The mycological and molecular study of Pneumocystis jiroveci pneumonia among HIV and non-HIV immunocompromised patients hospitalized in pulmonary units in Guilan, northern Iran
-
Zahra Rafat
,
Keyhan Ashrafi
,
Seyed Jamal Hashemi
,
Elahe Sasani
,
Alireza Naserani
,
Hasti Kamali Sarvestani
,
Farshid Hashemi
Abstract
Background and Objectives: Pneumocystis jirovecii pneumonia (PJP) is a serious infection that usually affects those with a weak immune system. Since the prevalence of this infection in Iran and in the world is not clearly defined, the present study aimed to evaluate the incidence, clinical spectrum, and demographic characteristics of PJP among HIV and non-HIV immunocompromised patients.
Materials and Methods: Bronchoalveolar Lavage (BAL) specimens were obtained from 3 groups of immunocompromised patients, including acquired immunodeficiency syndrome (AIDS) patients, diabetic patients, and patients receiving immunosuppressive therapies. All were hospitalized in pulmonary units. The specimens were examined using microscopic methods (Giemsa and calcofluor white staining) and the nested-PCR technique based on mtLSU-rRNA gene.
Results: A total of 120 BAL samples were collected. From 12.5% (5 from 40) of HIV-infected patients, 5% (2 from 40) of patients receiving immunosuppressive therapies, and 2.5% (1 from 40) of diabetic patients Pneumocystis jiroveci was isolated. There was not any association between the prevalence of PJP and the patient's gender (p= 0.557) and age (p= 0.681). Fever and dyspnea (n=7, 87.5%), nonproductive cough and abnormal auscultation sound (n=5, 62.5%), and also chills and weight loss (n=2, 25%) were the documented clinical symptoms of PJP. Also, the results showed that none of the samples had positive results for P. jiroveci with microscopic tests while using the nested-PCR method 8 samples had positive results.
Conclusion: Since PJP often causes symptoms that are similar to other illnesses, such as the flu or tuberculosis, clinical and laboratory findings should be used simultaneously for making the final decision on drug administration.
1. Wang RJ, Miller RF, Huang L. Approach to fungal infections in human immunodeficiency virus–infected individuals: pneumocystis and beyond. Clin Chest Med 2017;38: 465-477.
2. Salzer HJF, Schäfer G, Hoenigl M, Günther G, Hoffmann C, Kalsdorf B, et al. Clinical, diagnostic, and treatment disparities between HIV-infected and non-HIV-infected immunocompromised patients with Pneumocystis jirovecii pneumonia. Respiration 2018;96: 52-65.
3. Guo F, Chen Y, Yang SL, Xia H, Li XW, Tong ZH. Pneumocystis pneumonia in HIV-infected and immunocompromised non-HIV infected patients: a retrospective study of two centers in China. PLoS One 2014;9(7): e101943.
4. Truong J, Ashurst JV. Pneumocystis (Carinii) Jiroveci Pneumonia. In: StatPearls. StatPearls Publishing, Treasure Island (FL); 2019.
5. Gaborit BJ, Tessoulin B, Lavergne RA, Morio F, Sagan C, Canet E, et al. Outcome and prognostic factors of Pneumocystis jirovecii pneumonia in immunocompromised adults: a prospective observational study. Ann Intensive Care 2019;9: 131.
6. Gigliotti F, Limper AH, Wright T. Pneumocystis. Cold Spring Harb Perspect Med 2014;4: a019828.
7. Arsić Arsenijevic V, Vyzantiadis TA, Mares M, Otasevic S, Tragiannidis A, Janic D. Diagnosis of Pneumocystis jirovecii pneumonia in pediatric patients in Serbia, Greece, and Romania. current status and challenges for collaboration. J Fungi (Basel) 2020;6: 49.
8. Bienvenu AL, Traore K, Plekhanova I, Bouchrik M, Bossard C, Picot S. Pneumocystis pneumonia suspected cases in 604 non-HIV and HIV patients. Int J Infect Dis 2016;46: 11-17.
9. Tandukar S, Singh N, Naseer MS, Chand R, Brunet H, Shokouh-Amiri HM. Role of serum (1, 3)-Β-D-glucan to screen for Pneumocystis pneumonia in kidney transplant recipients. Transplant Proc 2021;53: 1075-1079.
10. Karam MB, Mosadegh L. Extra-pulmonary Pneumocystis jiroveci infection: a case report. Braz J Infect Dis 2014;18: 681-685.
11. Anuradha, Sinha A. Extrapulmonary Pneumocystis carinii infection in an AIDS patient: a case report. Acta Cytol 2007; 51:599-601.
12. O'Neal CB, Ball SC. Splenic pneumocystosis: an atypical presentation of extrapulmonary pneumocystis infection. AIDS Read 2008;18: 503-508.
13. Panos GZ, Karydis I, Velakoulis SE, Falagas ME. Multi-skeletal Pneumocystis jiroveci (carinii) in an HIV-seropositive patient. Int J STD AIDS 2007;18: 134-137.
14. Siddiqi AE, Liu AY, Charville GW, Kunder CA, Uzel G, Sadighi Akha AA, et al. Disseminated Pneumocystis jirovecii infection with osteomyelitis in a patient with CTLA-4 haploinsufficiency. J Clin Immunol 2020; 40:412-414.
15. Wakefield AE. Pneumocystis carinii. Br Med Bull 2002;61: 175-188.
16. Cillóniz C, Dominedò C, Álvarez-Martínez MJ, Moreno A, García F, Torres A, et al. Pneumocystis pneumonia in the twenty-first century: HIV-infected versus HIV-uninfected patients. Expert Rev Anti Infect Ther 2019; 17:787-801.
17. Khodadadi H, Mirhendi H, Mohebali M, Kordbacheh P, Zarrinfar H, Makimura K. Pneumocystis jirovecii colonization in non-HIV-infected patients based on nested-PCR detection in bronchoalveolar lavage samples. Iran J Public Health 2013;42: 298-305.
18. Chabe M, Herbreteau V, Hugot JP, Bouzard N, Deruyter L, Morand S, et al. Pneumocystis carinii and Pneumocystis wakefieldiae in wild Rattus norvegicus trapped in Thailand. J Eukaryot Microbiol 2010;57: 213-217.
19. Sheikholeslami FM, Sadraei J, Farnia P, Forozandeh M, Kochak HE. Rate of Pneumocystis pneumonia in Iranian HIV+ patients with pulmonaryn infiltrates. Jundishapur J Microbiol 2013;6: 295-300.
20. Aboualigalehdari E, Mahmoudabadi AZ, Fatahinia M, Idani E. The prevalence of Pneumocystis jirovecii among patients with different chronic pulmonary disorders in Ahvaz, Iran. Iran J Microbiol 2015;7: 333-337.
21. Parian M, Fata A, Najafzadeh MJ, Rezaeitalab F. Molecular detection of Pneumocystis jirovecii using polymerase chain reaction in immunocompromised patients with pulmonary disorders in northeast of Iran. Curr Med Mycol 2015;1: 13-18.
22. Azoulay E, Bergeron A, Chevret S, Bele N, Schlemmer B, Menotti J. Polymerase chain reaction for diagnosing Pneumocystis pneumonia in non-HIV immunocompromised patients with pulmonary infiltrates. Chest 2009;135: 655-661.
23. Morris A, Lundgren JD, Masur H, Walzer PD, Hanson DL, Frederick T, et al. Current epidemiology of Pneumocystis pneumonia. Emerg Infect Dis 2004;10: 1713-1720.
24. Kaplan JE, Hanson D, Dworkin MS, Frederick T, Bertolli J, Lindegren ML, et al. Epidemiology of human immunodeficiency virus associated opportunistic infections in the United States in the era of highly active antiretroviral therapy. Clin Infect Dis 2000; 30 Suppl 1: S5-14.
25. Rafat Z, Hashemi SJ, Ashrafi K, Nikokar I, Jafari A, Foroushani AR, et al. Fungal isolates of the respiratory tract in symptomatic patients hospitalized in pulmonary units: a mycological and molecular epidemiologic study. J Multidiscip Healthc 2020;13: 661-669.
26. Rafat Z, Hashemi SJ, Ashrafi K, Nikokar I, Jafari A, Foroushani AR, et al. Epidemiology, laboratory diagnosis and clinical aspects of fungal pulmonary infections in 384 patients hospitalized in pulmonary units in Guilan province, Iran. Iran J Microbiol 2020;12: 353-363.
27. Calero-Bernal ML, Martin-Garrido I, Donazar-Ezcurra M, Limper AH, Carmona EM. Intermittent courses of corticosteroids also present a risk for Pneumocystis pneumonia in non-HIV patients. Can Respir J 2016;2016: 2464791.
28. Krajicek BJ, Thomas CF, Limper AH. Pneumocystis pneumonia: current concepts in pathogenesis, diagnosis, and treatment. Clin Chest Med 2009;30: 265-278.
29. Togashi Y, Masago K, Ito Y, Sakamori Y, Okuda C, Fukuhara A, et al. Pneumocystis jiroveci pneumonia and colonization in patients with advanced lung cancer. Oncol Lett 2013;5: 601-604.
30. Izadi M, Jafari NJ, Sadraei J, Poornaki AM, Rezavand B, Zarrinfar H, et al. The prevalence of Pneumocystis jiroveci in bronchoalveolar lavage specimens of lung transplant recipients examined by the Nested PCR. Jundishapur J Microbiol 2014;7(12): e13518.
31. Sheikhi N, Rafat Z, Zaker Boostan Abad S, Ahmadi SM, Azizian R, Hamidi M. Evaluating the clinical application of nested PCR in the diagnosis of fungal infections. New Zealand J Med Lab Sci 2020;74: 115-118.
32. Summah H, Zhu YG, Falagas ME, Vouloumanou EK, Qu JM. Use of real-time polymerase chain reaction for the diagnosis of Pneumocystis pneumonia in immunocompromised patients: a meta-analysis. Chin Med J (Engl) 2013;126: 1965-1973.
33. Wilson JW, Limper AH, Grys TE, Karre T, Wengenack NL, Binnicker MJ. Pneumocystis jirovecii testing by real-time polymerase chain reaction and direct examination among immunocompetent and immunosuppressed patient groups and correlation to disease specificity. Diagn Microbiol Infect Dis 2011;69: 145-152.
34. Mahmoodzadeh A, Hajia M, Rezaiemanesh MR. Comparison of Gomori’s methenamine silver method with PCR technique on oral swab, bronchoalveolar lavage and lung Ho-mogenate specimens in detection of pneumocystis. Iran J Parasitol 2008;3 :21-25.
35. Tang YW. Molecular diagnostics of atypical pneumonia. Acta pharmacol Sin 2003;24:1308-1313.
36. Procop GW, Haddad S, Quinn J, Wilson ML, Henshaw NG, Reller LB, et al. Detection of Pneumocystis jiroveci in respiratory specimens by four staining methods. J Clin Microbiol 2004;42: 3333-3335.
37. Abdollahi A, Kamali Sarvestani H, Rafat Z, Ghaderkhani S, Mahmoudi‐Aliabadi M, Jafarzadeh B, et al. The Association between the level of serum 25 (OH) vitamin D, obesity, and underlying diseases with the risk of developing COVID‐19 Infection: a case‐control study of hospitalized patients in Tehran, Iran. J Med Virol 2021;93: 2359-2364.
2. Salzer HJF, Schäfer G, Hoenigl M, Günther G, Hoffmann C, Kalsdorf B, et al. Clinical, diagnostic, and treatment disparities between HIV-infected and non-HIV-infected immunocompromised patients with Pneumocystis jirovecii pneumonia. Respiration 2018;96: 52-65.
3. Guo F, Chen Y, Yang SL, Xia H, Li XW, Tong ZH. Pneumocystis pneumonia in HIV-infected and immunocompromised non-HIV infected patients: a retrospective study of two centers in China. PLoS One 2014;9(7): e101943.
4. Truong J, Ashurst JV. Pneumocystis (Carinii) Jiroveci Pneumonia. In: StatPearls. StatPearls Publishing, Treasure Island (FL); 2019.
5. Gaborit BJ, Tessoulin B, Lavergne RA, Morio F, Sagan C, Canet E, et al. Outcome and prognostic factors of Pneumocystis jirovecii pneumonia in immunocompromised adults: a prospective observational study. Ann Intensive Care 2019;9: 131.
6. Gigliotti F, Limper AH, Wright T. Pneumocystis. Cold Spring Harb Perspect Med 2014;4: a019828.
7. Arsić Arsenijevic V, Vyzantiadis TA, Mares M, Otasevic S, Tragiannidis A, Janic D. Diagnosis of Pneumocystis jirovecii pneumonia in pediatric patients in Serbia, Greece, and Romania. current status and challenges for collaboration. J Fungi (Basel) 2020;6: 49.
8. Bienvenu AL, Traore K, Plekhanova I, Bouchrik M, Bossard C, Picot S. Pneumocystis pneumonia suspected cases in 604 non-HIV and HIV patients. Int J Infect Dis 2016;46: 11-17.
9. Tandukar S, Singh N, Naseer MS, Chand R, Brunet H, Shokouh-Amiri HM. Role of serum (1, 3)-Β-D-glucan to screen for Pneumocystis pneumonia in kidney transplant recipients. Transplant Proc 2021;53: 1075-1079.
10. Karam MB, Mosadegh L. Extra-pulmonary Pneumocystis jiroveci infection: a case report. Braz J Infect Dis 2014;18: 681-685.
11. Anuradha, Sinha A. Extrapulmonary Pneumocystis carinii infection in an AIDS patient: a case report. Acta Cytol 2007; 51:599-601.
12. O'Neal CB, Ball SC. Splenic pneumocystosis: an atypical presentation of extrapulmonary pneumocystis infection. AIDS Read 2008;18: 503-508.
13. Panos GZ, Karydis I, Velakoulis SE, Falagas ME. Multi-skeletal Pneumocystis jiroveci (carinii) in an HIV-seropositive patient. Int J STD AIDS 2007;18: 134-137.
14. Siddiqi AE, Liu AY, Charville GW, Kunder CA, Uzel G, Sadighi Akha AA, et al. Disseminated Pneumocystis jirovecii infection with osteomyelitis in a patient with CTLA-4 haploinsufficiency. J Clin Immunol 2020; 40:412-414.
15. Wakefield AE. Pneumocystis carinii. Br Med Bull 2002;61: 175-188.
16. Cillóniz C, Dominedò C, Álvarez-Martínez MJ, Moreno A, García F, Torres A, et al. Pneumocystis pneumonia in the twenty-first century: HIV-infected versus HIV-uninfected patients. Expert Rev Anti Infect Ther 2019; 17:787-801.
17. Khodadadi H, Mirhendi H, Mohebali M, Kordbacheh P, Zarrinfar H, Makimura K. Pneumocystis jirovecii colonization in non-HIV-infected patients based on nested-PCR detection in bronchoalveolar lavage samples. Iran J Public Health 2013;42: 298-305.
18. Chabe M, Herbreteau V, Hugot JP, Bouzard N, Deruyter L, Morand S, et al. Pneumocystis carinii and Pneumocystis wakefieldiae in wild Rattus norvegicus trapped in Thailand. J Eukaryot Microbiol 2010;57: 213-217.
19. Sheikholeslami FM, Sadraei J, Farnia P, Forozandeh M, Kochak HE. Rate of Pneumocystis pneumonia in Iranian HIV+ patients with pulmonaryn infiltrates. Jundishapur J Microbiol 2013;6: 295-300.
20. Aboualigalehdari E, Mahmoudabadi AZ, Fatahinia M, Idani E. The prevalence of Pneumocystis jirovecii among patients with different chronic pulmonary disorders in Ahvaz, Iran. Iran J Microbiol 2015;7: 333-337.
21. Parian M, Fata A, Najafzadeh MJ, Rezaeitalab F. Molecular detection of Pneumocystis jirovecii using polymerase chain reaction in immunocompromised patients with pulmonary disorders in northeast of Iran. Curr Med Mycol 2015;1: 13-18.
22. Azoulay E, Bergeron A, Chevret S, Bele N, Schlemmer B, Menotti J. Polymerase chain reaction for diagnosing Pneumocystis pneumonia in non-HIV immunocompromised patients with pulmonary infiltrates. Chest 2009;135: 655-661.
23. Morris A, Lundgren JD, Masur H, Walzer PD, Hanson DL, Frederick T, et al. Current epidemiology of Pneumocystis pneumonia. Emerg Infect Dis 2004;10: 1713-1720.
24. Kaplan JE, Hanson D, Dworkin MS, Frederick T, Bertolli J, Lindegren ML, et al. Epidemiology of human immunodeficiency virus associated opportunistic infections in the United States in the era of highly active antiretroviral therapy. Clin Infect Dis 2000; 30 Suppl 1: S5-14.
25. Rafat Z, Hashemi SJ, Ashrafi K, Nikokar I, Jafari A, Foroushani AR, et al. Fungal isolates of the respiratory tract in symptomatic patients hospitalized in pulmonary units: a mycological and molecular epidemiologic study. J Multidiscip Healthc 2020;13: 661-669.
26. Rafat Z, Hashemi SJ, Ashrafi K, Nikokar I, Jafari A, Foroushani AR, et al. Epidemiology, laboratory diagnosis and clinical aspects of fungal pulmonary infections in 384 patients hospitalized in pulmonary units in Guilan province, Iran. Iran J Microbiol 2020;12: 353-363.
27. Calero-Bernal ML, Martin-Garrido I, Donazar-Ezcurra M, Limper AH, Carmona EM. Intermittent courses of corticosteroids also present a risk for Pneumocystis pneumonia in non-HIV patients. Can Respir J 2016;2016: 2464791.
28. Krajicek BJ, Thomas CF, Limper AH. Pneumocystis pneumonia: current concepts in pathogenesis, diagnosis, and treatment. Clin Chest Med 2009;30: 265-278.
29. Togashi Y, Masago K, Ito Y, Sakamori Y, Okuda C, Fukuhara A, et al. Pneumocystis jiroveci pneumonia and colonization in patients with advanced lung cancer. Oncol Lett 2013;5: 601-604.
30. Izadi M, Jafari NJ, Sadraei J, Poornaki AM, Rezavand B, Zarrinfar H, et al. The prevalence of Pneumocystis jiroveci in bronchoalveolar lavage specimens of lung transplant recipients examined by the Nested PCR. Jundishapur J Microbiol 2014;7(12): e13518.
31. Sheikhi N, Rafat Z, Zaker Boostan Abad S, Ahmadi SM, Azizian R, Hamidi M. Evaluating the clinical application of nested PCR in the diagnosis of fungal infections. New Zealand J Med Lab Sci 2020;74: 115-118.
32. Summah H, Zhu YG, Falagas ME, Vouloumanou EK, Qu JM. Use of real-time polymerase chain reaction for the diagnosis of Pneumocystis pneumonia in immunocompromised patients: a meta-analysis. Chin Med J (Engl) 2013;126: 1965-1973.
33. Wilson JW, Limper AH, Grys TE, Karre T, Wengenack NL, Binnicker MJ. Pneumocystis jirovecii testing by real-time polymerase chain reaction and direct examination among immunocompetent and immunosuppressed patient groups and correlation to disease specificity. Diagn Microbiol Infect Dis 2011;69: 145-152.
34. Mahmoodzadeh A, Hajia M, Rezaiemanesh MR. Comparison of Gomori’s methenamine silver method with PCR technique on oral swab, bronchoalveolar lavage and lung Ho-mogenate specimens in detection of pneumocystis. Iran J Parasitol 2008;3 :21-25.
35. Tang YW. Molecular diagnostics of atypical pneumonia. Acta pharmacol Sin 2003;24:1308-1313.
36. Procop GW, Haddad S, Quinn J, Wilson ML, Henshaw NG, Reller LB, et al. Detection of Pneumocystis jiroveci in respiratory specimens by four staining methods. J Clin Microbiol 2004;42: 3333-3335.
37. Abdollahi A, Kamali Sarvestani H, Rafat Z, Ghaderkhani S, Mahmoudi‐Aliabadi M, Jafarzadeh B, et al. The Association between the level of serum 25 (OH) vitamin D, obesity, and underlying diseases with the risk of developing COVID‐19 Infection: a case‐control study of hospitalized patients in Tehran, Iran. J Med Virol 2021;93: 2359-2364.
| Files | ||
| Issue | Vol 13 No 4 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v13i4.6977 | |
| Keywords | ||
| Pneumonia; Pneumocystis; Human immunodeficiency virus; Diabetes mellitus; Immunosuppression; Epidemiology; Iran | ||
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How to Cite
1.
Rafat Z, Ashrafi K, Hashemi SJ, Sasani E, Naserani A, Kamali Sarvestani H, Hashemi F. The mycological and molecular study of Pneumocystis jiroveci pneumonia among HIV and non-HIV immunocompromised patients hospitalized in pulmonary units in Guilan, northern Iran. Iran J Microbiol. 2021;13(4):518-524.
