Global Prevalence of Anemia Among Type 2 Diabetic Adult Patients: A Systematic Review and Meta-Analysis

Figures & data

Table 1 General Characteristics and Outcomes of the Included Studies Among Type 2 Diabetic Adult Patients

Author, Year of Publication	Study Setting	Study Year	Sample Size	Study Design	Sex (M/F)	Mean Age (Years)	DM Duration (Years)	Prevalence of Anemia, n (%)	Quality Score (JBI)
Awofisoye et al, 2019^Citation27	Nigeria	2014	155	CS	45/110	60.3 ± 10.2	7 (1–36)	70 (45.1)	8
Chung et al, 2019^Citation28	Republic of Korea	2017	1637	CS	797/840	59.8 ± 13.0	NR	579 (35.4)	8
Chung et al, 2017^Citation29	Republic of Korea	2014	2230	CS	1083/1147	NR	NR	750 (33.6)	8
Hosseini et al, 2014^Citation30	Iran	2011	305	CS	144/161	53.9 ± 1	8.2 ± 7.1	93 (30.4)	7
Praveen et al, 2020^Citation31	India	NR	89	CS	NR	49.76 ± 10.3	NR	15 (16.8)	7
Rathore et al, 2018^Citation32	India	2016	200	CS	126/74	56.8	5	65 (32.5)	6
Bekele et al, 2019^Citation33	Ethiopia	2019	374	CS	176/198	56.3 ± 11.5	5 (1–30)	130 (34.8)	8
Arkew et al, 2021^Citation34	Ethiopia	2020	134	CS	85/49	43.08±9.3	7.0 (4.0–9.0)	24 (17.9)	8
Ebrahim et al, 2022^Citation35	Ethiopia	2021	120	CS	64/56	38.75 ±10.5	5	31 (25.8)	8
Kebede et al, 2021^Citation36	Ethiopia	2019	372	CS	142/230	NR	8.87 ± 3.69	30 (8.0)	8
He et al, 2015^Citation37	China	2008	1997	CS	1141/856	59.67 ± 12.2	8.06 ± 6.71	439 (22.0)	7
Wu et al, 2017^Citation38	China	NR	1134	CS	645/489	57.1 ± 9.6	9 (4–13)	231 (20.4)	7
Srivastava et al, 2006^Citation39	Australia	NR	228	CS	144/84	62 ± 11	10	49 (21.4)	5
Feteh et al, 2016^Citation40	Cameroon	2013	636	CS	338/298	56.5 ± 10.6	4 (1–9)	263 (41.3)	6
Ezenwaka et al, 2008^Citation41	Caribbean	2006	155	CS	46/109	65.9 ± 0.9	10.6 ± 0.7	72 (46.4)	6
Brière et al, 2020^Citation42	France	2019	4145	CS	2226/1919	54 ± 16	15 ± 12	1065 (25.7)	5
Grossman et al 2014^Citation43	Israel	2010	445	CS	401/44	63±9.6	6.1±2.9	48 (10.7)	5
Idris et al, 2018^Citation44	Malaysia	2015	808	CS	454/354	60.5 ± 9.5	7.0 (8.0)	256 (31.6)	8
Sarosh et al, 2022^Citation45	Pakistan	2021	200	CS	82/118	49.64±13	5.98 ± 4.6	78 (39.0)	6
Al-ghazaly et al, 2019^Citation46	Yemen	2016	324	CS	141/183	53 ± 12	NR	77 (23.7)	7
Chiou et al, 2015^Citation47	Taiwan	NR	1142	CS	579/563	63 ± 11	11 ± 7	286 (25.0)	6
Bonakdaran et al, 2011^Citation48	Iran	NR	1962	CS	858/1104	52.47 ± 10.20	7.5 ± 6.1	385 (19.6)	5
Solomon et al, 2022^Citation49	Ethiopia	2020	135	CS	NR	44.65 ± 17.69	6.5±5.8	31 (22.9)	8
Abate et al, 2013^Citation50	Ethiopia	2012	191	CS	NR	40.96 ± 16.8	5.87 ± 4.7	57 (29.8)	8

Abbreviations: CS, cross-sectional; NR, not reported.

Figure 1 PRISMA 2020 Flow chart to describe the selection of studies for the systematic review and meta-analysis on the global prevalence of anemia among T2DM adult patients.

Figure 2 A forest plot showing the individual study and pooled prevalence of anemia among T2DM adult patients.

Figure 3 Predictive interval for population prevalence of anemia among T2DM adult patients.

Table 2 Subgroup Analyses Showing Pooled Prevalence of Anemia Among Type 2 Diabetic Adult Patients

Subgroups		Number of Studies	Prevalence (95% CI)	Heterogeneity
				I^2	P-value
Region	Asia	13	26.0 (22.0, 30.0)	96.61%	<0.001
	Africa	8	28.0 (17.0, 39.0)	97.31%	<0.001
	Europe	1	-	-	-
	Australia	1	-	-	-
	South America	1	-	-	-
Sample size	≤ 797	16	28.0 (21.0, 34.0)	96.29%	<0.001
	> 797	8	27.0 (23.0, 31.0)	96.89%	<0.001
Duration of DM	≤ 7.6	12	29 (23.0, 35.0)	96.14%	<0.001
	>7.6	8	24.0 (20.0, 29.0)	96.08%	<0.001
Publication year	2006–2015	8	25.0 (20.0, 29.0)	94.26%	<0.001
	2015–2022	16	28.0 (24.0, 33.0)	96.53%	<0.001

Figure 4 Sensitivity analysis showing the prevalence of anemia among T2DM adult patients.

Figure 5 Funnel plot depicting publication bias for the prevalence of anemia among T2DM adult patients.

Awofisoye OI, Adeleye JO, Olaniyi JA, Esan A. Prevalence and correlates of anemia in type 2 diabetes mellitus: a study of a Nigerian outpatient diabetic population. Sahel Med J. 2019;22:55–63.

 Google Scholar

Chung JO, Park S, Chung DJ, Chung MY. Relationship between anemia, serum bilirubin concentrations, and diabetic retinopathy in individuals with type 2 diabetes. Medicine. 2019;98(43):1–5.

 Web of Science ®Google Scholar

Chung JO, Park S, Cho DH, Chung DJ, Chung MY. Anemia, bilirubin, and cardiovascular autonomic neuropathy in patients with type 2 diabetes. Medicine. 2017;96(15):1–4. doi:10.1097/MD.0000000000006586

 Web of Science ®Google Scholar

Hosseini MS, Rostami Z. Anemia and Microvascular Complications in Patients With Type 2 Diabetes Mellitus. Nephro Urol Mon. 2014;6(4):1–7. doi:10.5812/numonthly.19976

 Google Scholar

Praveen M, Jain N, Raizada N, Sharma S, Narang S, Madhu SV. Anaemia in patients with type 2 diabetes mellitus without nephropathy is related to iron de fi ciency. Diabetes Metab Syndr Clin Res Rev. 2020;14:1837–1840. doi:10.1016/j.dsx.2020.09.020

 PubMedGoogle Scholar

Rathore S, Singh PK, Kumar A. Anemia in Type 2 Diabetes Mellitus (T2dm) and its association with vitamin B12 deficiency. India n J Pathol Oncol. 2018;5(1):51–54.

 Google Scholar

Bekele A, Roba KT, Egata G, Id BG. Anemia and associated factors among type-2 diabetes mellitus patients attending public hospitals in Harari Region, Eastern Ethiopia. PLoS One. 2019;14(12):1–17. doi:10.1371/journal.pone.0225725

 Web of Science ®Google Scholar

Arkew M, Yemane T, Mengistu Y, Gemechu K, Tesfaye G. Hematological parameters of type 2 diabetic adult patients at Debre Berhan Referral Hospital, Northeast Ethiopia: a comparative cross-sectional study. PLoS One. 2021;16(6):1–15. doi:10.1371/journal.pone.0253286

 Web of Science ®Google Scholar

Ebrahim H, Fiseha T, Ebrahim Y, Bisetegn H. Comparison of hematological parameters between type 2 diabetes mellitus patients and healthy controls at Dessie comprehensive specialized hospital, Northeast Ethiopia: comparative cross-sectional study. PLoS One. 2022;17(7):1–15. doi:10.1371/journal.pone.0272145

 Google Scholar

Kebede SA, Tusa BS, Weldesenbet AB. Prevalence of Anaemia and Its Associated Factors among Type 2 Diabetes Mellitus Patients in University of Gondar Comprehensive Specialized Hospital. Hindawi. 2021;2021:1–5.

 PubMedGoogle Scholar

B-B H, Xu M, Wei L, et al. Relationship between Anemia and Chronic Complications in Chinese Patients with Type 2 Diabetes Mellitus. Arch Iran Med. 2015;18(5):277–283.

 PubMed Web of Science ®Google Scholar

Wu F, Jing Y, Tang X, Li D, Gong L, Zhao H. Anemia: an independent risk factor of diabetic peripheral neuropathy in type 2 diabetic patients. Acta Diabetol. 2017;54:925–931. doi:10.1007/s00592-017-1025-7

 PubMed Web of Science ®Google Scholar

Srivastava PM, Thomas MC, Calafiore P, Isaac RJMAC, Jerums G, Burrell LM. Diastolic dysfunction is associated with anaemia in patients with Type II diabetes. Clin Sci. 2006;110:109–116. doi:10.1042/CS20050184

 Web of Science ®Google Scholar

Feteh VF, Choukem S, Kengne A, Nebongo DN. Anemia in type 2 diabetic patients and correlation with kidney function in a tertiary care sub-Saharan African hospital: a cross-sectional study. BMC Nephrol. 2016;17(29):1–7. doi:10.1186/s12882-016-0247-1

 PubMed Web of Science ®Google Scholar

Ezenwaka CE, Jones-lecointe A, Nwagbara E, Seales D, Okali F. Anaemia and kidney dysfunction in Caribbean Type 2 diabetic patients. Cardiovasc Diabetol. 2008;7(25):1–6. doi:10.1186/1475-2840-7-25

 PubMedGoogle Scholar

Brière M, Diedisheim M, Dehghani L, Dubois-laforgue D, Larger E. Anaemia and its risk factors and association with treatments in patients with diabetes: a cross-sectional study. Diabetes Metab. 2020;46:1–20. doi:10.1016/j.diabet.2019.02.003

 PubMedGoogle Scholar

Grossman C, Koren-morag N, Leibowitz A, Saba K. Diabetes mellitus with normal renal function is associated with anaemia. Diabetes Metab Res Rev. 2014;30:291–296. doi:10.1002/dmrr.2491

 PubMed Web of Science ®Google Scholar

Idris I, Tohid H, Muhammad NA, et al. Anaemia among primary care patients with type 2 diabetes mellitus (T2DM) and chronic kidney disease (CKD): a multicentred cross-sectional study. BMJ Open. 2018;8:1–9. doi:10.1136/bmjopen-2018-025125

 Google Scholar

Sarosh I, Ghafoor R, Haseeb A, Saeed J, Shafqat F, Kashif Z. Frequency of Anemia and its Types in Type II Diabetes Mellitus Patients without Renal Insufficiency. PJMHS. 2022;16(6):216–218. doi:10.53350/pjmhs22166216

 Google Scholar

Al-ghazaly J, Al-dubai W. Pattern and causes of anemia in Yemeni patients with type 2 Diabetes Mellitus. Eur J Biomed Pharm Sci. 2019;6(1):57.

 Google Scholar

Chiou TT, Lee J, Wang M, et al. Genetic disposition and modifiable factors independently associated with anemia in patients with type 2 diabetes mellitus. Diabetes Res Clin Pract. 2015;1:1–6.

 Google Scholar

Bonakdaran S, Gharebaghi M, Vahedian M. Prevalence of Anemia in Type 2 Diabetes and Role of Renal Involvement. Saudi J Kidney Dis Transpl. 2011;22(2):286–290.

 PubMedGoogle Scholar

Solomon D, Bekele K, Atlaw D, et al. Prevalence of anemia and associated factors among adult diabetic patients attending Bale zone hospitals, South-East Ethiopia. PLoS One. 2022;17(2):1–14. doi:10.1371/journal.pone.0264007

 Web of Science ®Google Scholar

Abate A, Birhan W, Alemu A. Association of anemia and renal function test among diabetes mellitus patients attending Fenote Selam Hospital, West Gojam, Northwest Ethiopia: a cross sectional study. BMC Blood Disord. 2013;13(1):1. doi:10.1186/2052-1839-13-6

 Google Scholar