Anemia in tuberculosis cases and household controls from Tanzania: Contribution of disease, coinfections, and the role of hepcidin

PLoS ONE

Volumn 13, Issue 4, 2018, Pages

  Hella, Jerry ^a,b,c   Cercamondi, Colin I ^d   Mhimbira, Francis ^a,b,c   Sasamalo, Mohamed ^a,b,c   Stoffel, Nicole ^d   Zwahlen, Marcel ^e   Bodmer, Thomas ^f   Gagneux, Sebastien ^b,c   Reither, Klaus ^b,c   Zimmermann, Michael B ^d   Risch, Lorenz ^f   Fenner, Lukas ^e,g  

^a IFAKARA HEALTH INSTITUTE   (Tanzania)

^b SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

^d ETH ZURICH   (Switzerland)

^e UNIVERSITY OF BERN   (Switzerland)

^f labormedizinisches zentrum Dr Risch ^*  (Switzerland)

^g Gesundheitsamt   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

HEPCIDIN; IRON;

ADULT; ANEMIA; ANEMIA OF CHRONIC DISEASE; ARTICLE; BACTERIAL LOAD; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; FEMALE; HELMINTHIASIS; HOUSEHOLD; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGICAL PARAMETERS; IRON DEFICIENCY ANEMIA; MAJOR CLINICAL STUDY; MALE; MICROBIOLOGICAL EXAMINATION; MIXED INFECTION; PATHOGENESIS; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; RESPIRATORY TRACT INFECTION; SCORING SYSTEM; TANZANIA; TUBERCULOSIS; BLOOD; CASE CONTROL STUDY; COMPLICATION; DISEASE EXACERBATION; FAMILY SIZE; METABOLISM; RISK FACTOR; STATISTICAL MODEL;

ADULT; ANEMIA; ANEMIA, IRON-DEFICIENCY; CASE-CONTROL STUDIES; COINFECTION; DISEASE PROGRESSION; FAMILY CHARACTERISTICS; FEMALE; HEPCIDINS; HUMANS; LINEAR MODELS; MALE; RISK FACTORS; TANZANIA; TUBERCULOSIS;

EID: 85045894553     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0195985     Document Type: Article

References (40)

1. Houben RMGJ, Dodd PJ. The global burden of latent tuberculosis infection: A re-estimation using mathematical modelling. PLoS Med. 2016; 13. https://doi.org/10.1371/journal.pmed.1002152 PMID: 27780211
2. Isanaka S, Aboud S, Mugusi F, Bosch RJ, Willett WC, Spiegelman D, et al. Iron status predicts treatment failure and mortality in tuberculosis patients: A prospective cohort study from Dar es Salaam, Tanzania. PLoS ONE. 2012; 7. https://doi.org/10.1371/journal.pone.0037350 PMID: 22606361
3. Isanaka S, Mugusi F, Urassa W, Willett WC, Bosch RJ, Villamor E, et al. Iron deficiency and anemia predict mortality in patients with tuberculosis. J Nutr. 2012; 142: 350–357. https://doi.org/10.3945/jn.111.144287 PMID: 22190024
4. Kassebaum NJ, Jasrasaria R, Naghavi M, Wulf SK, Johns N, Lozano R, et al. A systematic analysis of global anemia burden from 1990 to 2010. Blood. 2014; 123: 615–624. https://doi.org/10.1182/blood-2013-06-508325 PMID: 24297872
5. Zimmermann MB, Chaouki N, Hurrell RF. Iron deficiency due to consumption of a habitual diet low in bioavailable iron: a longitudinal cohort study in Moroccan children. Am J Clin Nutr. 2005; 81: 115–121. https://doi.org/10.1093/ajcn/81.1.115 PMID: 15640469
6. Kerkhoff AD, Meintjes G, Opie J, Vogt M, Jhilmeet N, Wood R, et al. Anaemia in patients with HIV-associated TB: relative contributions of anaemia of chronic disease and iron deficiency. Int J Tuberc Lung Dis. 2016; 20: 193–201. https://doi.org/10.5588/ijtld.15.0558 PMID: 26792471
7. Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM, et al. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science. 2004; 306. https://doi.org/10.1126/science.1104742 PMID: 15514116
8. Girelli D, Nemeth E, Swinkels DW. Hepcidin in the diagnosis of iron disorders. Blood. 2016; 127: 2809–2814. https://doi.org/10.1182/blood-2015-12-639112 The PMID: 27044621
9. Sow FB, Nandakumar S, Velu V, Kellar KL, Schlesinger LS, Amara RR, et al. Mycobacterium tuberculosis components stimulate production of the antimicrobial peptide hepcidin. Tuberc Edinb. 2011; 91: 314–321. https://doi.org/10.1016/j.tube.2011.03.003 PMID: 21482189
10. Drakesmith H, Prentice AM. Hepcidin and the iron-infection axis. Science. 2012; 338: 768–72. https://doi.org/10.1126/science.1224577 PMID: 23139325
11. Minchella PA, Armitage AE, Darboe B, Jallow MW, Drakesmith H, Jaye A, et al. Elevated hepcidin at HIV diagnosis is associated with incident tuberculosis in a retrospective cohort study. Int J Tuberc Lung Dis. 2014; 18. https://doi.org/10.5588/ijtld.14.0143 PMID: 25299867
12. Armitage AE, Stacey AR, Giannoulatou E, Marshall E, Sturges P, Chatha K, et al. Distinct patterns of hepcidin and iron regulation during HIV-1, HBV, and HCV infections. Proc Natl Acad Sci USA. 2014; 111: 12187–92. https://doi.org/10.1073/pnas.1402351111 PMID: 25092293
13. Wang CY, Babitt JL. Hepcidin regulation in the anemia of inflammation. Curr Opin Hematol. 2016; 23: 189–197. https://doi.org/10.1097/MOH.0000000000000236 PMID: 26886082
14. Voss JJ De, Rutter K, Schroeder BG, Iii CEB, Voss JJDE. Iron acquisition and metabolism by mycobacteria. J Bacteriol. 1999; 181: 4443–4451. https://doi.org/10.1128/JB.186.2.374–382.2004 PMID: 10419938
15. Shin D-M, Jo E-K. Antimicrobial peptides in innate immunity against mycobacteria. Immune Netw. 2011; 11: 245–52. https://doi.org/10.4110/in.2011.11.5.245 PMID: 22194707
16. Michels K, Nemeth E, Ganz T, Mehrad B. Hepcidin and host defense against infectious diseases. PLoS Pathog. 2015; 11: 1–14. https://doi.org/10.1371/journal.ppat.1004998 PMID: 26291319
17. Ministry of Health and Social Welfare. National Tuberculosis and Leprosy 2013 Annual Report. 2014.
18. Mhimbira FA, Hella J, Kamwela L, Sasamalo M, Chiryamkubi M, Maroa T, et al. Prevalence and clinical relevance of helminth and tuberculosis co-infections in urban Dar es Salaam, Tanzania. PLoS Negl Trop Dis. 2017; 11. https://doi.org/10.1371/journal.pntd.0005342 PMID: 28178325
19. Said K, Hella J, Mhalu G, Chiryankubi M, Masika E, Maroa T, et al. Diagnostic delay and associated factors among patients with pulmonary tuberculosis in Dar es Salaam, Tanzania. Infect Poverty. 2017; 6. https://doi.org/10.1186/s40249-017-0276-4 PMID: 28335816
20. Hiza H, Doulla B, Sasamalo M, Hella J, Kamwela L, Mhimbira F, et al. Preservation of sputum samples with cetylpyridinium chloride (CPC) for tuberculosis cultures and Xpert MTB/RIF in a low-income country. BMC Infect Dis. 2017; 17: 1–6. https://doi.org/10.1186/s12879-016-2122-x
21. Steiner A, Hella J, Gruninger S, Mhalu G, Mhimbira F, Cercamondi CI, et al. Managing research and surveillance projects in real-time with a novel open-source eManagement tool designed for under-resourced countries. J Am Med Inf Assoc. 2016; 23: 916–23. https://doi.org/10.1093/jamia/ocv185 PMID: 26911813
22. Mhimbira F, Hella J, Maroa T, Kisandu S, Chiryamkubi M, Said K, et al. Home-based and facility-based directly observed therapy of tuberculosis treatment under programmatic conditions in urban Tanzania. PLoS ONE. 2016; 11: e0161171. https://doi.org/10.1371/journal.pone.0161171 PMID: 27513331
23. Knopp S, Salim N, Schindler T, Karagiannis Voules DA, Rothen J, Lweno O, et al. Diagnostic accuracy of Kato-Katz, FLOTAC, Baermann, and PCR methods for the detection of light-intensity hookworm and Strongyloides stercoralis infections in Tanzania. Am J Trop Med Hyg. 2014; 90: 535–45. https://doi.org/10.4269/ajtmh.13-0268 PMID: 24445211
24. Kroot JJ, Laarakkers CM, Geurts-Moespot AJ, Grebenchtchikov N, Pickkers P, van Ede AE, et al. Immunochemical and mass-spectrometry-based serum hepcidin assays for iron metabolism disorders. Clin Chem. 2010; 56: 1570–1579. https://doi.org/10.1373/clinchem.2010.149187 PMID: 20739637
25. Kim HK, Oh SH, Yun KA, Sung H, Kim MN. Comparison of Anyplex II RV16 with the xTAG respiratory viral panel and Seeplex RV15 for detection of respiratory viruses. J Clin Microbiol. 2013; 51: 1137–1141. https://doi.org/10.1128/JCM.02958-12 PMID: 23363824
26. Weiss G, Goodnough LT. Anemia of chronic disease. N Engl J Med. 2005; 352: 1011–1023. https://doi.org/10.1056/NEJMra041809 PMID: 15758012
27. Koulaouzidis A, Said E, Cottier R, Saeed AA. Soluble transferrin receptors and iron deficiency, a step beyond ferritin. A systematic review. J Gastrointestin Liver Dis. 2009; 18: 345–352. PMID: 19795030
28. Minchella PA, Donkor S, McDermid JM, Sutherland JS. Iron homeostasis and progression to pulmonary tuberculosis disease among household contacts. Tuberc Edinb. 2015; 95: 288–293. https://doi.org/10.1016/j.tube.2015.02.042 PMID: 25764944
29. World Health Organization. Iron deficiency anaemia: assessment, prevention and control: a guide for programme managers. 2001.
30. Lumb R, Van Deun A, Bastian I, Fitz-Gerald M. Laboratory diagnosis of tuberculosis by sputum microscopy. SA Pathology; 2013.
31. Wejse C, Gustafson P, Nielsen J, Gomes VF, Aaby P, Andersen PL, et al. TBscore: Signs and symptoms from tuberculosis patients in a low-resource setting have predictive value and may be used to assess clinical course. Scand J Infect Dis. 2008; 40: 111–120. https://doi.org/10.1080/ 00365540701558698 PMID: 17852907
32. Minchella PA, Donkor S, Owolabi O, Sutherland JS, McDermid JM. Complex anemia in tuberculosis: the need to consider causes and timing when designing interventions. Clin Infect Dis. 2015; 60: 764–772. https://doi.org/10.1093/cid/ciu945 PMID: 25428413
33. Andrew KD, Wood R, Vogt M, Lawn SD. Predictive value of anaemia for tuberculosis in HIV-infected patients in sub-Saharan Africa: an indication for routine microbiological investigation using new rapid assays. J Acquir Immune Defic Syndr. 2014; 66: 33–40. https://doi.org/10.1097/QAI. 0000000000000091 PMID: 24346639
34. Thurnham DI, McCabe LD, Haldar S, Wieringa FT, Northrop-Clewes CA, McCabe GP. Adjusting plasma ferritin concentrations to remove the effects of subclinical inflammation in the assessment of iron deficiency: A meta-analysis. Am J Clin Nutr. 2010; 92: 546–555. https://doi.org/10.3945/ajcn.2010. 29284 PMID: 20610634
35. Rohner F, Namaste SM, Larson LM, Addo OY, Mei Z, Suchdev PS, et al. Adjusting soluble transferrin receptor concentrations for inflammation: biomarkers reflecting inflammation and nutritional determinants of anemia (BRINDA) project. Am J Clin Nutr. 2017; 106(Suppl): 372S–382S.
36. Corbett EL, Watt CJ, Walker N, Maher D, Williams BG, Raviglione MC, et al. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch Intern Med. 2003; 163: 1009–21. https://doi.org/10.1001/archinte.163.9.1009 PMID: 12742798
37. Kerkhoff AD, Meintjes G, Burton R, Vogt M, Wood R, Lawn SD. Relationship between blood concentrations of hepcidin and anemia severity, mycobacterial burden, and mortality among patients with HIV-associated tuberculosis. J Infect Dis. 2016; 213: 61–70. https://doi.org/10.1093/infdis/jiv364 PMID: 26136467
38. McDermid JM, Hennig BJ, van der Sande M, Hill AVS, Whittle HC, Jaye A, et al. Host iron redistribution as a risk factor for incident tuberculosis in HIV infection: an 11-year retrospective cohort study. BMC Infect Dis. 2013; 13. https://doi.org/10.1186/1471-2334-13-48 PMID: 23360117
39. Devi U, Mohan Rao C, Srivastava VK, Rath PK, Das BS. Effect of iron supplementation on mild to moderate anaemia in pulmonary tuberculosis. Br J Nutr. 2003; 90: 541–550. https://doi.org/10.1079/ BJN2003936 PMID: 13129459
40. Rathod DA, Kaur A, Patel V, Patel K, Kabrawala R, Patel V, et al. Usefulness of cell counter-based parameters and formulas in detection of beta-thalassemia trait in areas of high prevalence. Am J Clin Pathol. 2007; 128: 585–589. https://doi.org/10.1309/R1YL4B4BT2WCQDGV PMID: 17875509