REVIEW ARTICLE

Occurrence of Histoplasmosis in the Indian

Sub-Continent: An Overview and Update https://doi.org/10.20936/jmrp/07/03/02

Harbans S Randhawa* and Harish C Gugnani** ISSN : 2162-6391 (Print) 2162-6375 (Online)

ABSTRACT
The occurrence of histoplasmosis and its environmental sources of infection are reviewed. It covers the regional distribution of 388 cases of histoplasmosis
reported since 1995 to till date. The highest number of cases occurred in West Bengal, followed by Uttar Pradesh, Delhi Union territory (UT), Rajasthan,
Maharashtra, Haryana, and Bihar. A sharp rising trend in reporting cases observed in recent years is particularly noteworthy. Also, discussed are the variable
clinico-pathological manifestations of 388 cases from India, 20 from Bangladesh, five from Nepal, four from Pakistan, and three from Sri Lanka. Being a primary
pathogen, the etiological agent Histoplasma capsulatum can infect immunocompetent as well as the immunocompromised patients. The disease is fatal unless
diagnosed early and treated with specific antifungal drugs. It has a predilection for reticuloendothelial system, leading to hepatosplenomegaly, a prominent
feature of disseminated histoplasmosis. It poses an ever-increasing threat to public health due to burgeoning population of immunocompromised patients
resulting from the spread of AIDS and immunosuppressive therapy in patients undergoing organs transplantation. Non-recognition of the true burden of
histoplasmosis in the Indian sub-continent is attributed to possible misdiagnosis as tuberculosis, malignancy or other diseases, and to lack of awareness and
inadequate mycological diagnostic facilities. The need for exploring the natural foci of H. capsulatum infections, using molecular techniques, and delineating
the endemic zones of histoplasmosis is strongly emphasized.
Core tip Nomenclature of Histoplasma, its ecology, pathogenesis, clinical spectrum and laboratory diagnosis, and regional distribution of histoplasmosis in
India are described. The highest number of cases of the disease occurred in West Bengal. The varying clinical manifestations of 388 cases from India, 20 from
Bangladesh, five from Nepal, four from Pakistan, and three from Sri Lanka are described. The decade-wise occurrence of histoplasmosis in India showed a rising
trend of reporting 200 cases being recorded during the period 2004–2013, and 161 cases from 2014 to till date. In view of the available evidence, histoplas-
mosis is endemic in the subcontinent. However, supportive scientific evidence like demonstration of natural reservoirs of the pathogen and its occurrence in the
local animal populations remains largely unexplored.
KEYWORDS histoplasmosis, Histoplasma capsulatum var. capsulatum, Indian, subcontinent, update

INTRODUCTION
histoplasmosis. The organism may also enter the body
Histoplasmosis is a non-contagious systemic fungal through the mouth, and from there can cause infec-
infection of worldwide distribution, caused by a ther- tion in the intestines1,2. Histoplasmosis in humans has
mally dimorphic fungus, Histoplasma capsulatum which two clinical entities: Histoplasmosis capsulati caused by
thrives in a warm and humid environment such as soils H. capsulatum var. capsulatum (Darling’s disease,
enriched with nitrogenous compounds and phosphates American histoplasmosis, classical histoplasmosis, small
derived from avian excreta and bat guano. The microco- form histoplasmosis), and Histoplasmosis duboisii caused
nidia and short hyphal fragments of Histoplasma when by H. capsulatum var. duboisii, commonly called African
inhaled by mammalian hosts reach the alveoli, followed histoplasmosis (large form histoplasmosis). Investigators
by the rapid conversion to its yeast form that can per- linked to the division of medical mycology, VPCI, have
sist in host tissues and may disseminate through the been interested since 1960 in clinical and epidemiologi-
bloodstream and lymphatics to other organs, causing cal aspects of histoplasmosis3. The first case of histoplas-
mosis from India was reported in 1954 by Panja and Sen4
*
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Harish C Gugnani during the period 1957–1959. The prevalence of 12.3%
J 3/45, Rajouri Garden, New Delhi 110027, India. histoplasmin sensitivity found in the riverine area was
Email: harish.gugnani@gmail.com the highest reported from any part of India. However,
Conflicts of interest: None. no case of histoplasmosis was detected among the pos-
Source of funding: None. itive reactors. Data on histoplasmin sensitivity in other
Author contribution: Both authors contributed equally. parts of India have been reviewed by Randhawa and

J Med Res Prac | Volume 07 | Issue 03 | 71–83

Received: 01 March 2018 Accepted: 21 may 2018 Published Online: 06 June 2018
72 Harbans S Randhawa and Harish C Gugnani
Khan6. Since then, the disease has been the subject of a
large number of case reports7–9, and several reviews10–12.
A rare case of epididymal histoplasmosis masquerad-
ing as tuberculosis diagnosed by culture of semen was
reported by Randhawa et al.13 This paper reviews the
clinico-pathological and epidemiological features of
the 388 cases of histoplasmosis, reported in India since
1995, and also those reported from Bangladesh, Nepal,
Pakistan, and Sri Lanka.
METHODS
All publications on histoplasmosis in the Indian sub-
continent were scanned by thorough search of the litera-
ture, using PubMed, MEDLINE, Biomed Lib, Med Facts,
and different sets of keywords, viz. India, Bangladesh,
Pakistan, Nepal, Sri Lanka, Bhutan, histoplasmosis, sys-
temic/deep mycoses, etc. Besides, cross-references in the
papers collected were accessed. All of the papers were
critically reviewed to extract relevant clinico-pathological
features and demographic data of each case. Cases diag-
nosed solely on clinical suspicion without histopatholog-
ical evidence or positive cultures were excluded.
OBSERVATIONS
Nomenclature of Histoplasma and its ecology
Histoplasmosis has three clinical entities with separate
etiologic agents (Table 1). Based on phenotypic char-
acters, Histoplasma is divided into three varieties, viz.
H. capsulatum var. capsulatum, H. capsulatum var. duboi-
sii and H. capsulatum var. farciminosum. The commonest
environmental sources of H. capsulatum var. capsulatum
are soil around chicken houses, under roosting gregarious
birds such as starlings, blackbirds, and soil of bat-infested
caves or old buildings (CFU can exceed 105/g of soil/bat
guano)1,2. Birds cannot be infected by the fungus and do
not transmit the disease. However, avian excreta contam-
inate the soil, thereby providing an enriched medium for
growth of the fungus. On the other hand, bats can get
infected and transmit H. capsulatum to new sites through
their droppings1,2. The fungus is found in the upper 15 cm
of soil, never deeper than 22.5 cm, and requires a mean
TABLE 1 Nomenclature of Histoplasma, natural habitats and geographic distribution.
Etiological agent* Clinical entity
H. capsulatum var. capsulatum Histoplasmosis (histoplasmosis
(Teliomorph Ajellomyces capsualtus) capsualti, classical histoplasmosis)
H. capsulatum var. duboisii Histoplasmosis duboisii (African
(Teliomorph Ajellomyces capsualtus) histoplasmosis, large form histoplasmosis)
H. capsutatum var. farcinimosum Histoplasmosis farciminosi
(Teliomorph Ajellomyces capsualtus) (epizootic lymphagitis)
*Studies of isolates of H. capsulatum from Europe, Australasia, Asia, Netherlands, North America and South America by Kasuga et al.14 and Teixeira et al.15 have detected several phylogenetic
clades, suggesting that the existing varieties are taxonomically invalid.
temperature of 22–29°C and relative humidity of 67–97%
for optimum growth. Activities such as cleaning of chicken
coops, visiting bat-infested caves or other such sites, exca-
vation, demolition and remodeling of old buildings, and
cutting of dead trees lead to disruption of soil containing
the organism, and aerosolization of microconidia2.
Clinical spectrum and laboratory diagnosis
Histoplasmosis caused by H. capsulatum var. capsulatum
is a disease of reticuloendothelial system. A majority
(50–90%) of the infections result in clinically insignifi-
cant respiratory disease or mild influenza-like illness.
Some infections may cause acute pulmonary histoplas-
mosis, manifested by non-productive cough, dyspnea,
hoarseness, chest pain, cyanosis associated with fever,
night sweats, muscle/joint pain, weight loss, malaise, and
fatigue. Acute pulmonary histoplasmosis may be con-
fused with tuberculosis/miliary tuberculosis2, although
involvement of upper lobes and pleural effusion is more
common in the latter1,2. Chest X-ray findings in most
patients with asymptomatic pulmonary histoplasmo-
sis are normal. A single pulmonary nodule is, however,
frequently seen. Most patients recover within 2 weeks
of onset of symptoms, although fatigue may persist
longer. Progressive disseminated histoplasmosis occurs
in approximately 10% of the patients with hepatospleno-
megaly, fever, anemia, leukopenia, weight loss, and gen-
eralized lymphadenopathy, pulmonary symptoms being
less prominent2. Males are more frequently affected than
females by 4:1 ratio. Patients with AIDS are at high risk
for disseminated histoplasmosis; prevalence rates range
is 2–27% in United States and 29% in India1,6.
Laboratory diagnosis of histoplasmosis is based on
histopathology/cytopathology, recovery of Histoplasma
in culture from clinical samples, serological tests for
antibodies, and antigen detection. Cultures are 58–85%
positive in cases of disseminated and chronic forms of
histoplasmosis; usually, up to 4 weeks is required to iso-
late the organism in culture2. Several culture media have
been used for recovery of H. capsulatum var. capsulatum
from clinical specimens. In our experience, brain-heart
infusion (BHI) biphasic medium appears to be the best
Geographic
Yeast form morphology Natural habitat
distribution
Globose or ovoid 2–4 μm, thin- Soil enriched with Worldwide with variable
walled cells with a narrow base avian or bat excreta endemicity
Ovoid 6–15 μm thick-walled Rarely isolated Central and West Africa,
cells with a broad base from soil and Madagascar
Ovoid 2–3 μm, thin-walled Unknown Africa, Asia and Europe
cells with a narrow base
J Med Res Prac | Volume 07 | Issue 03 | 71–83
 Histoplasmosis in the Indian subcontinent 73

TABLE 2 Regional distribution of histoplasmosis reported from India (1995-to-date).

State/Union Territory No. of cases References
West Bengal 56 9, 16–39
Uttar Pradesh 37 9, 12, 13, 40–61
Delhi 26 62–83
Rajasthan 24 60, 84–93
Maharashtra 20 94–109
Haryana 19 60, 110–119
Bihar 18 9, 12, 60, 120–123
Chandigarh 17 124–129
Tamil Nadu 15 9, 21, 130–134
Assam 13 9, 21, 135–137
Kerala 11 9, 138–143
Karnataka 10 144–152
Andhra Pradesh 8 9, 153–156
Gujarat 8 93, 157
Madhya Pradesh 5 158–162
Manipur 5 163–166
Odisha 5 9, 167–170
Himachal Pradesh 4 171–174
Punjab 4 175–178
Uttarakhand 4 179–182
Telangana, Meghalaya, Tripura, Chhattisgarh, Jammu & 10 21, 183–189
Kashmir, Jharkhand
Cases of unknown origin 69 12, 190–199
Total 388

for rapid recovery of maximum growth of H. capsula-

tum. Yeast phosphate and BHI agar are nearly as good as
these media also recover multiple colonies of the fungus.
Galactomannan antigen detection in body fluids offers
a rapid means of diagnosis. The antigen is detectable in
80–95% of cases of progressive disseminated and sub-
acute histoplasmosis2.

Magnitude of problem in India

The data on the occurrence of histoplasmosis in
India reported since 1995 is presented in Table 2 and
depicted in Fig. 1. West Bengal accounted for the high-
est number of 56 cases, followed by Uttar Pradesh, Delhi
(UT), Rajasthan, Maharashtra, Haryana, and Bihar.
The diagnosis of a majority of the cases was based on
histological/cytopathological demonstration of the char-
acteristic yeast form of H. capsulatum. Confirmation by
culture was done in about 20% of the cases. Additional Fig. 1 3FHJPOBM
EJTUSJCVUJPO
PG
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PG
IJTUPQMBTNPTJT
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tests, viz. serology, PCR, and sequencing were done only UPEBUF

in a few cases. The literature search did not reveal the

J Med Res Prac | Volume 07 | Issue 03 | 71–83

74 Harbans S Randhawa and Harish C Gugnani
occurrence of any case from the States of Arunachal
Pradesh, Goa, Mizoram, Nagaland, and Sikkim, and the
Union Territories of Daman and Diu, Dadra and Nagar
Haveli and Pondicherry, and Andaman and Nicobar, and
Lakshadweep islands. Histoplasmosis possibly occurs in
these areas but has not been detected due to lack of aware-
ness among the physicians and paucity of laboratory
diagnostic facilities. It is noteworthy that a large number
of cases of oral and adrenal histoplasmosis (mostly in
renal transplant recipients) have been documented
during the period under review. The decade-wise occur-
rence of histoplasmosis is shown in Table 3 and depicted
in Fig. 2. Notably, the number of cases reported during
the period 1954–1993 was 37, followed by a sharp rising
trend of reporting. Thus, 200 cases were recorded during
the period 2004–2013, and 161 during the period from
2014 to till date. This significant change can be attributed
to increased awareness among clinicians, pathologists
and microbiologists, and their collaboration. The avail-
ability of enhanced laboratory facilities in many medi-
cal colleges and hospitals in some parts of the country is
another contributing factor for increased reporting from
those areas.
The predominant clinical features and the involve-
ment of different organs in the cases reviewed were
essentially the same as described previously2.6,7,11,12. The
commonest comorbidities were HIV infection, diabetes,
TABLE 3 Data on decade-wise occurrence of histoplasmosis in India,
showing a sharp rising trend in its reporting during the decade 2004–2013,
and thereafter during the period of 2014-to-date.
Period No. of cases
1954–1963 4
1964–1973 14
1974–1983 12
1984–1993 7 and palate; in many of the cases there was no indication
1994–2003 28
2004–2013 200
2014-to-date 161
Total 426
Fig. 2
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TIPXJOH histoplasmosis should be considered in the differen-
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EVSJOH
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BOE
tial diagnosis of patients with mucocutaneous lesions,
UIFSFBGUFS

UPEBUF
.
adrenal insufficiency, and renal transplant. It is notewor-
thy that adrenal histoplasmosis was frequently observed
in transplant recipients. Adrenal involvement also seems
to be common in immunocompetent patients with dis-
seminated histoplasmosis. Sometimes cutaneous lesions
were the only sign of serious systemic histoplasmosis in
post-transplant patients. A number of cases occurred
in association with hemophagocytic lymphocyto-
sis29,43,62,169,178,180; other unusual comorbidities included
hairy cell leukemia with ascites28, juvenile SLE38, lym-
phoidal co-infection with cryptococcosis55, CMV infec-
tion58, aplastic anaemia74, Coomb’s positive hemolytic
anaemia90, myelodysplastic syndrome/myeloproliferative
neoplasm (MDS/MPN)128, mixed phenotype leukemia129
and BK virus nephropathy194. Another unusual case of
comorbidity was the occurrence of rectal histoplasmosis
in a patient with Job’s syndrome51. A few cases of oral his-
toplasmosis simulated carcinoma111,122,149, whereas some
laryngeal/pulmonary/disseminated cases mimicked lung
and laryngeal carcinoma79,95,110,143,159,181. Likewise, one
each case simulated lepromatous leprosy82, non-Hodgkin
lymphoma83, idiopathic thrombocytopenic purpura89,
abdominal tuberculosis98,187, Langerhans cell histiocyto-
sis134, and two cases of eyelid involvement simulated basal
cell carcinoma109,152. Some other unusual presentations of
histoplasmosis were parenchymal diseases with ascites24,
colonic pseudotumors67, portal hypertension with bone
involvement105, pancreatic head mass with gastric outlet
obstruction114, and epididymitis and prostatitis148. The
frequent involvement of gastrointestinal tract in several
cases as observed in the current review points out the
need for considering gastrointestinal histoplasmosis in
the differential diagnosis of malignancy, inflammatory
bowel disease, and intestinal tuberculosis. Oral lesions
were common in the series of cases in our review, involv-
ing several sites, viz. buccal mucosa, tongue, gingivae,
of pulmonary lesions. However, the prior occurrence of
self-resolving pulmonary histoplasmosis cannot be ruled
out. In tuberculosis-endemic regions as in the Indian
sub-continent, disseminated histoplasmosis can easily
be mistaken for tuberculosis owing to its similar clini-
cal presentation. Presence of military shadows in chest
X-ray is frequently attributed to tuberculosis without
further etiological investigation1,2. In patients with pro-
longed fever, hepatosplenomegaly, and lymphadenopa-
thy, histoplasmosis must be considered in the differential
diagnosis, particularly, if there is no response to empir-
ical anti-tubercular therapy (ATT). Further, in patients
of pulmonary histoplasmosis with pre-existing lung dis-
ease, hilar, and peripheral lymphadenopathy, radiologi-
cal signs suggestive of histoplasmosis may not be present.
Also, several cases of histoplasmosis in the subcontinent
may present as non-healing oral ulcers mimicking muco-
cutaneous leishmaniasis. It needs to be emphasized that
J Med Res Prac | Volume 07 | Issue 03 | 71–83
 Histoplasmosis in the Indian subcontinent 75

hepatosplenomegaly, adrenal insufficiency, malignancy, reported. The clinico-epidemiological features of 20 pub-

inflammatory bowel disease, and in patients clinically
diagnosed as oral and abdominal tuberculosis.
CASES IN BANGLADESH, NEPAL, PAKISTAN, AND SRI LANKA
A brief account of the histoplasmosis cases reported
from Bangladesh, Nepal, Pakistan, and Sri Lanka is given
in Table 4 along with references.
Bangladesh
In a histoplasmin skin sensitivity survey in Bangladesh
(when it was called East Pakistan) in 1962200, 2,729 persons,
including patients in the hospital, students and nurses,
workers in a jute mill, a paper mill, and staff and students
of an agricultural farm area were tested. There was no sig-
nificant difference in the number of positive reactors to
histoplasmin in the first four groups (12.58–13.75%), but
the number of positive reactors in the agricultural farm
was nearly double (23.18%) of that of any other group.
Subsequently in 1971201, 461 of 2,522 (17.92%) patients in
institutions of tuberculosis and other chest diseases were
found to be positive reactors. These surveys indicated
endemicity of histoplasmosis in Bangladesh. Recently,
an increasing number of histoplasmosis cases have been
lished cases are provided in Table 4. All of the patients
were adult males of aged 30–75 years. As is evident,
most of the cases were disseminated with varying clini-
co-pathological manifestations, viz. hepatosplenomeg-
aly, generalized lymphadenopathy with oropharyngeal
and laryngeal ulcers, bilateral adrenomegaly, and skin
lesions in the form of a generalized maculopapular rash
or hyperpigmented skin nodules. Four of the patients had
AIDS, one of them with concurrent esophageal candidi-
asis; in addition to the five patients gave a history of TB
with ATT. One of the patients had Crohn’s colitis. It is
worth mentioning that eight of the patients were farm-
ers, and one each was a building maintenance and brick-
field worker. One of the patients, immigrant in New York
(Sr. no 5) had made several visits to Bangladesh, the last
one 6 months prior to his illness. Diagnosis of all the
cases was based on histopathology, barring one culture
positive for H. capsulatum.
Nepal
Four autochthonous cases have been reported.
Additionally, one case has occurred in a Nepalese
migrant to United Sates with evidence of infection
being acquired in Nepal (Table 4). Four of these cases

TABLE 4 Histoplasmosis in Bangladesh, Nepal, Pakistan, and Sri Lanka.

Sr. no Age/sex Place of reporting Clinico-pathological manifestations References
Bangladesh
1 60 M Dhaka Oral ulcer hepato-splenomegaly, odynophagia Islam et al. Bangladesh Med Res Counc Bull.
1982;8:21–22.
2 40 M Qatar h/o frequent Splenomegaly, bilateral adrenomegaly fever, night sweating Al Ani MA et al. Qatar Med J. 2002;11:57–59.
visits to Bangladesh
3 41 M Chittagong Hepato-splenomagaly, cervical lymphadenopathy, high fever, weight Rahman MM et al. J Bangladesh Coll Phys Surg.
loss with AIDS & esophageal candidiasis 2005;23:43–45.
4 Adult Vellore, Disseminated histoplasmosis. Details of organ involvement not Subramanian et al. JAPI. 2005;53:185–189.
Tamil Nadu, India known. Weight loss and fever
5 60 M New York Hyperpigmented nodules on left cheek and right fore-arm. Rappo U et al. Transpl Infect Dis. 2010;12:
Had a renal transplant 155–160.
6 57 M Dhaka Generalized lymphadenopathy, hepatomegaly, backache, fever, Parvin et al. J Med. 2010;11:170–175.
spastic paraplegia, paravertebral soft tissue mimicking TB
7 45 M Not given Generalized lymphadenopathy, oral ulcers, odynophagia, Parvin et al. J Med. 2010;11:170–175
fever, abdominal pain and jaundice, history of ATT

8 45 M Dhaka Generalized lymphadenopathy, oral ulcers, odynophagia Shamin Ahmad Md et al. BSMMU J. 2010;3:
fever, ascites, weight loss 44–46
9 56 M Dhaka Respiratory distress, fever disorientation, cough Mehbub Md S et al. J Med. 2010;11:70–73
10 32 M Not given Supraclavicular lymphadenitis, multiple ulcers in nasopharynx, fever, Parvez Md M et al. Health Popul Nutr.
weight loss, anorexia 2010;28:305–307.
11 75 Gopalganj Bilateral adrenomegaly, partial adrenal insufficiency, anorexia, Sarwar-e-Alam AMB et al. J Bangladesh Coll Phys
evening fever with chills, weight loss Surg. 2011;235–240.
12 60 M Dhaka Oral ulcers, bilateral sub-mandibular lymphadenopathy, odynophagia Sadat SMA et al. J Bangladesh Coll Phys Surg.
2012;30:229–233.

J Med Res Prac | Volume 07 | Issue 03 | 71–83

76 Harbans S Randhawa and Harish C Gugnani

TABLE 4 Histoplasmosis in Bangladesh, Nepal Pakistan, and Sri Lanka—(Continued).

Sr. no Age/sex Place of reporting Clinico-pathological manifestations References
13 65 M Dhaka Oral ulcers, bilateral sub-mandibular lymphadenopathy, odynophagia Sadat SMA et al. J Bangladesh Coll Phys Surg.
2012;30:229–233.
14 30 M Northern Bangladesh Cough, fever, weight loss, anorexia, hyper-pigmented papular Bhuyian MNZ et al. JAFMC Bangladesh.
(Place unspecified) eruptions on several parts of the body, bleeding from ear, nose, gums 2012;8(2);81–86.
and rectum, severe anemia with AIDS
15 45 M Dhaka Oral and genital ulcers, hepatomegaly, generalized maculo-papular Yasmin R et al. Bangladesh J Med. 2013;24:78–
rash 81.
16 62 M Dhaka Generalized lymphadenopathy, mild hepatomegaly, spastic Singha CK et al. J Med. 2013;4:201–203.
para-plague, fever, back pain
17 65 M Dhaka Hepato-splenomegaly, oral ulcers. History of pulmonary TB with Sadat SMA et al. Med Today. 2013;5:99–102.
irregular ATT, Heavy smoker
18 32 M Parbotinogar, Dhaka Bilateral adrenomegaly, hepato-splenomegaly, fever, weight loss, Parvin R, Rafique Udin AKM. J Gen Pract.
anorexia, history of ATT for presumed TB 2013;1:103. doi:10.4172/2329-9126.1000103
19 60 M Mymensingh Ulcerative growth in the left vocal cord, cough, hoarseness. History of Maasud MK et al. Mymensingh Med J.
ATT for presumed TB 2014;23(3):566–567.
20 34 M New York, USA Crohn’s colitis with persistent bloody diarrhea, high grade fever and Marion-Anna P et al. Inflamm Bowel Dis. 2014;20
joint pains. Colonoscopy revealed shallow rectosigmoid ulcers. (Suppl 1):S27–S28. doi:10.1097/01.
MIB.0000456773.37078.b6
Nepal
1 59 M Not given Hepato-splenomegaly, bilateral adrenomegaly, thrombovytopenia Sookpraneet et al. J Infect Dis Antimicrob Agents.
chronic fever, diabetic 1993;10(1):35–38.
2 40 M Dhahran Multiple, painless, non-healing, discharging lesions on the anterior Koirala et al. Health Renaissance Case Rep.
chest wall for the last 6 years. 2010;7(1):61–63.
3 52 M Kathmandu Bilateral adrenomegaly, fever, fatigue, weight loss Subedi et al. JSSN. 2014;17(1):42–43.
4 65 F New York Painless ulcer on the dorsum of tongue, fever, productive cough, chest Gandhi V et al. Chest Imaging and Pathology for
pain. Chest X-ray showed dense opacity in the right lung. h/o of ATT Clinicians. 2015;147(4):e140–e147.
in Nepal
5 14 M Rural Nepal (District Persistent multiple skin lesions on face, dry cough, hepato- Thapa S et al. Am J Trop Med Hyg.
not specified) splenomegaly, complicated by severe mitral stenosis. Chronic 2016;94(2):249–250.
exposure to chickens. h/o rheumatic heart disease
Pakistan
1 45 M Karachi Bilateral basal infiltrates in the lungs. Paratracheal, crainal, anterior Zia SA et al. JPMA. 2002. August issue.
aortic and hilar lymphadenopathy, hepatosplenomegaly, bilateral
adrenal gland enlargement, fever, weight loss, Jaundice, and history
of ATT
2 Adult M Karachi Endocarditis Bhatti S et al. J Infect. 2005;51(1):2–9.
(age?)
3 5M Karachi Mediastinal, para-aortal and mesenteric lymphadenitis, h/o**, Qureshi A. JPMA. 2008;58(8):457–458.
ATT***
4 60 M Battagram Chest pain, weight loss, dry cough, pleural effusion with h/o of ATT Aziz R et al. Unpublished data from Ayub Teaching
and left hydro-pneumothorax and long standing diabetes Hospital, Abbottabad.
Sri Lanka
1 Not Not given Ulcers in the buccal cavity. Details of the case not known Jayaweera FRB et al. Ceylon Med J.
known 1975;20(1):45–47.
2 30 M Kandy Oral ulcers and multiple, enlarged submandibular and submental Karunanayake L. et al. Abstract in the Bulletin
lymph nodes. HIV-positive. Had non-Hodgkin lymphoma with of the Annual Academic Sessions of the Kandy
extensive abdominal and pelvic lymphadenopathy Society of Medicine in February, 2009.
3 24 F Germany Disseminated histoplasmosis with hepatosplenomegaly, multiple Harten P et al. Clin Investig. 1994;72(11):
lymphadenopathy, ascites, fever, thrombocytopenia and polyserositis 878–882.
diagnosis based on histopathology

J Med Res Prac | Volume 07 | Issue 03 | 71–83


were disseminated, involving the lung, liver and spleen,
or adrenal glands; the fifth had multiple discharging
lesions on the anterior chest wall for the last 6 years.
Four of the patients were males and one female. One of
the males, a 14-year-old boy was persistently exposed
to chickens, and had a history of rheumatic heart dis-
ease, complicated by severe mitral stenosis. Two of
the patients were farmers, one of whom (Sr. no 4) had
recently migrated to New York, United States.
Pakistan
Altogether 575 subjects, comprising healthy men,
women, and school children, as also pulmonary tubercu-
losis and leprosy patients in Punjab province of Pakistan,
were tested for skin sensitivity to histoplasmin202. All
of the subjects were non-reactors, excepting those who
had traveled abroad to endemic areas indicting non-
endemicity of histoplasmosis in Pakistan. Our literature
search has now revealed four authentic indigenous cases
of histoplasmosis (Table 4). Three of them had symp-
toms of disseminated histoplasmosis with prior history
of ATT; the fourth was an unusual case of Histoplasma
endocarditis.
Sri Lanka
A survey of histoplasmin sensitivity conducted in 1969
comprised of 1,366 students and prisoners (524 males, 842
females). This included 133 tuberculosis patients diag-
nosed by bacteriologic or histopathologic examination
from different parts of the country. Notably, this group
revealed 78 strongly positive reactors203. However, only
three autochthonous cases of histoplasmosis have been
documented so far. One of them, a 24-year-old German
woman had possibly acquired infection in Sri Lanka or
Maldives, while on a 10 days holiday trip to this region.
Information on the occurrence of African histoplas-
mosis in the Indian subcontinent is lacking. The case
reported by Ravindran et al.204 in 2015 from Kerala state
of India lacks authentication. The photomicrograph pro-
vided in Fig. 6 of this publication is entirely incompatible
with H. capsulatum var. duboisii. It depicts arthrocon-
dida like bodies suggestive of Trichosporon and not the
large yeast form cells characteristic of H. capsulatum var.
duboisii.
HISTOPLASMOSIS IN ANIMALS
Histoplasmosis has been reported in several species
of small mammals including wild rats and oposums205.
Demonstration of histoplasmosis in animals helps to
establish endemicity of the disease in a given area. There
is no report of isolation of Histoplasma from small mam-
mals in India. Kalra and Wanchoo206 reported negative
findings in investigation of 325 rats, 65 bandicoots, nine
shrews, and four house mice examined from Pune State
J Med Res Prac | Volume 07 | Issue 03 | 71–83
Histoplasmosis in the Indian subcontinent 77
of Maharashtra. Investigation of 630 small wild animals
belonging to 11 species and 10 genera from different
parts of India by Gugnani207 did not yield any isolation
of this fungus. Epizootic lymphangitis caused by H. cap-
sulatum var. farciminosum has been reported in equines
and camels from several countries15 including India208.
SOIL AS NATURAL HABITAT OF H. CAPSULATUM VAR.
CAPSULATUM
Information on the natural habitats of H. capsulatum
var. capsulatum in the Indian subcontinent is restricted
to a single report of its isolation from a sample of soil
admixed with bat guano. The sample was collected from
a 300-year-old building infested with bats of the species
Scotophilus heathi in Serampur, near Kolkata, situated on
the Ganges river bank209. All of the 209 soil samples col-
lected from other areas in and around Kolkata were nega-
tive for Histoplasma. Likewise, 523 soil samples collected
from chicken pens, bat-infested sites, and rat burrows in
India and Nepal were negative210,211. Besides, 236 samples
of avian excreta examined from Delhi and other parts of
India and 419 samples of bat guano/soil and avian excreta
examined from Delhi were also negative212, Randhawa
et al. (unpublished data). Considering that many of the
cases in our review gave history of exposure to bats in
old buildings, the need for further environmental stud-
ies, using molecular techniques, can hardly be overem-
phasized.
CONCLUDING REMARKS
Histoplasmosis poses a difficult diagnostic challenge
because of its highly protean clinical manifestations.
Being a primary pathogen, the etiologic agent, H. cap-
sulatum var capsulatum infects the immunocompetent
as well as immunocompromised patients. At room tem-
perature (25–30°C) in the laboratory, H. capsulatum var.
capsulatum appears as a slow growing mold, requiring
3–6 weeks for its cultivation. Although culture has been
considered as the gold standard among the laboratory
diagnostic tests, its value is limited by the fact that most
of the diagnostic microbiology laboratories in the hospi-
tals discard their cultures after 48–72 hours. Moreover,
Sabouraud agar routinely used as a mycological medium
is unsuitable for this fastidious fungal pathogen. To add
further to these difficulties, direct microscopy of wet
mounts or stained tissue sections/smears of clinical spec-
imens is lacking in sensitivity and requires expertise of
a cytopathologist/histopathologist for interpretation.
The afore-mentioned difficulties have been overcome
with the development of PCR but this molecular tech-
nology is not accessible to a vast majority of the diagnos-
tic centers in the Indian subcontinent. Further studies
applying the latest molecular techniques are strongly
indicated. Disseminated histoplasmosis is fatal unless
diagnosed early and treated with specific antifungal
78 Harbans S Randhawa and Harish C Gugnani
agents. Histoplasma capsulatum var. capsulatum has a
predilection for the reticuloendothelial system. Hence,
hepatosplenomegaly is a prominent feature of dissemi-
nated histoplasmosis.
A sharp rising trend in the number of histoplasmosis
cases reported in recent years is a notable observation.
This is attributable to increased awareness apart from
further development and expansion of mycological diag-
nostic facilities. Although its occurrence is widespread,
the burden of disease in the subcontinent remains unde-
termined due to paucity of systematic and comprehensive
studies, using recently introduced molecular techniques.
Considering that an overwhelming number of the cases
had not traveled abroad to the endemic areas of the dis-
ease in North America, the disease is endemic in the
subcontinent. However, supportive scientific evidence
like the demonstration of natural reservoirs of the patho-
gen and its occurrence in the local animal populations
remains largely unexplored. To sum up, our current
knowledge of the global geographic distribution of his-
toplasmosis and other systemic mycoses is far from ade-
quate. We strongly uphold the observation made in 1966
by Ainsworth213 that the available literature reflects the
distribution of mycologists more accurately than it does
the distribution of mycoses and their relative importance
in a given area.
ACKNOWLEDGMENT
The authors are grateful to Monika Sardana, Architect,
Gensler ARC, Houston, Texas (USA) for the preparation
of Fig. 1.
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