Anemia in patients with diabetic foot ulcer and its impact on disease outcome among Nigerians: Results from the MEDFUN study

Autoři: Ibrahim D. Gezawa aff001;  Ejiofor T. Ugwu aff002;  Ignatius Ezeani aff003;  Olufunmilayo Adeleye aff004;  Innocent Okpe aff005;  Marcelina Enamino aff006
Působiště autorů: Division of Endocrinology, Diabetes and Metabolism, Department of Medicine, Bayero University, Kano, Nigeria aff001;  Division of Endocrinology, Diabetes and Metabolism, Department of Medicine, Enugu State University of Science and Technology, Enugu, Nigeria aff002;  Division of Endocrinology, Diabetes and Metabolism, Department of Medicine, Federal Medical Center, Umuahia, Nigeria aff003;  Division of Endocrinology, Diabetes and Metabolism, Department of Medicine, Lagos State University, Lagos, Nigeria aff004;  Division of Endocrinology, Diabetes and Metabolism, Department of Medicine, Ahmadu Bello University, Zaria, Nigeria aff005;  Division of Endocrinology, Diabetes and Metabolism, Department of Medicine, Federal Medical Center, Keffi, Nigeria aff006
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article



Diabetes is a life-long and debilitating disease that is fraught with both acute and chronic complications. Of particular concern to sufferers of the disease is the development of foot problems. These problems range from foot deformities to slowly healing or non-healing ulcers (that may necessitate amputation) and in the worst-case scenario, to death. Identification and prompt treatment of comorbid conditions, such as anemia may improve outcome in patients with diabetic foot ulcers (DFU). We determined the prevalence of anemia in Nigerians with DFU and its impact on disease outcome.


We prospectively followed 336 patients with diabetes hospitalized for DFU and managed by a multidisciplinary team until discharge or death. Demographic and diabetes-related information and ulcer characteristics were documented. We evaluated each patient for neuropathy, vasculopathy and medical co-morbidities. Relevant laboratory and imaging studies were performed. We present the results of the sub-group analysis of patients with anemia to determine its prevalence and impact on disease outcome in patients with DFU in the MEDFUN study.


Anemia was detected in 180(53.6%) subjects with 88(48.9%) of them requiring blood transfusion. Significant demographic and clinical determinants of anemia were ulcer duration more than one month prior to hospitalization (p<0.009), PAD (p<0.001) and presence of gangrene (p<0.001). The comorbid conditions that were significantly associated with anemia included proteinuria (p<0.003), osteomyelitis (p<0.006), moderate (p<0.002) as well as severe (p<0.001) vascular stenosis, history of stroke (p<0.014) and renal impairment (p<0.002). Anemia was significantly associated with poor wound healing (p<0.009), amputation (p<0.036) and risk of death (p<0.034).


We detected anemia in more than half of our cohort with DFU. We found significant association between anemia and poor wound healing, amputation and mortality among our studied subjects. Future studies should explore whether prompt correction of anemia in subjects hospitalized for DFU would improve outcome.

Klíčová slova:

anémia – Inflammation – Nigeria – Stenosis – stroke – Ulcers – Wound healing


1. International Diabetes Federation (IDF) Atlas, 8th Edition, 2017.

2. Sharif A, Younus S, Baig K, Ali N. Prevalence and risk of anemia in type-2 diabetic patients. Health. 2014; 6:1415–1419.

3. Singh N, Armstrong D.G, Lipsky B.A. Preventing foot ulcers in patients with diabetes. The Journal of the American Medical Association. 2005; 293:217–228. doi: 10.1001/jama.293.2.217 15644549

4. Bakri FG, Allan AH, Khader YS, Younes NA, Ajlouni KM. Prevalence of diabetic foot ulcer and its associated risk factors among diabetic patients in Jordan. J Med J.2012;46(2):118–25

5. Yazdanapah L, Nasiri M, Adarvishi S. Literature review on the management of diabetic foot ulcer. World J Diabetes.2015; 6(1):37–53 doi: 10.4239/wjd.v6.i1.37 25685277

6. Fasanmade O, Dagogo-Jack S. Diabetes Care in Nigeria. Ann Global Health.2015; 81(6):821–9

7. Brownrigg JRW, Apelqvist J, Bakker K, Schaper NC, Hinchliffe RJ. Evidence-based management of PAD & the diabetic foot. European Journal of Vascular and Endovascular Surgery.2013; 45(6):673–681. doi: 10.1016/j.ejvs.2013.02.014 23540807

8. Cawood TJ, Buckley U, Murray A, Corbett M, Dillon D, Goodwin B, et al., Prevalence of anemia in patients with diabetes mellitus. Irish Journal of Medical Science 2006; 175(2):25–27. doi: 10.1007/bf03167944 16872024

9. Wright JA, Oddy MJ, Richards T. Presence and characterization of anemia in diabetic foot ulceration. Anemia. 2014:104214. doi: 10.1155/2014/104214 25197565

10. Chen CXR, Li YC, Chan SL, Chan KH. Anaemia and type 2 diabetes: implications from a retrospectively studied primary care case series. Hong Kong Medical Journal 2013; 19(3):214–221. doi: 10.12809/hkmj133814 23568938

11. Ugwu E, Adeleye O, Gezawa I, Okpe I, Enamino M, Ezeani I. Burden of diabetic foot ulcer in Nigeria: Current evidence from the multicenter evaluation of diabetic foot ulcer in Nigeria. World J Diabetes 2019; 10(3): 200–211. doi: 10.4239/wjd.v10.i3.200 30891155

12. Chuan F, Zhang M, Yao Y, Tian W, He X, Zhou B.Anemia in Patients with Diabetic Foot Ulcer: Prevalence, Clinical Characteristics, and Outcome.Int J Low Extrem Wounds 2016; 15(3):220–6. doi: 10.1177/1534734616660224 27440798

13. Thomas MC, MacIsaac RJ, Tsalamandris C, Power D, and Jerums G. Unrecognized anemia in patients with diabetes: a cross-sectional survey.2003; 26(4):1164–1169.

14. Cawood TJ, Buckley U, Murray A, Corbett M, Dillon D, Goodwin B,et al. Prevalence of anemia in patients with diabetes mellitus. Irish Journal of Medical Science 2006; 175(2)25–27. doi: 10.1007/bf03167944 16872024

15. Stevens PE, O’Donoghue DJ, and Lameire NR. Anemia in patients with diabetes: unrecognised, undetected and untreated. Current Medical Research and Opinion 2003; 19(5):395–401. doi: 10.1185/030079903125002036 13678476

16. Babatunde IA, Uchechukwu D, Chinwe OE, Abduffatah AO, Azukaego TM, Tosan AE et al. Incidence and risk of anemia in type 2 diabetic patients in the absence of renal impairment, Health. 2012; 4: 304–308.

17. Ekpebegh CO, Iwuala SO, Fasanmade OA, Ogbera AO, Igumbor E, Ohwovoriole AE. Diabetes foot ulceration in a Nigerian Hospital: in-hospital mortality in relation to the presenting demographic, clinical and laboratory features. Int Wound J 2009;6:381–385. doi: 10.1111/j.1742-481X.2009.00627.x 19912395

18. Ogbera OA, Osa E, Edo A, Chukwum E. Common clinical features of diabetic foot ulcers: perspectives from a developing nation, International Journal o Lower Extremity Wounds 2008;7(2): 93–98.

19. WHO, Hemoglobin Concentrations for the Diagnosis of Anemia and Assessment of Severity, 2011.

20. Richards T. Anemia in hospital practice. The British Journal of Hospital Medicine. 2012; 73(10): 571–575. doi: 10.12968/hmed.2012.73.10.571 23124287

21. Mustafa K, Stavros L, Josephine W, Steven H, Toby R. Anemia, inflammation, renal function, and the diabetic foot: What are the relationships?. The diabetic foot journal. 2012; 15(4): 150–158.

22. Thomas MC, MacIsaac RJ, Tsalamandris C, Molyneaux L, Goubina I, Fulcher G, et al. The burden of anemia in type 2 diabetes and the role of nephropathy: a cross-sectional audit. Nephrol Dial Transplant. 2004; 19:1792–1797 doi: 10.1093/ndt/gfh248 15102962

23. New JP, Aung T, Baker PG, Yongsheng G, Pylypczuk R, Houghton J, et al. The high prevalence of unrecognized anemia in patients with diabetes and chronic kidney disease: a population-based study. Diabet Med. 2008; 25:564–569. doi: 10.1111/j.1464-5491.2008.02424.x 18445169

24. Lewis S, Raj D, Guzman NJ. Renal failure: Implications of chronic kidney disease in the management of the diabetic foot. Seminars in Vascular Surgery. 2012; 25(2):82–88. doi: 10.1053/j.semvascsurg.2012.04.007 22817857

25. Wang A, Xu Z, Mu Y, Ji L. Clinical characteristics and medical costs in patients with diabetic amputation and nondiabetic patients with nonacute amputation in central urban hospitals in China. Int J Low Extrem Wounds. 2014; 13:17–21. doi: 10.1177/1534734614521235 24659623

26. Cahn A, Livshits L, Srulevich A, Raz I, Yedgar S, Barshtein G. Diabetic foot disease is associated with reduced erythrocyte deformability. Int Wound J. 2016; 13: 500–4. doi: 10.1111/iwj.12466 26018868

27. Milionis H, Papavasileiou V, Eskandari A, D’Ambrogio Remillard S, Ntaios G, Michel P. Anemia on admission predicts short- and long-term outcomes in patients with acute ischemic stroke. Int J Stroke. 2015; 10:224–230. doi: 10.1111/ijs.12397 25427291

28. Costa RHR, Cardoso NA, Procópio RJ, Navarro TP, Dardik A, de Loiola Cisneros L.Diabetic foot ulcer carries high amputation and mortality rates, particularly in the presence of advanced age, peripheral artery disease and anemia. Diabetes Metab syndr. 2017; 11 (2):S583–S587.

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2019 Číslo 12
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