{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,25]],"date-time":"2026-06-25T23:09:20Z","timestamp":1782428960201,"version":"3.54.5"},"reference-count":96,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2023,2,17]],"date-time":"2023-02-17T00:00:00Z","timestamp":1676592000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Discovery Foundation","award":["034609\/2015"],"award-info":[{"award-number":["034609\/2015"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Background: Anaemia affects one in four adults in South Africa, with a higher prevalence in persons with HIV and tuberculosis. The aim of this study is to characterise the causes of anaemia in primary care and a district hospital setting. Methods: A cross-sectional study design investigated a purposive sample of adult males and non-pregnant females at two community health centres and a hospital casualty and outpatients. Fingerpick blood haemoglobin was measured with HemoCueHb201+. Those with moderate and severe anaemia underwent clinical examination and laboratory tests. Results: Of 1327 patients screened, median age was 48 years, and 63.5% were female. Of 471 (35.5%) with moderate and severe anaemia on HemoCue, 55.2% had HIV, 16.6% tuberculosis, 5.9% chronic kidney disease, 2.6% cancer, and 1.3% heart failure. Laboratory testing confirmed 227 (48.2%) with moderate and 111 (23.6%) with severe anaemia, of whom 72.3% had anaemia of inflammation, 26.5% iron-deficiency anaemia, 6.1% folate deficiency, and 2.5% vitamin B12 deficiency. Overall, 57.5% had two or more causes of anaemia. Multivariate modelling showed that patients with severe anaemia were three times more likely to have tuberculosis (OR = 3.1, 95% CI = 1.5\u20136.5; p-value = 0.002). Microcytosis was present in 40.5% with iron deficiency, macrocytosis in 22.2% with folate deficiency, and 33.3% with vitamin B12 deficiency. The sensitivities of the reticulocyte haemoglobin content and % hypochromic red blood cells in diagnosing iron deficiency were 34.7% and 29.7%, respectively. Conclusions: HIV, iron deficiency, and tuberculosis were the most prevalent causes of moderate and severe anaemia. The majority had multiple causes. Iron, folate, and vitamin B12 deficiencies should be identified by biochemical testing rather than by red cell volume.<\/jats:p>","DOI":"10.3390\/ijerph20043584","type":"journal-article","created":{"date-parts":[[2023,2,20]],"date-time":"2023-02-20T03:29:06Z","timestamp":1676863746000},"page":"3584","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Causes of Moderate and Severe Anaemia in a High-HIV and TB-Prevalent Adult Population in the Eastern Cape Province, South Africa"],"prefix":"10.3390","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7100-9999","authenticated-orcid":false,"given":"Don","family":"O\u2019Mahony","sequence":"first","affiliation":[{"name":"Department of Family Medicine and Rural Health, Walter Sisulu University, Mthatha 5117, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9458-3742","authenticated-orcid":false,"given":"Sikhumbuzo A.","family":"Mabunda","sequence":"additional","affiliation":[{"name":"School of Population Health, University of New South Wales, Sydney 2052, Australia"},{"name":"George Institute for Global Health, University of New South Wales, Sydney 2042, Australia"},{"name":"Department of Public Health, Walter Sisulu University, Mthatha 5117, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mbulelo","family":"Mntonintshi","sequence":"additional","affiliation":[{"name":"Department of Family Medicine and Rural Health, Walter Sisulu University, Mthatha 5117, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joshua","family":"Iruedo","sequence":"additional","affiliation":[{"name":"Department of Family Medicine and Rural Health, Walter Sisulu University, Mthatha 5117, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ramprakash","family":"Kaswa","sequence":"additional","affiliation":[{"name":"Department of Family Medicine and Rural Health, Walter Sisulu University, Mthatha 5117, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ernesto","family":"Blanco-Blanco","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine and Pathology, Walter Sisulu University, Mthatha 5100, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Basil","family":"Ogunsanwo","sequence":"additional","affiliation":[{"name":"Department of Surgery, Walter Sisulu University, Mthatha 5117, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kakia Anne Faith","family":"Namugenyi","sequence":"additional","affiliation":[{"name":"Department of Surgery, Walter Sisulu University, Mthatha 5117, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandeep","family":"Vasaikar","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Walter Sisulu University, Mthatha 5117, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Parimalaranie","family":"Yogeswaran","sequence":"additional","affiliation":[{"name":"Department of Family Medicine and Rural Health, Walter Sisulu University, Mthatha 5117, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,17]]},"reference":[{"key":"ref_1","unstructured":"WHO (2015). The Global Prevalence of Anaemia in 2011, World Health Organization."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1186\/s13045-021-01202-2","article-title":"Burden of anemia and its underlying causes in 204 countries and territories, 1990\u20132019: Results from the Global Burden of Disease Study 2019","volume":"14","author":"Safiri","year":"2021","journal-title":"J. Hematol. Oncol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"57","DOI":"10.2215\/CJN.01670408","article-title":"Iron indices in chronic kidney disease in the National Health and Nutritional Examination Survey 1988\u20132004","volume":"4","author":"Fishbane","year":"2009","journal-title":"Clin. J. Am. Soc. Nephrol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1161\/CIRCULATIONAHA.118.030099","article-title":"Anemia and iron deficiency in heart failure: Current concepts and emerging therapies","volume":"138","author":"Anand","year":"2018","journal-title":"Circulation"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1954","DOI":"10.1093\/annonc\/mds112","article-title":"Prevalence and management of cancer-related anaemia, iron deficiency and the specific role of i.v. iron","volume":"23","author":"Aapro","year":"2012","journal-title":"Ann. Oncol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1136\/pgmj.2003.015677","article-title":"Iron deficiency anaemia in general practice: Clinical outcomes over three years and factors influencing diagnostic investigations","volume":"80","author":"Yates","year":"2004","journal-title":"Postgrad. Med. J."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"bjgpopen17X101157","DOI":"10.3399\/bjgpopen17X101157","article-title":"The evaluation of anaemia in an older primary care population: Retrospective population-based study","volume":"1","author":"McCartney","year":"2017","journal-title":"BJGP Open"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1080\/02813432.2021.1970934","article-title":"Diagnostic workup of cancer in patients with new-onset anaemia: A Danish cohort study in general practice","volume":"39","author":"Boennelykke","year":"2021","journal-title":"Scand. J. Prim. Health Care"},{"key":"ref_9","unstructured":"Shisana, O., Labadarios, D., Rehle, T., Simbayi, L., Zuma, K., Dhansay, A., Reddy, P., Parker, W., Hoosain, E., and Naidoo, P. (2013). South African National Health and Nutrition Examination Survey (SANHANES-1), HSRC Press."},{"key":"ref_10","unstructured":"National Department of Health (NDoH), Statistics South Africa (Stats SA), South African Medical Research Council (SAMRC), and ICF (2019). South Africa Demographic and Health Survey 2016, National Department of Health."},{"key":"ref_11","unstructured":"Stats, S. (2021). Mid-Year Population Estimates 2021, Statistical Release P0302 Statistics South Africa."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Kerkhoff, A.D., Wood, R., Cobelens, F.G., Gupta-Wright, A., Bekker, L.-G., and Lawn, S.D. (2015). The predictive value of current haemoglobin levels for incident tuberculosis and\/or mortality during long-term antiretroviral therapy in South Africa: A cohort study. BMC Med., 13.","DOI":"10.1186\/s12916-015-0320-9"},{"key":"ref_13","unstructured":"SAMRC, HSRC, and NICD (2020). The First National TB Prevalence Survey South Africa 2018, South african Medical Research Council. Short Report."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/s12199-020-00931-z","article-title":"Anemia as a risk factor for tuberculosis: A systematic review and meta-analysis","volume":"26","author":"Gelaw","year":"2021","journal-title":"Environ. Health Prev. Med."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/j.ijtb.2019.04.002","article-title":"Prevalence of anemia among patients with tuberculosis: A systematic review and meta-analysis","volume":"66","author":"Barzegari","year":"2019","journal-title":"Indian J. Tuberc."},{"key":"ref_16","first-page":"40","article-title":"Anemia of inflammation","volume":"133","author":"Weiss","year":"2019","journal-title":"Blood J. Am. Soc. Hematol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1080\/20786204.2010.10873936","article-title":"Iron status and anaemia of chronic disease in HIV-infected African women in Mangaung, Bloemfontein","volume":"52","author":"Walsh","year":"2010","journal-title":"S. Afr. Fam. Pract."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1080\/20786190.2015.1071538","article-title":"Retrospective analysis of the prevalence and causes of anaemia in hospitalised elderly patients","volume":"57","author":"Weich","year":"2015","journal-title":"S. Afr. Fam. Pract."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"S105","DOI":"10.1086\/340202","article-title":"Biology of anemia, differential diagnosis, and treatment options in human immunodeficiency virus infection","volume":"185","author":"Claster","year":"2002","journal-title":"J. Infect. Dis."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1016\/j.trstmh.2005.01.002","article-title":"Treatable factors associated with severe anaemia in adults admitted to medical wards in Blantyre, Malawi, an area of high HIV seroprevalence","volume":"99","author":"Lewis","year":"2005","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"ofv173","DOI":"10.1093\/ofid\/ofv173","article-title":"Anemia, Blood Transfusion Requirements and Mortality Risk in Human Immunodeficiency Virus-Infected Adults Requiring Acute Medical Admission to Hospital in South Africa","volume":"2","author":"Kerkhoff","year":"2015","journal-title":"Open Forum Infect. Dis."},{"key":"ref_22","first-page":"a1406","article-title":"Undiagnosed tuberculosis in patients with HIV infection who present with severe anaemia at a district hospital","volume":"9","author":"Mntonintshi","year":"2017","journal-title":"Afr. J. Prm. Health Care Fam. Med."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"193","DOI":"10.5588\/ijtld.15.0558","article-title":"Anaemia in patients with HIV-associated TB: Relative contributions of anaemia of chronic disease and iron deficiency","volume":"20","author":"Kerkhoff","year":"2016","journal-title":"Int. J. Tuberc. Lung Dis."},{"key":"ref_24","unstructured":"Stats, S.A. (2018). Poverty Mapping in South Africa. Applying Small Area Estimation Techniques Using IES 2010\/11 and Census 2011, Statistics South Africa."},{"key":"ref_25","unstructured":"Joubert, G., Ehrlich, R., Katzenellenbogen, J.M., and Karim, S.A. (2007). Epidemiology: A Research Manual for South Africa, Oxford University Press Southern Africa. [2nd ed.]."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1186\/cc1521","article-title":"Statistics review 4: Sample size calculations","volume":"6","author":"Whitley","year":"2002","journal-title":"Crit Care"},{"key":"ref_27","unstructured":"WHO (2011). Vitamin and Mineral Nutrition Information System, World Health Organization. WHO\/NMH\/NHD\/MNM\/11.1."},{"key":"ref_28","unstructured":"NDoH (2016). Implementation of the Universal Test and Treat Strategy for HIV Positive Patients and Differentiated Care for Stable Patients, National Department of Health. Circular dated 16 August 2016."},{"key":"ref_29","unstructured":"NDoH (2014). Primary Healthcare Standard Treatment Guidelines and Essential Medicines List, National Department of Health, Republic of South Africa. [5th ed.]."},{"key":"ref_30","unstructured":"NDoH (2015). National Consolidated Guidelines for the Prevention of Mother-to-Child Transmission of HIV (PMTCT) and the Management of HIV in Children, Adolescents and Adults, Department of Health."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1186\/2036-7902-4-21","article-title":"Focused assessment with sonography for HIV-associated tuberculosis (FASH): A short protocol and a pictorial review","volume":"4","author":"Heller","year":"2012","journal-title":"Crit. Ultrasound J."},{"key":"ref_32","unstructured":"Kasper, D., Fauci, A., Hauser, S., Longo, D., Jameson, J., and Loscalzo, J. (2015). Harrison\u2019s Principles of Internal Medicine, 19e, McGraw-Hill."},{"key":"ref_33","unstructured":"NDoH (2019). Hospital Level (Adults) Standard Treatment Guidelines and Essential Medicines List, Department of Health. [5th ed.]."},{"key":"ref_34","unstructured":"NICE (2015). Anaemia Management in People with Chronic Kidney Disease, National Institute for Health and Care Excellence."},{"key":"ref_35","first-page":"2","article-title":"Diagnostic Approaches to Iron Deficient States and Iron Deficiency Anemia","volume":"10","author":"Brugnara","year":"2019","journal-title":"Haema"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1056\/NEJMcp1113996","article-title":"Clinical practice. Vitamin B12 deficiency","volume":"368","author":"Stabler","year":"2013","journal-title":"N. Engl. J. Med."},{"key":"ref_37","unstructured":"WHO (2015). Serum and Red Blood Cell Folate Concentrations for Assessing Folate Status in Populations, World Health Organization. WHO\/NMH\/NHD\/EPG\/15.01."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1093\/clinchem\/44.1.45","article-title":"Clinical utility of the soluble transferrin receptor and comparison with serum ferritin in several populations","volume":"44","author":"Mast","year":"1998","journal-title":"Clin. Chem."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"100861","DOI":"10.1016\/j.mam.2020.100861","article-title":"The changing landscape of iron deficiency","volume":"75","author":"Camaschella","year":"2020","journal-title":"Mol. Asp. Med."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1111\/joim.13004","article-title":"Iron deficiency anaemia revisited","volume":"287","author":"Cappellini","year":"2020","journal-title":"J. Intern. Med."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1148","DOI":"10.1056\/NEJMra1804281","article-title":"Anemia of Inflammation","volume":"381","author":"Ganz","year":"2019","journal-title":"N. Engl. J. Med."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2129","DOI":"10.1093\/eurheartj\/ehw128","article-title":"2016 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure","volume":"37","author":"Ponikowski","year":"2016","journal-title":"Eur. Heart J."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"iv96","DOI":"10.1093\/annonc\/mdx758","article-title":"Management of anaemia and iron deficiency in patients with cancer: ESMO Clinical Practice Guidelines","volume":"29","author":"Aapro","year":"2018","journal-title":"Ann. Oncol."},{"key":"ref_44","unstructured":"NICE (2021). Chronic Kidney Disease: Assessment and Management (NG203), National Institute for Health and Care Excellence."},{"key":"ref_45","unstructured":"KDIGO (2012). KDIGO clinical practice guidelines for acute kidney injury. Kidney Int. Suppl., 2, 1\u2013138."},{"key":"ref_46","unstructured":"KDIGO CKD Work Group (2013). KDIGO 2012. Clinical Practice Guideline for the Evaluation and Management of Chronic Kidney Disease. Kidney Int., 3, S1\u2013S150."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Mikhail, A., Brown, C., Williams, J.A., Mathrani, V., Shrivastava, R., Evans, J., Isaac, H., and Bhandari, S. (2017). Clinical Practice Guideline: Anaemia of Chronic Kidney Disease, The Renal Association.","DOI":"10.1186\/s12882-017-0688-1"},{"key":"ref_48","first-page":"1","article-title":"Revised surveillance case definition for HIV infection\u2014United States, 2014","volume":"63","author":"Selik","year":"2014","journal-title":"Morb. Mortal. Wkly. Rep. Recomm. Rep."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Mash, B., Fairall, L., Adejayan, O., Ikpefan, O., Kumari, J., Mathee, S., Okun, R., and Yogolelo, W. (2012). A morbidity survey of South African primary care. PLoS ONE, 7.","DOI":"10.1371\/annotation\/3545077e-aded-4eef-a460-be1edbd1845c"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1136\/jech-2018-210449","article-title":"Cross-sectional relationship between haemoglobin concentration and measures of physical and cognitive function in an older rural South African population","volume":"72","author":"Payne","year":"2018","journal-title":"J. Epidemiol. Community Health"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1111\/nyas.14124","article-title":"Methods and analyzers for hemoglobin measurement in clinical laboratories and field settings","volume":"1450","author":"Whitehead","year":"2019","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Randi, M.L., Bertozzi, I., Santarossa, C., Cosi, E., Lucente, F., Bogoni, G., Biagetti, G., and Fabris, F. (2020). Prevalence and Causes of Anemia in Hospitalized Patients: Impact on Diseases Outcome. J. Clin. Med., 9.","DOI":"10.3390\/jcm9040950"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2263","DOI":"10.1182\/blood-2004-05-1812","article-title":"Prevalence of anemia in persons 65 years and older in the United States: Evidence for a high rate of unexplained anemia","volume":"104","author":"Guralnik","year":"2004","journal-title":"Blood"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1007\/BF02598003","article-title":"Laboratory diagnosis of iron-deficiency anemia","volume":"7","author":"Guyatt","year":"1992","journal-title":"J. Gen. Intern. Med."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/j.arcmed.2018.12.005","article-title":"Are current serum and plasma ferritin cut-offs for iron deficiency and overload accurate and reflecting iron status? A systematic review","volume":"49","author":"Pasricha","year":"2018","journal-title":"Arch. Med. Res."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1080\/10408363.2019.1653820","article-title":"Using transferrin saturation as a diagnostic criterion for iron deficiency: A systematic review","volume":"56","author":"Cacoub","year":"2019","journal-title":"Crit. Rev. Clin. Lab. Sci."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"e40","DOI":"10.1097\/HS9.0000000000000040","article-title":"Anemia in the elderly","volume":"2","author":"Girelli","year":"2018","journal-title":"HemaSphere"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1016\/S0140-6736(73)91446-3","article-title":"Differentiation of iron deficiency from thalassaemia trait","volume":"301","author":"Mentzer","year":"1973","journal-title":"Lancet"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1136\/jmg.24.4.215","article-title":"Inherited haemoglobin variants in a South African population","volume":"24","author":"Bird","year":"1987","journal-title":"J. Med. Genet."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"276","DOI":"10.7196\/SAMJ.2016.v106i3.10005","article-title":"Alpha-thalassaemia trait as a cause of unexplained microcytosis in a South African population","volume":"106","author":"Loonat","year":"2016","journal-title":"S. Afr. Med. J."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"989","DOI":"10.7196\/SAMJ.7255","article-title":"Testing for haemoglobinopathies in Johannesburg, South Africa: A 30-year review","volume":"103","author":"Krause","year":"2013","journal-title":"S. Afr. Med. J."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/j.ebiom.2017.09.024","article-title":"How long can we store blood samples: A systematic review and meta-analysis","volume":"24","author":"Wu","year":"2017","journal-title":"EBioMedicine"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"S41","DOI":"10.7196\/SAMJ.2019.v109i8b.13829","article-title":"HIV and haematopoiesis","volume":"109","author":"Durandt","year":"2019","journal-title":"S. Afr. Med. J."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"101283","DOI":"10.1016\/j.eclinm.2022.101283","article-title":"Prevalence of anemia among people living with HIV: A systematic review and meta-analysis","volume":"44","author":"Cao","year":"2022","journal-title":"eClinicalMedicine"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1595","DOI":"10.1093\/cid\/ciw125","article-title":"Incidence of Opportunistic Infections and the Impact of Antiretroviral Therapy Among HIV-Infected Adults in Low- and Middle-Income Countries: A Systematic Review and Meta-analysis","volume":"62","author":"Low","year":"2016","journal-title":"Clin. Infect. Dis."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1713","DOI":"10.3201\/eid1010.030985","article-title":"Current epidemiology of Pneumocystis pneumonia","volume":"10","author":"Morris","year":"2014","journal-title":"Emerg. Infect. Dis."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1093\/cid\/ciu261","article-title":"Impact of Risk Factors for Specific Causes of Death in the First and Subsequent Years of Antiretroviral Therapy Among HIV-Infected Patients","volume":"59","author":"Ingle","year":"2014","journal-title":"Clin. Infect. Dis."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"828939","DOI":"10.1155\/2013\/828939","article-title":"Risk factors for tuberculosis","volume":"2013","author":"Narasimhan","year":"2013","journal-title":"Pulm. Med."},{"key":"ref_69","unstructured":"Merritt, B.Y. (2019). Mean Corpuscular Hemoglobin (MCH) and Mean Corpuscular Hemoglobin Concentration (MCHC), Medscape, WebMD LLC. Available online: https:\/\/emedicine.medscape.com\/article\/2054497."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1832","DOI":"10.1056\/NEJMra1401038","article-title":"Iron-Deficiency Anemia","volume":"372","author":"Camaschella","year":"2015","journal-title":"N. Engl. J. Med."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.5588\/ijtld.17.0078","article-title":"Diagnostic accuracy of C-reactive protein for active pulmonary tuberculosis: A meta-analysis","volume":"21","author":"Yoon","year":"2017","journal-title":"Int. J. Tuberc. Lung Dis"},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Brown, J., Clark, K., Smith, C., Hopwood, J., Lynard, O., Toolan, M., Creer, D., Barker, J., Breen, R., and Brown, T. (2016). Variation in C\u2014Reactive protein response according to host and mycobacterial characteristics in active tuberculosis. BMC Infect. Dis., 16.","DOI":"10.1186\/s12879-016-1612-1"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1016\/j.jinf.2013.12.012","article-title":"High serum levels of procalcitonin and soluble TREM-1 correlated with poor prognosis in pulmonary tuberculosis","volume":"68","author":"Huang","year":"2014","journal-title":"J. Infect."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Kaze, A.D., Ilori, T., Jaar, B.G., and Echouffo-Tcheugui, J.B. (2018). Burden of chronic kidney disease on the African continent: A systematic review and meta-analysis. BMC Nephrol., 19.","DOI":"10.1186\/s12882-018-0930-5"},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Hill, N.R., Fatoba, S.T., Oke, J.L., Hirst, J.A., O\u2019Callaghan, C.A., Lasserson, D.S., and Hobbs, F.R. (2016). Global prevalence of chronic kidney disease\u2013a systematic review and meta-analysis. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0158765"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.pcd.2014.05.002","article-title":"Diabetes care and complications in primary care in the Tshwane district of South Africa","volume":"9","author":"Webb","year":"2015","journal-title":"Prim. Care Diabetes"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"e1159","DOI":"10.1016\/S2214-109X(22)00239-X","article-title":"Measurement of kidney function in Malawi, South Africa, and Uganda: A multicentre cohort study","volume":"10","author":"Fabian","year":"2022","journal-title":"Lancet Glob. Health"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"e1080","DOI":"10.1016\/S2214-109X(22)00279-0","article-title":"Measuring kidney function: The voice of Africa","volume":"10","author":"Niang","year":"2022","journal-title":"Lancet Glob. Health"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"19","DOI":"10.2147\/IJNRD.S179802","article-title":"Ethnic prevalence of anemia and predictors of anemia among chronic kidney disease patients at a tertiary hospital in Johannesburg, South Africa","volume":"12","author":"Nalado","year":"2019","journal-title":"Int. J. Nephrol. Renov. Dis."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"1280","DOI":"10.1016\/j.kint.2021.03.020","article-title":"Controversies in optimal anemia management: Conclusions from a Kidney Disease: Improving Global Outcomes (KDIGO) Conference","volume":"99","author":"Babitt","year":"2021","journal-title":"Kidney Int."},{"key":"ref_81","unstructured":"KDIGO (2012). Kidney Disease: Improving Global Outcomes (KDIGO) Anaemia Work Group clinical practice guideline for anemia in chronic kidney disease. Kidney Int. Suppl., 2, 279\u2013335."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1053\/j.ajkd.2003.12.046","article-title":"Unreferred chronic kidney disease: A longitudinal study","volume":"43","author":"John","year":"2004","journal-title":"Am. J. Kidney Dis."},{"key":"ref_83","first-page":"89","article-title":"Folate and iron status of South African non-pregnant rural women of childbearing age, before and after fortification of foods","volume":"20","author":"Modjadji","year":"2007","journal-title":"S. Afr. J. Clin. Nutr."},{"key":"ref_84","unstructured":"NDOH (2015). Standard Treatment Guidelines and Essential Medicines List for South Africa. Hospital Level, Adults, NDOH. [4th ed.]."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1111\/bjh.13783","article-title":"Haematological manifestations of human immune deficiency virus infection","volume":"171","author":"Vishnu","year":"2015","journal-title":"Br. J. Haematol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1002\/ajh.2830490410","article-title":"Clinical correlates of subnormal vitamin B12 levels in patients infected with the human immunodeficiency virus","volume":"49","author":"Paltiel","year":"1995","journal-title":"Am. J. Hematol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1258\/095646204322764334","article-title":"Low serum vitamin B12 levels in an outpatient HIV-infected population","volume":"15","author":"Hepburn","year":"2004","journal-title":"Int. J. STD AIDS"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"978","DOI":"10.7196\/SAMJ.7022","article-title":"Haematological implications of folate food fortification","volume":"103","author":"Metz","year":"2013","journal-title":"S. Afr. Med. J."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"e1919274","DOI":"10.1001\/jamanetworkopen.2019.19274","article-title":"Association of plasma concentration of vitamin B12 with all-cause mortality in the general population in the Netherlands","volume":"3","author":"Groothof","year":"2020","journal-title":"JAMA Netw. Open"},{"key":"ref_90","doi-asserted-by":"crossref","unstructured":"Wolffenbuttel, B.H.R., Heiner-Fokkema, M.R., Green, R., and Gans, R.O.B. (2020). Relationship between serum B12 concentrations and mortality: Experience in NHANES. BMC Med., 18.","DOI":"10.1186\/s12916-020-01771-y"},{"key":"ref_91","unstructured":"Labadarios, D. (2007). National Food Consumption SurveyFortification Baseline (NFCS-FB): South Africa, 2005, Department of Health."},{"key":"ref_92","unstructured":"Greer, J.P., Arber, D.A., Glader, B., List, A.F., Means, R.T.J., Paraskevas, F., and Rodgers, G.M. (2014). Wintrobe\u2019s Clinical Hematology, Lippincott, Williams & Wilkins. [13th ed.]."},{"key":"ref_93","unstructured":"Kasper, D., Fauci, A., Hauser, S., Longo, D., Jameson, J., and Loscalzo, J. (2015). Harrison\u2019s Principles of Internal Medicine, 19e, McGraw-Hill."},{"key":"ref_94","unstructured":"NDoH (2020). Primary Healthcare Standard Treatment Guideline and Essential Medicine List, National Department of Health. [7th ed.]."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1016\/j.ejim.2012.03.013","article-title":"Anaemia in the elderly: An aetiologic profile of a prospective cohort of 95 hospitalised patients","volume":"23","author":"Petrosyan","year":"2012","journal-title":"Eur. J. Intern. Med."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"g2276","DOI":"10.1136\/bmj.g2276","article-title":"Cross sectional studies: Advantages and disadvantages","volume":"348","author":"Sedgwick","year":"2014","journal-title":"BMJ"}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/20\/4\/3584\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:39:36Z","timestamp":1760121576000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/20\/4\/3584"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,17]]},"references-count":96,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["ijerph20043584"],"URL":"https:\/\/doi.org\/10.3390\/ijerph20043584","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,17]]}}}