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Chapter 7, Part 1

Medical Science Publication No. 4, Volume II

THURSDAY AFTERNOON SESSION
29 April 1954

MODERATOR
LIEUTENANT COLONEL WILLIAM D. TIGERTT, MC


JAPANESE B ENCEPHALITIS-KOREA 1950*

COLONEL ARTHUR P. LONG, MC
COLONEL ROBERT L. HULLINGHORST, MC
ROSS L. GAULD, M. D.

Background

In this presentation, the scope of this symposium is taken literally and the experience with Japanese B encephalitis is reviewed for the period of the Korean war only. In fact, the discussion will be limited essentially to the experience of 1950 since time does not allow presentation of more recent ecologic studies of the virus in avian reservoirs and arthropod vectors. Furthermore, 1950 was the only year when the disease occurred in appreciable numbers in U. N. Forces.

The general aspects of preventive medicine in the Far East were presented at an earlier meeting of this symposium (1). The military and environmental factors involved were referred to briefly in that presentation. These undoubtedly were of considerable epidemiological importance in the occurrence of Japanese B encephalitis among U. S. forces in Korea.

Prior to 1950, Japanese B encephalitis had perhaps been considered most prominently as a hazard in Japan and the islands of the Ryukyus chain, particularly Okinawa. It was known to be present in Korea, however, where it was specifically demonstrated in 1949 (2). In that year alone, there were over 5,000 cases and more than 2,400 deaths reported among Korean nationals. This disease, then, was among the conditions considered as potential special hazards to U. S. forces operating in Korea (3).

By 1950, a considerable weight of evidence had accrued indicating the most likely vector of Japanese B encephalitis to be the mosquito and the most probable species to be Culex tritaeniorhynchus. Continuing observations and studies have added further confirmation to these earlier conclusions. Figure 1 shows the relationship of a mosquito population and a mosquito infectivity index to an epidemic of Japanese B encephalitis. These data were not collected in Korea but do serve to demonstrate an apparent relationship between at least one outbreak of Japanese B encephalitis and the occurrence of infected


*Presented 29 April 1954, to the Course on Recent Advances in Medicine and Surgery, Army Medical Service Graduate School, Walter Reed Army Medical Center, Washington, D. C.


318

Figure 1.
SOURCE: 406th Medical General Laboratory Annual Historical Report, 1950.

mosquitoes in large numbers. (Note: The figure here is taken from the Annual Report of the 406th Medical General Laboratory for 1950, page 199.) There is considerable evidence that a reservoir of the disease exists not only in the human population but also in domestic animals, particularly horses, and in some species of wild birds. A large proportion of the adult human population possess neutralizing antibodies against the virus of Japanese encephalitis. Mosquito control, then particularly in the vicinity of native habitations, was accepted as the best means for protection in the Korean operation. Valiant efforts were made to achieve this protection but under the conditions present in Korea, particularly during the early months of the campaign, the results attained were inevitably short of those desired. (The extent of malaria infection is further evidence of this fact.)

As an adjunct in the control of this disease, Japanese B encephalitis vaccine was administered, this with a killed virus vaccine produced in the developing chick embryo (4). This type of vaccine had been in use


319

in the Far East for American personnel since 1947, having that year replaced the mouse brain type of material which was used the two previous years (5). Despite the 5-year experience with vaccination, however, a true evaluation of its efficacy had not been possible. Its use had been continued largely because there was no reliable evidence that it was not effective. In view of the known hazards from Japanese B encephalitis in Korea, it was considered desirable to vaccinate all U. S. troops there as well as those in Japan and Okinawa. However, since the supply of vaccine had been based on normal requirements which did not contemplate war in Korea, there was insufficient material and the vaccination coverage of troops in Korea was quite variable. This led to the presence of large numbers of both vaccinated and unvaccinated in an area where the disease occurred in appreciable numbers. There was thus provided a certain opportunity for the evaluation of the vaccine. This will be discussed in some detail later.

The 1950 Experience

The Outbreak. Superimposed on the critical military and medical situation existing in the Pusan bridgehead in August 1950 there began to appear in our hospitals in ever increasing numbers a group of patients suffering from an acute febrile illness with evidence of involvement of the central nervous system. In certain instances the clinical picture of encephalitis with evanescent and changing neurologic abnormalities was strongly suggestive of Japanese B encephalitis. Laboratory confirmation of the etiology of a few sporadic cases was established shortly after the outbreak proper began in mid-August (fig. 2). The peak was reached in September and the epidemic continued into September. Figure 2 also indicates distribution by division which will be described later in the discussion. Approximately 300 cases were reported from U. N. troops in Korea with 30 deaths, giving a case fatality of 10 percent. For comparison the time distribution of 26 cases occurring in our forces in Japan in 1950 is shown.

Reporting and Diagnosis. The approximately 300 cases presented in the foregoing figure and forming the basis for the discussion were selected through the utilization of the best reporting and diagnostic procedures available. In accordance with FEC policy, all patients admitted to hospitals with or subsequently developing signs or symptoms of infectious encephalitis were reported by radiogram. Acute and convalescent blood specimens were submitted to the 406th Medical General Laboratory for serological diagnosis on patients so reported. In addition, appropriate specimens obtained at necropsy on fatal cases were submitted for virus isolation and histological examination.


320

A careful review of some 350 abstracts prepared from clinical records resulted in the selection of the approximately 300 referred to. These were considered to have a disease clinically consistent with Japanese B encephalitis.* The greatest problem in this selection was presented by the necessity for differentiation from poliomyelitis. Typical cases of encephalitis with the usual prodromal fevers, mental confusion and coma, coupled with a picture of changing abnormal reflexes and recovery without paralysis, gave little

FIGURE 2.
SOURCE: 406th Medical General Laboratory Annual Historical Report, 1950.

difficulty. Borderline cases, however, were troublesome and it is not unlikely that a few errors were made. This likelihood appears even greater when it is realized that about 70 percent of the reported cases could be classified as moderate or mild. The error here, however, was probably that too many cases were excluded. In fact, it appears more than likely that an appreciable number of individuals diagnosed as having "fever of undetermined origin" during the period under consideration may, in fact, have been experiencing mild infections with the virus of Japanese B encephalitis.


*Dr. Grant Taylor, Associate Member of the Neurotropic Virus Commission of the Army Epidemiological Board, assisted in this and other aspects of the study.


321

In the group selected on clinical grounds as compatible with encephalitis, adequate serum specimens for serological study were received in 237 instances. (This is rather remarkable and speaks well for the interest and cooperation of the various medical officers caring for those patients.) One hundred and twenty-one of these showed complement-fixing antibody titer rises of significant degree (fourfold or more) and 63 showed rises of questionable significance (twofold.) Of those with no rises in titer, 15 maintained antibody titers of one to four or higher and 38 showed no significant complement-fixation reactions. Thus, in about 85 percent of the group there was specific laboratory evidence of experience with the virus of Japanese B encephalitis other than through vaccination.*

Twenty-eight of the thirty fatalities in the group presented histopathological pictures typical for Japanese B encephalitis. One, while not typical, was consistent with such diagnosis and the other was considered to be histologically poliomyelitis. Eleven strains of Japanese B encephalitis were isolated from central nervous system tissue obtained at necropsy from fatal cases originating in Korea.

The most noteworthy clinical laboratory findings were those in the spinal fluid and peripheral blood. Of 211 spinal fluid cell counts on 194 patients between the first and fifth days of the disease, the total count varied from 0 to 3,350 WBC/cu. mm. The mean total count of the group was 277 WBC/cu. mm. with a mean of 65 percent lymphocytes. These counts tended to be somewhat lower as the disease progressed and showed an increase in the proportion of lymphocytes to a mean of about 85 percent between the sixth and tenth days. Remembering that this is a virus disease it is of some interest that the white blood count in the peripheral blood was over 12,000/cu. mm. in 45 percent and over 15,000 in 28 percent of 260 patients.

Management of Cases. It had been well learned by Far East Command Medical Services that maximal rest and minimal exertion are of paramount importance in the management of central nervous system infections, particularly those involving the higher centers. This concept while given full consideration in 1950 was not completely compatible with the urgent need for the limited medical facilities present in Korea at the time. Accordingly, the policy of early and rapid evacuation in all clinically suspected cases of encephalitis was adopted together with the convention that those patients with marked signs and symptoms of central nervous system disease were to be retained and treated in facilities in Korea. Thus, the intensive treatment for severe cases such as those with coma was made available to


*Experience has shown that vaccination with the available Japanese B vaccine does not stimulate detectable complement-fixing antibodies unless the individual concerned has had prior experience with the living virus.


322

the fullest extent possible with no more trauma to the patient than was absolutely necessary in the face of the situation. This practice proved to be reasonably successful as evidenced by the case fatality rate referred to previously (about 10 percent).

The effects of this practice on the duration of illness and the length of convalescence could not be measured. It was seen that under almost any circumstance of treatment and handling, those with moderately severe and severe cases required a long period of convalescence for complete recovery. With such convalescent periods, however, serious nervous system residuals were relatively uncommon and complete recovery was seen in many patients with what appeared to be a very extensive involvement of the central nervous system.

No specific value of antibiotic therapy was demonstrated. However, expectant treatment with these agents undoubtedly saved lives otherwise consigned to demise through intercurrent infections. As already indicated, rest as soon and as complete as possible, plus comprehensive supportive and nursing care were the principal and most effective therapeutic procedures. Very important among these were measures for relieving pharyngeal pooling of secretions, respiratory failures and severe circulatory embarrassment. It is believed that this watchful, careful, sympathetic treatment and management saved lives and restored useful function to many severely ill patients with potentially severe impairments.

Inapparent Infections. The occurrence and significance of inapparent infections with the virus of Japanese B encephalitis has been referred to and discussed by a number of authors (6-8). The great variability in the demonstrable severity of infections in the 1950 outbreak and the large numbers of fevers of undetermined origin observed during that time suggested the occurrence to a significant degree of unrecognizable infection with the Japanese B encephalitis among Army troops.

Demonstration of such infections was attempted late in the epidemic. For this purpose, a group of patients evacuated from Korea to Japan for reasons other than central nervous system infections were studied serologically. All of these individuals had been in Korea at least 1 to 2 weeks during the period 1 August to 30 September 1950. In addition, only those of known immunization status as determined by examination of individual immunization records were selected. Forty-nine percent of 90 completely vaccinated and exposed patients and 57 percent of 149 who had received no vaccine showed appreciable amounts of antibody as determined by the neutralization test. In support of the resultant deduction that roughly half of all troops in Korea during the epidemic period were infected with the virus, it


323

should be mentioned that no neutralizing antibodies could be demonstrated in 140 American soldiers newly arriving in Japan the following year.

Evaluation of Vaccine

Reference has already been made to the matter of evaluation of Japanese B encephalitis vaccine. For obvious reasons, such an evaluation was of extreme importance and considerable efforts were made to glean from the situation the best information available. As indicated before, those forces already in Japan and Okinawa were vaccinated early in the season. These vaccinations started in Okinawa about 1 May, in southern Japan about 15 May, and in the remainder of Japan about 1 June. For those previously unvaccinated, three doses of 1 cc. each of the vaccine were administered, the second injection being given a week after the first and the third 3 weeks later. In accordance with the recommendations of the Neurotropic Virus Commission (12 April 1949) those arriving in Japan after 15 June and in Okinawa after 1 June, were given the full course of three doses of vaccine at intervals of 2 to 4 days between doses. Individuals who had received as much as two doses of the Japanese B encephalitis vaccine during a previous season were given a single booster dose.

The "lead time" for procurement of Japanese B encephalitis vaccine was several months. Hence, the unexpected onset of the Korean campaign allowed insufficient time for the procurement of adequate quantities of the material for administration to all troops sent into the area. Thus, the early forces dispatched from Japan to Korea were reasonably well vaccinated while additional troops who were committed, particularly those sent directly from the United States, did not receive vaccine. Units and replacements processed through Japan were in many instances either not vaccinated or only partially so. Such vaccination of these personnel as was accomplished was done on an accelerated schedule, some receiving the agent on alternate days. There resulted a force of American troops some of whom were vaccinated and some of whom were not.

With the appearance of Japanese B encephalitis in this population, attempts were made to determine, if possible, the immunogenic efficacy of the vaccine. Here, only a brief résumé of the findings and conclusions can be presented. To do this, however, it is necessary to indicate the several categories of vaccination status which were established by definition. These were:

Vaccinated. Those personnel who had been vaccinated in accordance with theater regulations. This included those who had received the vaccine on an accelerated schedule as well as those who had received an initial course previously and whose vaccination had been kept current by one or more booster injections.


324

Partially vaccinated. Those individuals who had received two or more doses of Japanese B encephalitis vaccine regardless of time relation but whose immunization record showed that their vaccination was incomplete or not kept current.

Unvaccinated. Those personnel who had never received Japanese B encephalitis vaccine and those whose immunization record showed that they had at some time received a single dose of vaccine only.

The determination of vaccination status was made from a review of the individual immunization record. Unless this record was reviewed, the person was classified as vaccination status unknown. Despite the diligent efforts of a number of workers, complete vaccination information was unobtainable. For example, 40 percent of the immunization records of the cases and deaths were never located. It was, therefore, not possible to determine the proportion of troops in the area who were vaccinated nor to compare the incidence of disease in vaccinated and unvaccinated troops. Thus, the early hopes for a well defined and valid statistical evaluation of the vaccine were not realized. It was possible, however, to estimate within certain limits the vaccination status of major organizations. With this as background in considering the cases and fatalities in these organizations, certain comparisons were possible.

Case Fatality

Table 1 presents data concerning case fatalities. It is noted that four organizations-24th Infantry, 25th Infantry, First Cavalry Di-

Table 1. Japanese Encephalitis-Korea 1950 Case Fatality by Unit

Unit

Total cases

Confirmed cases

Cases

Deaths

Percent fatality

Cases

Deaths

Percent fatality

Part of personnel vaccinated:

24th Infantry

36

5

14

26

5

19

25th Infantry

68

0

0

58

0

0

1st Cavalry

35

5

14

21

5

24

F. E. A. F.

7

1

14

4

1

25

Personnel unvaccinated:

2d Infantry

104

12

12

76

12

16

1st Marines

27

4

15

15

4

27

5th R. C. T.

14

1

7

13

1

8

27th Brigade (British)

4

1

25

2

1

50

Miscellaneous

16

1

6

7

1

14


Total


311


30


9.6


222


30


13.5


325

vision, and the Far East Air Forces-were considered to have been at least partially vaccinated. The Second Infantry and First Marine Divisions, as well as the Fifth Regimental Combat Team and the 27th Brigade (British) plus certain miscellaneous troops were known not to have been vaccinated. The uniformity of case fatality rates among the divisions is striking, except for that of the 25th Infantry Division in which there were no deaths among 68 cases although 7 to 10 fatalities might have been expected based on the experience in the other divisions. This cannot be attributed to vaccination since both the 24th Infantry and the First Cavalry Divisions had large proportions of their personnel vaccinated. Also, it was determined that about one-half of the patients of the 25th Infantry Division whose vaccination status was known were unvaccinated. The data presented here, then, indicate only that there is no evidence that the case fatality was higher in nonvaccinated units than in those who were at least partially vaccinated.

Vaccination Status of Cases and Deaths

Table 2 presents available but admittedly incomplete data on the vaccination status of cases and deaths. (As indicated above, only about 60 percent of the immunization records were obtainable on these cases.) Relatively little is shown here other than that approximately 20 percent of the patients whose vaccination status was known had been vaccinated. This does not speak well for the potency of the antigen used.

Table 2. Japanese Encephalitis-Korea 1950 Vaccination Status of Cases and Deaths


Status

Cases


Deaths

Total

Confirmed

Number

Percent

Number

Percent

Vaccinated

36

19.1

31

21.4

1

Partially vaccinated

9

4.8

7

4.8

0

Unvaccinated

143

76.1

107

73.8

19

Status unknown

123

-----

77

-----

10

Incidence Rates of Units According to Vaccination Status of Personnel

In attempting to compare the incidence of Japanese B encephalitis among the various units concerned, many complicated factors were immediately involved. Among the most important of these was that of the military situation at the time. It is believed that all or nearly


326

all of the cases occurred among troops in the Pusan bridgehead. (There was never evidence that those who first entered Korea through Inchon on 15 September were exposed to infection.) In preparation for the Inchon maneuver, some units were withdrawn from the Pusan bridgehead just prior to the new assault, re-enforced to several times their previous strength and recommitted. These, then, were removed from exposure to encephalitis for a time. Considering these factors and taking into account the incubation period of Japanese B encephalitis (7 to 14 days), a comparison has been made based on the strength of units in Korea between 10 August and 10 September and the cases which occurred between 17 August and 30 September. If this introduces a bias, it is felt to be favorable to the units at least partially vaccinated.

Table 3. Japanese Encephalitis-Korea 1950 Incidence by Major Units


Unit

Man weeks in Korea (10 Aug. to 14 Sept.)

Cases Japanese encephalitis (17 Aug. to 30 Sept. 1950)

All cases

Confirmed cases

Number

Rate*

Number

Rate*

Part of personnel vaccinated:

1st Cavalry

62,837

31

49.3

21

33.4

24th Infantry

65,090

31

47.6

25

38.4

25th Infantry

70,268

63

89.7

53

75.4

F.E.A.F. (Korea)

16,060

6

37.4

4

24.9

Personnel unvaccinated:

1st Marines

21,327

27

126.6

15

70.3

2d Infantry

73,150

99

135.3

73

99.8

5th R.C.T.

16,566

14

84.5

13

78.5

27th Brigade (British)

3,770

4

106.1

2

53.1

*Per 100,000 man weeks.

Table 3 shows these comparisons. These findings indicate that, in general, the rate in unvaccinated units was higher than that in those units who were partially vaccinated. The experience of the 25th Infantry Division, however, stands out sharply. This organization with at least part of its personnel vaccinated had rates nearly twice those of units similarly conditioned and slightly higher than that of the Fifth Regimental Combat Team which was not vaccinated. A major factor in the inconclusiveness of these data may well have been the difficulty in measuring or even indicating the degree of exposure in the various organizations. In an effort to demonstrate the possible effect of geographic locations (which might influence degree of exposure) a comparison was made of the incidence of Japanese B


327

encephalitis in seven infantry regiments located in proximity to each other in the Naktong River Valley and along the seacoast near Masan.* The approximate location of these units together with their vaccination status and cases of encephalitis experienced are indicated in figure 3.**

The exact strength of these organizations was not obtainable but they were known to be sufficiently alike to make the direct comparison of case numbers valid. It appears from this information that location rather than vaccination may well have played the major role in the determination of the number of cases which occurred in these organizations. Certainly all of the units in the Naktong River Valley had similar disease experiences regardless of vaccination status as did those nearer the coast with some suggestion of a lower degree of exposure among the latter group.

From the study on the evaluation of the vaccine, it appears necessary to conclude that the evidence obtained pointed neither to the presence nor absence of the ability of the vaccine to protect against Japanese B encephalitis.

Relation of Prior Injury to Onset of Encephalitis

An interesting and perhaps irrelevant observation was that approximately 14 percent of 261 cases give a history of wound or injury in a 2-week period prior to onset. This contrasts sharply with the highest rate of wounded in action in Korea during any 14-day period of the summer of 1950. This rate was approximately 6 percent. This relationship has suggested two hypotheses:

1. A wound or injury favors the development of clinically apparent encephalitis, or

2. Early encephalitis may reduce normal caution or agility thus resulting in increased battlefield exposure and likelihood of being wounded.

Conclusions

1. The greatest problem posed by Japanese B encephalitis in the experience of United States troops in the Far East was presented during the 1950 summer campaign of the Korean conflict. During that period, there were approximately 300 cases of the disease with 10 fatalities.

2. The best known methods of control were practiced very well under the existing circumstances but were not effective.


*Lieutenant Colonel Wallace gave valuable information with respect to the location of these units at the time.
**Lieutenant Colonel Floyd Berry, MSC, gave valuable assistance in the collection of this information.


328

FIGURE 3.

3. No evidence was adduced demonstrating conclusively either the effectiveness or non-effectiveness of Japanese B encephalitis vaccine as an immunizing agent. (The practice of the administration of this vaccine in the Far East was discontinued after the 1951 season.)

4. No specifically effective therapy was demonstrated; though conservation of the patient's energy and strength, detailed supportive


329

and nursing care and expectant antibiotic therapy for intercurrent infections were all unquestionably of extreme value.

5. Only a relatively small proportion of cases of Japanese B encephalitis develop permanent central nervous system residual impairment.

6. As many as 50 percent of troops in the Pusan bridgehead of Korea in August and September of 1950 probably developed inapparent infections with Japanese B encephalitis virus and, hence, a resistance to the clinical disease. It appears that this natural process is at least as effective as immunization with vaccines now available.

7. The hazard from Japanese B encephalitis in areas where Americans have had experience lies in great part with the fear and concern over the disease as well as from the disease itself.

8. Continued study and search for improved control and management methods for Japanese B encephalitis and related central nervous system disorders are indicated. The true significance and importance of these conditions, however, should be recognized and maintained within their proper perspective.

Note. Grateful acknowledgment is made to the many workers, both military and civilian, whose contributions form the basis of this discussion. Much of the material presented here is drawn from the Annual Historical Reports for the 406th Medical General Laboratory for the years 1950, 1951 and 1952.

References

1. Long, A. P.: General Aspect of Preventive Medicine in the Far East Command. This Symposium, page 247.

2. Hullinghorst, R. L., Burns, K. F., et al.: Japanese B encephalitis in Korea. J. A. M. A. 145 : 460-466 (17 Feb.), 1951.

3. Estimate of Principal Health Hazards to Troops Operating in Korea. Far East Command Surgeon's Letter, Vol. 5, No. 7, July 1950.

4. Warren, J., and Hough, R. G.: A Vaccine Against Japanese Encephalitis Prepared from Infected Chick Embryos. Proc. Soc. Exp. Biol. and Med. 61 : 109-113, 1946.

5. Sabin, A. B.: The St. Louis and Japanese B Types of Epidemic Encephalitis. J. A. M. A. 122 : 477-486 (19 June), 1943.

6. Bawell, M. B., Deuel, R. E., Jr., et al.: Status and Significance of Inapparent Infection with Virus of Japanese B Encephalitis in Japan in 1946. Am. J. Hyg., Vol. 51, No. 1, pp. 1-12 January 1950.

7. Deuel, R. E., Jr., Bawell, M. B., et al.: Status and Significance of Inapparent Infection with Virus of Japanese B Encephalitis in Korea and Okinawa in 1946. Am. J. Hyg., Vol. 51, No. 1, pp. 13-20, January 1950.

8. Tigertt, W. D., Hammon, W. McD., et al.: Japanese B Encephalitis: A Complete Review of Experience on Okinawa 1945-1949. Am. J. Trop. Med., Vol. 30, No. 5, pp. 689-722, September 1950.