Skip to main content

Serious fungal infections in Pakistan

Abstract

The true burden of fungal infection in Pakistan is unknown. High-risk populations for fungal infections [tuberculosis (TB), diabetes, chronic respiratory diseases, asthma, cancer, transplant and human immunodeficiency virus (HIV) infection] are numerous. Here, we estimate the burden of fungal infections to highlight their public health significance. Whole and at-risk population estimates were obtained from the WHO (TB), BREATHE study (COPD), UNAIDS (HIV), GLOBOCAN (cancer) and Heartfile (diabetes). Published data from Pakistan reporting fungal infections rates in general and specific populations were reviewed and used when applicable. Estimates were made for the whole population or specific populations at risk, as previously described in the LIFE methodology. Of the 184,500,000 people in Pakistan, an estimated 3,280,549 (1.78%) are affected by a serious fungal infection, omitting all cutaneous infection, oral candidiasis and allergic fungal sinusitis, which we could not estimate. Compared with other countries, the rates of candidaemia (21/100,000) and mucormycosis (14/100,000) are estimated to be very high, and are based on data from India. Chronic pulmonary aspergillosis rates are estimated to be high (39/100,000) because of the high TB burden. Invasive aspergillosis was estimated to be around 5.9/100,000. Fungal keratitis is also problematic in Pakistan, with an estimated rate of 44/100,000. Pakistan probably has a high rate of certain life- or sight-threatening fungal infections.

This is a preview of subscription content, access via your institution.

References

  1. Sultan F, Khan A (2013) Infectious diseases in Pakistan: a clear and present danger. Lancet 381:2138–2140

    Article  PubMed  Google Scholar 

  2. Jafar TH, Haaland BA, Rahman A, Razzak JA, Bilger M, Naghavi M et al (2013) Non-communicable diseases and injuries in Pakistan: strategic priorities. Lancet 381:2281–2290

    Article  PubMed  Google Scholar 

  3. Brown GD, Denning DW, Gow NAR, Levitz SM, Netea MG, White TC (2012) Hidden killers: human fungal infections. Sci Transl Med 4:165rv13. doi:10.1126/scitranslmed.3004404

    Article  PubMed  Google Scholar 

  4. WHO, Pakistan Office, and Heartfile (2004) National Action Plan for prevention and control of non-communicable diseases and health promotion in Pakistan. Islamabad, Pakistan: tripartite collaboration of the Ministry of Health, Government of Pakistan. Available online at: http://www.physicalactivityplan.org/resources/Pakistan.pdf

  5. World Health Organization (WHO) (2015) Global tuberculosis report 2015. Available online at: http://apps.who.int/iris/bitstream/10665/191102/1/9789241565059_eng.pdf

  6. Nishtar S (2007) Health indicators of Pakistan—Gateway Paper II. Islamabad, Pakistan: Heartfile; 2007. Available online at: http://www.heartfile.org/pdf/GWP-II.pdf

  7. Ministry of National Health Services, Regulation and Coordination, Government of Pakistan (2015) Pakistan Global AIDS Response Progress Report (GARPR) 2015. Country progress report Pakistan,. National AIDS Control Program. Available online at: http://www.unaids.org/sites/default/files/country/documents/PAK_narrative_report_2015.pdf

  8. Baqi S, Kayani N, Khan JA (1999) Epidemiology and clinical profile of HIV/AIDS in Pakistan. Trop Doct 29:144–148

    CAS  Article  PubMed  Google Scholar 

  9. Luxmi S, Salahuddin N, Herekar F, Sultan F, Irshad H, Ansari NB (2012) Clinical and demographic pattern of HIV positive patients in two tertiary care hospitals in Pakistan: 20 years experience. Inf Dis J Pak 21:485–491

    Google Scholar 

  10. International Agency for Research on Cancer (2012) GLOBOCAN 2012. Estimated cancer incidence, mortality and prevalence worldwide in 2012. Available online at: http://globocan.iarc.fr/

  11. Mahboob A, Sultan F, Raza A, Khan SA (2014) Culture positive meningitis in cancer patients; an eleven-year experience. Inf Dis J Pak 23:650–653

    Google Scholar 

  12. Azfar NA, Khan AR, Zia MA, Humayun A, Malik LM, Jahangir M (2016) Frequency of mucocutaneous manifestations in HIV positive Pakistani patients. J Pakistan Assoc Dermatol 21(3):149–153

    Google Scholar 

  13. National Institute of Population Studies (NIPS) and ICF International (2013) Pakistan Demographic and Health Survey 2012–13. NIPS and ICF International, Islamabad, Pakistan, and Calverton, Maryland, USA

  14. Chakrabarti A, Sood P, Rudramurthy SM, Chen S, Kaur H, Capoor M et al (2015) Incidence, characteristics and outcome of ICU-acquired candidemia in India. Intensive Care Med 41:285–295. doi:10.1007/s00134-014-3603-2

    Article  PubMed  Google Scholar 

  15. Global Action for Funds for Fungal Infections (GAFFI) (2015) India has one of the highest rates of Candida bloodstream infection in the world. Available online at: http://www.gaffi.org/india-has-one-of-the-highest-rates-of-candida-bloodstream-infection-in-the-world/)

  16. Tageldin MA, Nafti S, Khan JA, Nejjari C, Beji M, Mahboub B et al (2012) Distribution of COPD-related symptoms in the Middle East and North Africa: results of the BREATHE study. Respir Med 106:S25–S32

    Article  PubMed  Google Scholar 

  17. Xu H, Li L, Huang WJ, Wang LX, Li WF, Yuan WF (2012) Invasive pulmonary aspergillosis in patients with chronic obstructive pulmonary disease: a case control study from China. Clin Microbiol Infect 18:403–408

    CAS  Article  PubMed  Google Scholar 

  18. Yan X, Li M, Jiang M, Zou LQ, Luo F, Jiang Y (2009) Clinical characteristics of 45 patients with invasive pulmonary aspergillosis: retrospective analysis of 1711 lung cancer cases. Cancer 115:5018–5025

    Article  PubMed  Google Scholar 

  19. Bhurgri Y, Bhurgri A, Hassan SH, Zaidi SHM, Rahim A, Sankaranarayanan R et al (2000) Cancer incidence in Karachi, Pakistan: first results from Karachi Cancer Registry. Int J Cancer 85:325–329

    CAS  Article  PubMed  Google Scholar 

  20. Caira M, Girmenia C, Fadda RM, Mitra ME, Picardi M, Van Lint MT et al (2008) Invasive fungal infections in patients with acute myeloid leukemia and in those submitted to allogeneic hemopoietic stem cell transplant: who is at highest risk? Eur J Haematol 81:242–243. doi:10.1111/j.1600-0609.2008.01096.x

    Article  PubMed  Google Scholar 

  21. Chakrabarti A, Sood P, Denning DW (2013) Estimating fungal infection burden in India using computational models: mucormycosis burden as a case study. Abstract presented at the 23rd European Congress of Clinical Microbiology and Infectious Diseases (ECCMID), Berlin, Germany, April 2013

  22. Foxman B, Muraglia R, Dietz JP, Sobel JD, Wagner J (2013) Prevalence of recurrent vulvovaginal candidiasis in 5 European countries and the United States: results from an internet panel survey. J Low Genit Tract Dis 17:340–345

    Article  PubMed  Google Scholar 

  23. To T, Stanojevic S, Moores G, Gershon AS, Bateman ED, Cruz AA et al (2012) Global asthma prevalence in adults: findings from the cross-sectional world health survey. BMC Public Health 12:204. http://www.biomedcentral.com/1471-2458/12/204

    Article  PubMed  PubMed Central  Google Scholar 

  24. Agarwal R, Denning DW, Chakrabarti A (2014) Estimation of the burden of chronic and allergic aspergillosis in India. PLoS One 9:e114745. doi:10.1371/journal.pone.0114745

    Article  PubMed  PubMed Central  Google Scholar 

  25. Mei-Zahav M, Durie P, Zielenski J, Solomon M, Tullis E, Tsui L-C et al (2005) The prevalence and clinical characteristics of cystic fibrosis in South Asian Canadian immigrants. Arch Dis Child 90:675–679

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. Maturu VN, Agarwal R (2015) Prevalence of Aspergillus sensitization and allergic bronchopulmonary aspergillosis in cystic fibrosis: systematic review and meta-analysis. Clin Exp Allergy 45:1765–1778

    CAS  Article  PubMed  Google Scholar 

  27. Denning DW, Pleuvry A, Cole DC (2011) Global burden of chronic pulmonary aspergillosis as a sequel to pulmonary tuberculosis. Bull World Health Organ 89:864–872

    Article  PubMed  PubMed Central  Google Scholar 

  28. Anantham D, Ong SJ, Chuah KL, Fook-Chong S, Hsu A, Eng P (2007) Sarcoidosis in Singapore: epidemiology, clinical presentation and ethnic differences. Respirology 12:355–360

    Article  PubMed  Google Scholar 

  29. Denning DW, Pleuvry A, Cole DC (2013) Global burden of chronic pulmonary aspergillosis complicating sarcoidosis. Eur Respir J 41:621–626. doi:10.1183/09031936.00226911

    Article  PubMed  Google Scholar 

  30. Cao J, Yang Y, Yang W, Wu R, Xiao X, Yuan J et al (2014) Prevalence of infectious keratitis in Central China. BMC Ophthalmol 14:43. doi:10.1186/1471-2415-14-43

    Article  PubMed  PubMed Central  Google Scholar 

  31. Riaz Q, Fawwad U, Bhatti N, Rehman A, Hasan M (2013) Epidemiology of microbial keratitis in a tertiary care center in Karachi. Pak J Ophthalmol 29:94–99

    Google Scholar 

  32. Narsani AK, Jatoi SM, Khanzada MA, Lohana MK (2010) Etiological diagnosis of microbial keratitis. J Coll Physicians Surg Pak 20:604–607

    PubMed  Google Scholar 

  33. Hussain I, Khan BS, Soni M, Iqbal M, Habibullah (2012) Non-viral microbial keratitis: etiology, clinical features and visual outcome. J Coll Physicians Surg Pak 22:151–154

    PubMed  Google Scholar 

  34. van de Sande WWJ (2013) Global burden of human mycetoma: a systematic review and meta-analysis. PLoS Negl Trop Dis 7:e2550. doi:10.1371/journal.pntd.0002550

    Article  PubMed  PubMed Central  Google Scholar 

  35. Khan A, Jamil B, Ali R, Sultan S (2009) Tuberculosis and cryptococcal meningitis in a setting with high TB and low HIV prevalence. J Coll Physicians Surg Pak 19:487–491

    PubMed  Google Scholar 

  36. Sarwar Zubairi AB, Shahzad H, Zafar A (2016) Clinical outcomes of pneumocystis pneumonia from a tertiary care centre in Pakistan. J Pak Med Assoc 66:1367–1371

    PubMed  Google Scholar 

  37. Yakoob J, Jafri W, Abid S, Jafri N, Islam M, Hamid S et al (2003) Candida esophagitis: risk factors in non-HIV population in Pakistan. World J Gastroenterol 9:2328–2331

    Article  PubMed  PubMed Central  Google Scholar 

  38. Kumar S, Kalam K, Ali S, Siddiqi S, Baqi S (2014) Frequency, clinical presentation and microbiological spectrum of candidemia in a tertiary care center in Karachi, Pakistan. J Pak Med Assoc 64:281–285

    PubMed  Google Scholar 

  39. Farooqi JQ, Jabeen K, Saeed N, Iqbal N, Malik B, Lockhart SR et al (2013) Invasive candidiasis in Pakistan: clinical characteristics, species distribution and antifungal susceptibility. J Med Microbiol 62:259–268. doi:10.1099/jmm.0.048785-0

    CAS  Article  PubMed  Google Scholar 

  40. Ariff S, Saleem AF, Soofi SB, Sajjad R (2011) Clinical spectrum and outcomes of neonatal candidiasis in a tertiary care hospital in Karachi, Pakistan. J Infect Dev Ctries 5:216–223

    Article  PubMed  Google Scholar 

  41. Clancy CJ, Nguyen MH (2013) Finding the “missing 50%” of invasive candidiasis: how nonculture diagnostics will improve understanding of disease spectrum and transform patient care. Clinic Infect Dis 56:1284–1292. doi:10.1093/cid/cit006

    Article  Google Scholar 

  42. Avni T, Leibovici L, Paul M (2011) PCR diagnosis of invasive candidiasis: systematic review and meta-analysis. J Clin Microbiol 49:665–670. doi:10.1128/JCM.01602-10

    Article  PubMed  PubMed Central  Google Scholar 

  43. Lockhart SR, Etienne KA, Vallabhaneni S, Farooqi J, Chowdhary A, Govender NP et al (2017) Simultaneous emergence of multidrug-resistant Candida auris on 3 continents confirmed by whole-genome sequencing and epidemiological analyses. Clin Infect Dis 64:134–140

    Article  PubMed  Google Scholar 

  44. Clancy CJ, Shields RK, Nguyen MH (2016) Invasive candidiasis in various patient populations: incorporating non-culture diagnostic tests into rational management strategies. J Fungi 2:10. doi:10.3390/jof2010010

    Article  Google Scholar 

  45. Yatawatte AB, Wanniarachchi CR, Goonasekera CD (2004) An audit of state sector intensive care services in Sri Lanka. Ceylon Med J 49:51–54

    CAS  PubMed  Google Scholar 

  46. Chakrabarti A, Singh R (2014) Mucormycosis in India: unique features. Mycoses 57:85–90

    Article  PubMed  Google Scholar 

  47. Ikram M, Iqbal M, Khan MA, Khan E, Shah M, Smego RA (2011) Rhinocerebral zygomycosis in Pakistan: clinical spectrum, management, and outcome. J Pak Med Assoc 61:477–480

    PubMed  Google Scholar 

  48. Shakoor S, Jabeen K, Idrees R, Jamil B, Irfan S, Zafar A (2011) Necrotising fasciitis due to Absidia corymbifera in wounds dressed with non sterile bandages. Int Wound J 8:651–655

    Article  PubMed  Google Scholar 

  49. Hussain S, Salahuddin N, Ahmad I, Salahuddin I, Jooma R (1995) Rhinocerebral invasive mycosis: occurrence in immunocompetent individuals. Eur J Radiol 20:151–155

    CAS  Article  PubMed  Google Scholar 

  50. World Health Organization—diabetes country profile; Pakistan. Available online at: http://www.who.int/diabetes/country-profiles/pak_en.pdf?ua=1

  51. World Health Organization—diabetes country profile; India. Available online at: http://www.who.int/diabetes/country-profiles/ind_en.pdf?ua=1

  52. Foxman B, Barlow R, D’Arcy H, Gillespie B, Sobel JD (2000) Candida vaginitis: self-reported incidence and associated costs. Sex Transm Dis 27:230–235

    CAS  Article  PubMed  Google Scholar 

  53. Durr-e-Nayab (2005) Reproductive tract infections among women in Pakistan: an urban case study. Pakistan Devel Rev 44:131–158. Published by: Pakistan Institute of Development Economics, Islamabad. Stable URL: http://www.jstor.org/stable/41260711

  54. Singh M, Das S, Chauhan A, Paul N, Sodhi KS, Mathew J et al (2015) The diagnostic criteria for allergic bronchopulmonary aspergillosis in children with poorly controlled asthma need to be re-evaluated. Acta Paediatr 104:e206–e209. doi:10.1111/apa.12930

    Article  PubMed  Google Scholar 

  55. Castanhinha S, Sherburn R, Walker S, Gupta A, Bossley CJ, Buckley J et al (2015) Pediatric severe asthma with fungal sensitization is mediated by steroid-resistant IL-33. J Allergy Clin Immunol 136:312–322.e7. doi:10.1016/j.jaci.2015.01.016

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. Rao TA, Shaikh AH, Ahmed M (2009) Airborne fungal flora of Karachi, Pakistan. Pak J Bot 41:1421–1428

    Google Scholar 

  57. Zubairi ABS, Azam I, Awan S, Zafar A, Imam AA (2014) Association of airborne Aspergillus with asthma exacerbation in Southern Pakistan. Asia Pac Allergy 4:91–98

    Article  PubMed  PubMed Central  Google Scholar 

  58. Hussain SF, Khan JA, Khan MA (1995) Allergic bronchopulmonary aspergillosis: an unusual complication of bronchial asthma. J Pak Med Assoc 45:329–331

    CAS  PubMed  Google Scholar 

  59. Khalil KF (2015) Therapeutic bronchoalveolar lavage with conventional treatment in allergic bronchopulmonary aspergillosis. J Coll Physicians Surg Pak 25:359–362

    PubMed  Google Scholar 

  60. Shah U, Frossard P, Moatter T (2009) Cystic fibrosis: defining a disease under-diagnosed in Pakistan. Trop Med Int Health 14:542–545

    CAS  Article  PubMed  Google Scholar 

  61. World Health Organization (WHO). The molecular genetic epidemiology of cystic fibrosis. Available online at: http://www.who.int/genomics/publications/en/HGN_WB_04.02_report.pdf

  62. Denning DW, Cadranel J, Beigelman-Aubry C, Ader F, Chakrabarti A, Blot S et al (2016) Chronic pulmonary aspergillosis: rationale and clinical guidelines for diagnosis and management. Eur Respir J 47:45–68

    CAS  Article  PubMed  Google Scholar 

  63. Karim M, Alam M, Shah AA, Ahmed R, Sheikh H (1997) Chronic invasive aspergillosis in apparently immunocompetent hosts. Clin Infect Dis 24:723–733

    CAS  Article  PubMed  Google Scholar 

  64. Chakrabarti A, Chatterjee SS, Das A, Shivaprakash MR (2011) Invasive aspergillosis in developing countries. Med Mycol 49:S35–S47

    Article  PubMed  Google Scholar 

  65. Asim M, Zaidi A, Ghafoor T, Qureshi Y (2011) Death analysis of childhood acute lymphoblastic leukaemia; experience at Shaukat Khanum Memorial Cancer Hospital and Research Centre, Pakistan. J Pak Med Assoc 61:666–670

    PubMed  Google Scholar 

  66. Ullah K, Raza S, Ahmed P, Chaudhry QU, Satti TM, Ahmed S et al (2008) Post-transplant infections: single center experience from the developing world. Int J Infect Dis 12:203–214

    Article  PubMed  Google Scholar 

  67. Dar FS, Bhatti ABH, Dogar AW, Zia H, Amin S, Rana A et al (2015) The travails of setting up a living donor liver transplant program: experience from Pakistan and lessons learned. Liver Transpl 21:982–990

    Article  PubMed  Google Scholar 

  68. Iqbal N, Irfan M, Zubairi ABS, Jabeen K, Awan S, Khan JA (2016) Clinical manifestations and outcomes of pulmonary aspergillosis: experience from Pakistan. BMJ Open Respir Res 3:e000155

    Article  PubMed  PubMed Central  Google Scholar 

  69. Khwakhali US, Denning DW (2015) Burden of serious fungal infections in Nepal. Mycoses 58:S45–S50

    Article  Google Scholar 

  70. Faqir F, Rehman A (2004) Mycetoma: a local experience. J Postgraduate Med Inst 18:172–175

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to K. Jabeen.

Additional information

In association with the LIFE program at http://www.LIFE-worldwide.org.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jabeen, K., Farooqi, J., Mirza, S. et al. Serious fungal infections in Pakistan. Eur J Clin Microbiol Infect Dis 36, 949–956 (2017). https://doi.org/10.1007/s10096-017-2919-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-017-2919-6

Keywords

  • Human Immunodeficiency Virus
  • Chronic Obstructive Pulmonary Disease
  • Candidiasis
  • Invasive Aspergillosis
  • Invasive Candidiasis