Journal of Medical and Veterinary Mycology (1986) 24, 313-327

An outbreak and review of cave-associated histoplasmosis capsulati

J E F F R E Y J. SACKS% LIBERO AJELLO 2 AND L A N D I S K. CROCKETT 3

Division of Field Service, Epidemiology Program Office, Centers for Disease Control and Office of Epidemiology, Division of Public Health, Georgia

Department of Human Resources, Atlanta, Georgia 30309, 2Division of Mycotic Diseases, Center for Infectious Diseases, Centers for Disease Control, U.S. Department of Health and Human Services Public Health Service, Atlanta,

Georgia 30333, 3Citrus County Health Department, Inverness, Florida 32650, U.S.A.

(Accepted 29 April 1986)

Three male college students from Florida developed acute onsets of fever, chills, shortness of breath, and cough within one day of each other, and all were eventually hospitalized for four to 29 days. All chest x-ray films showed diffuse reticulonodularities in both lung fields. Laboratory studies confirmed the diagnosis of histoplasmosis. The three students had been 'spelunking' (cave exploring) 6 to 7 days before their onset of symptoms. One of four soil samples collected in the caves was positive for Histoplasma capsulatum by the indirect mouse inoculation procedure. Of three investigators who entered the implicated caves, two developed acute febrile illness within 15-21 days. One investigator was hospitalized for 18 days with a confirmed diagnosis of histoplasmosis.

Investigation identified an additional case (the person had entered the caves 6 months before this episode), but was not reported to health authorities. Spelunkers should be aware of the potential risk of histoplasmosis and how to avoid infection. Physicians should be cognizant of cave-associated histoplasmosis, inquire about spelunking in persons who develop febrile respiratory illnesses with diffuse nodularities on chest x-ray films, and report such cases to their health department. A review of 42 reported oubtreaks of cave-associated histoplasmosis and the approach to environmental control of infected caves are included.

'Spelunking' (cave exploring) is not without its hazards. Not only does the spelunker risk trauma (abrasions, sprains, fractures, concussions) from slipping or falling rocks, animal bites, arthropod-borne disease exposures, rabies exposure, drowning, starva- tion, hypothermia, frostbite, toxic exposures (e.g. ammonia, hydrogen sulfide), acute claustrophobia, and asphyxiation [39], but also there is the risk of acquiring histoplas- mosis. This is primarily due to the presence of Histoplasma capsulatum in bat and bird guano found in some caves. The association of bats with histoplasmosis is well

Correspondence address: Dr L. Ajello, Division of Mycotic Diseases, Centers for Disease Control, Atlanta, Georgia 30333, U.S.A.

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documented [25, 27, 28, 41, 46, 70] and has led to the recognition of bat-associated histoplasmosis transmissions both inside [9, 12, 17, 20, 22, 30, 33, 40, 43, 44, 45, 48, 52, 53, 55, 56, 57, 60, 66, 67, 68, 72, 74] and outside of caves [7, 19, 29, 36, 65]. However, reviews suggest that cave-associated epidemic transmission has been un- common [37, 50]. This may be due to an infrequency of occurrence, a lack of recognition, a tendency toward mild illness, and/or a lack of reporting. This report describes histoplasmosis infections in three spelunkers and the subsequent detection of a previously unreported case in a person infected at the same site. Two of three outbreak investigators who visited the cave also developed illness. This report reviews the world-wide occurrence of cave-associated histoplasmosis and addresses possible control measures.

METHODS

Medical records of the three spelunkers with histoplasmosis were reviewed. The patients and their physicians were interviewed. All available serum specimens from the patients were tested at the Division of Mycotic Diseases' Mycoserology Reference Laboratory of the Centers for Disease Control (CDC) for M-band diffusion and complement fixing (CF) antibodies to histoplasmin and yeast form antigens.

The probable sites of the source of infection were visited on two occasions. During this phase of the investigation, a farmer who lived nearby told us that another group had previously visited these caves. Some of those persons and their physicians were interviewed by telephone.

One sample of soil was collected from each cave on each visit and sent to the Division of Mycotic Diseases at CDC. Saline suspensions of these specimens were introduced into mice, which were then autopsied 6 weeks after inoculation. Portions of mice livers and spleens were then cut into Sabouraud agar slants and incubated at 25°C [52, 71].

For the literature review, a cave was defined as a natural underground formation. Thus, cases of histoplasmosis occurring from exposure to other underground sites such as storm cellars [11] and tree stumps [37] were not included. A case of cave-associated histoplasmosis was defined as the occurrence of compatible symptoms in a person who had visited a cave; asymptomatically infected persons were not included in the tabulations. All references to histoplasmosis in this report refer to infections caused by H. capsulatum var capsulatum.

RESULTS

Case histories Case 1, a 26-year-old male college student, had been previously well with no medical

problems except a history of asbestos exposure in the Navy. On July 23, 1982, he presented to a hospital with chief complaints of one week of fever, chills, and cough productive of sputum with occasional blood. His temperature was 39. I°C (102.3°F) and ronchii were present in his lungs. A chest x-ray film revealed bilateral, fluffy, alveolar, and interstitial infiltrates. His white blood cell count was 7700 cells mm -3. He was admitted with a diagnosis of adult respiratory distress syndrome, probably viral in origin, and given erythromycin. Sputum smears for acid-fast bacilli were negative. Liver enzymes showed a modest elevation of lactic dehydrogenase. On July 25, the physician learned that the patient had been spelunking about 2 weeks before onset of symptoms. The following day, a serum specimen was obtained for histoplas- mosis serologic tests. Sputum taken on this day and the next grew Staphylococcus aureus. Arterial blood gas showed a PO2 of 57 on room air. The patient's fever rose to 39-4°C (103°F) and he was transfered to another hospital, where a pneumothorax was

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noted on admission, as well as a dense reticular infiltrate on the chest x-ray film. A chest tube was placed and a lung biopsy taken at this time showed budding yeast-like cells on Gomori silver methanamine strain. A culture of this tissue grew H. capsula- turn. The white blood cell count at this time was 12 400 cells mm -3. Amphotericin B therapy (10 mg per day) was begun shortly thereafter and maintained for 2 days when the dose was increased to 35 mg per day and maintained for 15 days. A convalescent- phase serum specimen was collected on August 9. The patient eventually recovered and was discharged on August 21. The demonstration of the M precipitin and of seroconversion with histoplasmin and yeast form antigens of H. capsulaturn provided additional evidence of histoplasmosis (Table 1).

Case 2, a 27-year-old male college student, presented to a hospital emergency room on July 24, 1982, with a one-week history of malaise and cough and a 3-day history of fever and headache. His temperature was 387°C (101-7°F). On rectal examination, a diffusely swollen prostrate was noted. A chest x-ray film was taken. Only the posterior anterior film was reviewed and it was considered normal. However, on retrospect, it was not. A lateral film revealed infiltrates. A diagnosis of prostatitis was made and ampicillin was prescribed.

Two days later the patient returned to the hospital and was admitted. His chief complaints were fever, chills, sweats, shortness of breath, cough productive of white sputum, headache, photophobia, dizziness, myalgia, malaise, and a 6-pound weight loss. One week before admission, he had noted arthralgia and had had one episode of vomiting. Past history revealed a positive 1974 tuberculin skin test for which one year of isoniazid had been intermittently taken. The patient also had a history of reflex esophagitis for which he occasionally took climetidine. He had smoked two packs of cigarettes a day for 9 years.

His temperature on admission was 39.4°C (103°F). Although physical examination was essentially normal, his chest x-ray film revealed diffuse reticulonodularities in both lung fields. Arterial blood gas on room air showed a p02 of 54. Lumbar puncture revealed no white cells, a protein of 70 mg% and glucose of 60 mg% (blood glu- cose= 114 mgdl-~). Amphotericin B therapy (35 mg per day) was begun on July 29 and ended August 6. On August 9, he was discharged. The single convalescent-phase serum specimen suggested that the patient had had histoplasmosis at some point in the past (Table 1).

Case number 3, a 23-year-old male, was seen on July 24 at an emergency room with chief complaints of fever, chills, difficulty breathing, and chest pain on the right side. For the past week he had noted fever, cough, chest pain, sputum production, sore throat, back pain, and headache. On physical examination, the physician noted diaphoresis, paleness, rales in the right middle lobe, and a fever of 37.8°C (100°F). A diagnosis of pneumonia was made and erythromycin and aspirin ordered for treat- ment. No x-ray films or cultures were taken.

The patient did not improve, and 3 days later he returned. He was admitted with the same symptoms and a diagnosis of "rule out pneumonia." His temperature was 38.9°C (102°F). Mild wheezes were noted in both lungs. Chest x-ray films revealed multiple miliary nodular densities--salt-and-pepper-like alveolar infiltrates in both lungs and some left mediastinal and hilar adenopathy. His admission white blood cell count was 7000 cells mm -3. Multiple blood and sputum cultures were negative. His liver enzymes were normal. An arterial blood gas showed a pO2 of 68 on room air. Past history revealed the patient was a smoker who had had asthma and bronchitis as a child. About 3 weeks before admission he had been bitten by a scorpion.

Shortly after his admission, the attending physician learned that one of the patient's friends had been diagnosed as a case of histoplasmosis and that both had been spelunking together about 3 weeks before admission. On July 29, a histoplasmin skin test was given. Within 24 h, it was positive with over 4 cm of induration. An acute-

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CAVE-ASSOCIATED HISTOPLASMOSIS 317

phase serum specimen was drawn and sent to a private laboratory for histoplasmosis tests. On that day, the health department was notified and the patient was started on ketoconazole (200 mg twice a day) and cephalothin (500 mg four times a day). On July 31, he was sent to another hospital. However 12 h after admission he signed out against medical advice; he recovered at home. His serologic tests were indicative of H. capsulatum infection (Table 1).

None of the patients owned psittacine birds, had been to bird roosts, cleaned out chicken coops, done excavation or coal mining, been in a silo or sugar cane field, had exposure to toxic fumes, or been out of the country recently. None of the patients had any known immunosuppressive disease. The three students had been spelunking on July 10, 1982. They saw no bats in the caves, while they were collecting guano for use in a vegetable garden. A family source indicated they had been throwing the bat guano at each other. The three lived in different towns, attended different classes at the same community college, and had served in the U.S. armed forces. Their only admitted commonly shared activity in the month prior to onset of illness was spelunking.

No bats were seen or heard in either cave although loose soil (guano?) was abundantly present. Both caves were damp and minimal dust was raised during the investigators' explorations. Maximal penetration of the caves was about 100 feet (30 m). Of the four specimens collected, one from Cave 1 was positive for H. capsulatum by the indirect mouse isolation procedure.

PREVIOUS UNREPORTED CASES

On December 19, 1982, eight persons explored the two caves, as well as the nearby farmer's private cave. They spent about one hour in Cave 1 and only a few minutes in Cave 2. No bats were seen in Caves 1 or 2. Three days later, one person developed a flu-like illness lasting 2-3 days. Two other members of the party also developed a flu- like illness of unknown onset and duration.

One member of the group, a 22-year-old male, presented to an infirmary on January 5, 1983, with a 37-8°C (100°F) fever and headache of 2 days' duration. He was examined and sent home with advice to take aspirin as needed. On January 20, he returned with complaints of increased lassitude, nausea, and vomiting of 10 days' duration. A nonproductive cough had been present for 2 weeks. He had seen a private physician on January 17 who treated him with cough medicine. Since the last infirmary visit he had lost 15 pounds. The evening before he had a 39-4°C (103°F) fever.

He was admitted to the infirmary. On physical examination, his lungs were clear and only his pallor was noted as unusual. His white blood cell count was 7600 cells mm -3. Chest x-ray films revealed an extensive reticulonodular miliary process in both lungs. Since histoplasmosis was suggested on the differential from the x-ray film, the physician questioned him, and learned that he had recently been in a cave. A histoplasmin skin test was applied and was positive with a very large reaction. He was transferred to a hospital under the care of an infectious disease specialist who also diagnosed histoplasmosis. A serum specimen drawn on January 21 had a negative CF test reaction to histoplasmosis. Follow-up specimens were not collected. Although a diagnosis of histoplasmosis (a legally notifiable disease) was made in two institutions by two separate physicians, the case was never reported to the health departments.

INVESTIGATOR ILLNESSES

Investigator 1, a 36-year-old male epidemiologist, who entered the caves on August 10 and on August 25, 1982, developed fever (up to 38.3°C), malaise, myalgia, backache, and headache. These symptoms persisted for 3 weeks. There were no

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pulmonary symptoms. A histoplasmin skin test on August 31 showed 25 mm of induration. Acute- and convalescent-phase serologies were negative for histoplasmosis (Table 1).

Investigator 2, a 36-year-old male health inspector for the Citrus County Health Department, Florida, on September 1, 1982 noticed increasing shortness of breath, malaise, fever, chills, cough, and weight loss. On September 8, he was hospitalized, at which time chest x-ray films showed diffuse miliary nodular densities bilaterally. His temperature rose as high as 39.3°C (1028°F). A histoplasmin skin test on September 10 showed 20 mm of induration; a tuberculin skin test was negative. Blood cultures taken at temperature spikes were negative. Arterial blood gas on room air showed a pO2 as low as 71. His highest white blood cell count was 5500 cells mm 3. The patient was treated with oxygen and oral ketoconazole, (200 mg twice a day) the latter being discontinued after 12 days when liver enzymes rose and mild hepatic enlargement and right upper quadrant abdominal tenderness developed. He was discharged on Septem- ber 25 in a progressively improving condition. Serologic studies showed evidence of recent histoplasmosis infection (Table 1).

Investigator 3 had no illness following exploration. He was skin tested on September 13, 1982 and showed 4-5 mm of induration. The three investigators wore surgical masks during their exploration of the caves and were careful to avoid stirring up aerosols.

LITERATURE REVIEW

Reported outbreaks of cave-associated histoplasmosis are shown in Table 2. For the 42 outbreaks, the total number of cases was 472. Skin tests were positive for 81.0% of the ill persons (192/237). Serologic studies (generally CF tests) showed evidence of histoplasmosis for 74.3% (185/249). Chest x-ray films were abnormal for 79.3% (138/174).

Of 325 cases for which gender was reported, 294 (90.5%) were male and 31 (9-5%) were female. The youngest person with histoplasmosis was 11 years old and the oldest 66. Of 102 cases for which age was reported, 53 (52-0%) were 11-19 years old, 39 (38.2%) were 20-29 years old, 6 (5.9%) were 30-39 years old, and 4 (3.9%) were over 40.

The reported range in incubation period was 3-44 days. Of 114 cases, where the incubation period was precisely reported, 9 (7.9%) cases occurred 3-7 days post- exposure; 32 (28.0%), 8-11 days after; 38 (33-3%), 12-15 days after; 8 (7.0%), 16-19 days after; 11 (9.6%), 20-23 days after; and 16 (14-0%), more than 24 days after exposure.

At outbreak sites 24% (43/176) of the soil specimens were positive for H. capsula- tum as were 18.7% (123/658) of the bats. In 12 outbreaks for which the cave was described, seven were in wet caves. In 26 outbreaks in which the investigators entered the cave, four (15%) led to illness in at least one of the investigators.

DISCUSSION

Spelunkers should take care not to raise dust nor disturb the soil unnecessarily while entering caves. Ambient gases (e.g. ammonia) and strenuous exertion may both raise the respiratory rate. This increases the possibility of infection if the conidia of H. capsulatum are present. The use of respirators would be desirable, particularly, if a spelunker is susceptible (as determined by skin test) and in an area where the disease has occurred. Following exploration, boots should be hosed off and the clothes worn in the cave should be removed at the site and placed in airtight plastic bags. Formal- dehyde fumigation followed by laundering of the bagged clothing should prevent

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TABLE 2. Reported Cave-Associated Histoplasmosis, 1947-1984

319

No. of Investigator Year Place [reference] cases Type of cave case

H. capsulatum studies

Soil Bats

1947 Arkansas [72] 21 DC - - 1951 Venezuela [51] 1 - - - - 1952 Venezuela [51] 1 - - - - 1953 So. Africa [56] 46 DC IC 1954 Venezuela [12] l 1 WC IC 1955 Florida [68] 1 - - - - 1955 Peru [47, 49] ~ 5 - - - - 1955 Rhodesia [22] b 2 - - - - 1957 Tanzania [2, 53] 2 - - - - 1958-9 Missouri [51] 4 - - - - 1959 Mexico [44] t2 - - - - 1959 Zaire [9] 4 WC - - 1960 Rhodesia [33] b 3 - - - - 1960 Cyprus [66] 2 DC - - 1960 Panama [67] 2 - - - - 1961 Colombia [51] 15 - - - - 1962 Cuba [57] 6 - - - - 1962 Cuba [57] 8 - - - - 1963 Cuba [18, 31, 57] 110 - - - - 1963 Panama [48] 2 - - - - 1963 So. Africa [74] 7 - - - - 1963 Puerto Rico [51] 2 - - IC 1965 Panama [40, 62] 8 WC IC 1966 Florida [45] 1 - - - - 1966 Colombia [51] 7 - - - - 1968 Puerto Rico [5l] 3 - - - - 1968 Guatemala [51] 2 - - - - 1969 Guatemala [51] 4 - - - - 1972 Florida [Unpub] 3 - - - - 1972 Australia [43] 11 WC - - 1973 Florida [52] 23 - - - - 1975 Belize [60] 10 DC - - 1977 So. Africa [20] 10 WC - - 1977 Australia [42] c 3 WC - - 1978 New Guinea [59] ~ 1 - - - - 1978 Jamaica [30] 25 WC - - 1979 Texas [55] 3 WC - - 1979 Colombia [16, 17] 17 - - - - 1980 So. Africa [21] 2 - - - - 1983 Mexico [34] 5 DC - - 1984 Mexico [32] 51 - - - - 1984 Mexico [6] 16 - - - -

N P P P

P

N N

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P P N

P N P N N P P P P P

P ?

N N

P P

P P P

P

P P

N N

Key: DC, dry cave; WC, wet cave; IC, investigator case; N, negative; P, positive. ~Oil bird (Steatornis caripensis) cave. ~Now divided into Zimbabwe and Zambia. cSame cave as [43]; cases occurred in 1977-1983. aSwiflet (genus Collocalia) guano in cave.

c o n t a m i n a t e d g a r m e n t s f r o m d i s s e m i n a t i n g i n f e c t i o u s c o n i d i a t o o t h e r s w h o n e v e r

e n t e r e d t h e cave .

L a c k o f p o s i t i v e s e r o l o g y , s k i n t e s t s , o r c h e s t x - r a y f i l m s a m o n g p e r s o n s w i t h

h i s t o p l a s m o s i s is c o n s i s t e n t w i t h o t h e r s t u d i e s [35] . T h e o c c u r r e n c e o f d i s e a s e in t h e

o u t b r e a k i n v e s t i g a t o r s , w h o t o o k c a r e n o t to r a i s e d u s t , p o i n t s to t h e n e e d to w e a r

a d e q u a t e m a s k s c a p a b l e o f f i l t e r i ng p a r t i c l e s a s s m a l l a s 2 m i c r o n s . I f a m a s k is w o r n ,

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3 2 0 SACKS ET AL.

it should fit closely. Investigator illnesses during histoplasmosis outbreak studies are not infrequent [12, 19, 40, 51, 56, 65, 73]. Even laboratory workers may be at risk [191.

In one cave-associated outbreak, 15 caged mice were placed on the floor of the cave for 4-5 h. Despite the relative stillness of the cave air the lack of disturbance of the guano, one mouse became infected [55]. One investigator remained 5 m (15 fee t ) f rom the entrance of a cave and still developed histoplasmosis. An air sample taken 2 m (6 feet) away from him was positive for H. capsulatum [40]. These reports attest to the danger implicit in entering an infested cave.

TABLE 3. Isolations of Histoplasma capsulatum from soils, bats, or birds in caves

Place [references]

Outbreak- related isolation

Foreign countries Australia [42] Yes Belize [60] Yes Colombia [ 17, 51 ] Yes Cuba [31, 57] Yes E1 Salvador [46] No Jamaica [30] Yes Israel [4] No Malaya [58] No Mexico [1, 32] Yes/No New Guinea [59] Yes Panama [40, 47, 48, 62, 67] Yes/No Peru [49] Yes Tanzania [2, 531 Yes Trinidad [3] No Venezuela [ 12] Yes

United States Alabama [70] No Arizona [24l No Florida [25, 45, 52, 68, 70] Yes/No Indiana [70] No New Mexico [51] Yes Oklahoma [ 10, 70] No Puerto Rico [ 13, 14, 15] Yes Tennessee [461 No Texas [25, 55, 70] Yes/No Virginia [46] No

Although cave-associated outbreaks have been reported from many areas, other caves not documented to be associated with human cases, have shown evidence of bat or cave soil infestation (Table 3). H. capsulatum has been isolated from multiple species of bats [24, 41 ]. Given the range and distribution of bats, it is quite likely that many other harborages are also infected. Even when both soil and bat studies were conducted at known outbreak foci, the results have been quite variable. Of 11 studies reporting both results: five showed both positive soil and infected bats; three soil positive, bats negative; two soil negative, bats positive; and one, both negative. The type of culturing technique is very important, as different methods yield different results at the same site [42]. It has been suggested that wet caves are less likely to be infectious than dry ones [25, 63, 70]. However, it would appear from the literature review that outbreaks have occurred in either type of cave.

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Skin testing results have suggested that the endemic area for histoplasmosis in the United States primarily involves the Mississippi and Ohio River valleys [26]. Florida, which is well outside of this endemic region, has had only 66 reported cases from 1955 to 1981. Of the 28 autochronous cases in this group, all were cave-associated (Table 2). Studies of Florida bats and cave soils have shown variable rates of histoplasmosis and isolation of H. capsulatum (Table 4).

TABLE 4. Histoplasma capsulatum surveys of soil and bats in Florida caves

Soil Bats

% Caves with at % of % Caves % of

least one Soils with Bats No. caves positive soil positive infected positive

County [references] examined sample (no.+/no. tested) bats (no.+/no. tested)

Suwannee [52] 1 100 30(3/10) 100 12(38/308) Alachua [25, 45] 1 0 (0/34) 100 5(1/20) Alachua [25] 4 25 3(2/69) 25 2(3/109) Citrus [25] 1 0 0(0/10) 100 64(37/58) Jackson [25] 2 50 12(3/25) 100 50(8/16) Marion [25] 1 100 50(5/10) 100 62(23/3"]) Alachua [70] 1 ND ND i00 76(80/105) Citrus [70] 1 ND ND 100 46(23/50) Jackson [70] 1 ND ND 0 0(0/1)

ND, Not done.

Unlike infected surface soil, where proximity to the risk area has been associated with infection [65], below ground the risk of histoplasmosis appears directly associated with spelunking and not merely living near infected caves. Johnson et al. found a 4.3% rate of histoplasmin skin-test sensitivity for rural residents near Florida caves com- pared to a 64.3% rate for members of a spelunking club [45]. Murray et al. reported a 94-5% skin test positivity for spelunkers compared to a 0% rate for age-, sex-, and socioeconomic-matched controls from the same area [56]. However, Quinones et al. found that among persons 6-20 years old living near an infected cave, 58.8% were skin test positive compared to 28-6% of similar age hospitalized patients living away from the site [60]. This difference was not statistically significant and was not seen for those 21 years and older. Interestingly, the likelihood of skin-test positivity in the control group was associated with a history of spelunking.

As long as an area remains infested with H. capsulatum, it may serve as a focus for human infection. Accordingly, to decontaminate an area CDC recommends the use of a 3% formalin solution (1-1% formaldehyde) applied at the rate of one-third gallon (1.2 1) per square foot (0.9 sq. m) of infected area for 3 successive days. Ambient temperature at the site should range between 15.6°C (60°F) and 32.2°C (90°F) or the t reatment may be ineffective. Since formalin vapors are intensely irritating, and possibly carcinogenic, CDC also urges staying up-wind of spraying activity, the use of protective clothing, and masks capable of removing formaldehyde fumes [5, 8]. This type of approach has been used at outbreak sites [7, 19, 23]. However, it is not uniformly successful, and conidia 15.2 cm (6 inches) below the surface may remain viable [71]. At one site, viable H. capsulatum was found 30-5 cm (1 foot) below the surface [64].

Given the characteristics of caves, it would be extremely difficult, impractical, t ime consuming, and expensive to apply formalin to H. capsulatum infected caves at the recommended levels. Rock and other debris may shield infected areas or prevent

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adequate penetration of the fungicide. Furthermore, the process could be hazardous to the applicators because of the limited airflow in most caves. The use of protective gear and an effective filtered air supply would further restrict the ability of the applicator to move in the cave. The cool temperature that generally exists in caves may interfere with effective fungicidal action. Even if effective treatment could be applied, experi- mental and field work suggests that in some bat species a chronic infection may occur that causes intestinal excretion of viable fungal cells for long periods of t ime [38, 41, 54, 62, 69]. Unlike birds, the bat is susceptible to histoplasmosis [35]. Excrement from infected bats could cause a reinfection of a cave after t reatment unless some way was found to deny bat access [63]. Thus, formalin treatment does not seem a possible option.

Destruction of a cave to prevent human or bat access also destroys the b a t s - - s o m e of which may be endangered species. Bats help maintain control over insect popula- tions and thereby serve the communi ty by balancing the local ecology. Furthermore, bats currently present in the cave may not be the ones responsible for the introduction of H. capsulatum [41]. Cave destuction also 'blames the bat, ' when it is the encroach- ment of unprotected humans into the bats ' natural environment that creates the potential for transmission.

A warning sign may be posted. However, it can be ignored, defaced, or torn down. I f such a sign is posted, it should be of a durable nature and securely erected. Other options include fencing off access to the cave or erecting a physical barrier to stop humans (but not bats) from entering the cave. A grate over the entrance may interfere with the bat 's flight pattern. The attraction of these options is that they allow bats access to their natural habitat and that they protect the ecology.

In only three of the 42 outbreaks reported were control measures described [30, 51, 60]. In all, warning signs were posted. In one outbreak, the cave entrance was blocked by bulldozing, local cavers were alerted, and local physicians advised of the problem [60]. In the outbreak described here, a warning sign was posted.

How far does responsibility extend of a public health agency to protect the public? Should infected caves be destroyed? Should public funds be used to erect barriers to access? Should cave surveys be conducted to determine if they are infested with H. capsulatum? Given the variable rate of recovery of H. capsulatum at known outbreak foci, how many and what type of samples would be necessary? Despite these unre- solved questions, it appears clear that had the initial cave-associated case been reported (as mandated by Florida regulations) and had the health department investi- gated and taken some preventive action (e.g. a warning sign), the three subsequent cases might have been prevented.

A C K N O W L E D G E M E N T

The authors thank Gary Maidoff and Bob Simonson of Florida's Citrus County Health Department for their cave explorations, Robert J. Weeks and Leo Kaufman, Ph.D. of the Division of Mycotic Diseases of the Centers for Disease Control for the laboratory studies, Harriet Owens and Connie Soule of the Florida Department of Health and Rehabilitative Services and Janice H. Brookshire of the Centers for Disease Control's Division of Mycotic Diseases for the manuscript preparation.

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