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Chapter II



Sandfly Fever

William A. Reilly, M.D., Roberto F. Escamilla, M.D., and Perrin H. Long, M.D.

The diagnosis of sandfly fever was not made as frequently as it should have been, because of an unfamiliarity with the disease and a certain reluctance on the part of medical officers to make the diagnosis solely from the clinical picture.1

Sandfly fever, also known as Phlebotomus fever and pappataci fever, attained importance in Allied and Axis forces in the Mediterranean (formerly North African) Theater of Operations, U.S. Army, in World War II by incapacitating large numbers of men for periods of 7 to 14 days, or longer. This disease was known to be endemic in the Mediterranean littoral and was first recognized in U.S. forces in North Africa toward the end of April 1943. Although not reported as such in the statistical health report (WD MD Form 86ab), the first patients were seen at the 77th Evacuation Hospital then situated near Bône, Algeria. At that time, typical cases were described, and a careful study was made of the relation and importance of meningeal irritation to the general findings in the disease. The patients had come from the U.S. II Corps which was then engaged against the enemy in northern Tunisia. At the same time that these patients were being studied and the disease recognized in the 77th Evacuation Hospital, an increased incidence of influenza was observed by the medical services of the other evacuation hospitals within the corps area and also a sharp increase in the number of cases of F.U.O. (fever of undetermined origin) was noted in the statistical health report for April 1943. While no careful search for sandflies was conducted by trained entomologists during that period, it is known that sandflies, Phlebotomus papatasii, were captured and identified as such in northern Tunisia by certain British medical officers and by members of the hygiene section of the British First Army.

While knowledge concerning the incidence of sandfly fever in U.S. forces in North Africa during the summer of 1943 is obscured by the fact that the diagnosis was infrequently made and doubtlessly most of the cases were classified as F.U.O., the disease is known to have occurred frequently in the region of Tunis, Mateur, Ferryville, and Bizerte in Tunisia; also

1Letter, Lt. Col. Perrin H. Long, MC, Consulting Physician, Office of the Surgeon, Headquarters, NATOUSA, to the Surgeon, NATOUSA, 24 Aug. 1943, subject: A Report Upon Medical Services in Sicily.


around Oran and Algiers in Algeria.2 Cases of the endemic disease were noted in members of the Allied forces in Algiers and, in at least one instance, a fairly extensive outbreak occurred among members of a signal corps detachment which was situated just outside the city. In this outbreak, the disease was thought to be dengue until a review of the clinical findings in the disease revealed an absence of secondary rises in fever. An entomological survey of the area of this detachment established the presence of many sandflies of the variety P. papatasii.

A review of the plans for the amphibious operation in Sicily which dealt with the professional services shows that sandfly fever was considered a likely threat to manpower during the Battle of Sicily and that the peak of the disease would be reached after 1 August 1943. This prediction was more than realized, because the disease which had been contracted in North Africa began to make its appearance on D-day in Sicily, and, while no cases of the disease were reported in the statistical health report for NATOUSA (North African Theater of Operations, U.S. Army) for July 1943, in reality, there were hundreds of cases of sandfly fever in the troops in Sicily during that month. This lack of reporting was due to the diffidence that medical officers then showed in making the diagnosis of the disease from the clinical findings alone.3

Despite the reporting of but 104 cases, the disease reached epidemic proportions in Sicily because it was a favorable summer for the propagation of sandflies, the type of fighting was from village to village, native habitations were used as billets, and discipline in respect to the use of nets and insect repellents was poor. Sampling studies made in division clearing companies and evacuation hospitals during the first 2 weeks in August produced clinical evidence that, at a minimum, at least 25 percent of the cases diagnosed as F.U.O. should have been diagnosed as sandfly fever. During the latter half of the month of August and the first half of September, this same percentage probably prevailed.

The invasion of Italy by way of the beaches at Salerno (an area in which sandflies were common) was attended by a large number of cases of sandfly fever. This invasion was spearheaded by the 36th Infantry Divi-

2In May 1943, shortly after Von Armin's army was driven out of Tunis, contact was possible with U.S. Army Forces in the Middle East (Egypt) and the Persian Gulf Service Command (Iran-Iraq). Reports of the extensive outbreaks of sandfly fever there, which occurred in U.S. personnel, were beginning to be available although it was apparent that in these areas, too, medical officers were loath to make the diagnosis, preferring F.U.O. or influenza.
3An analysis of the possible extent of sandfly fever cases in the Sicilian campaign, nearly all of which were probably erroneously diagnosed as malaria or conservatively labeled F.U.O., was the subject of a special report made by Maj. (later Lt. Col.) Albert B. Sabin, MC, in September 1943. This report was subsequently published in part by Major Sabin, Lt. Col. Cornelius B. Philip, MC, and Dr. John R. Paul. The conclusion reached by Major Sabin was that sandfly fever was probably responsible for as many, if not more, cases of fever as malaria. (1. Letter, Maj. Albert B. Sabin, MC, to Chief Surgeon, Seventh Army: Col. Daniel Franklin, 7 Sept. 1943, subject: Estimate of Extent to Which Sandfly Fever Was and Is a Problem Among American Forces in Sicily. 2. Sabin, A. B., Philip, C. B., and Paul, J. R.: Phlebotomus (Pappataci or Sandfly) Fever; A Disease of Military Importance: Summary of Existing Knowledge and Preliminary Report of Original Investigations. J.A.M.A. 125: 603-606, 1 July 1944.)


sion, a unit which had had little experience with sandfly fever and hence was comprised mainly of susceptible persons. Again, as in Sicily, the troops made use of buildings both as strong points during the fighting and subsequently as billets, and discipline in the use of nets and repellents was poor. Because of certain command difficulties, it was impossible to have an adequate study made of the F.U.O. cases in Fifth U.S. Army hospitals during September and early October, so that an approximation of the number of cases of sandfly fever was not made, although from the rather meager data at hand it seemed probable that the incidence of the disease in the Fifth U.S. Army during this period was similar to that experienced by the Seventh U.S. Army in Sicily.

In 1944, in Italy, the situation in respect to the diagnosis of sandfly fever was considerably improved, and the figures for that year were much more representative of the actual incidence of the disease than they were in 1943. However, it must be recorded that, even after an indoctrination campaign had been conducted in the diagnosis of sandfly fever, there were many medical officers who, because a specific diagnostic test for this disease did not exist, preferred to make the diagnosis of F.U.O. Frequent examples of this failure to make the proper diagnosis were encountered in the monthly essential technical medical data reports, in which medical officers, after having described classical examples of the disease, would state that although sandflies are known to exist in this area, the fact that none of the patients had seen the insects and few if any gave a history of having been bitten by sandflies, the diagnosis of sandfly fever could not be definitely established and that, hence, the cases were classified as being F.U.O.

In MTOUSA (Mediterranean Theater of Operations, U.S. Army), during the winter of 1944 and spring of 1945, an intensive campaign of education was carried out in respect to the clinical findings in sandfly fever. The effect of this campaign became evident because the incidence of sandfly fever as reported in the statistical health reports for May, June, and July, 1945, reflected the true incidence of the disease.

While the literature upon disease in the Wehrmacht was scanty, it was known that German troops based in the Mediterranean area suffered from sandfly fever. Hallmann,4 in 1941, described an outbreak of sandfly fever that occurred in German soldiers who were stationed in the islands and the Greek mainland near Athens. The majority of the cases of the disease were seen in July and August, and it was estimated that 20 percent of all the troops in the area had the disease during this time. In a report printed in Berlin in 1944,5 an analysis of 5,890,000 records for admissions to hospitals for sickness in the German Army from 1 September 1939 to 31 March 1943 was made. Of the admissions recorded in this report, 1,062,920 were for

4 Hallman: Beitrag zum Pappatacifieber 1941 auf der Balkanhalbinsel. Deut. trop. Ztschr. 43: 64-68, 1 Feb. 1943.
5Die Infektionskrankheiten im jetzigen Kriege, Anlage zu Der Heeres-Sanitätsinspekteur. Nr. 8715/44 geh. (Wi G) Prüf Nr. 50. Berlin, den 28.8.1944.


infectious diseases. Sandfly fever (Pappatacifieber) was 13th on the list as a cause for admission with 4,941 cases recorded without any deaths and with an average period of hospitalization of 13.4 days. Inasmuch as the Wehrmacht had a large number of troops stationed in the Mediterranean and Black Sea littorals in 1941, 1942, and 1943, it is astounding that but 4,941 cases of sandfly fever were recorded. It is especially surprising when one considers that in this study no mention was made of the existence of F.U.O. The truth of the matter probably lies in the fact that during this same period a total of 159,890 cases of "grippe" were recorded from hospital reports. It is likely that many cases of sandfly fever were reported incorrectly under this diagnosis.


It was established in 1908 by Doerr, Franz, and Taussig6 that the causative agent of sandfly fever is a filterable virus and that the midge, P. papatasii, is the vector of this disease. This finding was confirmed by other observers7 and also by Sabin, Philip, and Paul. Sabin and Paul studied the disease in Sicily after the end of the Sicilian campaign in 1943. As a result of their studies, they obtained the following information regarding the virus of sandfly fever:

Virus is present in the blood of patients 24 hours before the onset of fever and during the first 24 hours thereafter; it is no longer demonstrable 48 hours after onset. It may be passed serially in volunteers by parenteral inoculation although the intracutaneous and intravenous routes were more effective than the intramuscular or subcutaneous routes. Attempts to recover virus from the spinal fluid obtained in the first 2 days of the experimentally produced disease were unsuccessful. The virus survived in the frozen state at Dry Ice box temperature or in the lyophilized state in an ordinary refrigerator for 6 months. The size of the virus as determined by filtration through gradocol membranes appeared to be not larger than 25 to 37 mμ, although the low titer of virus (1,000 minimum infectious doses per ml. of serum) suggests the possibility that it might be even smaller. Unsuccessful attempts were made to inject embryonated eggs and a wide variety of species including young baboons (Papio hamadryas) and monkeys of the following species: grivet (Cercopithecus griseoviridis), vervet (Cercopithecus aethiops pygerythrus), red African hussar (Cercopithecus [Erythrocebus] patas), Macaca radiata and Macaca mulatta (rhesus). The rodents included young white mice, wild gray mice, Syrian hamsters, Egyptian desert rats (jerboas), rabbits, guinea pigs, and cotton rats.

As cited by Warren and Johnson,8 Sabin also showed that there was more than one strain of sandfly fever virus. Volunteers who had been inoculated

6Doerr, R., Franz, K., and Taussig, S.: Das Pappatacifieber. Leipzig und Wien: Franz Deuticke, 1909.
7(1) Birt, C.: Phlebotomus Fever in Malta and Crete. J. Roy. Army M. Corps 14: 236-258, 1910. (2) Birt, C.: Sandfly Fever in India. J. Roy. Army M. Corps 15: 140-147, 1910. (3) Tedeschi, A., and Napolitani, M.: Experimentelle Untersuchungen über die Aetiologie des Sommerfiebers. Centralbl. F. Bakteriol. 57: 208-211, 1911. (4) Shortt, H. E., Poole, L. T., and Stephens, E. D.: Sandfly Fever on the Indian Frontier; A Preliminary Note on Some Laboratory Investigations. J. Roy. Army M. Corps 63: 361, December 1934; and 64: 17, January 1935. (5) Shortt, H. E., Poole, L. T., and Stephens, E. D.: Note on Some Experiments With Sandfly Fever Blood and Serum. Indian J.M. Research 23: 279-284, July 1935. (6) Moshkovsky, Sh. D.: Studies on Pappataci-Fever. Med. Parasitol. and Parasitic Dis. Moscow 5 (No. 6): 823-862, 1936.
8Warren, R. O. Y., and Johnson, J. W., Jr.: Sandfly Fever in NATOUSA. M. Bull. Mediterranean Theat. Op. 3: 160-164, May 1945.


with a strain of virus obtained from a patient in the first day of his illness in Caserta, Italy, developed typical sandfly fever; they were not subsequently protected by this attack against an inoculation with the Sicilian strain of the virus.


It is believed that P. papatasii is the chief vector of sandfly fever in NATOUSA. The adjacent shores and islands of the Mediterranean, Adriatic, and Aegean Seas which were included in the North African and Mediterranean theaters have long been known as favorable breeding places for the moth midges of the genus Phlebotomus. The hilly and rocky terrains of Algeria, Tunisia, Sicily, Sardinia, Corsica, and Italy and the adobe or stone houses which dot these areas give rise to what was aptly called "the classical sandfly situation," by Maj. Marshall Hertig, SnC. The female sandfly by choice seeks rocky places, cracks in masonry, buildings, stone walls, or rubble and caves in which to lay its eggs; the adult midges seek outdoor shelter in caves, cracks in stones and buildings, and under the eaves of buildings. A cool, shaded, slightly damp environment is ideal for the life of this insect.

Sandflies rest during the day and feed during the night. The female alone bites, an act which she performs persistently and viciously; a meal of blood is necessary for proper ovulation (fig. 1).

The incidence curves of sandfly fever and F.U.O. in NATOUSA-MTOUSA from January 1943 to December 1945 are presented in chart 1. The first cases of sandfly fever were reported in August 1943 although the disease was recognized in North Africa as early as April 1943. In 1943, the peak monthly rate (September) was 7.9 per 1,000 per annum, a rate doubtlessly far below the actual rate, because the vast majority of cases of sandfly fever were reported as F.U.O. Since careful studies were not made upon any sample group of cases of F.U.O. in 1943, there was little information about the correct diagnoses at the time of the final disposition of these patients, and it will never be known what percentage of patients diagnosed as having F.U.O. during the summer of 1943 were in reality suffering from sandfly fever. It is to be remembered, however, at this point, that many cases of malaria were also classed as F.U.O. in 1943 and that the total rate does not primarily represent undiagnosed cases of sandfly fever.

The incidence curve during 1944 more closely approximated the true incidence, since medical officers were beginning to have some familiarity with the disease and hence were more prone to make the correct diagnosis. In an interesting study of F.U.O.9 made by Maj. Emil C. Beyer, MC, it was found that a diagnosis of sandfly fever was made at the final disposition in 2.4 percent of 450 cases initially undiagnosed upon admission as F.U.O. during the months of June, July, and August, 1944. However, in this same group,

9Beyer, E. C.: Fever of Undetermined Origin. M. Bull. Mediterranean Theat. Op. 3: 208-209, June 1945.


FIGURE 1.-Male and female of Phlebotomus papatasii, the vector of sandfly fever. (Sabin, Philip, and Paul. J.A.M.A. 125: 603-606, 1 July 1944.)


CHART l.-Incidence of sandfly fever and fever of undetermined origin in the North African-Mediterranean Theater of Operations, U.S. Army,1 1943-45

the diagnosis of F.U.O. or of febricula appeared in 8.4 and 10.7 percent, respectively, of the final dispositions made during that period. Thus, the etiology of 19.1 percent of the patients having fever was in doubt at the time of their final disposition, and it is possible that many of those patients may have had sandfly fever. That this is probable is evidenced by a further study of the diagnoses which were recorded at the time of the final disposition of a similar group of patients, which was made by Major Beyer during January 1945. In this group only 8.9 percent were discharged with a final diagnosis of febricula or F.U.O. It is unknown how many times the original diagnosis of F.U.O. was changed to sandfly fever in the statistical health reports, but on the basis of these figures, there is a possibility that about 10 percent of the patients originally diagnosed as having F.U.O. in the summer and early fall of 1944 had sandfly fever.

The incidence curve of sandfly fever for 1945 probably represented the incidence of this disease quite accurately as the rates for F.U.O. were at low levels in comparison with corresponding months in 1943 and 1944.

As will be noted from chart 1, cases of sandfly fever made their initial appearance in NATOUSA-MTOUSA in April and gradually built up to a peak in September; following this, there was a rapid decline within the next 2 months. Thus, the epidemiological pattern of the disease reflected accurately the life cycle of P. papatasii.


A natural resistance to sandfly fever apparently does not exist, and a large percentage of susceptibles develop the disease if left unprotected in an


endemic area. Livschitz10 reported that practically 100 percent of experimentally inoculated volunteers who had had no previous contact with the disease were found to be susceptible, while Sabin, Philip, and Paul stated that approximately 95 percent of their volunteers contracted the disease following their inoculation with virus. This same high rate of susceptibility was observed in U.S. forces when they were introduced into NATOUSA-MTOUSA, and instances were recorded in which 80 percent of a command contracted the disease in certain areas around Caserta. These observations were similar to those made by Cullinan and Whittaker11 in the Middle East, where rates for sandfly fever of approximately 1,000 per 1,000 per annum or more were recorded in other ranks in two British general hospitals which had been located in areas in which sandflies were abundant and in which sandfly fever was epidemic.

It was recognized also that second, third, or even more attacks of sandfly fever could occur in the same individual and even the same epidemic season. Livschitz observed that the initial rate of attack of the natural infections in a group of 1,076 persons, who were newcomers in an endemic area, was about 50 percent and that 22.8 percent and 0.9 percent, respectively, of 416 persons who had recovered from an initial infection had second and third attacks of the disease within the same epidemic season. Cullinan and Whittaker reported that 15 percent of the noncommissioned officers and other ranks in two British general hospitals had second attacks (and some even third attacks) of sandfly fever during a period of 3 months in which these men were exposed to the disease in an epidemic area.

While there can be little doubt that an immunity to sandfly fever generally results from an attack of the disease, the observations which have just been recorded suggest that at times the immunity may not be solid. However, Sabin's investigations,12 previously mentioned, indicated the existence of at least two different strains of virus and suggested the possibility that second attacks within the same epidemic season or later may have been the result of an infection with a different strain of virus rather than waning immunity from the first attack.


Sandfly fever in NATOUSA-MTOUSA was characterized by the sudden onset of fever, headache and severe retro-orbital pain, photophobia, generalized aching, malaise, and chilly and feverish sensations. Anorexia, nausea, and vomiting occurred in some patients. The face was suffused, the conjunctivas and scleras injected, and not infrequently pressure over the eyeballs caused pain. At times, a very faint pink erythema was present over

10Livschitz, J. M.: Studies on Pappataci Fever. Med. Parasitol. and Parasitic Dis. Moscow 6 (No. 6): 938-943, 1937.
11Cullinan, E. R., and Whittaker, S. R. F.: Outbreak of Sandfly Fever in Two General Hospitals in the Middle East. Brit. M.J. 2: 543-545, 30 Oct. 1943.
12See footnote 8, p. 52.


the shoulders and thorax, and the spleen was palpable in a small percentage of patients. Many of the patients had relative bradycardia. The fever lasted from 1 to 11 days, averaging 4 days, and was followed by a variable period of asthenia. In one large group of patients, the period of hospitalization ranged from 1 to 25 days, averaging 6.2 days. Leukopenia was present in most cases at the time the patients entered the hospital with the lowest counts being recorded in the immediate postfebrile period. The differential count was characterized by a relative or absolute increase in the lymphocytes (often with the appearance of large atypical forms) and an absolute increase in many patients in the younger types of the polymorphonuclear cells.

It is not unusual that the disease caused diagnostic difficulties in medical installations in MTOUSA. In its milder aspects, it simulated the milder forms of influenza. At times, the onset was similar to that of malaria, infectious hepatitis, or primary atypical pneumonia, and it required much aid from the laboratory to differentiate promptly and accurately between these diseases and sandfly fever.

On occasion, the occurrence of nuchal rigidity in patients with signs and symptoms characteristic of sandfly fever made the differential diagnosis between this disease of aseptic meningitis difficult.13 Because of the lack of specific serological tests, the diagnosis of sandfly fever could not be made in patients with evidence of meningeal irritation and pleocytosis of the spinal fluid, and it could not be proved that sandfly fever virus caused the aseptic meningitis syndrome. In experiments with volunteers, Sabin, Philip, and Paul did not believe that it occurred in any of 150 volunteers.

It is evident that, at times, the diagnosis of sandfly fever was difficult and that it required much clinical acumen and confirmation by the laboratory. However, too often in MTOUSA, the reluctance to make the diagnosis resulted from intellectual slovenliness and from the ease with which, for diagnostic purposes, the disease could be classified as F.U.O.


The treatment of sandfly fever in NATOUSA-MTOUSA was purely symptomatic in type.

It was found in NATOUSA-MTOUSA that the prevention of sandfly fever was dependent upon the precautions taken by the individual against being bitten by sandflies and upon environmental control measures aimed at the eradication of sandflies.


Sandfly fever was a problem of great importance to the U.S. Army in NATOUSA-MTOUSA, and it was responsible for much loss of manpower during the summers of 1943 and 1944.

13See footnote 8, p. 52.


Due to the variations in the clinical picture of sandfly fever, and because specific tests for establishing its identity were not available, medical officers were often reluctant to make the diagnosis of this disease on the basis of their clinical findings. As a result, many thousands of cases of sandfly fever were probably recorded as F.U.O., and hence, the data recorded in the statistical health reports from NATOUSA-MTOUSA regarding this disease were inaccurate.

Sandfly fever could have been prevented in the areas in which the disease was endemic if the proper individual precautions for the prevention of this disease had been observed and if a program for the environmental control of sandflies based upon the use of DDT (dichlorodiphenyltrichloroethane) sprays had been instituted.