Regional Differences in the Prevalence of Major Opportunistic Infections among Antiretroviral-Naïve Human Immunodeficiency Virus Patients in Japan, Northern Thailand, Northern Vietnam, and the Philippines

Louie Mar A. Gangcuangco Institute of Tropical Medicine (NEKKEN), Graduate School of Biomedical Science, Nagasaki University, Nagasaki, Japan
Bridgeport Hospital-Yale New Haven Health, Bridgeport, Connecticut

Search for other papers by Louie Mar A. Gangcuangco in
Current site
Google Scholar
PubMed
Close
,
Ikumi Sawada Institute of Tropical Medicine (NEKKEN), Graduate School of Biomedical Science, Nagasaki University, Nagasaki, Japan

Search for other papers by Ikumi Sawada in
Current site
Google Scholar
PubMed
Close
,
Naho Tsuchiya Institute of Tropical Medicine (NEKKEN), Graduate School of Biomedical Science, Nagasaki University, Nagasaki, Japan
Tohoku Medical Megabank Organization, Tohoku University, Miyagi, Japan

Search for other papers by Naho Tsuchiya in
Current site
Google Scholar
PubMed
Close
,
Cuong D. Do Bach Mai Hospital, Hanoi, Vietnam

Search for other papers by Cuong D. Do in
Current site
Google Scholar
PubMed
Close
,
Thanh Thuy T. Pham Bach Mai Hospital, Hanoi, Vietnam

Search for other papers by Thanh Thuy T. Pham in
Current site
Google Scholar
PubMed
Close
,
Archawin Rojanawiwat Ministry of Public Health, Nonthaburi, Thailand

Search for other papers by Archawin Rojanawiwat in
Current site
Google Scholar
PubMed
Close
,
Marissa Alejandria Philippine General Hospital, University of the Philippines, Manila, Philippines

Search for other papers by Marissa Alejandria in
Current site
Google Scholar
PubMed
Close
,
Katerina Leyritana Philippine General Hospital, University of the Philippines, Manila, Philippines

Search for other papers by Katerina Leyritana in
Current site
Google Scholar
PubMed
Close
,
Yoshiyuki Yokomaku National Hospital Organization Nagoya Medical Center, Nagoya, Japan

Search for other papers by Yoshiyuki Yokomaku in
Current site
Google Scholar
PubMed
Close
,
Panita Pathipvanich Lampang Hospital, Lampang, Thailand

Search for other papers by Panita Pathipvanich in
Current site
Google Scholar
PubMed
Close
, and
Koya Ariyoshi Institute of Tropical Medicine (NEKKEN), Graduate School of Biomedical Science, Nagasaki University, Nagasaki, Japan

Search for other papers by Koya Ariyoshi in
Current site
Google Scholar
PubMed
Close
Restricted access

To identify regional differences in the distribution of opportunistic infections (OIs) among human immunodeficiency virus (HIV)-infected patients in Asia, the medical records of antiretroviral therapy (ART)-naïve patients who attended the following tertiary hospitals from 2003 to 2011 were reviewed: Nagoya Medical Center (NMC, Nagoya, Japan), Lampang Hospital (LPH, Lampang, northern Thailand), Bach Mai Hospital (BMH, Hanoi, northern Vietnam), and Philippine General Hospital (PGH, Manila, Philippines). Logistic regression analyses were performed to identify associations between country of origin and risk of major OIs. In total, 1,505 patients were included: NMC, N = 365; LPH, N = 442; BMH, N = 384; and PGH, N = 314. The median age was 32 years, and 73.3% of all patients were male. The median CD4 count was 200 cells/μL. Most patients at NMC and PGH were men who have sex with men. Injection drug users were most common at BMH (35.7%). Mycobacterium tuberculosis (TB) was most common at PGH (N = 75) but was rare at NMC (N = 4). Pneumocystis pneumonia (PCP) prevalence was highest at NMC (N = 74) and lowest at BMH (N = 13). Multivariable logistic regression showed increased odds of TB at PGH (adjusted odds ratio [aOR] = 42.2, 95% confidence interval [CI] = 14.6–122.1), BMH (aOR = 12.6, CI = 3.9–40.3), and LPH (aOR = 6.6, CI = 2.1–21.1) but decreased odds of PCP at BMH (aOR = 0.1, CI = 0.04–0.2) and LPH (aOR = 0.2, CI = 0.1–0.4) compared with those at NMC. The cryptococcosis risk was increased at LPH (aOR = 6.2, CI = 0.9–41.0) compared with that at NMC. Cytomegalovirus (CMV) retinitis prevalences were similar in all countries. OI prevalence remained high among ART-naïve patients in our cohort. The risks of TB, PCP, and cryptococcosis, but not CMV retinitis, differed between countries. Improved early HIV detection is warranted.

    • Supplemental Materials (PDF 45 KB)

Author Notes

Address correspondence to Koya Ariyoshi, Institute of Tropical Medicine, Nagasaki University, 1-12-4 Sakamoto, P.O. Box 852-8523, Nagasaki, Japan. E-mail: kari@nagasaki-u.ac.jp
These authors contributed equally to this work.

Note: Supplemental tables appear at www.ajtmh.org.

Authors' addresses: Louie Mar A. Gangcuangco, Department of Clinical Tropical Medicine, Institute of Tropical Medicine (NEKKEN), Graduate School of Biomedical Science, Nagasaki University, Nagasaki, Japan, and Department of Internal Medicine, Bridgeport Hospital-Yale New Haven Health, Bridgeport, CT, E-mail: louiemarmd@gmail.com. Ikumi Sawada and Koya Ariyoshi, Department of Clinical Tropical Medicine, Institute of Tropical Medicine (NEKKEN), Graduate School of Biomedical Science, Nagasaki University, Nagasaki, Japan, E-mails: sawada.ikumi@gmail.com and kari@nagasaki-u.ac.jp. Naho Tsuchiya, Department of Clinical Tropical Medicine, Institute of Tropical Medicine (NEKKEN), Graduate School of Biomedical Science, Nagasaki University, Nagasaki, Japan, and Department of Preventive Medicine and Epidemiology, Tohoku Medical Megabank Organization, Tohoku University, Miyagi, Japan, E-mail: nahot@megabank.tohoku.ac.jp. Cuong D. Do and Thanh Thuy T. Pham, Department of Infectious Diseases, Bach Mai Hospital, Hanoi, Vietnam, E-mails: doduy.cuong@gmail.com and phamthanhthuy714@gmail.com. Archawin Rojanawiwat, Department of Medical Sciences, Ministry of Public Health, Nonthaburi, Thailand, E-mail: archawin191@yahoo.com. Marissa Alejandria and Katerina Leyritana, Section of Infectious Diseases, Department of Medicine, Philippine General Hospital, University of the Philippines, Manila, Philippines, E-mails: mmalejandria@gmail.com and kateleyritana@yahoo.com. Yoshiyuki Yokomaku, Department of Infectious Diseases and Immunology, National Hospital Organization Nagoya Medical Center, Nagoya, Japan, E-mail: yokomaku@nnh.hosp.go.jp. Panita Pathipvanich, Day Care Center, Lampang Hospital, Lampang, Thailand, E-mail: panitapa@yahoo.com.

  • 1.

    Blaxhult A, Kirk O, Pedersen C, Dietrich M, Barton SE, Gatell JM, Mulcahy F, Hirschel B, Mocroft A, Lundgren JD, 2000. Regional differences in presentation of AIDS in Europe. Epidemiol Infect 125: 143151.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Nucci M, Queiroz-Telles F, Tobon AM, Restrepo A, Colombo AL, 2010. Epidemiology of opportunistic fungal infections in Latin America. Clin Infect Dis 51: 561570.

  • 3.

    Handford CD, Rackal JM, Tynan AM, Rzeznikiewiz D, Glazier RH, 2012. The association of hospital, clinic and provider volume with HIV/AIDS care and mortality: systematic review and meta-analysis. AIDS Care 24: 267282.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Kaslow RA, Carrington M, Apple R, Park L, Munoz A, Saah AJ, Goedert JJ, Winkler C, O'Brien SJ, Rinaldo C, Detels R, Blattner W, Phair J, Erlich H, Mann DL, 1996. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat Med 2: 405411.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Pant Pai N, Shivkumar S, Cajas JM, 2012. Does genetic diversity of HIV-1 non-B subtypes differentially impact disease progression in treatment-naive HIV-1-infected individuals? A systematic review of evidence: 1996–2010. J Acquir Immune Defic Syndr 59: 382388.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Ruxrungtham K, Brown T, Phanuphak P, 2004. HIV/AIDS in Asia. Lancet 364: 6982.

  • 7.

    Yang CH, Huang YF, Hsiao CF, Yeh YL, Liou HR, Hung CC, Yang SY, 2008. Trends of mortality and causes of death among HIV-infected patients in Taiwan, 1984–2005. HIV Med 9: 535543.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    AIDS Surveillance Committee, Ministry of Health Labour and Welfare, 2014. HIV/AIDS Surveillance in 2014. Available at: http://api-net.jfap.or.jp/status/2014/14nenpo/14nenpo_menu.html. Accessed April 27, 2016.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Dickson N, McAllister S, Sharples K, Paul C, 2012. Late presentation of HIV infection among adults in New Zealand: 2005–2010. HIV Med 13: 182189.

  • 10.

    Kiertiburanakul S, Boonyarattaphun K, Atamasirikul K, Sungkanuparph S, 2008. Clinical presentations of newly diagnosed HIV-infected patients at a university hospital in Bangkok, Thailand. J Int Assoc Physicians AIDS Care (Chic) 7: 8287.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Kong BN, Harwell JI, Suos P, Lynen L, Mohiuddin S, Reinert S, Pugatch D, 2007. Opportunistic infections and HIV clinical disease stage among patients presenting for care in Phnom Penh, Cambodia. Southeast Asian J Trop Med Public Health 38: 6268.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Zhou J, Kumarasamy N, Ditangco R, Kamarulzaman A, Lee CK, Li PC, Paton NI, Phanuphak P, Pujari S, Vibhagool A, Wong WW, Zhang F, Chuah J, Frost KR, Cooper DA, Law MG, 2005. The TREAT Asia HIV Observational Database: baseline and retrospective data. J Acquir Immune Defic Syndr 38: 174179.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Chariyalertsak S, Sirisanthana T, Saengwonloey O, Nelson KE, 2001. Clinical presentation and risk behaviors of patients with acquired immunodeficiency syndrome in Thailand, 1994–1998: regional variation and temporal trends. Clin Infect Dis 32: 955962.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Yasuoka A, Tsukamoto M, Kurihara S, Takami Y, Shiki N, 2012. A National Survey of HIV-Related Opportunistic Infections in 2010. AIDS Research Project. Tokyo, Japan: Ministry of Health, Labour and Welfare, 1634.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Louie JK, Chi NH, Thao LTT, Quang VM, Campbell J, Chau NV, Rutherford GW, Farrar JJ, Parry CM, 2004. Opportunistic infections in hospitalized HIV-infected adults in Ho Chi Minh City, Vietnam: a cross-sectional study. Int J STD AIDS 15: 758761.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Klotz SA, Nguyen HC, Van Pham T, Nguyen LT, Ngo DT, Vu SN, 2007. Clinical features of HIV/AIDS patients presenting to an inner city clinic in Ho Chi Minh City, Vietnam. Int J STD AIDS 18: 482485.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Section Bureau of Epidemiology, Department of Disease Control, Ministry of Public Health, 2008. Epidemiological Information. Bangkok, Thailand: Ministry of Public Health.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    World Health Organization, 2007. WHO Case Definitions of HIV for Surveillance and Revised Clinial Staging and Immunological Classification of HIV-Related Diseases in Adults and Children. Available at: http://www.who.int/hiv/pub/guidelines/hivstaging/en/. Accessed May 4, 2015.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Ministry of Health Labour and Welfare, 2011. Anti HIV Treatment Guideline. Available at: http://www.haart-support.jp/guideline.htm. Accessed April 1, 2015.

  • 20.

    Ministry of Public Health, 2000. National Guidelines for the Clinical Management of HIV Infection in Children and Adults, 6th Edition. Bangkok, Thailand: Ministry of Public Health.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Vietnam Ministry of Health, 2009. Guidelines for HIV/AIDS Diagnosis and Treatment. Available at: http://www.who.int/hiv/pub/guidelines/vietnam_art.pdf. Accessed June 4, 2015.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Philippine Society for Microbiology and Infectious Diseases, 2006. Clinical Practice Guidelines for the Diagnosis, Treatment, Prevention and Control of Tuberculosis in Adult Filipinos: 2006 Update. Available at: http://www.psmid.org.ph/pdf/Introduction_Edited_4.pdf. Accessed June 4, 2015.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Vanittanakom N, Cooper CR Jr, Fisher MC, Sirisanthana T, 2006. Penicillium marneffei infection and recent advances in the epidemiology and molecular biology aspects. Clin Microbiol Rev 19: 95110.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Vietnam Authority of HIV/AIDS Control, 2014. An Annual Update on the HIV Epidemic in Vietnam. Available at: http://www.aidsdatahub.org/annual-update-hiv-epidemic-viet-nam-viet nam-authority-hivaids-control-vaac-2014. Accessed February 2, 2016.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Farr AC, Wilson DP, 2010. An HIV epidemic is ready to emerge in the Philippines. J Int AIDS Soc 13: 16.

  • 26.

    HIV and AIDS Data Hub for Asia-Pacific, 2015. Country Profiles. Available at: http://www.aidsdatahub.org. Accessed May 11, 2015.

  • 27.

    Trinh QM, Nguyen HL, Nguyen VN, Nguyen TV, Sintchenko V, Marais BJ, 2015. Tuberculosis and HIV co-infection-focus on the Asia-Pacific region. Int J Infect Dis 32: 170178.

  • 28.

    World Health Organization, 2012. Global Tuberculosis Control: WHO Report 2011. Available at: http://apps.who.int/iris/bitstream/10665/44728/1/9789241564380_eng.pdf. Accessed February 2, 2016.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Janssens JP, Rieder HL, 2008. An ecological analysis of incidence of tuberculosis and per capita gross domestic product. Eur Respir J 32: 14151416.

  • 30.

    Kufa T, Mabuto T, Muchiri E, Charalambous S, Rosillon D, Churchyard G, Harris RC, 2014. Incidence of HIV-associated tuberculosis among individuals taking combination antiretroviral therapy: a systematic review and meta-analysis. PLoS One 9: e111209.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Narasimhan P, Wood J, Macintyre CR, Mathai D, 2013. Risk factors for tuberculosis. Pulm Med 2013 :828939.

  • 32.

    Deiss RG, Rodwell TC, Garfein RS, 2009. Tuberculosis and illicit drug use: review and update. Clin Infect Dis 48: 7282.

  • 33.

    Friedman H, Newton C, Klein TW, 2003. Microbial infections, immunomodulation, and drugs of abuse. Clin Microbiol Rev 16: 209219.

  • 34.

    Lowe DM, Rangaka MX, Gordon F, James CD, Miller RF, 2013. Pneumocystis jirovecii pneumonia in tropical and low and middle income countries: a systematic review and meta-regression. PLoS One 8: e69969.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Smulian AG, Sullivan DW, Linke MJ, Halsey NA, Quinn TC, MacPhail AP, Hernandez-Avila MA, Hong ST, Walzer PD, 1993. Geographic variation in the humoral response to Pneumocystis carinii .J Infect Dis 167: 12431247.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    An P, Penugonda S, Thorball CW, Bartha I, Goedert JJ, Donfield S, Buchbinder S, Binns-Roemer E, Kirk GD, Zhang W, Fellay J, Yu XF, Winkler CA, 2016. Role of APOBEC3F gene variation in HIV-1 disease progression and Pneumocystis pneumonia. PLoS Genet 12: e1005921.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Ashton LJ, Stewart GJ, Biti R, Law M, Cooper DA, Kaldor JM, 2002. Heterozygosity for CCR5-Delta32 but not CCR2b-64I protects against certain intracellular pathogens. HIV Med 3: 9196.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Saijo S, Fujikado N, Furuta T, Chung SH, Kotaki H, Seki K, Sudo K, Akira S, Adachi Y, Ohno N, Kinjo T, Nakamura K, Kawakami K, Iwakura Y, 2007. Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans. Nat Immunol 8: 3946.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Yanagisawa K, Ogawa Y, Uchiumi H, Gohda F, Mawatari M, Ishizaki T, Mitsui T, Yokohama A, Handa H, Tsukamoto N, Nojima Y, 2015. Gene polymorphisms of mannose-binding lectin confer susceptibility to Pneumocystis pneumonia in HIV-infected patients. J Infect Chemother 21: 769775.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    An P, Li R, Wang JM, Yoshimura T, Takahashi M, Samudralal R, O'Brien SJ, Phair J, Goedert JJ, Kirk GD, Troyer JL, Sezgin E, Buchbinder SP, Donfield S, Nelson GW, Winkler CA, 2011. Role of exonic variation in chemokine receptor genes on AIDS: CCRL2 F167Y association with Pneumocystis pneumonia. PLoS Genet 7: e1002328.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Forthal DN, Landucci G, Bream J, Jacobson LP, Phan TB, Montoya B, 2007. FcgammaRIIa genotype predicts progression of HIV infection. J Immunol 179: 79167923.

  • 42.

    Schoffelen AF, van Lelyveld SF, Barth RE, Gras L, de Wolf F, Netea MG, Hoepelman AI, 2013. Lower incidence of Pneumocystis jirovecii pneumonia among Africans in The Netherlands host or environmental factors? AIDS 27: 11791184.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Kamei K, Sano A, Kikuchi K, Makimura K, Niimi M, Suzuki K, Uehara Y, Okabe N, Nishimura K, Miyaji M, 2003. The trend of imported mycoses in Japan. J Infect Chemother 9: 1620.

  • 44.

    Kuroki M, Phichaichumpon C, Yasuoka A, Chiranairadul P, Chosa T, Sirinirund P, Miyazaki T, Kakeya H, Higashiyama Y, Miyazaki Y, Ishida Y, Kohno S, 2004. Environmental isolation of Cryptococcus neoformans from an endemic region of HIV-associated cryptococcosis in Thailand. Yeast 21: 809812.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Chaiwarith R, Vongsanim S, Supparatpinyo K, 2014. Cryptococcal meningitis in HIV-infected patients at Chiang Mai University Hospital: a retrospective study. Southeast Asian J Trop Med Public Health 45: 636646.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Kiertiburanakul S, Likhitpongwit S, Ratanasiri S, Sungkanuparph S, 2007. Malignancies in HIV-infected Thai patients. HIV Med 8: 322323.

  • 47.

    Rojanawiwat A, Miura T, Thaisri H, Pathipvanich P, Umnajsirisuk S, Koibuchi T, Vongsheree S, Iwamoto A, Ariyoshi K, Sawanpanyalert P, 2005. Frequent detection of Epstein-Barr virus and cytomegalovirus but not JC virus DNA in cerebrospinal fluid samples from human immunodeficiency virus-infected patients in northern Thailand. J Clin Microbiol 43: 34843486.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Ebrahim SH, Peterman TA, Zaidi AA, Hamers FF, 1997. Geography of AIDS-associated Kaposi's sarcoma in Europe. AIDS 11: 17391745.

  • 49.

    Rohner E, Wyss N, Heg Z, Faralli Z, Mbulaiteye SM, Novak U, Zwahlen M, Egger M, Bohlius J, 2016. HIV and human herpesvirus 8 co-infection across the globe: systematic review and meta-analysis. Int J Cancer 138: 4554.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50.

    Sugiura W, 2009. Subtypes of HIV prevalent in Japan, 2003–2007. Infect Agents Surv Rep 30: 234235.

  • 51.

    Paladin FJ, Monzon OT, Tsuchie H, Aplasca MR, Learn GH Jr, Kurimura T, 1998. Genetic subtypes of HIV-1 in the Philippines. AIDS 12: 291300.

  • 52.

    Schwem B, Itable J, Ching P, Ganchua S, Alejandria M, Lim J, Destura R, Salvana EM, 2014. The Changing Molecular Epidemiology of HIV in the Philippines: Major Shift from Subtype B to CRF01_AE. ID Week 2014. Philadelphia, PA: Infectious Diseases Society of America.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53.

    Hemelaar J, Gouws E, Ghys PD, Osmanov S, 2006. Global and regional distribution of HIV-1 genetic subtypes and recombinants in 2004. AIDS 20: W13W23.

Past two years Past Year Past 30 Days
Abstract Views 547 387 28
Full Text Views 529 8 0
PDF Downloads 231 12 0
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save