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DOI: 10.4103/liuj.liuj_62_21
Diabetic peripheral neuropathy: A systematic review of Nigerian patients
- Abstract
- Introduction and General Definitions
- Diabetic Microangiopathy
- Diabetic Neuropathy
- Objectives
- Methods
- Results
- Discussion
- Conclusion
- References
Abstract
Diabetes mellitus is associated with microvascular and macrovascular complications. Diabetic neuropathy is the most common long-term complication of diabetes. The study was aimed at determining the prevalence of diabetic peripheral neuropathy and identifying its associated factors. Medical databases, including PubMed, Google Scholar, African Journal Online, and SCOPUS were searched and eligible studies were selected using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses algorithm. The prevalence of diabetic peripheral neuropathy in Nigeria was dependent on the modality used in diagnosing peripheral neuropathy. The overall prevalence of diabetic peripheral neuropathy in Nigeria was 31.2%–97.5%. The modality-dependent prevalences were 37%–97.5% (by biothesiometry), 41.7%–75% (by Michigan Neuropathy Screening Instrument), 31.2%–43.3% (by United Kingdom screening test), and 43.3%–69.9% (by diabetic neuropathic examination score). The associated factors were duration and control of diabetes, the age of the patient, presence of cardiovascular risk factors such as hypertension and dyslipidemia and other microvascular complications (e.g., diabetic retinopathy and nephropathy). The prevalence of diabetic peripheral neuropathy was found to be high in Nigeria and the associated risk factors were age, glycemic control, and cardiovascular risk factors.
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Introduction and General Definitions
Diabetes mellitus comprises a group of heterogeneous metabolic disorders in which the common denominator is hyperglycemia resulting from a defect in insulin secretion, action, or both.[[1]] The prevalence is rising rapidly across the various continents of the world.[[2]] The estimated prevalence of diabetes mellitus in Africa is 3.1%.[[3]] In Sub-Saharan Africa, Nigeria has the highest number of persons living with diabetes mellitus.[[4]] According to the International Diabetes Federation, as of 2020, about 2.7 million adults had diabetes in Nigeria.[[5]] [[Figure 1]] shows the regional distribution of diabetes mellitus prevalence rates across the various geopolitical zones of Nigeria.[[6]]
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Diabetic Microangiopathy
Chronic hyperglycemia induces pathological changes in the microvasculature of nerves, retina, and glomeruli resulting in the development of diabetic microangiopathy.[[7]] These are the underlying mechanisms for the development of diabetic neuropathy, retinopathy, and nephropathy. There are various pathways involved in the development of diabetic microangiopathy. Hyperglycemia, through the advanced glycation end products, polyol and hexosamine pathways, triggers an injurious cascade to the basement membrane of the microvasculature.[[8]] Hyperosmotic stress can induce inflammation by stimulating the release of pro-inflammatory cytokines, which has been found to contribute to diabetic microangiopathy.[[9]] The role of oxidative stress in the development and progression of microangiopathy has been extensively described in the literature.[[10]] Endothelial dysfunction, through deranged nitric oxide synthase function, has also been documented to contribute to diabetic microangiopathy.[[11]] The mechanisms underlying diabetic microangiopathy are summarized in [[Figure 2]].
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Diabetic Neuropathy
Diabetic neuropathy refers to symptoms and/or signs of nerve dysfunction in a patient with diabetes when other causes of nerve dysfunction have been excluded from the study.[[12]] Diabetic neuropathy is the most common long-term complication of diabetes with a huge contribution to the morbidity and mortality of patients with diabetes.[[13]] It is also the most common cause of neuropathy, especially in the advanced economies.[[14]] In Northern America and Europe, the estimated prevalence of diabetic neuropathy is 6%–51% depending on the population that was studied.[[15]] In a meta-analysis involving 23 studies done across Africa, the estimated prevalence of diabetic neuropathy in Africa was 46%.[[16]] In another meta-analysis, the identified factors associated with diabetic neuropathy were duration of diabetes, age, glycated hemoglobin, and diabetic retinopathy.[[17]] [[Table 1]] shows the classification of diabetic neuropathy, as published by the American Diabetes Association.[[18]] Diabetic symmetric polyneuropathy is the most common form of diabetic neuropathy.[[19]]
The pathophysiology of diabetic peripheral neuropathy involves both metabolic and vascular mechanisms.[[20]] As evidenced by nerve biopsy studies, the nerve microvasculature showed thickening of the basement membrane as well as hyperplasia and hypertrophy of endothelial cells.[[21]] The metabolic pathways usually involve reduction-oxidation stress.[[22]] Diabetic peripheral neuropathy often starts from the toes until it involves both the lower and upper limbs in the gloves and stockings distribution pattern.[[23]] A significant proportion of patients with diabetic peripheral neuropathy present with painful symptoms such as dysaesthesia, allodynia, and hyperaesthesia.[[24]] Sometimes, the patient presents with numbness and it is not uncommon for patients with diabetes to be asymptomatic of diabetic peripheral neuropathy.[[25]] The various modalities for diagnosing diabetic peripheral neuropathy include nerve conduction studies (the gold standard), nerve biopsy, various scoring methods using signs and symptoms of peripheral neuropathy (such as Michigan Neuropathy Screening Instrument, Diabetic Neuropathy Symptoms Score, and Toronto Clinical Scoring System), vibration threshold potential using a biothesiometer, and using a monofilament.[[25]] Based on the reports of previous studies, the sensitivity of the various modalities of diagnosing diabetes ranged from 63% to 98%.[[26]],[[27]],[[28]]
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Objectives
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To determine the prevalence of diabetic peripheral neuropathy in Nigeria
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To identify the factors associated with the development of prevalence of diabetic peripheral neuropathy in Nigeria.
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Methods
Medical databases including African Journals online, Google Scholar, Medline, and SCOPUS were used to retrieve studies on diabetic peripheral neuropathy in Nigeria. The search terms used were “diabetic neuropathy,” “diabetic peripheral neuropathy,” “peripheral neuropathy,” and “diabetic symmetrical polyneuropathy.” Other terms used in the data search included “diabetic neuropathy in Nigeria,” “diabetic microangiopathy,” “complications of diabetes” and “diabetic peripheral neuropathy in Nigeria.” In order to improve the quantity and quality of retrieved articles, Boolean operators such as “AND” as well as “OR” were used. The gray literature was also searched to enhance the depth of the retrieved studies. The literature search was done by strictly following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. The PRISMA flow diagram is shown in [[Figure 3]].
Inclusion criteria
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Studies done/published between January 1, 2000, and December 31, 2020, to determine the prevalence of diabetic peripheral neuropathy and its associated factors in Nigeria
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Studies whose abstracts and or full text were available at the searched databases or from the gray literature.
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Exclusion criteria
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Studies on diabetic peripheral neuropathy outside Nigeria
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Studies on diabetic peripheral neuropathy inside Nigeria but not focusing on the prevalence of diabetic peripheral neuropathy or its associated risk factors in Nigeria.
The studies were identified and screened independently by the authors. The ones selected were agreed upon by at least two out of the three authors. Data extraction was done on a spreadsheet and the results were presented as tables and charts.
#
#
Results
Thirteen studies were selected for the systematic review. The range of the average age in the systematic review was 42–60 years. The various studies and the geopolitical zones are shown in [[Table 2]]. All the selected studies were cross-sectional studies. The sample size in each study is shown in [[Table 3]]. The total sample size was 2848.
The various modalities used in diagnosing diabetic peripheral neuropathy are shown in [[Table 4]]. Some studies used two different modalities in diagnosing diabetic peripheral neuropathy. The four modalities of diagnosing diabetic peripheral neuropathy employed in the various studies include biothesiometry, Michigan Neuropathy Screening Instrument, United Kingdom Screening Test, and diabetic neuropathy examination score. The most commonly used modality was biothesiometry.
The prevalence of diabetic peripheral neuropathy in each study is shown in [[Table 5]]. The prevalence of diabetic peripheral neuropathy in this systematic review was 31.2%–97.5%. The prevalence of diabetic peripheral neuropathy with respect to the modality of diagnosis is shown in [[Table 6]]. Averagely, the prevalence of diabetic peripheral neuropathy in Nigeria is lowest using the United Kingdom screening test and highest using the biothesiometry modality.
The associated risk factors for diabetic peripheral neuropathy according to the different studies are shown in As shown in [[Figure 4]], the most commonly reported risk factors for diabetic peripheral neuropathy in Nigeria were the duration of diabetes and the current age of the patient as of the time of performing each study.
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Discussion
The frequency of diabetic peripheral neuropathy in Nigeria, according to this systematic review, was 37.2%–97.5%. This is a wide range largely due to differences in sociodemographics and methodology. In a systematic review and meta-analysis, involving studies across the African continent, the prevalence rate of diabetic peripheral neuropathy ranged between 16.6% and 83.4%.[[29]] The range was also wide and the rate is comparable with the present study. The main reasons put forward for the wide range were differences in sociodemographics, type of diabetes and the methods employed in diagnosing diabetic peripheral neuropathy, just as was found in this systematic review. In another systematic review done in China, the prevalence rate of diabetic peripheral neuropathy was also found to be very wide and variations in demographics and methods of diagnosing the disease were reported as being responsible for this wide range.[[42]]
Similarly, in a systematic review done in Iran, the prevalence of diabetic peripheral neuropathy in the various studies ranged from 27.4% to 87.3%. Just as it was stated for the African and Chinese systematic reviews, the authors in the Iranian study also acknowledged a wide range in the prevalence of diabetic peripheral neuropathy and ascribed this wide variation to the differences in sociodemographics and research methods.[[12]] The sensitivity and specificity of the various diagnostic modalities for diabetic peripheral neuropathy vary, so it is expected that the different methods will yield different prevalence rates.[[12]]
The most prominent associated risk factor for diabetic peripheral neuropathy in this study was the duration of diabetes. A similar finding has been reported from other previous systematic reviews in Africa and Asia.[[16]],[[42]],[[43]] This is important because the prevalence of early-onset diabetes is increasing in Nigeria due to the adoption of Western lifestyles and the risk of developing peripheral neuropathy with its attendant complication of diabetic foot ulcer will also increase in this population.[[44]] It is therefore of crucial importance to prevent or delay the onset of diabetes.
The age of the patients was also another strong predictor of the occurrence of diabetic peripheral neuropathy, according to the findings of this study. Other studies have also documented age as a prominent factor associated with the development of diabetic peripheral neuropathy.[[17]],[[45]],[[46]] It has been reported that nerve conduction velocity declines with age and this may be responsible for the effect of age on the incidence of peripheral neuropathy in individuals with diabetes.[[47]]
The present systematic review also showed that poor glycemic control was associated with diabetic peripheral neuropathy. Similarly, Aleidan et al.[[48]] in Saudi Arabia, Awadalla et al.[[49]] in Sudan and Gill et al.[[50]] in Ethiopia independently reported that poor glycemic control was associated with diabetic peripheral neuropathy. Studies have shown that prolonged exposure of nerves to hyperglycemia is critically important for the development of diabetic peripheral neuropathy.[[51]],[[52]]
This study also found the universal cardiovascular risk factors such as hypertension, obesity, dyslipidaemia, smoking, and alcohol ingestion to be associated with diabetic neuropathy. Smith et al., also reported an association between dyslipidemia as well as obesity and diabetic peripheral neuropathy.[[53]] Papanas and Ziegler, also reported a strong association between traditional cardiovascular risk factors such as hypertension, obesity, dyslipidaemia, smoking and alcohol ingestion, and diabetic peripheral neuropathy.[[54]]
In addition, the presence of other microangiopathic disorders such as diabetic retinopathy and diabetic nephropathy was found to be associated with the development of diabetic peripheral neuropathy. Other authors have documented a similar association among the microvascular complications of diabetes.[[55]],[[56]],[[57]]
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Conclusion
Diabetic peripheral neuropathy is a common microvascular complication among patients with diabetes mellitus in Nigeria. The factors associated with the presence of diabetic peripheral neuropathy are the duration of diabetes, age of the patient, and cardiovascular risk factors such as hypertension and dyslipidemia and other microvascular complications such as diabetic retinopathy and nephropathy.
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Conflict of Interest
There are no conflicts of interest.
Financial support and sponsorship
Nil.
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References
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- 22 Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010;107:1058-70.
- 23 Marchettini P, Lacerenza M, Mauri E, Marangoni C. Painful peripheral neuropathies. Curr Neuropharmacol 2006;4:175-81.
- 24 Vinik A, Casselini C, Nevoret ML. Diabetic Neuropathies. Available from: https://www.ncbi.nlm.nih.gov/books/NBK279175/. [Last accessed on 2021 Jan 20].
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- 26 Martin CL, Waberski BH, Pop-Busui R, Cleary PA, Catton S, Albers JW, et al. Vibration perception threshold as a measure of distal symmetric neuropathy in type 1 diabetes – Results from the DCCT/EDIC study. Diabetes Care 2010;33:2635-41.
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- 28 Mythili A, Kumar KD, Subrahmanyam KA, Venkateswarlu K, Butchi RG. A Comparative study of examination scores and quantitative sensory testing in diagnosis of diabetic polyneuropathy. Int J Diabetes Dev Ctries 2010;30:43-8.
- 29 Owolabi MO, Ipadeola A. Total vascular risk as a strong correlate of severity of diabetic peripheral neuropathy in Nigerian Africans. Ethn Dis 2012;22:106-12.
- 30 Olamoyegun M, Ibraheem W, Iwuala S, Audu M, Kolawole B. Burdens and patterns of microvascular complications in type 2 diabetes in a tertiary health institution in Nigeria. Afr Health Sci 2015;15:1136-41.
- 31 Ogbera AO, Adeleye O, Solagberu B, Azenabor A. Screening for peripheral neuropathy and peripheral arterial disease in persons with diabetes mellitus in a Nigerian University Teaching Hospital. BMC Res Notes 2015;8:533.
- 32 Adesina O, Adewusi F, Alalade B, Otukoya O, Olukunle G, Bello A. Correlation between the duration of diabetes mellitus and neuropathy in a Nigerian tertiary hospitall. Endocr Abstr 2016;44:104.
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- 34 Uwakwe JN, Odoh G, Edah JO, Enanimo M, Chuhwak EK, Puepet FH. Diabetic peripheral neuropathy and its risk factors: A community-based study. Int Res J Med Biomed Sci 2017;2:9-13.
- 35 Bello A, Biliaminu S, Wahab K, Sanya E. Distal symmetrical polyneuropathy and cardiovascular autonomic neuropathy among diabetic patients in Ilorin: Prevalence and predictors. Niger Postgrad Med J 2019;26:123-8.
- 36 Asomugha AL. Assessment of Diabetic Peripheral Neuropathy in Nigerians Using the Diabetic Neuropathy Examination Instrument and Quantitative Sensory Testing – A Fellowship Dissertation Submitted to the National Postgraduate Medical College of Nigeria. Unpublished. Available from: https///C:/Users/USER/Downloads/628-Article%20Text-3643-1-10-20190326.pdf. [Last accessed on 2021 Jan 20].
- 37 Ede O, Eyichukwu GO, Madu KA, Ogbonnaya IS, Okoro KA, Basil-Nwachuku C, et al. Evaluation of peripheral neuropathy in diabetic adults with and without foot ulcers in an African population. J Biomed Sci 2018;6:71-8.
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- 39 Kaoje YS, Bello F, Bansi IK, Bakari AG, Yakubu IM, Lawal AY. Prevalence and severity of distal symmetrical polyneuropathy among patients with type 2 diabetes mellitus in Zaria, Nigeria. Open Access Text 2020;6:1-4. [doi: 10.15761].
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- 48 Aleidan FA, Ahmad BA, Alotaibi FA, Aleesa DH, Alhefdhi NA, Badri M. Prevalence and risk factors for diabetic peripheral neuropathy among Saudi hospitalized patents: A nested case-control study. Int J Gen Med 2020;2020:881-9.
- 49 Awadalla H, Noor SK, Elmadhoun WM, Almobarak AO, Elmak NE, Abdelaziz SI, et al. Diabetes complications in Sudanese individuals with type 2 diabetes: Overlooked problems in sub-Saharan Africa? Diabetes Metab Syndr 2017;11 Suppl 2:S1047-51.
- 50 Gill GV, Gebrekidan A, English P, Wile D, Tesfaye F. Diabete complications and glycaemic control in remote North Africa. QJM 2008;101:793-8.
- 51 Bansal D, Gudala K, Muthyala H, Esam HP, Nayakallu R, Bhansali A. Prevalence and risk factors of development of peripheral diabetic neuropathy in type 2 diabetes mellitus in a tertiary care setting. J Diabetes Investig 2014;5:714-21.
- 52 Manschot SM, Biessels GJ, Rutten GE, Kessels RP, Gispen WH, Kappelle LJ, et al. Peripheral and central neurologic complications in type 2 diabetes mellitus: No association in individual patients. J Neurol Sci 2008;264:157-62.
- 53 Smith AG, Singleton JR. Obesity and hyperlipidaemia are risk factors for early diabetic neuropathy. J Diabet Complications 2013;27:436-42.
- 54 Papanas N, Ziegler D. Risk factors and comorbidities in diabetic neuropathy: An update 2015. Rev Diabet Stud 2015;12:48-62.
- 55 Chandy A, Pawar B, John M, Isaac R. Association between diabetic nephropathy and other diabetic microvascular and macrovascular complications. Saudi J Kidney Dis Transpl 2008;19:924-8.
- 56 Abdollahi A, Moghimi S, Tabasi A, Rajabi MT, Sabet B. Neuropathy and retinopathy in diabetes: Is there any association? Int J Ophthalmol 2009;2:57-60.
- 57 Li J, Cao Y, Liu W, Wang Q, Qian Y, Lu P. Correlations among diabetic microvascular complications: A systematic review and meta-analysis. Sci Rep 2019;9:3137.
Corresponding author
Publication History
Received: 15 March 2021
Accepted: 23 May 2021
Article published online:
14 June 2022
© 2021. Libyan International Medical University. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)
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References
- 1 Harreiter J, Roden M. Diabetes mellitus-Definition, classification, diagnosis, screening and prevention (Update 2019). Wien Klin Wochenschr 2019;131:6-15.
- 2 Harding JL, Pavkov ME, Magliano DJ, Shaw JE, Gregg EW. Global trends in diabetes complications: A review of current evidence. Diabetologia 2019;62:3-16.
- 3 Kibirige D, Lumu W, Jones AG, Smeeth L, Hattersley AT, Nyirenda MJ. Understanding the manifestation of diabetes in sub Saharan Africa to inform therapeutic approaches and preventive strategies: A narrative review. Clin Diabetes Endocrinol 2019;5:2.
- 4 Dahiru T, Aliyu AA, Sheu AU. A review of population-based studies of diabetes in Nigeria. Sub Saharan Afr J Med 2016;3:59-64.
- 5 International Diabetes Federation. IDF Africa Members. Available from: https://idf.org/our-network/regions-members/africa/members/20- nigeria.html. [Last accessed on 2021 Jan 20].
- 6 Uloko AE, Musa BM, Ramalan MA, Gezawa ID, Puepet FH, Uloko AT, et al. Prevalence and risk factors for diabetes mellitus in Nigeria: A systematic review and meta-analysis. Diabetes Ther 2018;9:1307-16.
- 7 Chawla A, Chawla R, Jaggi S. Microvascular and macrovascular complications in diabetes: Distinct or continuum. Indian J Endocrinol Metab 2016;20:546-51.
- 8 Madonna R, Balistreri CR, Geng YJ, De Caterina R. Diabetic microangiopathy: Pathogenetic insights and novel therapeutic approaches. Vascul Pharmacol 2017;90:1-7.
- 9 Brocker C, Thompson DC, Vasiliou V. The role of hyperosmotic stress in inflammation and disease. Biomol Concepts 2012;3:345-64.
- 10 Steven S, Frenis K, Oelze M, Kalinovic S, Kuntic M, Jimenez MT, et al. Vascular inflammation and oxidative stress: Major triggers for cardiovascular diseases. Oxid Med Cell Longev 2019;2019:7092151.
- 11 Sena CM, Pereira AM, Seiça R. Endothelial dysfunction – A major mediator of diabetic vascular disease. Biochim Biophys Acta 2013;1832:2216-31.
- 12 Bansal V, Kalita J, Misra UK. Diabetic neuropathy. BMJ Postgrad Med J 2006;82:95.
- 13 Vinik AI, Nevoret ML, Casellini C, Parson H. Diabetic neuropathy. Endocrinol Metab Clin North Am 2013;42:747-87.
- 14 Said G. Diabetic neuropathy – A review. Nat Clin Pract Neurol 2007;3:331-40.
- 15 Hicks CW, Selvin E. Epidemiology of peripheral neuropathy and lower extremity disease in diabetes. Curr Diab Rep 2019;19:86.
- 16 Shiferaw WS, Akalu TY, Work Y, Aynalem YA. Prevalence of diabetic peripheral neuropathy in Africa: A systematic review and meta-analysis. BMC Endocr Disord 2020;20:49.
- 17 Liu X, Xu Y, An M, Zeng Q. The risk factors for diabetic peripheral neuropathy: A meta-analysis. PLoS One 2019;14:e0212574.
- 18 Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, et al. Diabetic neuropathies: Update on definition, diagnostic criteria, estimation of severity and treatments. Diabetes Care 2020;33:2285-93.
- 19 Llewelyn JG. The diabetic neuropathies: Types, diagnosis and management. J Neurol Neurosurg Psychiatry 2003;74 Suppl 2:i15-9.
- 20 Tesfaye S, Selvarajah D. Advances in the epidemiology, pathogenesis and management of diabetic peripheral neuropathy. Diabetes Metab Res Rev 2012;28 Suppl 1:8-14.
- 21 Malik RA, Tesfaye S, Newrick PG, Walker D, Rajbhandari SM, Siddique I, et al. Sural nerve pathology in diabetic patients with minimal but progressive neuropathy. Diabetologia 2005;48:578-85.
- 22 Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010;107:1058-70.
- 23 Marchettini P, Lacerenza M, Mauri E, Marangoni C. Painful peripheral neuropathies. Curr Neuropharmacol 2006;4:175-81.
- 24 Vinik A, Casselini C, Nevoret ML. Diabetic Neuropathies. Available from: https://www.ncbi.nlm.nih.gov/books/NBK279175/. [Last accessed on 2021 Jan 20].
- 25 Russell JW, Zilliox LA. Diabetic neuropathies. Continuum (Minneap Minn) 2014;20:1226-40.
- 26 Martin CL, Waberski BH, Pop-Busui R, Cleary PA, Catton S, Albers JW, et al. Vibration perception threshold as a measure of distal symmetric neuropathy in type 1 diabetes – Results from the DCCT/EDIC study. Diabetes Care 2010;33:2635-41.
- 27 Fateh HR, Madani SP, Heshmat R, Larijani B. Correlation of Michigan neuropathy screening instrument, United Kingdom screening test and electrodiagnosis for early detection of diabetic peripheral neuropathy. J Diabetes Metab Disord 2015;15:8.
- 28 Mythili A, Kumar KD, Subrahmanyam KA, Venkateswarlu K, Butchi RG. A Comparative study of examination scores and quantitative sensory testing in diagnosis of diabetic polyneuropathy. Int J Diabetes Dev Ctries 2010;30:43-8.
- 29 Owolabi MO, Ipadeola A. Total vascular risk as a strong correlate of severity of diabetic peripheral neuropathy in Nigerian Africans. Ethn Dis 2012;22:106-12.
- 30 Olamoyegun M, Ibraheem W, Iwuala S, Audu M, Kolawole B. Burdens and patterns of microvascular complications in type 2 diabetes in a tertiary health institution in Nigeria. Afr Health Sci 2015;15:1136-41.
- 31 Ogbera AO, Adeleye O, Solagberu B, Azenabor A. Screening for peripheral neuropathy and peripheral arterial disease in persons with diabetes mellitus in a Nigerian University Teaching Hospital. BMC Res Notes 2015;8:533.
- 32 Adesina O, Adewusi F, Alalade B, Otukoya O, Olukunle G, Bello A. Correlation between the duration of diabetes mellitus and neuropathy in a Nigerian tertiary hospitall. Endocr Abstr 2016;44:104.
- 33 Ugoya SO, Echejoh GO, Ugoya TA, Agaba EI, Puepet FH, Ogunniyi A. Clinically diagnosed diabetic neuropathy: Frequency, types and severity. J Natl Med Assoc 2006;98:1763-6.
- 34 Uwakwe JN, Odoh G, Edah JO, Enanimo M, Chuhwak EK, Puepet FH. Diabetic peripheral neuropathy and its risk factors: A community-based study. Int Res J Med Biomed Sci 2017;2:9-13.
- 35 Bello A, Biliaminu S, Wahab K, Sanya E. Distal symmetrical polyneuropathy and cardiovascular autonomic neuropathy among diabetic patients in Ilorin: Prevalence and predictors. Niger Postgrad Med J 2019;26:123-8.
- 36 Asomugha AL. Assessment of Diabetic Peripheral Neuropathy in Nigerians Using the Diabetic Neuropathy Examination Instrument and Quantitative Sensory Testing – A Fellowship Dissertation Submitted to the National Postgraduate Medical College of Nigeria. Unpublished. Available from: https///C:/Users/USER/Downloads/628-Article%20Text-3643-1-10-20190326.pdf. [Last accessed on 2021 Jan 20].
- 37 Ede O, Eyichukwu GO, Madu KA, Ogbonnaya IS, Okoro KA, Basil-Nwachuku C, et al. Evaluation of peripheral neuropathy in diabetic adults with and without foot ulcers in an African population. J Biomed Sci 2018;6:71-8.
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