Anemia in Patients with Diabetic Foot Ulcer: Effects on Diabetic Microvascular Complications and Related Conditions

Author(s): Mehtap E. Olgun*, Seher Ç. Altuntaş, Murat Sert, Tamer Tetiker.

Journal Name: Endocrine, Metabolic & Immune Disorders - Drug Targets
(Formerly Current Drug Targets - Immune, Endocrine & Metabolic Disorders)

Volume 19 , Issue 7 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Objective: We aimed to investigate the etiology and prevalence of anemia in patients with diabetic foot ulcers and the relationship between both microvascular complications and related conditions and anemia.

Methods: We retrospectively collected and evaluated the data of 225 patients with diabetic foot ulcer followed at our clinic. The demographic characteristics of the patients were analyzed. Complete blood count for those with anemia, serum iron, iron-binding capacity, ferritin, transferrin saturation index, vitamin B12, folic acid and thin blood film were performed. The diabetic microvascular complications and related conditions such as osteomyelitis, peripheral artery disease, and amputations were also determined. IBM SPSS Statistics Version 20.0 package software was used for the statistical analysis of the data.

Results: Of 225 patients were 67 (29%) female and 158 (70.2%) male. The mean age of the patients was 62 ± 10.5 years (30-87). Duration of diabetes was 16.2 ± 6.7 years (2-31). Of the 225 patients, 41 had hypertension, 14 had chronic kidney failure, and 34 had coronary artery disease. Anemia was found in 192 (85.3%) of the 225 patients. Of 192, 126 (56%) had iron deficiency anemia, 50 had folate- deficiency anemia, and the remaining 16 had anemia of chronic disease. Iron deficiency anemia was significantly found to be higher in women. There was no significant difference between patients with and without anemia in terms of diabetic microvascular complications (neuropathy, retinopathy, nephropathy) and the related conditions.

Conclusion: We have found that the most common cause of anemia was iron deficiency anemia. However, in our study, the prevalences of microvascular complications did not vary between patients with and without anemia. On the other hand, since all of our patients are having DFU and the high rates of microvascular complications and correlation with the presence of anemia could not be clearly portrayed.

Keywords: Anemia, diabetic foot ulcers, microvascular complications, related conditions, iron deficiency anemia, anemia of chronic disease.

[1]
Zhang, P.; Lu, J.; Jing, Y.; Tang, S.; Zhu, D.; Bi, Y. Global epidemiology of diabetic foot ulceration: a systematic review and meta-analysis . Ann. Med., 2017, 49(2), 106-116.
[http://dx.doi.org/10.1080/07853890.2016.1231932] [PMID: 27585063]
[2]
Boulton, A.J.; Kirsner, R.S.; Vileikyte, L. Clinical practice. Neuropathic diabetic foot ulcers. N. Engl. J. Med., 2004, 351(1), 48-55.
[http://dx.doi.org/10.1056/NEJMcp032966] [PMID: 15229307]
[3]
Amstrong, D.G.; Lavery, L.A. Diabetic foot ulcers: preventation, diagnosis and classification. Am Fam Phys, 1998, 57(6), 1325-1332.
[4]
Thomas, M.C.; MacIsaac, R.J.; Tsalamandris, C.; Molyneaux, L.; Goubina, I.; Fulcher, G.; Yue, D.; Jerums, G. The burden of anaemia in type 2 diabetes and the role of nephropathy: a cross-sectional audit. Nephrol. Dial. Transplant., 2004, 19(7), 1792-1797.
[http://dx.doi.org/10.1093/ndt/gfh248] [PMID: 15102962]
[5]
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), 220-226.
[http://dx.doi.org/10.1177/1534734616660224] [PMID: 27440798]
[6]
Craig, K.J.; Williams, J.D.; Riley, S.G.; Smith, H.; Owens, D.R.; Worthing, D.; Cavill, I.; Phillips, A.O. Anemia and diabetes in the absence of nephropathy. Diabetes Care, 2005, 28(5), 1118-1123.
[http://dx.doi.org/10.2337/diacare.28.5.1118] [PMID: 15855576]
[7]
Wright, J.A.; Oddy, M.J.; Richards, T. Clinical Study Presence and Characterisation of Anaemia in Diabetic Foot Ulceration., 2014.
[8]
Singh, M.; Shin, S. Changes in erythrocyte aggregation and deformability in diabetes mellitus: a brief review. Indian J. Exp. Biol., 2009, 47(1), 7-15.
[PMID: 19317346]
[9]
Fine, L.G.; Bandyopadhay, D.; Norman, J.T. Is there a common mechanism for the progression of different types of renal disease other than proteinuria? Toward the unifying theme of chronic hypoxia. Kidney Int., 2000, 57(75), S22-S26.
[http://dx.doi.org/10.1046/j.1523-1755.2000.07512.x]
[10]
Grune, T.; Sommerburg, O.; Siems, W.G. Oxidative stress in anemia. Clin. Nephrol., 2000, 53(1)(Suppl.), S18-S22.
[PMID: 10746801]
[11]
Conway, B.N.; Miller, R.G.; Klein, R.; Orchard, T.J. Prediction of proliferative diabetic retinopathy with hemoglobin level. Arch. Ophthalmol., 2009, 127(11), 1494-1499.
[http://dx.doi.org/10.1001/archophthalmol.2009.274] [PMID: 19901215]
[12]
Salman, I.S; Wadood, S.A; Abualkasem, B.A. Low Hemoglobin Levels in Infected Diabetic Foot Ulcer IOSR Journal of Pharmacy and Biological Sciences (IOSR-JPBS), 2017, 12(1), 5-9.
[13]
Wagner, F.W., Jr The dysvascular foot: a system for diagnosis and treatment. Foot Ankle, 1981, 2(2), 64-122.
[http://dx.doi.org/10.1177/107110078100200202] [PMID: 7319435]
[14]
Snyder, L.M.; Williamson, M.A. Wallach’s Interpretation of Diagnostic Tests. (9. Ed..),, 2012.
[15]
Weiss, G.; Goodnough, L.T. Anemia of chronic disease. N. Engl. J. Med., 2005, 352(10), 1011-1023.
[http://dx.doi.org/10.1056/NEJMra041809] [PMID: 15758012]
[16]
Hokkam, E.N. Assessment of risk factors in diabetic foot ulceration and their impact on the outcome of the disease. Prim. Care Diabetes, 2009, 3(4), 219-224.
[http://dx.doi.org/10.1016/j.pcd.2009.08.009] [PMID: 19783493]
[17]
Chen, C.X.R.; Li, Y.C.; Chan, S.L.; Chan, K.H. Anaemia and type 2 diabetes: implications from a retrospectively studied primary care case series. Hong Kong Med. J., 2013, 19(3), 214-221.
[http://dx.doi.org/10.12809/hkmj133814] [PMID: 23568938]
[18]
Kengne, A.P.; Czernichow, S.; Hamer, M.; Batty, G.D.; Stamatakis, E. Anaemia, haemoglobin level and cause-specific mortality in people with and without diabetes. PLoS One, 2012, 7(8)e41875
[http://dx.doi.org/10.1371/journal.pone.0041875] [PMID: 22876293]
[19]
Nagyl, J.; Kiss, I.; Wittmann, I. Early anemia in diabetic nepropathy. Orv. Hefil, 2005, 146(9), 397-401.
[20]
McClellan, W.M.; Flanders, W.D.; Langston, R.D.; Jurkovitz, C.; Presley, R. Anemia and renal insufficiency are independent risk factors for death among patients with congestive heart failure admitted to community hospitals: a population-based study. J. Am. Soc. Nephrol., 2002, 13(7), 1928-1936.
[http://dx.doi.org/10.1097/01.ASN.0000018409.45834.FA] [PMID: 12089390]
[21]
Laville, M. New strategies in anaemia management: ACORD (Anaemia CORrection in Diabetes) trial. Acta Diabetol., 2004, 41(1)(Suppl. 1), S18-S22.
[http://dx.doi.org/10.1007/s00592-004-0134-2] [PMID: 15103544]
[22]
He, B.B.; Xu, M.; Wei, L.; Gu, Y.J.; Han, J.F.; Liu, Y.X.; Bao, Y.Q.; Jia, W.P. Relationship between anemia and chronic complications in Chinese patients with type 2 diabetes mellitus. Arch. Iran Med., 2015, 18(5), 277-283.
[PMID: 25959909]
[23]
Brownrigg, J.R.W.; Apelqvist, J.; Bakker, K.; Schaper, N.C.; Hinchliffe, R.J. Evidence-based management of PAD & the diabetic foot. Eur. J. Vasc. Endovasc. Surg., 2013, 45(6), 673-681.
[http://dx.doi.org/10.1016/j.ejvs.2013.02.014] [PMID: 23540807]
[24]
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(2), 224-230.
[http://dx.doi.org/10.1111/ijs.12397] [PMID: 25427291]
[25]
De Block, C.E.M.; Van Campenhout, C.M.; De Leeuw, I.H.; Keenoy, B.M.; Martin, M.; Van Hoof, V.; Van Gaal, L.F. Soluble transferrin receptor level: a new marker of iron deficiency anemia, a common manifestation of gastric autoimmunity in type 1 diabetes. Diabetes Care, 2000, 23(9), 1384-1388.
[http://dx.doi.org/10.2337/diacare.23.9.1384] [PMID: 10977038]
[26]
Qiaro, Q. Keinanan- Kiuhanniemi, S; Laura, E. The relationship between hemoglobin levels and diabetic retinopathy. J. Clin. Epidemiol., 1997, •••, 50-158.
[27]
Friedman, E.A.; Brown, C.D.; Berman, D.H. Erythropoietin in diabetic macular edema and renal insufficiency. Am. J. Kidney Dis., 1995, 26(1), 202-208.
[http://dx.doi.org/10.1016/0272-6386(95)90175-2] [PMID: 7611253]
[28]
Berman, D.H.; Friedman, E.A. Partial absorption of hard exudates in patients with diabetic end-stage renal disease and severe anemia after treatment with erythropoietin. Retina, 1994, 14(1), 1-5.
[http://dx.doi.org/10.1097/00006982-199401000-00001] [PMID: 8016453]
[29]
Kim, M.K.; Baek, K.H.; Lim, D.J.; Kim, Y.K.; Kang, M.I.; Lee, K.W.; Song, K.H. Erythropoietin response to anemia and its association with autonomic neuropathy in type 2 diabetic patients without advanced renal failure. J. Diabetes Complications, 2010, 24(2), 90-95.
[http://dx.doi.org/10.1016/j.jdiacomp.2009.02.002] [PMID: 19303331]
[30]
Saito, T.; Tojo, K.; Morimoto, A.; Tajima, N. Normocytic normochromic anemia due to automatic neuropathy in type 2 diabetic patients without severe nephropathy: a possible role of microangiopathy. Diabetes Res. Clin. Pract., 2005, 70(3), 239-247.
[http://dx.doi.org/10.1016/j.diabres.2005.04.003] [PMID: 16323260]
[31]
Aziz, Z.; Lin, W.K.; Nather, A.; Huak, C.Y. Predictive factors for lower extremity amputations in diabetic foot infections. Diabet. Foot Ankle, 2011, 2, 2.
[http://dx.doi.org/10.3402/dfa.v2i0.7463] [PMID: 22396824]
[32]
Ekpebegh, C.O.; Iwuala, S.O.; Fasanmade, O.A.; Ogbera, A.O.; Igumbor, E.; Ohwovoriole, A.E. 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(5), 381-385.
[http://dx.doi.org/10.1111/j.1742-481X.2009.00627.x] [PMID: 19912395]
[33]
Yesil, S.; Akinci, B.; Yener, S.; Bayraktar, F.; Karabay, O.; Havitcioglu, H.; Yapar, N.; Atabey, A.; Kucukyavas, Y.; Comlekci, A.; Eraslan, S. Predictors of amputation in diabetics with foot ulcer: single center experience in a large Turkish cohort. Hormones (Athens), 2009, 8(4), 286-295.
[http://dx.doi.org/10.14310/horm.2002.1245] [PMID: 20045802]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 19
ISSUE: 7
Year: 2019
Page: [985 - 990]
Pages: 6
DOI: 10.2174/1871530319666190111121913
Price: $65

Article Metrics

PDF: 25
HTML: 2