outbreak of acute pulmonary histoplasmosis in members of a wagon train

Outbreak of Acute Pulmonary Histoplasmosis in

Members of a Wagon Train

TRACY L. GUSTAFSON, M.D.

LEO KAUFMAN, Ph.D.

ROBERT WEEKS, B.S.

LIBERO AJELLO, Ph.D.

Atlanta, Georgia

ROBERT H. HUTCHESON, Jr., M.D.

Nashville, Tennessee

STANLEY L. WIENER, M.D.

DWIGHT W. LAMBE, Jr., Ph.D.

Johnson City, Tennessee

TOM A. SAYVETZ, M.D.

Atlanta, Georgia

WILLIAM SCHAFFNER, M.D.

Nashville, Tennessee

From the Field Services Division, Epidemiology Program Office, and the Mycology Division, Center for Infectious Diseases, Centers for Disease Control, Atlanta, Georgia; Tennessee Department of Public Health, Nashville, Tennessee; Quillen- Dishner College of Medicine, Johnson City, Ten- nessee; and the Vanderbilt University School of Medicine, Nashville, Tennessee. Reprint requests should be addressed to Dr. Gustafson at the Epi- demiology Program Office, Centers for Disease Control, Atlanta, GA 30333. Manuscript accepted April 7, 1981.

In August 1980, an outbreak of acute pulmonary histoplasmosis occurred among participants in a wagon train as it traveled through eastern Tennessee. Of the 85 people on the train 69 (81 percent) had evidence of infection with Histoplasma capsulatum. Fifty-four people had symptomatic disease. The source of infection was traced to the site of a former winter blackbird roost in Charleston, Ten- nessee, that had been partially cleared five years earlier to make a park. Fourteen of 25 soil samples from this site were cuiture- positive for H. capsuiatum. This is the first reported outbreak to in- volve a large migrant group. The outbreak is unusual in that exposure occurred without excavation, construction or tree-cutting at the site.

Acute pulmonary histopiasmosis is a common disease in states in the

Ohio and Mississippi River valleys. However, because its clinical

manifestations are similar to those of other self-limited pulmonary

infections, the disease is difficult to recognize except in epidemic

situations. In August 1980, a migrant group of teenagers and young

adults traveling by mule-drawn wagon train experienced an epidemic

of acute pulmonary histoplasmosis. Thirty-three wagon train members

were hospitalized in a period of one week with severe influenza-like

symptoms. The infection was acquired at the site of a former winter

blackbird roost where the train had camped for only one day. Although

the soil surface was not disrupted, the group was apparently exposed

to a large dose of inhaled spores aerosolized in the course of routine

camping activities.

The wagon train was a private enterprise for the rehabilitation of

adolescents with behavior and adjustment problems. It provided an

outdoor experience in work and travel for troubled youths who would

otherwise have been referred to criminal justice or mental health in- stitutions. Most of the participants came from Pennsylvania, Arizona

and other states where histopiasmosis is not prevalent. The wagon

train originated in Tucson, Arizona, in March and completed its

cross-country trip to Pennsylvania in November 1980.

The wagon train traveled about 20 miles a day, and members

camped outdoors every night. At the time of the outbreak, the train

included 50 youths and 35 staff counselors. It consisted of seven

covered wagons, two water tanks, one bus, several trucks, and 80

horses and mules. Most of the wagon train members slept in six In- dian-style tepees, but a few slept outside or in motor vehicles. Each

tepee group functioned as a unit and was responsible for its own wagon, horses and mules. Youth members spent their time traveling, or at campsites caring for equipment and animals. Staff counselors

November 1981 The American Journal of Medlclne Volume 71 759

WAGON TRAIN HISTOPLASMOSIS-GUSTAFSON ET AL

TABLE I Symptoms in 54 Cases of Acute Pulmonary Histoplasmosis

JULY AUGUST

DATE OF ONSET

Figure 1. Epidemic curve for 54 symptomatic cases of acute pulmonary histoplasmosis in members of a wagon train.

had many additional responsibilities: buying food,

equipment and animals, as well as maintaining tele-

phone contact with the train’s headquarters. Staff

members were given 48 hours of leave after every six working days. Leave was taken from 6:00 P.M. the first

day until 6:00 P.M. two days later. Counselors usually

spent the full free day sightseeing in towns somewhat

distant from the wagon train.

OUTBREAK INVESTIGATION

Fifty-four of the 85 (63.5 percent) wagon train members became ill during the first two weeks in August (Figure

1) with a febrile disease characterized by prominent

myalgias and pulmonary symptoms (Table I). Thirty-

three persons were admitted to a hospital in Johnson City, Tennessee. Although pulmonary findings on ex-

amination were few, 16 of 32 chest roentgenograms showed evidence of pneumonitis or hilar adenopathy.

Only five showed the classic “snowstorm” appearance

of acute pulmonary histoplasmosis. Routine blood and

serum laboratory examinations were unrevealing and bacterial, fungal and viral cultures were not diagnostic.

Symptom

Fever Headache Substernal chest pain Pleuritic chest pain Nonproductive cough Stiff neck Abdominal pain Sore throat Nasal congestion Diffuse myalgias Thigh pain Diarrhea Vomiting

Number Percent of Cases of Cases

47 87 46 85 41 76 38 70 37 69 31 57 30 56 28 52 26 48 25 46 19 35 10 19 8 15

All patients recovered without specific therapy and

returned to the wagon train to complete the trip.

Acute-phase serum specimens from 30 patients

were obtained on admission to the hospital; convales-

cent-phase specimens were drawn three weeks later.

Twenty-four of 30 acute-phase serum samples showed

no complement fixation antibody to H. capsulatum yeast

antigen, four were anticomplementary, and only 2 had titers of 1:8. Twenty-eight of 30 paired serum samples

showed a four-fold or greater rise in complement fixa-

tion titer to H. capsulatum yeast antigen. Convales-

cent-phase titers ranged from 1:16 to 1:256. Whereas

none of the acute-phase serum samples showed any

precipitins by the immunodiffusion test, all 28 conva-

lescent-phase serum samples with positive comple-

ment fixation titers demonstrated M precipitins with

histoplasmin and nine of these (30 percent) also had H

precipitins. Complement fixation and immunodiffusion tests were

also performed with Blastomyces dermatitidis and Coccidioides immitis (coccidioidin) antigens. Low

complement fixation titer rises to B. dermatitidis yeast

antigen occurred in 28 persons, but in only one case did

TABLE II Relationship of Histoplasmin Skin Test or Serologic Results to Various Characteristics of the 85 Wagon Train Members

Characteristic

Male Female Age I 21 yr Age > 21 yr Cigarette smokers Nonsmokers Youth member Staff counselor

Test Results Attack Rate Positive Negative Total (percent) p=’

53 12 65 a2 16 4 20 60 NS 47 7 54 87 22 9 31 71 NS 45 8 53 85 24 8 32 75 NS 45 5 50 90 24 11 35 69 0.027

l Chi-square test.

760 November 1961 The American Journal of Medicine Volume 71

WAGON TRAIN HISTOPLASMOSIS-GUSTAFSON ET AL.

TABLE III Positive Histoplasmin Skin Test or Serologic Results Correlated with Dates of Leave for 35 Staff Counselors

Date

On Leave This Dale Not on Leave This Date Positive Percent Positive Percent Results Total Positive Results Total Positive p=*

July 19 July 21 July 23 July 25 July 27 July 29 July 31 August 2

75 20 31 65 NS 75 20 31 65 NS 83 18 29 62 NS

0 23 29 79 0.0006 100 19 31 61 NS

71 18 28 64 NS 100 21 33 64 NS

40 21 30 70 NS

* Fisher’s exact test (one-tailed).

the titer to B. dermatitidis antigen exceed that to H.

capsulatum yeast antigen. Only one person showed a

complement fixation titer rise to coccidioidin. Immu-

nodiffusion tests for B. dermatitidis and C. immitis

precipitins all gave negative results. Serologic tests

were also performed that excluded influenza, parain-

fluenza, adenovirus, respiratory syncytial virus, psit-

tacosis, mycoplasma and Legionnaire’s disease.

Six weeks after the outbreak, histoplasmin skin tests

were applied to the 85 original wagon train members.

Twenty-one new wagon train members, who had joined

the train after it left Tennessee, also were tested.

Sixty-seven of the 85 original wagon train members (79

percent) showed induration of more than 5 mm. In two

cases, the skin tests gave negative results, but the

persons had serologic evidence of acute histoplas-

mosis. Only two of 21 (10 percent) new wagon train

members had positive skin test results.

A “case” was defined as a positive skin test result

or a four-fold or greater rise in complement fixation titer

to H. capsulatum yeast antigen in any wagon train

member. This case definition was met in 69 of the 85

wagon train members (81 percent). A “symptomatic

case” was defined as any case in which documented

fever and one other symptom, or three of the symptoms

in Table I without fever, occurred. Fifty-four of the 69

cases (78 percent) were “symptomatic.”

As shown in Table II, sex, age and smoking status

were not associated with increased susceptibility to histoplasmosis. There was, however, a significant dif-

ference in attack rates among youth members (90 percent) and staff counselors (69 percent) (p = 0.027

by Chi-square test). Unlike youth members, staff

counselors did not spend all their time with the wagon

train. From two to seven counselors were on leave at

any given time, and every other day a few counselors would miss one campsite entirely. Table III lists the dates of possible exposure to H. capsulatum for the 20

days before the peak of the epidemic and the number

of staff counselors on leave on each of these days. Only campsites comptetely missed by some counselors are

shown. It is clear from this analysis that wagon train

members were exposed on July 25, 14 days before the

peak of the clinical epidemic. None of the six staff counselors on leave on July 25 had a positive histo-

plasmin skin test or serologic result, whereas 23 of the

29 staff counselors (79 percent) present at the July 25 campsite had a positive test result. In addition, one youth

member who had run away and was absent on July 25 had a negative skin test result.

On July 25, the wagon train had camped in a grassy

field adjacent to the municipal building in Charleston,

a small town in southeast Tennessee (Figure 2). Next

to that field was a l-acre wooded lot that had been a

known winter blackbird roost for more than 10 years.

There had been no construction, excavation or other

disturbance of the roost for several years. The field itself

had been part of the bird roost until the trees were

cleared in 1975 to make a park. Twenty-five soil

specimens were taken at this site and processed by the

indirect mouse isolation technique [ 11. Fourteen of 25

cultures grew H. capsulatum (Figure 2).

-.

Figure 2. Site of exposure to Histoplasma capsdatum, Charleston, Tennessee, July 25, 1980.

November 1981 The American Journal of Medicine Volume 71 761


TABLE IV Relationship Between Tepee Group and Histoplasmin Skin Test or Serologic Results in 49 Youths Present on July 25’

Tepee Group Positive Results Attack Rate

Negative Total (percent) p=t

5 4 4 8

1,2,3,4,6 41 0 41 Totals 45 4 49

l The one youth (ruhaway) not present on July 25 is excluded from this table. 7 Fisher’s exact test (on&ailed).

50 100 .0003

The wagon train traveled through Tennessee during

the record-setting heat wave of 1980, and virtually no

rain had fallen for more than a month. On July 25, the

high temperature in this town was 89’F, the humidity

was 52 percent and the wind was from the south at 8

to 10 knots. There were several brief, light thunder-

showers on the afternoon of the 25th.

The wagon train began arriving at the campsite

around 10:00 A.M. The wagon train’s horses and mules

were tethered at the junction of the field and wooded

area, and undoubtedly raised some dust. There were,

however, no group activities or games that would have

raised large amounts of dust. Setting up camp involved

placing some stakes in the ground and digging a small firepit. Several members also entered the wooded area

to seek shade, gather firewood or urinate.

Only one group activity could be confirmed; tepee Group 5 spent the afternoon of July 25 in a nearby town.

Youth members in tepee Group 5 had a significantly

lower attack rate than did youth members in all other

tepee groups (Table IV). Ail youth members (except the

one runaway) and ail staff counselors (except the six

on leave) slept in this field on the night of July 25. It

appears, therefore, that the afternoon of July 25 was

the period of highest risk for acquiring histoplas-

mosis.

COMMENTS

The first reported outbreak of acute pulmonary histo-

plasmosis occurred in 1938, but the fact that it was

caused by the same fungus responsible for the fatal disseminated form of the disease was not recognized

until more than 10 years later [2,3]. Since then, nu-

merous outbreaks have been reported and reviewed

[3-51. These investigations have firmly established the

clinical manifestations of acute pulmonary histopias-

mosis and the association of the fungus with chicken

houses, blackbird roosts and pigeon- or bat-occupied buildings and caves.

Analyses of these outbreaks suggest that H. capsuiatum, although worldwide in distribution, produces the large concentrations of spores necessary to cause

epidemic illness only in certain moist and heavily fer- tilized “microfoci” [6,7]. Several authors also contend

that most endemic histoplasmosis is attributable not to

small numbers of fungi distributed throughout the soil,

but to airborne spread of spores from a relatively few

concentrated foci [ 8- 111.

Despite detailed clinical descriptions and excellent

reviews, the clinical diagnosis of acute pulmonary histoplasmosis remains difficult [ 12- 151. In epidemics,

prolonged febrile illness or unusual roentgenographic

infiltrates may be the first clues that a viral agent is not

responsible. in sporadic cases, the diagnosis is rarely made at all. Improved serologic tests to confirm the

diagnosis are now available. A four-fold rise in com-

plement fixation titer to H. capsuiatum yeast antigen

provides strong evidence of acute infection. This test

can now be supplemented by the less sensitive but more specific immunodiffusion tests. The new ap-

pearance of M precipitins in convalescent serum is

considered diagnostic of acute disease. H precipitins

are the least sensitive of ail the tests (20 to 30 percent),

but are nearly 100 percent specific for recent active

infection [ 16,171.

Large epidemics of acute pulmonary histopiasmosis are not rare. Sixteen of the reported outbreaks in the

United States involved 10 or more symptomatic cases

(Table V). All the states represented are considered within the endemic region [28]. Reported outbreaks

have tended to cluster in low or “fringe” endemic areas

where the “susceptible” population may be larger, but this may be a bias resulting from reports of the un-

usual.

There is no seasonal trend for outbreaks, except that indoor sites predominate in cold weather, and outdoor

locations are more common in spring and summer. Warm or dry weather is apparently not required for

aerosolization of spores. In two situations, sites were

purposely disturbed in winter after the soil was wetted

down to minimize dust. Nevertheless, both disturbances

resulted in infections [ 13,221.

Clinical attack rates have varied in these outbreaks from 10 percent to 100 percent. Because more than 99 percent of all H. capsulatum infections are asymptomatic, it is generally held that particularly heavy in-

halation exposure is required to produce symptomatic acute pulmonary disease [ 151. in most outbreaks, a

clear relation between the degree of dust exposure and

severity of disease can be demonstrated.


WAGON TRAIN HISTOPLASMOSIS--GUSTAFSON ET AL.

TABLE V Outbreaks of Acute Pulmonary Histoplasmosis in the United States with 10 or More Clinical Cases

Mean Number Popula- Clinical incubation

of Clinical tion Anack Period Place (Ref.] Month Year Cases Exposed Rate (days) Group Affected Site Implicated Activity Implicated

Ceiling and bell tower of abandoned school

Underground storm cellar

Shoveling pigeon droppings

Plattsburgh,

NY [21 Nov 1938 19 21 90% WPA workers

1944 31 42

July 1947

Sept. 1947

June-Aug. 1948

March 1955

12 12

25 25

Chopping rotten wood and building fire

Shoveling pigeon droppings

Digging for treasure hunt

Digging for angleworms

Shoveling coal and dirt

Camp Gruber, OK [ 141

Cincinnati,

OH [31 Forman, AR

[ 181 Madison, WI [3]

Mountain Home, AR [ 191

74%

100%

100%

10

36 356 10%

11.4 Army squad

Abandoned water tower

Abandoned chalk mine

Blackbird roost

Workers

Neighbors

Children and school personnel

11.3 Construction workers

School grounds (filled with chicken manure in 1953)

Vacant lot (former blackbird roost)

Blackbird roost soil

Walworth, WI

t 751 July-Nov 1956 19 23 83%

Sturgis, MS [ 201 Nov. 1958 12 33 36%

Digging sewer lines and building basement

‘Tossing bag of soil around class during a potting project

Raking and burning leaves

Bulldozing roost

Clearing and sawing rotten trees

Digging and building new porch

Raking leaves and sweeping dirt

Throwing dirt at bats

Shoveling pigeon droppings and dumping them off the roof

Sawing rotten tree and raking leaves

Camping in tepees

12.2 Children in one sixth grade class

Children in a boy scout troop

Workers and some passers-by

Workers and general public

Workers and family members

15.4 Children and school personnel

13.7 Youth group from a church

13.9 Employees and clients at courthouse

Mexico, MO [S]

Mason City, IA

(271 Mason City, IA

[221

Northwest IL

[ 231

Delaware, OH (Earth Day)

[24,25] Suwanee Co.,

FL [ 261

Hot Springs, AR [27]

April 1959 10

Aug.-Sept. 1962 28

Feb. 1964 87

1967 12

April 1970

1973

1975

383

Feb. 23

68

64 16% Blackbird roost

Blackbird roost

Blackbird roost

19

949

29

63%

40%

79%

Blackbird roost in yard of old house

Blackbird roost :‘1 school courtyard

Cave

Roof and tower of courthouse

Yard where fallen oak tree located

Blackbird roost

42 48% 14.4 Workers and neighbors

78 69% 13.4 Wagon train members

Brentwood. TN [ 161

Charleston, TN (reported here)

1977

Aug. 1980

20

54

* Clinical illness occurred in 44 of 84 employees (52%) in building. Other cases occurred in clients visiting courthouse.

The severity of clinical disease probably also relates sponse. In others, it may occur because immunity is to host factors. Previous infection with the fungus incomplete or has waned with time [ 151. Both com- confers a degree of protection but does not always plement fixation titers and histoplasmin skin test results prevent reinfection following heavy exposure tend to revert to negative in the absence of continuing [ 10,27,29,30]. In some cases, “reinfection histoplas- exposure [ 17,311. Even in an endemic area, Zeidberg mosis” appears to be due to a hypersensitivity re- et al. [32] found that 15 percent of those with positive



skin test results had negative results when retested two

years later [32]. A second host factor thought to influence the clinical

attack rate is age. In the wagon train members, whose

ages ranged from 13 to 58 years, age was not related

to acquisition or severity of disease. Younger children

are said to have a high rate of asymptomatic and mild

infections. In the four major outbreaks involving chil-

dren, the proportions of infected children with asymp-

tomatic disease were significant: 75 percent in Moun-

tain Home [ 191, 50 percent in Sturgis [20], 73 percent in Mexico [6] and 48 percent in the Earth Day outbreak

[24]. However, their exposure was less direct than that

in most outbreaks involving adults.

The incubation period of acute pulmonary histoplasmosis is best estimated from large outbreaks in-

which exposure was limitedto one or two days. There

is excellent agreement among eight such outbreaks

listed in Table V in which the incubation period ranges

from five to 25 days with a mean of 14 days, as in this

outbreak. Reinfection histoplasmosis may have a

shorter incubation period (three to seven days), but this

is not as well established [ 15,291.

The sources of these outbreaks include all the

common habitats of H. capsulatum. One outbreak was

attributed to chicken manure, two to soil in bat-infested

caves, three to the sawing of rotten wood, three to pi-

geon droppings in old buildings and seven to the soil of

blackbird roosts. These sources are also representative

of smaller reported outbreaks, except that chicken

houses figure more prominently in small family out-

breaks [4,5]. In every outbreak, digging, raking or

otherwise aerosolizing contaminated dust or manure

was the activity leading to exposure. In most cases, only people within 10 to 20 feet of dust-raising activities

acquired the disease. Indeed, in only five outbreaks did

persons other than those actually performing the work

become ill. In three of these five outbreaks, large

populations were exposed when spores were aero-

solized within a few feet of air-conditioning intake vents

[ 19,24,27]. In the other two outbreaks, disruption of the

sites continued for several weeksand the exact nature

of exposure at these locations could not be determined

[21,22]. Sporadic cases and small family outbreaks of acute

pulmonary histoplasmosis have been attributed to seemingly mild dust exposures [ 10,331. This is the first large outbreak, however, in which no obvious disruption

of infected soil or rotten wood occurred. There was no

major dust-raising activity in the wooded area or the field

on which the wagon train members camped. Since

most of the wagon train members never entered the

wooded area, exposure probably resulted from the small

amount of dust raised in the field by the animals and by

the setting up of camp.

No previous report of an outbreak has implicated a

roost site that had been cleared of trees for years. It is

known, however, that soil can remain positive for at

least 10 years after a roost is cleared [ 71. The recently

demonstrated ability to decontaminate H. capsul-

atum-infected soil with formalin has led some to call for

regulations regarding the disturbance of blackbird roosts

[34-361. A major hindrance to efforts to control epi-

demic histoplasmosis, and perhaps to have an impact on endemic diseases as well, is the difficulty and ex-

pense involved in culturing soil samples for H. capsul-

atum. We are also unable to predict which microfoci will

support exuberant growth and heavy spore production

by the fungus. Most blackbird roosts in endemic areas

that have been occupied by birds for more than three

years are believed to support heavy growth of H. capsulatum. Of more than 100 of these older roosts sam-

pled in the Mississippi and Ohio River valleys, 79 per-

cent have yielded positive soil cultures (Weeks R, un-

published data). The potential public health hazard of blackbird roosts

is large, and the continuing blackbird and starling pop-

ulation explosion has provided impetus to efforts to

control the spread of H. capsulatum microfoci. Blackbird

roosts, commonly inhabited by both blackbirds and

starlings, are frequently disrupted to eliminate the nui-

sance created by large concentrations of birds. The

experience of the wagon train members suggests that caution should be exercised not only in clearing or

disrupting a roost, but also in considering possible future

uses of contaminated sites.

ADDENDUM

Since submission of the manuscript for publication, a

large outbreak of histoplasmosis due to an unidentified

source has been reported in Indianapolis [37].

ACKNOWLEDGMENT

We thank Ms. Mildred Cooper, Immunization Repre-

sentative, Tennessee Department of Public Health; Mr.

Tpm DeMelfi, Pennsylvania Department of Public Health; and Ms. Diane Riley and other members of the

wagon train for their cooperation.

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outbreak of acute pulmonary histoplasmosis in members of a wagon train

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