Deficiency of Mannose-binding Lectin is a Risk of Pneumocystis Jirovecii Pneumonia in a Natural History Cohort of People Living with HIV/AIDS in Northern Thailand

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2020 Dec 28

PMID 33362211

Citations 5

Authors

Kunio Yanagisawa

Nuanjun Wichukchinda

Naho Tsuchiya

Michio Yasunami

Archawin Rojanawiwat

Hidenori Tanaka

Hiroh Saji

Yoshiyuki Ogawa

Hiroshi Handa

Panita Pathipvanich

Koya Ariyoshi

Pathom Sawanpanyalert

Affiliations

Soon will be listed here.

Abstract

Background: Mannose-binding lectin (MBL) plays a pivotal role in innate immunity; however, its impact on susceptibility to opportunistic infections (OIs) has not yet been examined in a natural history cohort of people living with HIV/AIDS.

Methods: We used archived samples to analyze the association between MBL expression types and risk of major OIs including Pneumocystis jirovecii pneumonia (PCP), cryptococcosis, talaromycosis, toxoplasmosis, and tuberculosis in a prospective cohort in Northern Thailand conducted from 1 July 2000 to 15 October 2002 before the national antiretroviral treatment programme was launched.

Results: Of 632 patients, PCP was diagnosed in 96 (15.2%) patients, including 45 patients with new episodes during the follow-up period (1006.5 person-years). The total history of PCP was significantly associated with low MBL expression type: high/intermediate (81/587, 13.8%), low (10/33, 30.3%) and deficient (5/12, 41.7%) (p = 0.001), whereas the history of other OIs showed no relation with any MBL expression type. Kaplan-Meier analysis (n = 569; log-rank p = 0.011) and Cox's proportional hazards model revealed that deficient genotype dramatically increased the risk of PCP, which is independent upon sex, age, CD4 count, HIV-1 viral load and hepatitis B and C status (adjusted hazard ratio 7.93, 95% confidence interval 2.19-28.67, p = 0.002).

Conclusions: Deficiency of MBL expression is a strong risk factor determining the incidence of PCP but not other major OIs.

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References

Goyal S, Castrillon-Betancur J, Klaile E, Slevogt H . The Interaction of Human Pathogenic Fungi With C-Type Lectin Receptors. Front Immunol. 2018; 9:1261. PMC: 5994417. DOI: 10.3389/fimmu.2018.01261. View

Tsuchiya N, Pathipvanich P, Wichukchinda N, Rojanawiwat A, Auwanit W, Ariyoshi K . Incidence and predictors of regimen-modification from first-line antiretroviral therapy in Thailand: a cohort study. BMC Infect Dis. 2014; 14:565. PMC: 4226857. DOI: 10.1186/s12879-014-0565-5. View

Zhou J, Kumarasamy N, Ditangco R, Kamarulzaman A, Lee C, Li P . The TREAT Asia HIV Observational Database: baseline and retrospective data. J Acquir Immune Defic Syndr. 2005; 38(2):174-9. PMC: 3070962. DOI: 10.1097/01.qai.0000145351.96815.d5. View

Carvalho A, Cunha C, Pasqualotto A, Pitzurra L, Denning D, Romani L . Genetic variability of innate immunity impacts human susceptibility to fungal diseases. Int J Infect Dis. 2009; 14(6):e460-8. DOI: 10.1016/j.ijid.2009.06.028. View

Pathipvanich P, Rojanawiwat A, Ariyoshi K, Miura T, Pumpradit W, Wongchoosie S . Mortality analysis of HIV-1 infected patients for prioritizing antiretroviral drug therapy. J Med Assoc Thai. 2004; 87(8):951-4. View

Romani L . Immunity to fungal infections. Nat Rev Immunol. 2011; 11(4):275-88. DOI: 10.1038/nri2939. View

Chalmers J, McHugh B, Doherty C, Smith M, Govan J, Kilpatrick D . Mannose-binding lectin deficiency and disease severity in non-cystic fibrosis bronchiectasis: a prospective study. Lancet Respir Med. 2014; 1(3):224-32. DOI: 10.1016/S2213-2600(13)70001-8. View

Yanagisawa K, Ogawa Y, Uchiumi H, Gohda F, Mawatari M, Ishizaki T . Gene polymorphisms of mannose-binding lectin confer susceptibility to Pneumocystis pneumonia in HIV-infected patients. J Infect Chemother. 2015; 21(11):769-75. DOI: 10.1016/j.jiac.2015.07.006. View

Sorensen C, Hansen T, Steffensen R, Jensenius J, Thiel S . Hormonal regulation of mannan-binding lectin synthesis in hepatocytes. Clin Exp Immunol. 2006; 145(1):173-82. PMC: 1942004. DOI: 10.1111/j.1365-2249.2006.03101.x. View

10.

Eisen D, Minchinton R . Impact of mannose-binding lectin on susceptibility to infectious diseases. Clin Infect Dis. 2003; 37(11):1496-505. DOI: 10.1086/379324. View

11.

Thomas Jr C, Limper A . Current insights into the biology and pathogenesis of Pneumocystis pneumonia. Nat Rev Microbiol. 2007; 5(4):298-308. DOI: 10.1038/nrmicro1621. View

12.

Kerrigan A, Brown G . C-type lectins and phagocytosis. Immunobiology. 2009; 214(7):562-75. PMC: 2702671. DOI: 10.1016/j.imbio.2008.11.003. View

13.

Pathipvanich P, Ariyoshi K, Rojanawiwat A, Wongchoosie S, Yingseree P, Yoshiike K . Survival benefit from non-highly active antiretroviral therapy in a resource-constrained setting. J Acquir Immune Defic Syndr. 2003; 32(2):157-60. DOI: 10.1097/00126334-200302010-00007. View

14.

Masur H, Ognibene F, Yarchoan R, Shelhamer J, Baird B, Travis W . CD4 counts as predictors of opportunistic pneumonias in human immunodeficiency virus (HIV) infection. Ann Intern Med. 1989; 111(3):223-31. DOI: 10.7326/0003-4819-111-3-223. View

15.

Schoffelen A, Van Lelyveld S, Barth R, Gras L, de Wolf F, Netea M . Lower incidence of Pneumocystis jirovecii pneumonia among Africans in the Netherlands host or environmental factors?. AIDS. 2013; 27(7):1179-84. DOI: 10.1097/QAD.0b013e32835e2c90. View

16.

Rojanawiwat A, Tsuchiya N, Pathipvanich P, Pumpradit W, Schmidt W, Honda S . Impact of the National Access to Antiretroviral Program on the incidence of opportunistic infections in Thailand. Int Health. 2013; 3(2):101-7. DOI: 10.1016/j.inhe.2010.12.004. View

17.

Wojtowicz A, Bibert S, Taffe P, Bernasconi E, Furrer H, Gunthard H . IL-4 polymorphism influences susceptibility to Pneumocystis jirovecii pneumonia in HIV-positive patients. AIDS. 2019; 33(11):1719-1727. PMC: 6686957. DOI: 10.1097/QAD.0000000000002283. View

18.

Ezekowitz R . Role of the mannose-binding lectin in innate immunity. J Infect Dis. 2003; 187 Suppl 2:S335-9. DOI: 10.1086/374746. View

19.

Garred P, Larsen F, Seyfarth J, Fujita R, Madsen H . Mannose-binding lectin and its genetic variants. Genes Immun. 2006; 7(2):85-94. DOI: 10.1038/sj.gene.6364283. View

20.

Tian C, Hromatka B, Kiefer A, Eriksson N, Noble S, Tung J . Genome-wide association and HLA region fine-mapping studies identify susceptibility loci for multiple common infections. Nat Commun. 2017; 8(1):599. PMC: 5605711. DOI: 10.1038/s41467-017-00257-5. View