© JAPI • VOL. 53 • MAY 2005 www.japi.org 437
Original Article
Pneumocystis  Carinii  Pneumonia  in  HIV  Infected
Patients from  Mumbai
ZF Udwadia*, Amita V Doshi*, Anita S Bhaduri**
Abstract
Objective : Pneumocystis carinii pneumonia (PCP) is believed to be rare in the developing world and no large
prospective Indian series have been reported to date. The present study was conducted to study the clinical
profile and outcome of PCP in patients with HIV infection.
Methods : All HIV positive patients with PCP admitted over 4 years (2000-2003) to a tertiary referral centre in
Mumbai were prospectively studied.
Results : There were 38 patients with proven PCP from 300 HIV admissions. The patients with PCP were
predominantly male (M : F = 5.4 : 1), with a mean age of 40.1 years. The median CD4 count of the PCP group
was 96 cells/µL. Bronchoscopy was needed to make a definitive diagnosis in 17 of the 38 patients. PCP co-
existed with tuberculosis in 4 of the 38 patients. The mortality of the group was high at 15.8% with all patients
needing ventilatory support dying.
Conclusions : PCP is not an uncommon infection in Indians with advanced HIV. Lack of recognition has
probably been responsible for the absence of any large series from this country. In our series of hospitalised
HIV positive patients, PCP was the second commonest pulmonary disease after tuberculosis accounting for
32% of pulmonary admissions and 13 % of all HIV positive admissions. ©
METHODS
All HIV positive admissions at our private hospital
which is a tertiary referral centre had their clinical data
prospectively collected over a 4 year period from 2000-
2003. All patients proven to have PCP were included for
separate analysis. From each patients’ records we
obtained the following data: (1) age, sex, symptoms,
signs, chest radiograph, high resolution computed
tomogram (HRCT) of the chest features, arterial blood
gas, lactate dehydrogenase (LDH) and CD4 count. (2)
Methods needed to make a diagnosis of PCP;
spontaneously expectorated sputum, induced sputum,
bronchoalveolar lavage (BAL) fluid or transbronchial
lung  biopsy. (3) Details of treatment received by each
patient. (4) Mortality in hospital.
All PCP diagnosis was performed by a single
cytologist using an indirect immunofluorescence
staining technique on sputum or BAL. The primary
antibody was a mouse monoclonal anti-pneumocystic
carinii from DAKOPATTS with a fluorescein
isothiocyanate conjugated secondary rabbit anti-mouse
antibody. Direct sputum smears and cytospin smears of
BAL fluid were made, air dried, fixed in methanol-H2O2
and stained in a humidified chamber at room
temperature. The smears were mounted in glycerine and
viewed under a Zeiss fluorescent microscope. Apple
Department of Chest Medicine* and Pathology**, PD Hinduja
National Hospital and Medical Research Centre, Veer Savarkar
Marg, Mahim, Mumbai 400016.
Received : 26.6.2004; Accepted : 28.3.2005
INTRODUCTION
Tuberculosis (TB) and bacterial pneumonia dominate
first decade of the epidemic, Pneumocystis carinii
pneumonia  (PCP) was rarely reported from the
developing world and authors concluded that PCP was
uncommon in the developing world.1  Recent reports,
however have noted a significantly higher prevalence
of PCP among HIV-infected patients in Sub-Saharan
Africa.2,3  Fisk et al in their comprehensive recent review
of PCP in the developing world failed to find a single
PCP series from India.4  Our study prospectively looked
at all HIV positive patients hospitalised at a tertiary
referral hospital with an active pulmonary service. From
the 300 admissions over a 4 year period (2000-2003), we
analysed the profile of the 38 patients with
microbiologically confirmed PCP. This is the only large
prospective PCP series from the Indian subcontinent and
confirms that PCP is not uncommon here but has
probably been under-recognized to date.
438 www.japi.org © JAPI • VOL. 53 • MAY 2005
green membranous-stained bodies of about 5-6 µ were
reported positive for Pneumocystis carinii either singly or
in clusters. Primary antibody was used in 1:2 dilution
and the secondary antibody as a 1:20 dilution.5  This
antibody reacts with an antigenic epitope of human
Pneumocystis carinii that is resistant to fixation in formalin
and ethanol extraction. It does not react with
Toxoplasma, Candida, Aspergillus or Cryptosporidium
species.6  Transbronchial lung biopsies were stained by
Grocott’s methanamine silver stain.
RESULTS
Thirty eight patients with PCP were obtained from
the 300 HIV positive patients hospitalised over this 4
year period (2000-2003). PCP accounted for 13% of all
HIV hospitalisations. If the HIV positive patients with
pulmonary manifestations were analysed as a separate
group (120 patients), PCP accounted for 32% of all
pulmonary admissions and was second only to
pulmonary TB which accounted for 40% of all
pulmonary admissions. PCP was more frequent than
bacterial pneumonia which was the 3rd most common
pulmonary cause of admission.
The mean age of the PCP patients was 40.1 years (18-
62 years) with a male to female sex ratio of 5.4:1 (32
males and 6 females). Cough was the commonest
symptom (27/38), followed by dyspnoea (22/38) and
fever (20/38). Only 1 patient was asymptomatic when
the diagnosis of PCP was established.
The commonest respiratory sign was a respiratory
rate > 26/min which was found in 25/38 patients with
PCP. The respiratory rate was > 30/min in 15/38
patients. Fine crackles were found in 19/38 and ronchi
in 6/38 patients. 9/38 patients were normal on
examination.
The chest radiograph was reported as compatible
with PCP with bilateral interstitial shadows in 29
patients. Chest radiographs were normal in 8 patients
(21%) and atypical radiographic appearances (a solitary
pulmonary nodule) were present in only 1 patient. HRCT
chest scans were done in 18 of the 38 patients. Diffuse
ground glass and nodules were present in HRCT chest
scans of 17 of these 18 patients and were reported to be
“highly suggestive of PCP”.
Nineteen of the 38 patients had a PaO2 < 70 mm Hg.
LDH was checked in only 13 of the 38 patients and was
found to be elevated in 12. A rising LDH level was found
to be an important prognostic marker in all the 6 patients
who died in our series.
The median CD4 count of the 38 PCP patients was 96
cells/µL in contrast to a median CD4 of 137 cells/µL in
the TB-HIV patients. Whilst sputum (direct or induced)
gave a microbiological diagnosis in 21 of the 38 patients,
more invasive tests were needed to establish the diagnosis
in the other 17 patients. Thus the diagnosis was made at
bronchoscopy from BAL fluid in 15 patients and from
transbronchial biopsy alone in 2 patients where sputum
and BAL failed to identify PCP. Four patients (10.5%)
had Mycobacterium tuberculosis isolated with their PCP
in sputum or BAL samples.
All patients were initially treated with trimethoprim-
sulfamethoxazole (TMP-SMX). Six patients however
needed to be switched to a clindamycin-primaquine
combination because TMP-SMX proved ineffective (2
patients) or toxic (severe rash in 2, nephrotoxicity in 2).
Steroids were used along with initial antibiotics in 19
PCP patients whose PaO2 was less than 70 mm Hg . Six
patients required mechanical ventilation for worsening
respiratory failure, all of whom died.
DISCUSSION
In the first decade of the HIV epidemic, PCP was
considered an uncommon pathogen in the developing
world. In studies from Zambia7, Tanzania8 and Rwanda9,
PCP accounted for 3-9% of all hospitalised HIV patients
with pneumonia. The picture has changed in the last
few years and more recent studies using sensitive
methods to diagnose PCP have shown that PCP accounts
for a greater percentage of cases of pneumonia among
African adult HIV infected patients than noted in earlier
reports. More recent studies (1990-1993) from South
Africa2 and Zimbabwe3 using more sophisticated
diagnostic techniques like BAL and monoclonal
antibodies revealed rates of PCP of 43% and 33%
respectively.
Studies from Asia have been even less frequent. Fisk
et al in their comprehensive review of PCP in the
developing world found only a few Asian studies from
Thailand10, South Korea11, Taiwan12 and The
Philippines13 but none from India. We conducted a more
detailed search focusing on PCP in Indian journals and
found that Indian data on PCP was restricted to a few
isolated case reports or small autopsy series but no large
prospective series existed. The relevant Indian data is
summarized here. The first case report on PCP in India
was from Udwadia et al in a single case in 1987.14  This
patient had advanced immunosuppression and died
despite TMP-SMX and ventilatory support. In the 17
years since this first description of PCP, this disease has
been considered rare in India as is evident from the
scanty data available. There are a number of small PCP
series of 2-5 cases written up mainly as case reports in
Indian medical journals.15,16,17  Some series reported larger
numbers but included patients where PCP was
suspected on clinical and radiological grounds but not
proven microbiologically.18
There are some autopsy series and here mention must
be made of work by Lanjewar from a large public hospital
in Mumbai. He found evidence of PCP in only 7 of 143
(5%) lung autopsies.19   In his series, as in most autopsy
series from this country, TB dominated, accounting for
60% of all cases. In the only other autopsy series reported
© JAPI • VOL. 53 • MAY 2005 www.japi.org 439
from our country, Deshmukh from Pune reported 5 cases
of PCP out of 34 AIDS autopsies20, whilst Santosh
reported only 2 cases of PCP from 47 AIDS autopsies.21
Kumarasamy in his large cohort of 594 HIV patients
from a tertiary referral centre in southern India reported
36 patients (6.1%) with PCP.22  However details of these
PCP patients as a group have not been discussed.
There have been various postulated reasons for the
lack of PCP reports from India and the developing world
including the absence of PCP from the environment,
differences in host susceptibility to the organism and
death at an earlier stage from more pathogenic organisms
like Mycobacterium tuberculosis.23  In our opinion it is
simply delayed recognition and lack of diagnostic
facilities that are responsible for this under-reporting.24
As many as 45% of our patients would not have been
diagnosed if sputum alone had been tested. The
bronchoscopic techniques required to make a firm
diagnosis of PCP are not available in the majority of
Indian hospitals. The availability of expensive
immunofluorescent staining techniques, an experienced
cytologist and the presence of a CT scanner are other
luxuries beyond the reach of the average Indian hospital
and these are the likely reasons for under-reporting of
PCP from the Indian subcontinent.
We found a high prevalence of PCP in our series,
accounting for 32% of pulmonary admissions and 13%
of all hospitalized HIV positive admissions. The other
interesting features of the PCP patients in our series are
the co-existence of TB and PCP noted in 4 (10.5%) of the
patients. Other studies from the developing world have
reported PCP and TB co-infection in 13-66% of their
patients.4  The mortality of our patients was also higher
than in Western series with 15.8% of PCP patients dying.
This trend towards higher mortality has been noted in
other series from the developing world and may be linked
to lack of recognition leading to late diagnosis and
treatment.
In conclusion, HIV-AIDS is gaining a firm foothold in
India. With at least 4 million Indians already infected,
India houses the world’s second largest HIV positive
population. Despite this there is almost no Indian data
available on PCP, one of the commonest AIDS defining
infections globally, from a country with a population of
1 billion. This study attempts to redress this imbalance
and is the only large PCP series from India. It is almost
certainly lack of awareness coupled with lack of access
to special diagnostic tools that is responsible for the
absence of data on PCP from the Indian subcontinent.
REFERENCES
1. Walzer P Pneumocystosis. In:  Guerrant RL, Walker DH,
Weller PF eds. Tropical infectious diseases: principles,
pathogens, and practice. Philadelphia: Churchill Livingstone,
1999:673-84.
2. Mohamed AG, Murray J Klempman GR, Richards G, Feldman
C, Levy NT, et al. Pneumocystis carinii pneumonia in HIV
infected patients from South Africa.  East Afr Med J
1999;76:80-4.
3. Malin AS, Gwanzura LKZ, Klein S, Robertson VJ, Musvaire
P, Mason PR. Pneumocystis carinii pneumonia in Zimbabwe.
Lancet 1995;346:1258-61.
4. Fisk DT, Meshnick S, Kazanjian PH. Pneumocystis carinii
pneumonia in patients in the developing world who have
Acquired Immunodeficiency Syndrome. Clin Infect Dis
2003;36:70-8.
5. Linder E, Lundin L, Vorma H. Detection of P. Carinii in lung
derived samples using monoclonal antibodies to an 82kDa
parasitic component. J Immunol Methods 1987;98:57-62.
6. Elvin KM, Bjorkman A, Linder E, Heurlin N, Hjerpe A. P.
carinii pneumonia; detection of parasites in sputum and
bronchoalveolar lavage fluid by monoclonal antibodies. Br
Med J 1988;297:381-4.
7. Machiels G, Urban MI. Pneumocystis carinii as a cause of
pneumonia in HIV infected patients in Lusaka, Zambia.
Trans R Soc Trop Med Hyg 1992;86:399-400.
8. Atzori C, Bruno A, Chichino G, Gatti S, Scaglia M.
Pneumocystis carinii pneumonia and tuberculosis in
Tanzanian patients infected with HIV. Trans R Soc Trop Med
Hyg 1993;87:55-6.
9. Batungwanayo J, Taelnan H, Lucas SB, Bogaerts J, Alard D,
Kagame A et al. Pulmonary disease associated with HIV in
Kigali, Rwanda. Am J Respir Crit Care Med 1994;149:1591-6.
10. Mootsikapun P, Chetchotisakd P, Intarapoka B. Pulmonary
infections in HIV infected patients.  J Med Assoc Thai
1996;79:477-85.
11. Oh MD, Park SW, Kim HB, Kim US, Kim NJ, Choi HJ et al.
Spectrum of opportunistic infections and malignancies in
patients with human immunodeficiency virus infection in
South Korea. Clin Infect Dis 1999;29:1524-8.
12. Hsiao CH, Huang SH, Huang SF, Song CL, Su IJ, Chuang
CY et al. Autopsy findings on patients with AIDS in Taiwan.
J Microbiol Immunol Infect 1997;30:145-59.
13. Manaloto CR, Perrault JG, Caringal LT, Santiago EG, Wignall
FS, Gonzales VL et al. Natural history of HIV infection in
Filipino female commercial sex workers. J Acquir Immune
Defic Syndr 1994;7:1157-68.
14. Udwadia FE, Advani S, Jain M, Gupta R. Acquired
Immunodeficiency Syndrome- a study of two case reports
with manifest HIV infection.  J Assoc Physicians India
1987;35:454-7.
15. Singh YN, Singh S, Rattan A, Ray JC, Sriniwas TR, Kumar A
et al. Pneumocystis carinii infection in patients of AIDS in
India. J Assoc Physicians India 1993;41:41-2.
16. Bijur S, Menon L, Iyer E, Deshpande J, Sivaraman A,
Vaideeswar P et al. Pneumocystis carinii pneumonia in human
immunodeficiency virus infected patients in Bombay :
diagnosed by bronchoalveolar lavage cytology and
transbronchial biopsy. Ind J Chest Dis Allied Sci 1996;38:227-
33.
17. Arora VK, Tumbanatham A, Kumar SV, Ratnakar C.
Pneumocystis carinii pneumonia simulating as pulmonary
tuberculosis in AIDS. Ind J Chest Dis Allied Sci 1996;38:253-
58.
18. Rani NU, Reddy VVR, Kumar AP, Kumar KVVV, Babu GR,
Rao DB. Clinical profile of Pneumocystis carinii pneumonia
in HIV infected persons. Ind J Tub 2000;47:93-6.
19. Lanjewar DN. Pulmonary pathology in AIDS: an autopsy
study from Mumbai. HIV Medicine 2001;2:266-71.
20. Deshmukh SD, Ghaisas MV, Rane SR, Bapat VM.
Pneumocystis carinii pneumonia and its association with
other opportunistic infections in AIDS - an autopsy report
of five cases. Indian J Pathol Microbiol 2003;46:207-11.
440 www.japi.org © JAPI • VOL. 53 • MAY 2005
21. Santosh V, Yasha TC, Panda KM. Pathology of AIDS – study
from a neuropsychiatric centre from South India. Ann Ind
Acad Neurol 1998;1:71-82.
22. Kumarasamy N, Solomon S, Flanigan TP, Hemalatha R,
Thyagrajan SP, Mayer KH. Natural history of human
immunodeficiency virus disease in Southern India. Clin Infect
Dis 2003;36:79-85.
23. Daley CL. Pulmonary infections in the tropics: impact of
HIV infection. Thorax 1994;49:370-8.
24. Udwadia ZF. Pneumocystis pneumonia: taming the beast.
The Indian Practitioner 1999;52:593-4.
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