of the American Association for Thoracic Surgery (6), in the course of which much emphasis was put upon the differences in the infections of the pleural cavity encountered in the two World Wars. The presentations on chronic organizing hemothorax, hemothoracic empyema, and decortication were prepared by the thoracic surgeons who had had the widest experience in this field during World War II. The discussion was participated in not only by these surgeons but also by a number of other surgeons, among them Dr. Evarts A. Graham, who had had the widest experience in chest trauma and postinfluenzal empyema in World War I.

Graham contended that no comparison was possible between the empyemas of World War I and World War II because there was no similarity between them. The surgeons of World War I, he said, were called upon to treat empyemas which were, in the Hippocratic sense, true abscesses of the pleural cavity. The empyemas encountered by the World War II surgeons were pleural infections attenuated by drugs. In other words, the World War II surgeons dealt with conditions never before seen. If Hippocrates could listen in on the discussion, Graham concluded, he would not know what the World War II surgeons were talking about.

The surgeons of World War II naturally took issue with this point of view. They contended that hemothoracic empyema was true empyema, and they


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pointed out that their first patients, as well as some of their later patients, were treated without benefit of chemotherapeutic or antibiotic agents. Many of these casualties, they emphasized, were very ill and highly toxic, and problems of management were quite as serious as those encountered in World War I.

The clinical and other distinctions between the empyemas encountered in the two World Wars were well stated by Dr. Carl Eggers:

1. Chronic empyema was the chief problem of thoracic surgeons in World War I, while posttraumatic hemothoracic empyema was apparently the chief problem of these surgeons in World War II.

2. The patients with chronic empyema encountered in World War I were chronic invalids. They had survived measles, influenza, lobar pneumonia, and the other diseases that were widespread in Army camps and that were frequently complicated by bilateral bronchopneumonia. They had withstood prolonged sepsis. They had usually undergone drainage operations for acute empyema. Structural organizing changes had frequently taken place in the chest wall, the pleura, and even the lung. As a result, their resistance was materially lowered.

3. In World War II, patients who developed hemothoracic empyema after combat wounds of the chest were usually in good physical condition. They had normally functioning organs. Their chest walls were usually intact or almost intact and were therefore mobile. Their lungs were usually uninvolved; if there was any pulmonary involvement, it was usually traumatic and not infectious. These casualties might have lost blood and been in shock, but their resuscitation had been uniformly excellent, and their resistance was generally good. In short, there was a striking difference in the general condition and the surgical risk presented by the casualties of the two World Wars.

In discussing the procedures possible in empyema in the two wars, Eggers pointed out that it would not have been possible, in World War I, to insert a rib spreader after making the incision, which was part of the technique of decortication in World War II. It would have been impossible because the ribs were usually fused and were firmly embedded in the thickened parietal pleura. Resection of portions of all the ribs overlying the pleural cavity was therefore prerequisite to mobilization of the chest wall. In World War II, the chest wall was practically always mobile. In World War I, the parietal pleura was often half an inch or more in thickness. Mobilization of the compressed lung, the most important surgical objective, had to be accomplished by reflection of the thickened tissue forming the angle of reflection from the parietal pleura onto the lung. Then, if it were possible, the remaining layer of tissue compressing the lung was peeled off. Often this was not possible. Then the solution was to make crisscross incisions into it. Complete reexpansion of the lung occasionally followed this procedure but, as a rule, success was only partial.

The degree of success achieved in individual patients in World War I, Eggers concluded, depended not only upon the surgery performed but upon


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the condition of the pulmonary parenchyma. If the lung was fibrotic, as it frequently was, complete reexpansion could not possibly occur. From this standpoint, conditions in World War II were very much more favorable, a point of view which the World War II surgeons present did not accept.

MANAGEMENT OF INFECTED HEMOTHORAX AND HEMOTHORACIC EMPYEMA

General Considerations of Treatment

Aspiration, with or without the instillation of penicillin, was occasionally used in small infected hemothoraces in the Mediterranean theater, but it was never a theater policy. This method was used only when cultures were sterile, compression of the lung did not exceed 25 percent, and the patient's condition was good. If a purulent exudate appeared, drainage was instituted at once. The unwise use of continued aspiration was an invitation to chronic empyema. In World War I, the patients who were thus treated endured months and years of suppuration and, if they survived, eventually required multistaged deforming obliterative operations. Such patients were scarcely ever seen in World War II.4

In some European chest centers, a so-called irritating pack was occasionally used in chronic empyemas in which the cavities were small or of moderate size, in the belief that maintenance of an acute inflammatory state would produce an obliterative pleuritis more rapidly. This method, which is usually employed only as a supplement to a small Schede thoracoplasty, was not used in the Mediterranean theater.

Intercostal catheter drainage as the sole method of treatment of empyema was never considered adequate. The catheter was promptly blocked by large amounts of partially degenerated clot, fibrin, and exudate, and drainage simply ceased. Early in the war, some surgeons employed catheter drainage as a preliminary to rib resection, but as experience increased, it came to be appreciated that if drainage was indicated, almost the only contraindication to rib-resection drainage was that the patient was too ill to tolerate it as a primary procedure.

Selection of Therapeutic Method

When treatment of infected hemothorax and hemothoracic empyema became standardized in the Mediterranean theater, three methods were employed:

1. Rib-resection drainage alone.

4The basic difference, of course, was that in World War I the empyemas encountered were of the synpneumonic or metapneumonic varieties. In World War II, the empyemas were chiefly caused by infection of hemothoraces. They occurred in healthy pleural cavities and in association with healthy lungs.-F. B. B.


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2. Primary decortication; that is, a procedure to eradicate infection or empyema by securing immediate normal expansion of the lung, without preliminary drainage of the pleural cavity.

3. Secondary decortication; that is, a procedure for the same purpose after adequate rib-resection drainage for several weeks.

The choice of treatment depended upon several factors:

1. The size and location of the empyema cavity. If the cavity were small, unilocular, and basal, rib-resection drainage alone was usually adequate.

2. The percentage collapse of the lung and its distribution. To World War II thoracic surgeons, the status of the lung was of primary importance. Their position was based on the truism: "As goes the lung, so goes the pleural space."

If collapse involved 50 percent or more of the lung, primary decortication was the method of choice, particularly if the pulmonary apex was involved in the collapse. Because of the increased technical difficulties if apical collapse ensued after rib-resection drainage, collapse at the apex was considered a more important indication for primary decortication than a similar degree of basal collapse.

The common method of estimating the percentage of pulmonary collapse was based upon the distance of the lung border from the lateral thoracic wall as it was observed in posteroanterior roentgenograms. The measurement was frequently found to be in error and was nearly always found to be a minimal estimate. The lung was usually collapsed for an equal distance from the anterior and the posterior thoracic walls. In most instances, if the lung border did not approximate the lateral thoracic wall by a third of the width of the hemithorax, the collapse was usually found to be 50 percent or more. A consistent lack of correlation was found between the percentage collapse of the lung as determined by roentgenograms and as observed at operation (fig. 94).

3. The status of the patient. A few patients were so seriously ill as the result of massive pleural infection that a procedure of the magnitude of decortication could not be considered as a primary procedure. This operation sometimes lasted 3 hours or more, and there was a considerable loss of blood during decortication of the visceral pleural surfaces.

Most patients treated by primary decortication had had fever to 102° or 103° F. daily for several days or longer before operation. When other features of the illness were favorable, pyrexia was not regarded as a contraindication to its performance. Much more important was the estimation of the general status of the patient and his ability to withstand surgery as shown by simple observations of the color of his skin, his appetite and nutrition, his general strength and alertness, and his response to transfusion.

4. The results of rib-resection drainage when it had been used as a primary procedure. In these cases, it was observed that if satisfactory results were to


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FIGURE 94.-Decortication in hemothoracic empyema. A. Posteroanterior roentgenogram showing original extent of empyema. B. Same, 2 weeks after thoracotomy and decortication, which resulted in complete cure. At operation, degree of pulmonary collapse was found to be considerably greater than indicated in figure 90A.

follow, they would be evident within the first 4 to 6 weeks after operation (fig. 95). If the lung expanded rapidly within that period, so that it seemed reasonable to anticipate continued complete obliteration of the cavity, no further surgery was considered necessary. If progress during this period was not satisfactory (fig. 96) and the collapse of the lung remained at 50 percent or more, secondary decortication was considered indicated, not only to prevent possible or probable chronic empyema but also to reduce the duration of pleural suppuration.

These considerations applied to all cases of empyema as well as to infections of clotted hemothoraces. Because of the tendency to loculation in both lesions, there was little reason for assuming that all septa would be broken and all loculi drained through the relatively small wound made at rib resection. This was true whether the purpose of the procedure was to provide an outlet for frank pus or for drainage of a clotted hemothorax. Rib-resection drainage was a satisfactory procedure, in short, only when the cavity was so small that all parts of it were readily accessible.

Multiple empyemas associated with fistula formation in a traumatized lung that had fully reexpanded offered a real therapeutic challenge. The precise origin of the pathologic process in such cases was frequently not clear. The blowouts might have occurred primarily along the missile track. Another theory was that a primary vascular injury might have resulted in areas of pneumomalacia that later ruptured, thus giving rise to isolated fistulas with separate encapsulated pockets of empyema.


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FIGURE 95.-Management of hemothoracic empyema by rib-resection drainage. A. Posteroanterior roentgenogram showing massive liquid hemothoracic empyema on left just before operation. B. Same, 4 weeks after institution of drainage by rib resection. Lung is now almost completely expanded. This patient went on to recovery without further surgery.

Decortication was obviously not the solution in this group of cases, and great care was required in the institution of drainage. A misplaced incision could result in unnecessary mutilation or even introduce a real threat to life. Attempts to drain one cavity through another, however closely adjacent the two cavities might be, were usually ill-conceived and might well cause complications by tearing into a lung that was normal or only slightly involved. The best technique in this kind of case was drainage by multiple rib resections.

DECORTICATION OF THE LUNG

Development and Rationale

The first decortication recorded in World War II was performed in the North African Theater of Operations, U.S. Army, in April 1943, by Major Burford, on a patient with an uninfected organizing hemothorax, 5 weeks after injury (vol. I). The smooth recovery and successful end result in this case elucidated many previously obscure problems of clotted hemothorax. Thoracotomy had sometimes been undertaken before this date for removal of the clot, but the operation was seldom successful, as might have been expected, for it made no attack upon the essential pathologic feature of clotted hemothorax; that is, the fibroblastic membrane or peel. It was the continued presence of this constrictive pulmonary investment that prevented reexpansion of the lung compressed by it.


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FIGURE 96.-Posteroanterior roentgenogram showing massive liquid empyema on right side 4 weeks after institution of rib-resection drainage. Lung is still collapsed. Patient later required secondary decortication.

The rationale of decortication was incontrovertible:

1. The continued presence of an organizing hemothorax prevents pulmonary reexpansion.

2. The intrapleural mass must therefore be removed.

3. A line of cleavage exists between the pleural surfaces and the membrane until such time as the process, if not interrupted, becomes chronic in the pathologic rather than in the chronologic sense.

4. Decortication, which removes the compressing membrane, if performed before the process becomes chronic, will result in immediate and total pulmonary reexpansion and will also obliterate all pleural dead space.

In the beginning, decortication was undertaken only on the indication of uninfected organizing hemothorax. At a number of operations, however, unexpected loculations of pus were found, and inadvertent decortication for infected hemothoraces and hematothoracic empyema proved the suitability of the operation for both of these conditions. The extension of the operation to these conditions was perfectly logical. The basic pathologic process was the same in both. Microscopic examination of the rind over the pleura in early empyema showed it to be identical, cytologically and chronologically, with the rind in noninfected hemothoraces.

With the advent of penicillin and the demonstration of its usefulness by Maj. Champ Lyons, MC, the next step in the evolution of decortication was natural, the use of the operation without preliminary drainage in massive empyema. The first deliberate primary decortication for hemothoracic empyema was performed by Maj. (later Lt. Col.) Paul C. Samson, MC, under penicillin protection, in March 1944. It was a complete success.


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Decortication was then extended to cases in which concomitant lesions justified operation even if the size of the clotted hemothorax or the empyema present would not, in themselves, have warranted the operation. In many residual empyemas, other persistent pulmonary processes required surgical correction, including obliteration of bronchial fistulas; wedge resections for multiple fistulas; or, occasionally, the same procedures for posttraumatic abscesses.

The rationale of early decortication in properly selected cases of sterile organizing hemothorax, infected hemothorax, and posttraumatic or hemothoracic empyema rapidly led to the concept that it was not tenable to consider that a patient with massive hemothorax was convalescing satisfactorily merely because he showed no signs of infection. Such a point of view took no cognizance of the primary concern of the surgeon; namely, the early restitution of pulmonary function and the prevention of the crippling effects of chronic fibrothorax.

The most effective reply to the arguments of those who advocated a more conservative approach to the therapy of posttraumatic empyema was the not insignificant case fatality rate in adequately drained cases in which progress was apparently satisfactory. Progress in even the most competently managed case was unpredictable, and the road from drainage to complete cure was beset with many dangers. Chronicity could develop at any stage, and at the best, the elapsed time between drainage and cure was a matter of many weeks, and often of many months.

The rediscovery and reapplication of total pulmonary decortication (vol. I) to organizing hemothorax and to hemothoracic empyema resulted in a prompt decrease in the duration of recovery after chest wounds and a reduction in the number of potential pulmonary cripples. In properly selected cases, decortication was almost invariably followed by prompt eradication of intrapleural fibrosis and sepsis and prompt pulmonary reexpansion.

As Col. Edward D. Churchill, MC, pointed out in the discussion of decortication at the 1946 meeting of the American Association for Thoracic Surgery (p. 273), the principle for which the Empyema Commission fought in World War I was to wait to establish drainage until a generalized empyema had become localized. In World War II, the procedure was the exact reverse: It was to take a localizing empyema and convert it into a generalized pleural contamination in order to achieve prompt reexpansion of the lung. When the principle was thus stated, Colonel Churchill concluded, it was as startling as it was important.

In the excitement of this discussion, three points of major importance in the management of the hemothoracic empyema encountered in World War II were not explicitly stated:

1. There was no emphasis on the status of the mediastinum. As Graham had pointed out in World War I, when the mediastinum had become fixed,


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drainage was indicated and safe. When it was still labile, drainage was not indicated and could be lethal.

2. The status of the pleural space depended upon the status of the lung, according to the truism, already mentioned: "As goes the lung, so goes the pleural space."

3. The point emphasized in Colonel Churchill's discussion, that it was safe to take a localizing empyema and convert it into a generalized pleural contamination in order to achieve prompt reexpansion of the lung, was possible only because penicillin was available and was capable of protecting the pleural cavity against bacterial invasion.

Indications

Before the concept of decortication for organizing hemothorax, infected hemothorax, and empyema could be properly formulated, it was necessary to bear in mind certain fundamental facts:

1. The essential nature of the pathologic process. The demonstration of the fibroblastic membrane that invested the pleura explained the chronicity of many hemothoraces with infection, made clear the object of treatment, and pointed to the procedure that would achieve the desired results.

2. The efficacy of penicillin in protecting against and controlling invasive infection, so that surgery could be safely applied at the optimum time to secure maximum functional results.

3. The selection of cases on the basis of strict indications. This was not a procedure for promiscuous use. After decortication was first introduced, the initial wave of overenthusiasm, as often happens, led to its use in some patients in whom it was not indicated. The original excess of enthusiasm was soon tempered by experience, and the scope of the operation was properly delimited and its indications defined.

There were four chief indications for decortication:

1. Uninfected organizing hemothorax.-Patients in this group were treated conservatively for periods ranging from 3 to 6 weeks. During this time, repeated aspirations were carried out. Even if all the blood in the pleural cavity could not be removed and some clotting had already occurred, the removal, from time to time, of as little as from 50 to 100 cc. of currant-jelly-like material through a large caliber needle was found to be advantageous. Breathing exercises (vol. I) were also instituted, in an effort to aid reexpansion of the lung.

Between the third and sixth weeks of conservative treatment, the patient's status was carefully appraised. If aspiration was yielding only a few cubic centimeters of blood and serum and if roentgenograms failed to show progressive improvement, decortication was regarded as indicated if the patient presented some or all of the following symptoms and signs: Diffuse pulmonary pain or discomfort; dyspnea on exertion; and poor thoracic expansion, with


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FIGURE 97.-Management of clotted hemothorax with retained foreign body. A. Poisteroanterior roentgenogram showing extensive left hemothorax, with foreign body in left lung. B. Same, showing clotted hemothorax of moderate size after 2 weeks' trial of aspiration. A clotted hemothorax of this size would not, in itself, have constituted sufficient indication for decortication at end of 2 weeks, but surgery was considered indicated because of missile in lung.

retraction and narrowing of the intercostal spaces. A generalized hazy appearance on the roentgenograms provided additional support for decortication.

Patients with organizing hemothorax associated with retained foreign bodies a centimeter or more in diameter often presented good expansion of the upper lobe by the third or the fourth week, although a lower lobe might still be partly compressed by organizing hemothorax. In cases of this kind, the combination of an organizing hemothorax, even of moderate degree, and of a retained foreign body was regarded as sufficient indication for decortication and removal of the missile (figs. 97 and 98).

2. Infected organizing hemothorax.-Decortication was undertaken, as soon as the patient's condition permitted, in all cases in which the pulmonary collapse was more than 25 percent, particularly if the collapse involved the apex. Although infection sometimes became evident by the 10th to the 12th day after wounding, it usually manifested itself at a somewhat later date. Positive smears or cultures frequently could not be obtained, and presumptive evidence of infection had to be based on signs of increasing toxicity, mounting fever, or rapid enlargement of the hemothorax. Massive clotting was likely to be present in these cases, and a policy of delay often led to the development of empyema.

Many surgeons took the position that bacteria were consistently present in hemothorax, even if cultures were negative and even if frank suppuration did not supervene. If this concept were correct and the intrapleural mass


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FIGURE 97.-Continued. C. Same, 2 weeks after decortication. Progress after operation was entirely satisfactory and patient went on to complete cure.

were left in situ, it seemed logical to postulate that true latency might result from foci of infection left deep in the hemothorax.

If this latter hypothesis were correct, then it could be further postulated that in the postwar period, patients with fibrothorax or neglected organizing hemothorax would present the persistent roentgenologic finding that in the past has been erroneously termed "thickened pleura." It is characteristically present in patients subject to recurrent febrile episodes caused by recrudescence of activity in foci of infection in the chest, as well as in patients who have become chronic respiratory invalids.

3. Posttraumatic (hemothoracic) empyema.-As already pointed out, the distinction between hemothorax with infection and frank hemothoracic empyema was not great in many cases. In frank empyema, the infection might have been present for a longer period of time or might be more virulent. In general, the patients were more critically ill than those with infected hemothoraces, and the aspirated material was more grossly purulent. All the patients on whom decortication was performed on the indication of empyema had clinical evidence of infection; that is, fever, anorexia, malaise, and other signs of toxicity. The majority were acutely and seriously ill, and at operation all were found to have purulent fluid in the pleural cavity.

The type of organism recovered from the pleural fluid was not a factor in the decision for or against decortication. Clostridial empyemas were treated by the same routine as other empyemas. The percentage of negative cultures was probably no greater than would be encountered in any series of empyemas. Negative cultures were to be expected after chemotherapy and antibiotic therapy had been employed.

Focal points of intense reaction were occasionally seen in hemothoracic empyema, and miliary abscesses were occasionally observed in the older portion of the organizing clot. On the whole, however, these layers (fig. 79) were remarkably free from inflammatory reaction. For all practical purposes, the pleura and the layers of adjacent organized clot, with their blood supply, had


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FIGURE 98.-Management of clotted hemothorax with retained foreign body. A. Posteroanterior roentgenogram showing clotted hemothorax on right, without infection, and foreign body in right lung. B. Same, 2 weeks after decortication and removal of foreign body. There is no residual hemothorax, and lung is fully expanded. 

cleared themselves of infection. This observation helps to explain why such good results could be obtained by decortication even when there was frank suppuration in the center of the organizing mass.

4. Other indications.-Persistent bronchopleural fistulas, esophagopleural fistulas, and transdiaphragmatic biliary fistulas were not frequent, but all played their part in the genesis of chronic empyema and therefore demanded energetic management. Early decortication, with excision and closure of the fistula, gave excellent results. In a few cases, decortication under penicillin protection was combined with the excision and closure of small intrapulmonary abscesses (up to 5 cm. in diameter) associated with empyema.

Penicillin, with its established bacteriostatic properties and its resultant ability to diminish the dangers of invasive infection at operation in the presence of acute intrapleural infection, proved to be the adjunct which had long been desired to render early surgery safe in such cases. Perhaps the most valuable role of penicillin was in the management of chronic empyema, in which it afforded efficient protection against spreading infection when a radical operation such as decortication was undertaken for the obliteration of a chronic empyema cavity.

A precise estimate of its benefits was naturally not possible. It seemed reasonable to assume, however, that, when the surgeon was obliged to work in a potentially or actually infected field, penicillin protection often prevented serious wound infections and other complications. When it became available, it was possible to pursue a rational plan of therapy in infected hemothorax and hemothoracic empyema, directed toward the achievement of (1) early


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pleuropulmonary lysis, (2) total ablation of infected tissue, (3) complete pulmonary reexpansion, and (4) absolute obliteration of residual pleural dead space. Under penicillin protection, all of these objectives could be achieved by a procedure relatively free from the risk of septic dissemination.

When penicillin became available, in the spring of 1944, the indications for decortication in hemothoracic empyema became stabilized. Rib resection with drainage was considered wisest when the pleural infection was limited to the basal portion of the thorax or when it was small and definitely encapsuled. If these empyemas were drained adequately, persistent cavitation seldom developed. If complete obliteration of the cavity and complete pulmonary reexpansion did not take place promptly, however, the patient was regarded as a candidate for decortication.

Preliminary rib-resection drainage was also used in patients who were too ill and too toxic to be subjected initially to open thoracotomy and decortication.

Decortication without preliminary rib-resection drainage had a number of advantages:

1. Complete pulmonary expansion occurred at once, with the immediate elimination of all intrapleural dead space.

2. Chronic empyema, which was a distinct possibility after rib-resection drainage, was prevented.

3. Weeks and months of disability were eliminated, as was the risk of serious and even fatal complications, such as brain abscesses.

4. The patient was spared a great deal of discomfort and inconvenience, and the hospital staff was saved the time and effort required by repeated dressings.

At least three factors were responsible for the poorer results in secondary decortication:

1. The patients requiring preliminary drainage were, as a group, more seriously ill than those who did not require it. In particular, they were likely to be much more toxic.

2. The intrathoracic wounds were generally more severe.

3. The interval between wounding and decortication was longer in secondary decortications, because of the original poor condition of the patients and the additional time necessary for the drainage operation and recovery from it.

Two questions arose in connection with the selection of cases for decortication:

The first question was whether it would be possible to develop a peel in the particular case. This was not a question that could be answered positively. Timing of surgery played an important part in the possibility. Roentgenograms did not furnish a clue, nor did a study of the parietal pleura at a preliminary drainage operation. As a matter of fact, the pleural membrane was


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usually thicker, and the pulmonary collapse more pronounced, than the films suggested. Unsuspected pleural pockets were also often found.

The answer to the second question, whether or not the lung would reexpand, depended upon the extent and type of pulmonary damage and whether or not infection was present. The description written by the forward surgeon might be helpful in estimating the extent of the pulmonary injury. If the injury was a contusion, a roentgenogram taken immediately afterward, before the development of hemothorax, was also helpful. Again, timing was a factor. If decortication were performed too soon after wounding, the lung would not have had time to heal after injury and regain sufficient elasticity to permit adequate reexpansion. If a homolateral pneumonitis was present, decortication was not performed until it had cleared up, not only to give the lung a chance to recover but also to avoid the risk of introducing organisms into the bloodstream by opening the lung; septicemia could easily result. As these statements indicate, the expansile ability of the lung could not be settled by generalizations but had to be estimated in the individual case.

Timing

As early as 1904, Violet (7) had stated that if decortication were to be employed, it should be employed promptly, as soon as it was evident that an empyema would not undergo spontaneous cure and before the walls of the cavity had become rigid and separated by too wide a space. Lilienthal (8), in 1915, had resorted to the operation in a matter of weeks, but most American surgeons who used it believed that it should be employed only after many months had elapsed and after other methods of treatment had failed. In 1928, Lockwood (9) reported that there were more failures in cavities that had lasted from 6 to 18 months than in those of longer standing. He had himself achieved partial success with decortication in an empyema of 21 years' standing, and he had had some good results in cases which had lasted for 16 years.5

The surgeons in the North African theater who first performed decortication for organizing hemothorax originally thought that a period of at least 8 weeks should elapse from wounding to operation. Their reasoning was that clearing of the pleural space would occur in a great many instances within this period. It proved fallacious as applied to all but small cavities. Eventually, by the trial-and-error method, it was found that the optimum period for operation in uninfected chronic traumatic hemothorax was between 3 and 5 to 6 weeks after wounding. If infection occurred, especially if it were of the rapidly developing type, operation was done earlier.

The timing was logical for several reasons:

1. If operation was deferred for 5 or 6 weeks, many patients who originally had seemed candidates for decortication showed satisfactory resolution. The

5These observers, it should be noted, were dealing with the type of empyema associated with the pneumonias, not with the hemothoracic variety of World War II.-F.B.B.


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size of the clot played a part in this decision. In perhaps 90 percent of all decortications, the intrapleural clot exceeded 1,000 cc. in volume. It was not conceivable that a mass of such size could be absorbed within 5 or 6 weeks, or even within a much longer period.

2. In uninfected cases, a rind less than 3 weeks old was usually so thin and so poorly defined that it had to be wiped off the pleural surface or stripped away piecemeal. It could seldom be removed in toto, as was desirable.

3. If operation was postponed for more than 5 or 6 weeks after wounding, the increasing cellular intimacy between the rind and the visceral pleura made the operation technically difficult. By the fifth or the sixth week, hemo-organization and fibroplasia had advanced to the point at which the membrane was substantial enough to be handled with ease. Extensions into the pleural and subpleural tissues, and sometimes complete synechiae between the rind and the pleura, made clean separation difficult and even impossible, and tears of the lung were frequent.

The length of time necessary for complete definition of the rind varied from patient to patient. In some instances, decortication was performed successfully within 10 to 14 days after wounding. At the other extreme, it was also performed successfully from 12 to 14 weeks after wounding, and the time was extended to even longer periods in some hospitals in the Zone of Interior (p. 405). On the whole, the best results were obtained within 3 to 5 or 6 weeks after wounding.

An obvious advantage of performing decortication early in uninfected organizing hemothorax was that infection was prevented at the same time that recovery was expedited. The tendency to infection and prolonged disability in organizing hemothorax weighed heavily in the decision to perform decortication.

Since the optimum time for decortication was within 3 to 6 weeks after wounding, evacuation to the Zone of Interior was not usually possible, and decortication had to be performed on most patients in oversea hospitals. It was preferably performed in a base hospital or chest center, but occasionally, if fighting had slowed down and evacuation to the rear was delayed, it was performed in an evacuation hospital.

Preoperative Preparation

The excellent results secured by decortication in World War II might lead those unfamiliar with the operation to conclude that it was not major surgery. The conclusion would be completely unwarranted. The operation was always one of magnitude and was never performed without careful preoperative preparation.

Preoperative measures included:

1. Identification of the infecting organism.


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2. Complete roentgenologic investigation, to determine the presence of retained foreign bodies, bronchopleural fistulas, lung abscesses, and other complicating lesions.

3. Replacement therapy. Daily transfusions were given, in amounts of 500 to 1,000 cc., until the hematocrit level was 40 or higher.

4. Nutrition. The nutritional status was brought to as near normal as possible by a high-caloric, high-protein diet. The serum protein is always low in any condition in which proteins are lost by exudation, and plasma infusions, as well as a protein dietary supplement, were therefore employed as indicated.

5. Penicillin therapy. Penicillin was given intramuscularly in amounts of 200,000 units every 24 hours (25,000 units every 3 hours), usually for 48 to 72 hours before operation. Some patients were apparently safely prepared in 24 hours, though this was probably not long enough in most cases, and other patients received penicillin for 14 days or more, which was usually unnecessarily long. It was useless to wait for defervescence. That could come only with the extirpation of the infected focus.

All of these measures were important. Compromise with any of them would have put the morbidity and mortality of decortication on a prohibitively high basis. The unavailability of most of these supplemental measures, as pointed out elsewhere (vol. I), furnishes at least part of the explanation of the poor results of decortication when it was first employed.

Principles

The principles upon which decortication was based were as follows:

1. The object of the operation was to peel off the membrane immediately overlying the visceral pleura and to remove all blood clot and fibrin in the pleural cavity, thus permitting complete reexpansion of the collapsed lung.

2. To accomplish this, adequate exposure was essential.

3. The first step of the procedure was to obtain a proper plane of cleavage between the peel and the visceral pleura, beginning at the junction of the collapsed lung with the chest wall or over the undamaged portion of the lung.

4. The peel was removed by blunt dissection, carried out digitally or with gauze.

5. The success of the operation depended upon complete freeing of the lung wherever it was directly adherent to the thoracic wall and the mediastinum, as well as along the fissural margins, so that complete circumferential reexpansion could be obtained. The apex of the lung had to be freed, so that it would fill the cupola of the pleural cavity. The operation could not be regarded as a failure if the diaphragm was not decorticated and mobilized, but if it could be released, pulmonary efficiency was greatly enhanced. Particular attention was paid to the redevelopment of the costophrenic sulcus.

6. Generally speaking, the greater the area of lung decorticated, the better were the results.


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7. Bronchopleural fistulas had to be closed, especially fistulas in the upper pulmonary lobe. If this lobe remained collapsed, the operation was a failure.

8. If intrapleural bleeding occurred and complete hemostasis was not obtained, the status of the pleural cavity would be about as it was before operation. It was best to leave the parietal pleura in situ if stripping it seemed likely to cause excessive bleeding. The membrane in this area was thicker and more vascular than elsewhere, and bleeding in it was not controlled by pulmonary reexpansion. It therefore became the practice to leave it in situ in most cases, on the ground that removal increased the surgical risks unnecessarily and did not appreciably increase the benefits of operation.

Anesthesia

Decortication was performed under cyclopropane or nitrous-oxide-oxygen-ether anesthesia, always by the endotracheal technique. The services of a trained anesthesiologist, experienced in thoracic surgery, were mandatory.

It was part of his task to administer blood to the patient during the operation, usually in the amount of 1,000 to 2,000 cc., according to the indications. It was just as important for the patient to leave the operating room with the hematocrit approximately normal as it was for it to be raised to normal level before operation. This aspect of blood transfusion was quite as essential in the end results of decortication as was its shock-preventing function.

Bronchoscopy was practically always performed at the end of the operation. It was never omitted if moisture was audible after catheter aspiration or if pulmonary reexpansion had been difficult.

TECHNIQUE OF DECORTICATION

Management of unhealed wounds.-Unhealed wounds on the hemolateral thorax were either closed before decortication was undertaken or were excised and closed just before the incision for decortication was made. If the two operations were done at the same sitting, fresh instruments were used for decortication.

The detailed technique of decortication was as follows:

Incision and exposure.-The patient was placed in the lateral decubitus position, with the affected side uppermost. A posterolateral intercostal incision, just below the angle of the scapula, was most often employed (fig. 99). It usually permitted excellent exposure, without section or resection of any ribs. There was no serious objection to removal of a rib posteriorly, but if an anterior incision was employed, costal resection was not necessary. Most decortications were done without section or resection of a rib unless previous surgery or comminuted compound fractures made it advisable to remove all or part of one or more (fig. 100). Exposure was usually entirely adequate without


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FIGURE 99.-Technique of decortication. Position of patient on operating table and site of incision.

costal mutilation, and intercostal incision, with retraction of the serratus anterior, was the method of choice.

Entrance to the chest was usually gained through the sixth intercostal interspace, but either the fifth or the seventh interspace could be used if a more generous intrathoracic exposure was thought desirable at either the apex or the base. Selection of the incision depended somewhat upon the individual thoracic habitus but was chiefly dependent upon the extent and the location of the process to be dealt with.

The first view of the interior of the chest, after the retractors had been slowly spread and full exposure had been secured, was of varying amounts of liquid or clotted blood, fibrin, or purulent exudate.

Release of lung.-As soon as the pleural cavity was entered, the lung was freed widely from the parietal pleural rind about the region of the incision. If this precaution was not taken, extensive damage to the lung could be caused when the ribs were separated. Great caution was necessary if there were many adhesions.

Since the lung was often compressed into the posterior gutter, much of the separation at this point was behind and mesial to the membranous envelope. Since the peel on the parietal pleura was usually left in situ (p. 289), it was important during the process of paraincisional mobilization of the lung that the proper line of cleavage be established. This was between the layers of the fibroblastic membrane and not between the pleura and the peel (fig. 79).

As soon as the necessary dissection had been accomplished, rib spreaders were introduced and the blades were widened gradually. It was important that they be spread gradually, especially if a rib had not been sectioned or resected, to allow for muscular relaxation and prevent costal fracture, pleural tears, and muscle avulsion.

Exploration.-All liquid exudate, fragments of blood clot, and masses of fibrin were evacuated, and all loculi were broken down. The cavity was then carefully examined for retained foreign bodies, fragments of cloth and other debris, and bronchopleural fistulas. After it was certain that a fistula did not exist, the cavity was thoroughly irrigated with physiologic salt solution.

Further inspection was then undertaken. All anatomic landmarks were obliterated, and the underlying lung was relatively immobile. Typically, the


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FIGURE 100.-Techniques of decortication showing alternate methods of entering pleural cavity: Intercostal incision (a), and rib resection (b). The sixth intercostal space was the most common site of entrance into the pleural cavity for decortication.

inner or younger surface of the peel had a brownish-red surface, with the appearance of shagreen leather. The contours were smooth.

Decortication.-The first step of decortication was a sharp incision through the fibroblastic membrane down to the visceral pleura (fig. 101). This step was facilitated if the anesthesiologist used moderate positive pressure, to brace the lung against the incision. The incised edges of the membrane were grasped by forceps and decortication was begun. As soon as the peel was completely disrupted in any segment, herniation of the underlying lung, under pressure, through the incision demonstrated the desired plane of cleavage (fig. 102).

Once a cleavage plane had been established between the organizing peel and the visceral pleura, dissection was continued digitally, or with small, firmly packed gauze pushers, or with small bronchoscopic sponges attached to long hemostatic forceps (fig. 103). The main pressure was always directed toward the rind. If the fingers were used, the palmar surfaces were turned toward the rind, and dissection was accomplished by sweeping motions. The pleura underlying the peel was nearly always thin, transparent, and expansile, and beginning reexpansion of the lung could be observed almost as soon as the regional peel was released.

Oozing was likely to be considerable from the visceral pleura, because of the numerous capillaries torn during the dissection and the gaping ends left on


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FIGURE 101.-Technique of decortication. Sharp incision through fibroblastic peel down to visceral pleura. Edges of incision are now grasped with instruments, and dissection is begun.

FIGURE 102.-Technique of decortication. Herniation of lung through incision in peel as anesthesiologist uses moderate positive pressure. Majority of lung is still compressed by intact peel.


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FIGURE 103.-Technique of decortication. Removal of peel by blunt dissection. At this point in the operation, nearly all of the peel has been dissected free from visceral pleura and elevated. Exposed pleura is grossly normal, as is lung.

the pleural surface. It could usually be controlled by warm, moist packs, supplemented by gentle pulmonary expansion under positive pressure.

If the peel was several weeks old, it was usually laminated, and great care had to be taken that the pleura was exposed in every area and that no laminations were left in situ. Reexpansion was inhibited if this precaution was omitted. These scattered islands, while thin, were surprisingly tough, and their removal was essential, for they caused crossings and infoldings of the lung that materially hampered complete pulmonary reexpansion. Crosshatching of the membrane, with piecemeal removal, was not a satisfactory substitute. If islands of thin, tough membrane remained in situ after removal of the primary peel, the correct procedure was to remove them separately.

Decortication was carried to the edge of the collapsed lung, where the peel was reflected onto the parietal pleura. After the fissures and apex had been freed, the lung was separated from the diaphragm, mediastinum, and pericardium, down to the hilus and the pulmonary ligament. This was another extremely important step of the procedure.

The diaphragm was almost always elevated and fixed. If it could not be decorticated completely without difficulty, it was freed circumferentially and thus mobilized. Decortication was never omitted if diaphragmatic disruption or fistula formation was suspected.


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FIGURE 104.-Technique of decortication. Lung completely liberated. When inflated by positive pressure, it fills the hemithorax.

The costophrenic and cardiophrenic sulci were examined, to make sure that they were free of clots and membrane. Their reestablishment increased the motion of the diaphragm and aided in pulmonary reexpansion.

As already mentioned, no attempt was made to remove membrane adherent to the parietal pleura because of the risk of bleeding (p. 290). The costal segment of peel, however, was scraped and scrubbed with gauze, to remove fibrin and to provide a smooth surface. Great care was taken in decorticating the fissural margins, about fistulas, and at the sites of healed pulmonary lacerations. Transdiaphragmatic fistulas were excised and closed.

Management of the lung.-After the initial release of the lung, it was expanded at intervals throughout the operation under increased positive pressure. This gradual method was preferable to attempts at sudden, complete re-expansion at the end of the operation. Such attempts were always ill-advised and could be harmful.

The visceral pleura was kept moist, and atelectatic areas of the lung were gently stroked as it was reexpanded. As a rule, the lung almost completely filled the pleural cavity before the chest was closed (fig. 104), though it was sometimes necessary to rearrange the lobes before they occupied their normal positions.

After the lung had been completely freed, any necessary pulmonary surgery was carried out. Although every effort was made to protect the visceral pleura, it was almost impossible to avoid small tears and areas of traumatism.


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FIGURE 105.-Management of clotted hemothorax by decortication. A. Posteroanterior roentgenogram showing massive clotted hemothorax on right after 4 weeks of observation without improvement. B. Same, 4 weeks after primary decortication. There is no residual hemothorax. Foreign bodies are in chest wall.

The leaks were plugged with fibrin foam or repaired with interrupted sutures of fine silk on atraumatic needles. If tears were overlooked, or if plugs and repairs were not completely successful, the multiple drainage provided at the end of the operation could be depended upon to maintain expansion until the openings were occluded.

Single superficial fistulas were closed after the edges had been freshened. Long sinus tracts were laid open as far as possible, and the lining membrane was curetted before the lung was closed in layers. Superficial closure of sinus tracts was not adequate.

Rib fragments in the lung, foreign bodies in the chest wall (figs. 105 and 106) and lung, and indriven rib fragments were also removed if their size warranted it or if they were readily accessible. It was seldom possible to identify intrapulmonary foreign bodies while the lung was still compressed by the rind of an organizing hemothorax, but they could usually be located and removed without difficulty after decortication (fig. 107).

Infected hematomas and lung abscesses were usually opened, and the necrotic lining membrane was dissected free and removed. The remaining dead space was obliterated by closure in layers with fine silk, nylon, or cotton.

A routine search for areas of infolding (p. 183) was carried out at the conclusion of all decortications. Exploration was particularly necessary when, although the pleura appeared grossly normal, the lateral fringe was abnormally blunt or the lingula was unusually short or a lower lobe was relatively small.

In all correctly performed decortications, the lung was freed from its points of attachment along the parietal or the diaphragmatic pleura; when this had been accomplished, areas of infolding were promptly evident. The freeing


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FIGURE 106.-Managment of massive liquid hemothoracic empyema. A. Posteroanterior roentgenogram showing hemothoracic process in left hemithorax. B. Same, 4 weeks after primary decortication. Foreign bodies are in chest wall. Complete cure resulted.

FIGURE 107.-Technique of decortication. A. Dissection of rind over upper lobe of lung. B. Lung incised over foreign body which has been fixed by finger compression.


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of points of attachment between the visceral and parietal surfaces at the costophrenic fringe might not permit unfolding of the involved fringe if basal distortion was extensive. In such a case, there might also be a symphysis between the opposed diaphragmatic surfaces of the visceral pleura. The attachment of one visceral surface to another was usually much less firm than the attachment between visceral and parietal surfaces. The surgeon, therefore, could readily slip his finger into the groove. Here it would encounter an intrapleural tunnel, covered only by a veil of thin adhesions. Release of these adhesions permitted unfolding of the involved portion of the lung and restoration of its normal contour.

Complete reexpansion of the lung, with obliteration of intrapleural dead space, was the best possible insurance against a complicating empyema. Any compromise with this ideal was an invitation to failure. An operation that ended without bringing the lung into absolute contiguity with the chest wall and without making certain that it remained there had failed to achieve its purpose. It was a fallacy to assume that half measures in this direction would, by the generous intervention of Providence or something else equally unlikely, result in cure. Unless a complete operation was performed, the patient might be left in a situation only slightly more favorable than his original state.

Final steps.-When all of these procedures had been accomplished, the inner thoracic walls were carefully inspected and palpated, to be certain that their surfaces were perfectly smooth. Tags and cuffs of tissue were removed as they were encountered; they encouraged pocketing and the creation of dead space.

Two or three of the intercostal nerves above and below the incision were injected with procaine hydrochloride solution (1- or 2-percent). The pleural cavity was thoroughly lavaged with at least 1,000 cc. of physiologic salt solution and then was dried by aspiration. After it was certain that it was empty and that there were no bleeding points, the lung was brought gradually to complete expansion and then was tested again for air leaks.

Modifications of technique.-The technique just described was followed in most decortications. Some surgeons varied it in small details. Thus, some thought it essential to free that portion of the lung which, while not encased, was slightly adherent to the chest wall beneath the reflection of the peel to the surface of the parietal pleura or was adherent to the diaphragm and the mediastinum. An occasional surgeon removed all three elements forming the capsule of the pleural pocket; that is, the visceral, diaphragmatic, and parietal elements. When this technique was followed, the visceral element was completely removed before, by a return to the original incision, a plane of cleavage was found between the parietal element and the chest wall. The separation, which was quickly accomplished with the finger or a blunt instrument, was continued until the previous field of dissection was encountered along the line at which the visceral element was reflected onto the parietal pleura.


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Drainage.-The sites for drainage were selected with the aim of obliterating dead space and maintaining pulmonary expansion. Soft rubber tubing, with an internal diameter of 10 mm., was used in all areas except the second interspace. Here, a de Pezzer catheter (No. 12 or No. 14) was used. The tip of the catheter was cut off, so that just the flange remained, and the tube was brought out anteriorly in the midclavicular line. A second drainage tube was used in the eighth interspace in the posterior axillary line. It was introduced for 2½ or 3 inches, and the proximal end was tacked to the parietal pleural wall, about 6 cm. from the skin surface, by a single silk suture. In infected hemothorax or empyema, a third tube was used in the fifth or sixth interspace in the midclavicular line, and a fourth tube was sometimes used in the seventh interspace in the midclavicular line.

If there had been a previous rib resection for drainage, the site of election for the posterior drainage tube usually corresponded with the site of previous drainage. In such cases, the margins of the wound were freshened, the tube introduced through it, and airtight closure accomplished about it. The drainage tube introduced at the first operation was sometimes removed 3 or 4 days before decortication, in anticipation of this procedure.

Closure.-Closure was accomplished in layers after the lung was completely within the chest. Sutures were placed in the inner layer of the incision but were not tied until the ribs had been approximated with lion-jawed forceps or retractors. Pericostal sutures were not used.

Local penicillin instillation.-Penicillin solution, in roughly equal amounts, was introduced into each drainage tube in infected cases. Each cubic centimeter of the solution contained 1,000 units of penicillin. The total amount used was from 25,000 to 50,000 units in 100 to 200 cc. of physiologic salt solution. All tubes were clamped when the patient left the operating room. The posterior tube was kept clamped for 4 to 6 hours, to permit contact between the penicillin and the tissues for this period of time. The other tubes were connected with water-seal bottles as soon as the patient was placed in bed.

POSTOPERATIVE MANAGEMENT AFTER DECORTICATION

General measures.-The postoperative management of a patient who had undergone pulmonary decortication was much the same as the regimen instituted after any other major thoracic operation. The reaction to operation was usually minimal, and the temperature and the pulse remained generally level in most cases (fig. 108). Even if empyema recurred, the temperature elevation was usually minimal.

Replacement therapy, in the form of blood, plasma, or dextrose infusions, was employed as necessary in each case. Return to a full diet, high in calories and protein, was usually possible within 24 hours after operation.


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FIGURE 108.-Typical temperature charts of patients with hemothoracic empyema treated by primary decortication with penicillin coverage. Note absence of postoperative reaction and prompt defervescence in all cases.


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As soon as he had fully reacted, the patient was elevated on a backrest, and the importance of deep breathing, forced expiration, and voluntary coughing, which had been explained to him before operation, was reiterated. These were all essential measures in the maintenance of pulmonary reexpansion.

Many surgeons regarded early ambulation as an important phase of the postoperative regimen. Some failures after decortication, in fact, were attributed to the immobility required by management of fractures of the extremities in traction. Thereafter, orthopedic surgeons were requested to manage these injuries in some way that would permit movement about the bed, at least.

Postural consciousness was stressed during the period of bed rest, and motion of the shoulder and arm was encouraged in the early postoperative period, before formal exercises were begun. Return to full activity was as rapid as was consistent with progress.

Penicillin therapy.-Intramuscular injections of penicillin were given by the dosage schedule used before operation until the drainage tubes had been removed and the patient had been afebrile for at least 2 or 3 days. This usually required that it be given for 10 to 14 days after operation.

Drainage.-The drainage tubes required close supervision. They were useful only as long as they functioned to maintain pulmonary reexpansion and to obliterate intrapleural dead space. They were essential for these purposes. Once these purposes had been achieved, the tubes simply acted as unnecessary foreign bodies. If the tubes had been placed correctly and hemostasis had been satisfactory, so that there was no undue oozing, it was only occasionally that any trouble was encountered in maintaining satisfactory drainage.

If a fistula developed, the anterior tube was kept in place as long as the air leak persisted, which might sometimes be as long as from 10 to 14 days. In none of these cases did intrapleural infection develop.

Complications.-Recovery was usually without incident, but fistulas and empyemas or recurrent empyemas were occasionally encountered. The low incidence of postoperative empyema was attributed both to good surgery and to penicillin protection.

If infection developed, as shown by a change from serous to purulent drainage, the postoperative empyema was usually basal and small. Dependent drainage was instituted at once. After a 2-inch resection of the eighth rib, a large airtight tube was inserted in the posterior axillary line and was attached to a water-seal bottle, to prevent secondary collapse of the lung.

DECORTICATION IN EMPYEMA OF NONTRAUMATIC ORIGIN

The experience with decortication in postpneumonic empyema in World War II was limited, one reason being (table 14) that the number of such cases was limited.

The rationale of the use of this operation in this variety of empyema was, however, entirely clear. If one compares the description of the histologic


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appearance of the fibrinofibrous membrane in such cases in World War I (2), it is evident that there is little difference between it and the membrane observed in the posttraumatic empyemas of World War II. This similarity, together with the fact that, at least in the early stages of postpneumonic empyema, the pleura is essentially normal, suggested the use in World War II of decortication in early, carefully selected cases of subacute or impending chronic post-pneumonic empyema. When the indication for surgery was total or subtotal empyema with collapse of the apex, loculation of the exudate was a further reason for considering decortication.

The thoracic surgeons who revived decortication in World War II believed that it would be technically possible to employ it in early or subacute tuberculous empyema, but their wartime experiences provided no opportunity to test the theory. It will be remembered that decortication had been originally used by Delorme (10) in 1893 for a "tuberculous" abscess of the chest wall with intrapleural extension (vol. I).

Although postpneumonic empyema was only a minor problem in World War II, enough of it was observed to evaluate the role of penicillin in its management during the acute stage. Observations at the various thoracic centers showed that this agent was a valuable adjunct, but that it did not take the place of adequate surgical drainage or, in the selected cases just mentioned, of decortication.

SPECIAL STUDIES OF PULMONARY DECORTICATION

Approximately 1,500 pulmonary decortications were performed in the Mediterranean and European theaters during World War II on the various indications outlined earlier in this chapter (p. 281). It is known that the surgical mortality rate was less than 2 percent. Lack of facilities and the general circumstances of wartime prevented a followup of these patients, but analyses of several series show that superior results were obtained. There was no doubt that decortication gave better results than methods used earlier. There was also no doubt that the results in primary decortication without drainage were much better than the results of secondary, postdrainage decortication (p. 310).

As already pointed out (p. 240), the incidence of empyema in the Mediterranean theater was far lower than even the most optimistic had dared to hope. The very favorable rate was the result of a totally integrated program of management of chest wounds that reflected credit on all echelons of medical care, particularly forward echelons.

The reduction in the incidence of posttraumatic empyema as the war progressed could not be attributed to any single therapeutic advance. Instead, it was due to a combination of improvements. The most important of these was the increasing emphasis put upon adequate debridement of chest wounds and


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FIGURE 109.-Comparative results of management of empyema in World Wars I and II. A. Typical patients with chronic empyema in Zone of Interior hospitals in World War I (2).

upon early, rapid, vigorous evacuation of the pleural cavity and prompt reexpansion of the lung. Another extremely important consideration was the decrease in the number of ill-advised thoracotomies in forward areas. The acceptance of the concept that a hemothorax is for all practical purposes a hematoma carried with it an implied warning as to how to avoid pleural sepsis, a warning that eventually was widely heeded. Fewer and fewer hemothoraces that required multiple aspirations were encountered in base hospitals in the last year of the war. The use of pencillin in forward areas no doubt favorably influenced the empyema statistics, but good surgery was the chief explanation of the improvement.

In base hospitals, the proper management of large clotted hemothoraces further tended to reduce significantly the incidence of empyema. The prophylaxis of chronic empyema was, in fact, one of the most important functions of a chest center. Early pulmonary decortication was of great value in accomplishing this purpose as well as in curing empyema that had become established.


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FIGURE 109.-Continued. B. Typical World War II casualties after primary decortication for posttraumatic empyema. In each of these cases, recovery was without complications, and patients were left with no residual disabilities.

The most striking and most convincing evidence of the value of decortication was the almost total elimination of the group of unfortunate victims of World War I (fig. 109A) who spent the post bellum years doggedly undergoing one major surgical procedure after another or living through a shortened lifespan of chronic invalidism due to recurrent episodes of suppuration. Many of the casualties treated by decortication in World War II (fig. 109B) were sent back to full duty, and a considerable saving in human suffering as well as in military manpower was thus effected.

Criteria of cure.-Several criteria of cure were set up in decortication for organizing hemothorax, infected hemothorax, and hemothoracic empyema:

1. The lung must be fully expanded at operation or within 2 weeks thereafter and the pleural cavity must be completely obliterated within 2 weeks of operation, as demonstrated by roentgenologic evidence (figs. 110, 111, 112, and 113) and by cessation of fluctuation in the water-seal drainage apparatus.

2. There must be no clinical or roentgenologic evidence of occurrence, persistence, or recurrence of empyema during the period of postoperative observation, which ranged from 4 to 12 weeks.

3. There must be no evidence of embolic spread of infection.


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FIGURE 110.-Management of hemothorax by secondary decortication. A. Posteroanterior roentgenogram showing massive liquid hemothorax on left before operation. Treatment by rib-resection drainage had been ineffective. B. Same, 4 weeks after decortication. Primary cure occurred.

FIGURE 111.-Management of hemothoracic empyema by primary decortication. A. Posteroanterior roentgenogram showing massive clotted right-sided empyema before operation. B. Same, showing practically normal chest 3 weeks after primary decortication.


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FIGURE 112.-Management of hemothoracic empyema by decortication. A. Posteroanterior roentgenogram showing early massive hemothoracic empyema just before operation. B. Same, 2 weeks after primary decortication. Note that lung has completely reexpanded and there is no evidence of residual empyema.

FIGURE 113.-Management of clotted hemothorax by primary decortication. A. Posteroanterior roentgenogram showing large clotted hemothorax on right. B. Same, 3 weeks after decortication. Complete cure resulted.


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Earliest Operations

An analysis of the first 25 decortications performed in North Africa, all by surgeons of the 2d Auxiliary Surgical Group, showed that all the patients were seriously ill and that the outlook in many of them was distinctly unfavorable. The single death in the series occurred 8 weeks after operation and was not related to it. In spite of the gloomy prognosis, there were 18 primary cures. In every instance, the temperature and the pulse returned to normal levels within 7 to 10 days after operation and there they remained. At the same time, there was a striking improvement in every patient in general appearance, in appetite and nutrition, in a rapidly restored sense of well-being, and in the capacity for a resumption of essentially normal activity.

One of the five recurrent empyemas was explained, at least in part, by the fact that the patient was treated in traction for a fractured femur and was almost completely immobile throughout the postoperative course. In the other four patients with empyema, the original cavities were greatly reduced in size and became progressively smaller during the period of observation after operation.

Of the 24 survivors, 2 were returned to full duty and 7 to limited duty in the theater, with the recommendation that their status be reviewed within 90 days. The other 15 were evacuated to the Zone of Interior, 5 because of recurrent empyema and 2 because of concomitant wounds. All were in good condition when they left the theater.

Decortication at the 21st and 300th General Hospitals

An analysis of 125 decortications performed at the 21st and 300th General Hospitals in the Mediterranean theater, between 1 April and 20 December 1944, showed no surgical deaths and only one complete failure in one of the earliest cases. There were no instances of invasive infection, and the only two wound infections were superficial.

Primary healing, with complete pulmonary restoration, occurred in over 90 percent of the cases in which the lung was normal at operation. The same results were accomplished in just over 75 percent of the group in which intrapleural infection had been present before operation. On the other hand, when the lung was involved in the original pathologic process, empyema was recurrent in 40 percent of the cases. Practically all of the recurrent empyemas, however, were basal and small, and they therefore responded well to rib resection and drainage. It seems fair to say that, with the exception of the single complete failure, all the patients in this series who did not obtain a primary cure at least benefited materially from decortication.

Decortication at the 12th and 36th General Hospitals

In a followup study of 140 of the 160 decortications performed at the 12th and 36th General Hospitals in the Mediterranean theater, Maj. William M.


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Tuttle, MC, Capt. (later Maj.) Hiram T. Langston, MC, and Maj. Robert T. Crowley, MC, published the following data:

There were no deaths in the 140 patients followed up, and, so far as could be determined, there were no deaths in the 20 not followed up.

In the 140 patients followed up, the hemothorax was organized but not grossly infected in 89. In all of the other 51 cases, infection either was known to be present before operation or was encountered unexpectedly at operation. In 90 percent of the total (160) series, the intrapleural mass exceeded 1,000 cc. in volume. 

In 90 of the 140 patients followed up, pulmonary reexpansion was complete within the first 24 hours, and in 18 others, it was complete within the next 24 hours. Twenty-six patients required 72 hours or more for complete reexpansion, and in the 6 remaining patients, the results from this standpoint were not satisfactory.

Of the 89 patients with organizing uninfected hemothoraces, 8 developed empyema after decortication. Most of the infections were merely small pockets that responded readily to drainage. All were either completely healed when the patients were evacuated or were progressing so favorably that it was thought that no further surgery would be necessary.

Recovery was without incident in 25 of the 51 patients who had grossly infected hemothoraces before operation. In 23 cases, small residual empyemas recurred, ranging in volume from 30 to 200 cubic centimeters. These pockets, as in the group just described, were either completely obliterated before the patients were evacuated or were progressing so satisfactorily that no further surgery seemed likely to be required. In the three remaining cases, additional surgery seemed inevitable.

The only other complications in the series were two wound infections. Although both patients had had preoperative empyema caused by Clostridium welchii, neither infection was severe. The absence of serious wound infections in this series is rather remarkable when it is recalled that many of the operations lasted from 1 to 3 hours and that the infected material traversed the wound during most of this time.

Penicillin became available while the operations in this series were in progress and was used in 77 cases. They are not consecutive; even when restrictions on its use were removed, it was employed only on indications. Of the eight patients who developed empyema after decortication of a presumably uninfected organizing hemothorax, five received penicillin during the immediate postoperative period and three did not. All 25 patients who recovered uneventfully after decortication performed in the presence of infection received it, which suggests the value of this form of therapy. Sulfonamides were not used in any case in the series.

The duty status of 3 of the 140 patients was not known when the report was made. Six were returned to full duty and 64 to limited duty in the theater, in a number of instances with the recommendation that their status be reviewed


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in 90 days. Twenty-three other men could have been returned to duty in the theater as far as their thoracic wounds were concerned, but associated wounds made this impossible. The remaining 44 patients had to be evacuated to the Zone of Interior because of the severity of their chest wounds.

Comparative Results of Rib-Resection Drainage and Decortication

An analysis of 94 cases of hemothoracic empyema treated by surgeons of the 2d Auxiliary Surgical Group after the indications for decortication had been stabilized permits a comparison of the results obtained in hemothoracic empyema by rib-resection drainage, primary decortication, and secondary decortication. 

Rib resection was the method of treatment in 72 cases, in 6 of which secondary decortication was necessary later. The other 22 patients were treated by primary decortication.

Rib-resection drainage.-Excluding the 6 cases in which rib-resection drainage was followed by secondary decortication and which will be discussed separately (p. 310), 66 patients, 5 of whom died, were treated by rib-resection drainage.

Of the 66 patients, 59 had small or moderately large empyemas, many of them basal. The majority still had small residual cavities when they were evacuated to the Zone of Interior, but progressive obliteration had occurred, and it was not thought that any of the patients would require further surgery.

The other seven patients had massive infections, and primary decortication would have been the treatment of choice had their condition permitted it. In some cases, their serious status was due to associated wounds rather than to empyema. Satisfactory pulmonary reexpansion occurred in only four of the seven cases.

In one of the three failures, a large fistula in the right main bronchus opened into a persistent large empyema cavity. The fistula would ordinarily have been closed and secondary decortication performed, but an associated laceration of the dorsal spine, with paraplegia, made the prognosis hopeless. In the two remaining cases, exploratory thoracotomy was carried out, in the hope that decortication could be done, but in both, the infectious process was already chronic, and operation was not considered feasible. All three patients were evacuated to the Zone of Interior, with recommendations for later surgery.

One of the 5 deaths in the 66 patients treated by rib-resection drainage was caused by a metastatic brain abscess, which is one of the hazards of empyema treated by this method. Two deaths were due to overwhelming pleural infection secondary to esophagopleural fistulas, and two were due, in large part, to severe associated wounds.

Primary decortication.-All 22 patients who underwent primary decortication had massive involvement of the pleural cavity, 4 on the basis of liquid hemothoraces and 18 on the basis of clotted hemothoraces.


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In a few instances, decortication had to be deferred longer than was considered desirable because of the gravity of associated extrathoracic wounds. In one case, the delay was 63 days. One or two patients did not come under observation until more than a month after wounding. Excluding these patients, the timelag between wounding and decortication ranged from 7 to 31 days and averaged 20 days. This timelag included a purposeful delay of 2 to 4 days after the diagnosis of empyema was made, to prepare the patients for operation.

The results in these 22 decortications were as follows:

A prompt cure was obtained in 18 cases, in 16 of which the empyema had originated in clotted hemothoraces. Included in these 18 cured patients were 2 who had small lung abscesses, each of which was associated with a foreign body and a bronchopleural fistula at the site of the abscess. In each instance, the foreign body was removed at decortication, the walls of the abscess excised, and the residual defect, including the fistula, closed in layers. There were no postoperative complications in either case.

In the four remaining cases in which primary decortication was done, there was a postoperative recurrence of empyema. All four patients were then treated by rib-resection drainage, with the following results:

In two cases, the recurrent cavity was small, and in both instances, it was almost completely obliterated when the patients were evacuated to the Zone of Interior. One of these patients had a late bronchopleural fistula, which closed spontaneously. It was not thought that additional surgery would be necessary in either instance. Why the empyema recurred in these two cases is not clear, for in both, complete expansion of the lung was obtained at operation.

In the third case, the cause of the recurrence was readily apparent. A large lung abscess was found at operation, surrounding a large foreign body and also the site of a bronchopleural fistula. To excise the abscess completely would have required lobectomy, and the patient's condition was too critical for such radical surgery. The fistula was closed, but the infection was not eliminated, and recurrence was regarded as inevitable. The recurrent cavity was small, but the closure of the fistula broke down, and further surgery would be necessary in the Zone of Interior.

In the fourth case, the cause of the recurrence was also apparent. This patient had a large lung abscess. It involved almost half of the lower and middle lobes on the right side and was also the site of a bronchopleural fistula. Partial lobectomy was performed on each of the affected lobes, and the fistula was closed. The remaining lung reexpanded normally after decortication, but the recurrence was expected because of the large amount of dead space left after lobectomy. Both the original and the recurrent infections were caused by Escherichia coli. The patient was seriously ill, and it was debatable, before the first operation, whether primary decortication or rib-resection drainage should be performed. He did not improve after decortication and lobectomy, and death occurred on the 30th postoperative day, from persistent and overwhelming


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intrapleural infection. There was no response to either penicillin or the sulfonamides. This was the only death in the 28 patients treated by decortication.

Secondary decortication.-In all six cases in which secondary decortication was employed after rib-resection drainage, the operation would have been done primarily had the patient's condition permitted it; in three cases, drainage was done for empyema necessitatis. In five of the six cases, the empyema had developed in liquid hemothoraces.

In all six cases, although drainage was apparently adequate, there was either no reexpansion, or only unsatisfactory reexpansion, of the lung, and decortication was resorted to because chronic empyema seemed to be impending. The duration of drainage before decortication ranged from 26 to 53 days and averaged 37 days. The timelag from wounding to the secondary operation ranged from 44 to 64 days and averaged 52 days. 

The outcome in these six cases shows again that primary decortication gives better results than the secondary operation. Prompt recovery ensued in two cases, but empyema recurred in the other four. On the other hand, these four operations cannot be considered total failures. They were performed because there was no significant pulmonary reexpansion, in spite of adequate drainage, and because in each instance more than 50 percent of the lung was collapsed. Even though the empyema recurred, it was thought that the purpose of decortication had been accomplished: In two cases, chronic empyema was positively prevented, and the anticipated duration of continued pleural suppuration was materially reduced. In the other two cases, while the situation was improved, it was thought that additional surgery would be necessary.

Conclusions.--The results obtained with decortication in these various series might be compared with the results reported by Nicholson and Scadding (11) in 291 wounds of the chest treated in British hospitals in the Middle East between November 1941 and May 1943, before decortication came into use. Hemothorax became evident in 187 cases and became infected in a third of these. The case fatality rate in 52 infected hemothoraces uncomplicated by pulmonary or subphrenic suppuration and managed by standard conservative measures was almost 20 percent, while at the time of the report, only 12 of the surviving patients were known to be entirely well.

Two points concerning the advantages of decortication over drainage operations for organizing hemothorax and hemothoracic empyema, although they have been made before, should be stressed again:

1. In favor of decortication was the short interval, usually from 6 to 8 weeks, necessary to effect a cure, compared with the weeks of suppuration, changes of drainage tubes, and daily dressings necessary in other methods. With their wounds cleanly and solidly healed, and their lungs fully expanded, the patients were well on the way to recovery within 2 to 3 weeks after operation.

2. In pleural infections treated by drainage, the road from the institution of drainage to a complete cure was not only long, it was also beset with dan-


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FIGURE 114 (case 1).-Spontaneous clearing of clotted hemothorax. A. Posteroanterior roentgenogram showing clotted hemothorax of moderate size, without infection, 2 weeks after injury. B. Same, 1 month later. Chest was almost completely cleared without surgery or additional thoracenteses.

gerous pitfalls. Chronicity might eventuate at any stage, and death might occur from a number of causes, including metastatic brain abscess. With this method, the outcome was uncertain as long as a vestige of the empyema cavity remained.

CASE HISTORIES

Case 1.-A soldier who sustained a perforating gunshot wound of the right hemithorax on 14 June 1944, with a laceration of the right lung, developed a hemothorax of considerable size. The wounds were debrided, and a sucking wound of exit was closed. A flapper valve intercostal tube was inserted after 800 cc. of blood had been removed from the chest by thoracentesis.

Drainage was unsatisfactory, and the tube was removed 48 hours after wounding. Roentgenograms 14 days after injury showed a moderately large, clotted right hemothorax (fig. 114A). There was no evidence of intrapleural infection.

Repeated aspirations yielded only a few cubic centimeters of serum and fragments of clot, but, because of the moderate size of the hemothorax and the absence of any evidence of intrapleural infection, spontaneous clearing was allowed to progress. Recovery was smooth, and within 6 weeks after wounding the chest was almost clear (fig. 114B). The soldier was returned to duty on 17 August 1944, 2 months after he had been injured.

Comment.-This case illustrates the successful outcome of a hemothorax of moderate size, without infection, treated conservatively. Clotting occurred in spite of the prompt removal of blood by aspiration.

Case 2.-When this soldier was wounded in action on 6 February 1944, he sustained a severe penetrating wound of the left thorax, with a laceration of the left lung. Initial


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FIGURE 115 (case 2).-Management of clotted hemothorax by decortication. A. Posteroanterior roentgenogram showing massive clotted hemothorax, without infection, but with no tendency toward clearing after 6 weeks. Repeated thoracenteses were not effective. B. Same 10 days after primary decortication. This patient went on to complete cure and was returned to duty. Foreign body was in chest wall.

therapy consisted of debridement of the wound and left thoracenteses. A metallic foreign body in the chest wall was left in situ.

Repeated thoracenteses were ineffective. Only small amounts of serum and fragments of clot could be obtained. Roentgenograms (fig. 115A) showed persistence of pleural fluid, with no evidence of resorption after 6 weeks. Thoracotomy with pulmonary decortication was then performed. A complete cure was obtained (fig. 115B), and the soldier returned to duty 3½ months after wounding.

Comment.-On the surface, there seems little difference originally between this case and the case just described (case 1). In both, clotting occurred, and additional aspirations were unsuccessful. Conservative treatment was practiced in both, with practically complete resolution at the end of 6 weeks in the first case, while in the second, no tendency toward resolution was evident. Decortication produced highly satisfactory results, and might, perhaps, have been employed earlier. If no tendency toward clearing was observed at the end of the third week after wounding, it was the general experience that it was unlikely to occur.

Case 3.-This soldier sustained a shell-fragment wound of the right chest on 31 May 1944. He had a sucking wound, a laceration of the lung, and a hemopneumothorax, all on the right side. Thoracotomy was performed in a forward hospital, with removal of the shell fragment in the lung, suture of the lung, and evacuation of the blood in the right pleural cavity.

When the patient was admitted to a chest center 11 days after wounding, he was desperately ill from massive empyema. The thoracotomy incision was reopened and the empyema drained through the bed of the rib that had been resected at initial wound surgery.

Drainage was apparently adequate, but the lung did not reexpand satisfactorily, and chronic empyema was evidently impending. Decortication was therefore performed 6 weeks


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FIGURE 116 (case 4).-Management of hemothoracic empyema by primary decortication. A. Posteroanterior roentgenogram showing right-sided hydropneumothorax, with 50-percent compression of lung. Fluid component secured by aspiration soon became thick and purulent. Ninth rib had been partly resected when thoracotomy was done immediately after wounding in forward hospital. B. Same, 2 weeks after decortication. Regeneration is evident in this roentgenogram. Complete cure was obtained, with total pulmonary reexpansion and total obliteration of empyema cavity.

after the drainage operation. The lung was freed without difficulty from the fibrinofibrous membrane which encased it. As soon as this was accomplished, reexpansion was entirely satisfactory. Convalescence was without incident, and the end result was excellent.

Comment.-This patient was far too ill for such a major procedure as decortication when he was seen in the chest center 11 days after wounding. Rib-resection drainage was lifesaving, but it was not sufficient to accomplish a cure. In World War I, this soldier would have become a chest cripple. Decortication saved him from this fate in World War II. Whether the thoracotomy performed at initial wound surgery was necessary is at least debatable. He might have been better off without it.

Case 4.-This soldier, who was wounded in action on 4 June 1944, suffered a severe penetrating shell-fragment wound of the right thorax, with a laceration of the right lung and right hemopneumothorax. A foreign body was seen in the lung. Thoracotomy was performed at a forward hospital on the day of injury. The foreign body was removed and the pulmonary laceration sutured.

The immediate convalescence was uneventful, but a few days after operation, a clotted hemothorax was found on the right side (fig. 116A). The patient was toxic, and his temperature rose daily to 101° or 102° F. Purulent fluid was eventually recovered from the chest, and Staphylococcus aureus was cultured from it. Thoracotomy and decortication were done at once, without preliminary drainage. Recovery was uneventful, and the end result was excellent (fig. 116B).

Comment.-This is another case in which prompt decortication saved the casualty from a long period of drainage and disability, and perhaps from chronic invalidism. It is also another case in which the patient might have done better without thoracotomy as part of the initial wound surgery.


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FIGURE 117 (case 5).-Management of clotted hemothorax by primary decortication. A. Posteroanterior roentgenogram 33 days after wounding, showing diffuse left-sided obscuration and narrowing of intercostal spaces caused by organizing clotted hemothorax. Thoracenteses had been ineffective. B. Same, 5½ months after primary decortication, showing essentially normal left hemithorax.

Case 5.-A 27-year-old soldier sustained an accidental sucking wound of the left anterior thorax during bayonet practice on 11 June 1943. A tension hemopneumothorax was managed by water-seal drainage for 48 hours. The sucking wound was trimmed and closed. Repeated thoracenteses produced no fluid.

When the patient was admitted to a thoracic surgery service on 10 July, the left chest was flattened anteriorly, and there was a slight scoliosis concave to the left. Expansion was appreciably limited. Horizontal expansion measurements showed the following differentials: Ensiform cartilage to spine on right, 1½, inches, on left 5/8 inch; nipple to spine on right, 1 inch, on left ¼ inch. Breath sounds were distant over the entire left chest.

For the past 2 weeks, the patient had been complaining of increasing dyspnea on exertion. He was now incapacitated for any activity except the most minor exercise, and he was showing no appreciable improvement.

Analysis of serial roentgenograms showed a persistent diffuse obscuration on the left, with the greatest density at the base. The roentgenogram taken on 14 July (fig. 117A) showed diffuse clouding. The intercostal spaces were narrowed, and there was a slight scoliosis concave to the left. There had been no essential change in these findings for the preceding 2 weeks.

On 16 July 1943, 35 days after injury, thoracotomy and decortication were performed. More than 500 cc. of clotted, degenerating blood was found occupying the space in the left hemithorax from the apex to the base and forward to the midaxillary line. The peel adherent to the visceral pleura was 3 mm. thick, and that adherent to the parietal pleura, which was left in situ, was 5 mm. thick. After decortication had been accomplished, there was immediate and almost complete reexpansion of the lung under slight positive pressure. A few bubbles of air escaped from a small tear in the visceral pleura, which was easily repaired.

Under the microscope, the visceral layer of rind showed adult fibrous tissue, with many penetrating capillaries, which were larger and more numerous on the visceral pleural surface.


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Frequent thoracenteses were carried out for the next 5 days. Roentgenograms 20 days after operation showed a small residual lateral pneumothorax, with complete pulmonary reexpansion at the base. Measurements taken 30 days after operation showed the horizontal expansion from the ensiform cartilage to the spine to be 1¾ inches on the right and 1½ inches on the left. Expansion from the horizontal nipple to the spine was 1 inch on each side.

The patient was discharged to limited duty 60 days after operation. A followup roentgenogram on 6 January 1944 (fig. 117B) showed the left thorax to be essentially normal.

Comment.-In this case, clotting apparently occurred almost immediately, for prompt and repeated thoracenteses produced no fluid. The patient was well on his way to becoming a chest invalid when thoracotomy and decortication were performed. As this case shows, the risks of removing the thicker and more vascular parietal peel need not be taken. It was left in situ at operation, and the patient made an excellent recovery. Repeated thoracenteses were employed after operation because drainage had been omitted.

Case 6.-A 19-year-old German prisoner of war sustained perforating wounds of the left chest from a high explosive shell fragment. The small wound of entry was located in the second interspace in the midclavicular line and the slightly larger wound of exit, in the eighth interspace in the midscapular line. Neither was sucking.

The wounds were debrided 24 hours after injury. At this time, roentgenograms revealed a left-sided hemothorax that was causing approximately 45-percent collapse of the lung. No fluid was obtained on thoracentesis.

For the next 8 days, the patient ran a febrile course, the temperature on one occasion reaching 103.2° F. Repeated aspirations during this period yielded only fragments of clot and shreds of fibrin. Smears and cultures were negative.

A roentgenogram 9 days after injury (fig. 118) showed the left hemithorax obscured and the lung compressed. The following day, a catheter (No. 22) was inserted into the left pleural cavity, but neither fluid nor clot could be evacuated.

Because of the continued fever and toxicity, it seemed probable, in spite of consistently negative cultures, that infection was developing in an organizing hemothorax. Thoracotomy and decortication were therefore performed 14 days after wounding. The pleural cavity was filled with clots and with loculated pools of thick, sirupy blood. The hemothorax was, as usual, larger than the roentgenograms had indicated. The lung was held immobile by a 2-mm. peel of fibrin, which was undergoing early organization. Decortication was technically tedious and difficult because of the thinness and friability of the peel. It stripped easily, but piecemeal removal was necessary. The underlying visceral pleura was grossly normal and did not bleed. No attempt was made to decorticate the parietal pleura. The wounds of entrance and exit in the upper lobe were solidly healed, and the fibrin peel over both areas was left undisturbed. When the diaphragm was freed, it immediately resumed its normal excursion. Before decortication, positive pressure up to 15 cm. H2O did not result in any pulmonary expansion. After decortication, the lung expanded promptly and filled the hemithorax.

Drainage was instituted through two intercostal tubes. The anterior tube was removed at the end of 24 hours and the posterior tube on the third day. The patient then became ambulatory. Roentgenograms on the seventh day after operation showed complete pulmonary reexpansion. When the patient was evacuated to a prisoner-of-war camp on the 14th day after operation, he was in excellent condition.

Cultures of the clot and peel removed at decortication were negative on both aerobic and anaerobic media.

Comment.-This case is an illustration of the prophylactic use of decortication. Obviously, infection was impending in an organizing hemothorax, and while the operation is somewhat more difficult as early as 14 days after wounding, because the rind is not yet well organized, it can be safely performed.


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FIGURE 118 (case 6).-Posteroanterior roentgenogram showing organizing clotted hemothorax on left side. Note apical compression and almost 50-percent pulmonary collapse.

Case 7.-A 34-year-old soldier sustained a sucking wound of the right posterior thorax on 23 September 1943. The wound was closed immediately by an occlusive dressing, and 24 hours later, primary closure of the pleura was performed. Water-seal drainage was continued for the next 48 hours.

On 27 September, 1,800 cc. of air and fluid were aspirated from the right hemithorax. The following day, roentgenograms (fig. 119A) showed a large amount of blood in the right pleural cavity, with a 75-percent collapse of the lung. On 30 September, 100 cc. of bloody fluid was aspirated, with considerable difficulty. A second attempt to evacuate the chest with intercostal water-seal drainage produced only 200 cc. of bloody fluid in 24 hours. On 5 October, all that could be obtained on aspiration was 20 cc. of sterile fluid. At this time, a lateral roentgenogram (fig. 119B) showed extensive obscuration at the base and multiple fluid levels, characteristic of intrapleural infection. The patient continued toxic and febrile.

On 7 October, right-sided posterior thoracotomy was performed after two small granulating wounds of the right posterior chest wall had been excised and closed with a separate set of instruments. Short posterior segments of the seventh and eighth ribs were removed, and the pleural cavity was entered through the seventh intercostal space. The lung was found bound down with characteristic organizing exudate and approximately 90 percent collapsed. The pleural cavity was filled with liquid blood, serum, masses of fibrin, and blood clot in various stages of degeneration.

When the peel was removed from the visceral pleura, there was immediate and almost complete reexpansion of the lung under slight positive pressure. The lacerations at the sites of the through-and-through pulmonary wounds were repaired with fine silk. Drainage was instituted. Immediate bronchoscopy was productive of a moderate amount of bloody mucoid secretion.


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FIGURE 119 (case 7).-Management of organizing clotted hemothorax by decortication. A. Posteroanterior roentgenogram 6 days after wounding showing extensive right-side hemothorax. Note compression of apex of lung. B. Lateral roentgenogram 3 days later showing extensive obscuration at left base and characteristic multiple fluid levels. C. Posteroanterior roentgenogram 30 days after decortication. Right lung has completely reexpanded,  but there is still basal pleural reaction present.

Recovery was uneventful except for an unexplained, transient temperature elevation to 103° F. on the third postoperative day. There was no wound infection and no evidence at any time that an empyema was developing. Roentgenograms 30 days after operation (fig. 119C) showed complete pulmonary reexpansion, with a moderate residual pleural reaction at the right base. The patient was fully ambulatory when he was evacuated on 11 November.

Pleural fluid cultured at operation showed a heavy growth of nonhemolytic streptococci. Microscopic examination of the peel revealed dense fibrinopurulent exudate, beneath which was a characteristic thickened membrane of organizing fibrin, showing fibroblastic and angioblastic proliferation.

Comment.-In this case, thoracentesis was not begun until the fourth day after wounding. In spite of roentgenologic evidence of hemothorax, aspiration was increasingly less productive, and there was clear clinical evidence of infection. This is another instance of the successful performance of decortication shortly after wounding as a means of avoiding the development of empyema.

Case 8.-A 22-year-old staff sergeant sustained shell-fragment wounds of the anterior right thorax, right buttock, and right wrist on 10 November 1943. He was expectorating bright red blood when he was received in an evacuation hospital. Because of pronounced abdominal rigidity, a laparotomy was performed 12 hours after wounding. No injuries


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FIGURE 120 (case 8).-Management of clotted hemothorax with retained foreign body and bronchopleural fistula by primary decortication. A. Posteroanterior roentgenogram 6 days after wounding showing extensive right-sided hemopneumothorax with compression of pulmonary apex. B. Lateral roentgenogram taken 6 days after wounding showing characteristic multiple fluid levels and large intrathoracic shell fragment. C. Posteroanterior roentgenogram 6 days after decortication, closure of bronchopleural fistula, and removal of shell fragment. Lung has completely reexpanded.

were found. Thoracentesis immediately after operation yielded 500 cc. of blood, which was used for autotransfusion.

For the next 10 days, bloody fluid and air were frequently aspirated from the right hemithorax. On 16 November, an abrupt attack of dyspnea was relieved by aspiration of 1,500 cc. of air. Clinically, there was no doubt of the existence of a bronchopleural fistula. Roentgenograms (fig. 120A, B) showed a partially collapsed lung with numerous intrapleural adhesions and extensive hemopneumothorax with multiple fluid levels. A large intrapulmonary shell fragment was seen indistinctly at the inner end of the ninth rib posteriorly (fig. 120A).

When the patient was admitted to a thoracic surgery service on 30 November, he was comfortable except for moderate dyspnea. Shortly after admission, 1,250 cc. of air was removed from the pleural cavity. Final manometric negative pressures of 12, 6 cm. H2O were maintained in spite of episodes of coughing.

Daily thoracenteses for the next 3 days yielded a total of 1,200 cc. of air and of 500 cc. of dark brownish-red fluid. The temperature rose to 102° F. daily. Two smears and a culture revealed many gram-positive intracellular and extracellular nonhemolytic streptococci.

Because of increasing toxicity and other clinical evidences of infection, thoracotomy was performed on 4 December. The pleural cavity contained 600 cc. of degenerating


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blood and exudate. The lung, which was partly collapsed, was immobilized by a firm organizing peel partly covered by yellowish-green exudate. The apex of the lung was encased in a tubular sheath that was attached to the cupola of the thorax. After complete visceral decortication, the shell fragment seen in the roentgenograms was easily found and removed from the right lower lobe; it measured 20 by 7 by 5 millimeters. A posterolateral, moderate-sized bronchopleural fistula in the upper lobe was repaired with interrupted sutures of fine silk. Drainage was instituted before closure.

The lung was completely reexpanded within 48 hours. Roentgenograms on the sixth postoperative day (fig. 120C) showed no abnormality except a triangular area of density in the right cardiophrenic angle. The collection of pleural fluid which it represented was promptly absorbed.

The patient was ambulatory 7 days after operation and was asymptomatic when he was evacuated to the rear 6 weeks after wounding.

Comment.-In this case, because of increasing toxicity, decortication was performed 3½ weeks after wounding. Thoracotomy would have been indicated, in any event, for the repair of the persistent bronchopleural fistula; and the foreign body in the lung was of sufficiently large size to require removal also. The combined procedure was carried out expeditiously and without difficulty, and convalescence was uneventful. This is another instance of prompt recovery after decortication as compared with a probable long period of invalidism and disability if conservative measures had been used and if the infection of the organizing hemothorax had been allowed to progress to empyema.

Case 9.-A 24-year-old Italian officer, a prisoner of war, on 10 July 1943 sustained an extensive perforating sucking wound of the right posterior thorax, with compound comminuted fractures of the right scapula and the third, fifth, and sixth ribs. The wounds were debrided, but the pleura was not closed.

By 17 July, increasing pressure was evident in the right hemithorax, and little clinical relief was afforded by repeated aspirations. Roentgenograms (fig. 121A) showed complete collapse of the right lung, cardiac shift, and subtotal compression of the left lung. Wide

FIGURE 121 (case 9).-Management of tension hemopneumothorax and total hemothoracic empyema by secondary decortication. A. Posteroanterior roentgenogram 8 days after wounding showing enormous right-sided tension hemopneumothorax, with mediastinal herniation; cardiac shift to left; complete collapse of right lung; subtotal compression of left lung. B. Same, 23 days after institution of dependent rib-resection drainage. Right lung is still totally collapsed.


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FIGURE 121.-Continued. C. Technique of right pulmonary decortication: (a) Appearance of totally collapsed right lung, which is completely immobilized by thick sheet of organizing fibrin and exudate, so that individual structures are scarcely discernible. After initial sharp dissection, a small flap of thick, organizing peel has been elevated by blunt dissection. Positive pressure has caused a slight herniation of lung through opening. (b) Mobilization of lung and diaphragm after complete decortication of visceral pleura. Visceral pleura is essentially normal and lung is expansile but not yet completely reexpanded. The ridge represents line along which thickened fibrous rind was reflected from visceral onto parietal pleurae. D. Posteroanterior roentgenogram 14 days after decortication. All drainage has ceased, and lung now completely fills pleural cavity.

mediastinal herniation and depression of the right diaphragm completed the picture of massive tension hemothorax.

The patient's condition became increasingly serious. The intrapleural tension was controlled between 20 July and 31 July by the use of an intercostal water-seal catheter, but the lung on the right continued collapsed, and a total empyema developed.

The patient was received in a thoracic surgery center on 2 August. The following day, 6 cm. of the tenth rib was resected, and a large tube was placed in the pleural cavity and connected to a water-seal bottle. For the first 24 hours, there was evidence of a small bronchopleural fistula. For the next 14 days, negative intrapleural pressure of from 10 to 15 cm. H2O was constantly maintained. Total collapse of the right lung (fig. 121B) persisted for more than 4 weeks, in spite of the negative pressure, adequate drainage, and frequent intrapleural irrigations with aqueous solution (1:3,000) of Azochloramid (chloroazodin). Bronchoscopic examination showed no bronchial obstruction.


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Sequestrectomy on the scapula was performed on 24 August. On 2 September, right-sided posterior thoracotomy was performed, with complete visceral decortication (fig. 121C). As roentgenograms had shown, the lung was found totally collapsed, and its margins could not be identified. It did not reexpand on positive pressure, and the diaphragm remained depressed and immobile. By combined blunt and sharp dissection, a proper cleavage plane was established between the visceral pleura and the adherent organized peel, which was 5 to 6 mm. thick. The visceral pleura was normally thin, but slight loss of translucency, with subpleural scarring, was observed in occasional areas. There was considerable oozing from the pleural surface.

Removal of the investing peel from the diaphragm mobilized it completely. When the lung, including the entire mediastinal surface of the upper lobe, had been completely freed, slight positive pressure produced 80-percent reexpansion. Drainage was instituted.

By the fourth day after operation, both drainage tubes had been removed, and the lung completely filled the pleural cavity. Convalescence was entirely uneventful. Two weeks after operation, roentgenograms (fig. 121D) showed the right lung to be well aerated. There was considerable resorption of the extensive peripheral reaction during the next 6 weeks. The reaction was to be expected, since no attempt had been made to remove the thick organizing peel from the parietal pleura.

When the patient was heard from by letter 3 months after operation, he had no complaints referable to the chest and was in excellent general condition.

Comment.-This is another instance of a desperately ill patient who did not respond to conservative treatment and who, as the result of decortication, was spared weeks and months of invalidism. Had conservative treatment been continued, he might have lost his life. The conditions found at operation made it clear that only decortication could have permitted the lung to expand.

Case 10.-A 26-year-old soldier, on 21 September 1943, suffered a perforating sucking wound of the left posterior thorax, with compound comminuted fractures of the seventh, eighth, and ninth ribs posteriorly. On the day of injury, the sucking wound was closed surgically by using a strip of latissimus dorsi to reinforce the intercostal muscles. The skin was left open. Five days later, although the patient seemed to be recovering satisfactorily, anterior roentgenograms showed, in addition to the rib fractures, a probable encapsulated area of pleural fluid superimposed on the cardiac shadow. They also showed a moderate amount of pulmonary infiltration that was considered due to bleeding.

On the 10th day after wounding, the patient became suddenly and rapidly dyspneic and complained of a sensation of tightness in the thorax and abdomen. When he was received in a thoracic surgery center shortly afterward, his temperature was ranging from 100° to 102° F. The left hemothorax had increased greatly, and there was some cardiac shift to the right. The immediate aspiration of 1,500 cc. of dark blood produced great subjective improvement. Smears and cultures were negative.

During the next 48 hours, although no additional blood could be aspirated from the chest, there was evidence of increasing intrapleural pressure. Roentgenograms (fig. 122A) showed increased left-sided obscuration, with further cardiac and mediastinal shift.

Left posterior thoracotomy was performed on 5 October, 14 days after injury. Fragmented portions of the three fractured ribs were removed, and the pleural cavity was entered through the eighth intercostal interspace. The lung was 75 percent collapsed. The pleural space was filled with about 1,000 cc. of firmly clotted blood; there was practically no liquid blood. A thin layer of fibrin, which showed early organization, was removed from the visceral pleural surface.

Posterolaterally, there was a laceration in the left upper lobe, 3 cm. deep, which contained four fragments of ribs. The lung bled briskly when these were removed. The laceration was repaired with fine silk. Anterior and posterolateral intercostal water-seal drainage was instituted. Closure of the chest wall was difficult posteriorly in the area in which the wound of entrance had been excised.


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FIGURE 122 (case 10).-Management of infected clotted hemothorax by early primary decortication. A. Posteroanterior roentgenogram 17 days after wounding and 7 days after thoracentesis, showing large hemorrhage on left, with cardiac shift to right. B. Same, 6 weeks after decortication and 2 weeks after secondary rib-resection drainage of small postoperative empyema. Pulmonary field is now clear, and posterolateral empyema has been well drained.

Both grossly and microscopically, the organizing exudate showed miliary abscesses. Culture of the blood clot removed at operation was positive for aerobic hemolytic Staphylococcus aureus.

Within 48 hours, thin, purulent drainage was evident from the lower tube. At this time, roentgenograms showed the lung to be well expanded at the apex. Laterally, an oval area of obscuration was seen, which later proved to be a small loculated empyema. By the seventh day after operation, the posterior portion of the incision, in the area in which the entrance wound had been excised, had become grossly infected. By the 14th day, it was evident that the localized empyema just described was connected with a small bronchopleural fistula and that intercostal drainage was not adequate. The following day, a 15-cm. segment of the ninth rib was removed, and the empyema cavity was opened widely and packed.

Convalescence thereafter was rapid. The small bronchopleural fistula closed spontaneously. When the patient was evacuated to the Zone of Interior 6 weeks after the second operation, roentgenograms (fig. 122B) showed good pulmonary expansion and almost complete clearing of the lateral and basal obscuration.

Comment.-This case is an illustration of the difficulties and complications which could arise when thoracentesis was delayed. It was not resorted to in this case until the 10th day after wounding, when the patient was seriously ill, and when, as later ineffectual aspirations showed, organization of the clot had already begun. The seriousness of his condition, with evidence of beginning infection, was considered a justification for early decortication, only 14 days after wounding. Miliary abscesses were already present at operation, and empyema developed later, but the cavity was small and the response to standard measures was good. This is another patient who would undoubtedly have gone on to a long period of established infection if decortication had not been resorted to promptly.


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FIGURE 123 (case 11).-Management of infected clotted hemothorax, complicated by segmental pulmonary necrosis and retained foreign body, by early primary decortication. A. Posteroanterior roentgenogram, 10 days after wounding and after induction of diagnostic pneumoperitoneum for localization of foreign body. Note large left-sided hemothorax, which has increased in size in spite of repeated thoracenteses. B. Same, 8 weeks after wounding and 6½ weeks after primary decortication, segmental lobectomy, and removal of shell fragment.

Case 11.- A 19-year-old soldier sustained a penetrating wound of the left thorax on the Salerno beachhead on 11 September 1943. There was no hemoptysis or dyspnea at any time. Roentgenologic examination on 16 September showed a hemothorax of moderate size and a large shell fragment lying well posteriorly at the level of the tenth interspace.

At this time the patient was somewhat toxic. His fever increased progressively, the highest elevation being 103.4° F. Repeated aspirations were productive of only small amounts of old, sterile blood. After diagnostic pneumoperitoneum on 20 September, roentgenograms (fig. 123A) showed that fluid was increasing in the left thorax, in spite of repeated thoracenteses.

On 23 September, left posterior thoracotomy was performed through the sixth intercostal space, after removal of posterior segments of the sixth and seventh ribs. The lung was collapsed, and there was extensive clotting of the hemothorax, with early organization. The shell fragment, which was intrapleural and had no clothing attached to it, measured 22 by 16 by 11 millimeters. It lay in a loculus of clotted blood mixed with greenish exudate, which had a foul odor. After the pleural cavity had been emptied, decortication showed the visceral pleura to be relatively normal. The lower half of the lower left pulmonary lobe was so badly lacerated and necrotic that segmental lobectomy was necessary. Drainage was instituted. Bronchoscopy at the end of the procedure produced bloodstained mucus.

Cultures of the organizing blood clot showed a mixture of staphylococci and anaerobic nonhemolytic streptococci.

After operation, the lung reexpanded well at the apex, but a loculated pocket of serosanguineous fluid developed in the axilla. It cleared with aspiration.

For the first 14 days after operation, the temperature ranged from 101° to 103° F. By the end of this time, drainage from the posterior intercostal tube had become purulent. When the tube was removed on 10 October, after drainage had apparently ceased, there was an immediate febrile flareup, and roentgenograms showed increased basal obscuration.


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On 16 October, open thoracotomy, with rib resection, was performed and tube drainage was instituted. The small basal empyema was rapidly obliterated, and roentgenograms taken on 13 November (fig. 123B) showed complete left-sided pulmonary expansion, with a minimal pleural reaction at the base. The patient was in excellent condition when he was evacuated to the Zone of Interior a few days later.

Comment.-In this case, decortication was performed in the face of existing infection and pulmonary necrosis. Convalescence was stormy, but the postoperative empyema was basal and readily cleared with the proper drainage. This case represents one of the few in the Mediterranean theater in which segmental lobectomy or any other excisional pulmonary operation was necessary.6

References

1. Neurosurgery and Thoracic Surgery. Prepared and edited by the Subcommittees on Neurosurgery and Thoracic Surgery, Committee on Surgery, Division of Medical Sciences, National Research Council. Philadelphia and London: W. B. Saunders Co., 1943.

2. Dunham, E. K., Stevens, F. A., Graham, E. A., and Keller, W. L.: Empyema. In The Medical Department of the United States Army in the World War. Washington: Government Printing Office, 1927, vol. XI, pt. II, pp. 33-392.

3. D'Abreu, A. L.: War Wounds of the Chest. In War Surgery Supplement No. 3, War Injuries of the Chest and Abdomen, Brit. J. Surg., 1952, pp. 383-403.

4. Edwards, F. R., and Davies, H. M.: Traumatic Hemothorax. Lancet 2: 673-675, 30 Nov. 1940.

5. Sellors, T. H.: Late Results of Missile Injuries of the Chest Treated in Britain. Penetrating Chest Wounds Treated at Leicester Thoracic Unit. In War Surgery Supplement No. 3, War Injuries of the Chest and Abdomen, Brit. J. Surg., 1952, pp. 403-408.

6. Samson, P. C., and Burford, T. H.: Total Pulmonary Decortication. Its Evolution and Present Concepts of Indications and Operative Technique. J. Thoracic Surg. 16: 127-153, April 1947.

7. Violet (de Lyon): De la décortication pulmonaire dans 1'empyème chronique. Arch. gén. de méd. 193 (vol. 1, series 10) : 657-678, 1904.

8. Lilienthal, H.: Empyema: Exploration of the Thorax With Primary Mobilization of the Lung. Ann. Surg. 62: 309-314, September 1915.

9. Lockwood, A. L.: The Empyema Problem. Arch. Surg. 16: 297-321, January 1928.

10. Delorme, E.: Nouveau traitement des empyèmes chronique. Gaz. d' hôp. 67:94-96, 25 Jan. 1894.

11. Nicholson, W. F., and Scadding, J. G.: Penetrating Wounds of the Chest. Review of 291 Cases in the Middle East. Lancet 1: 299-303, 4 Mar. 1944.

6The reader is referred to chapter XI (p. 441) for long-term followup studies on casualties whose chest wounds were complicated by hemothorax and hemothoracic empyema.

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