ORIGINAL ARTICLE

Trans R Soc Trop Med Hyg 2014; 108: 206–212 doi:10.1093/trstmh/tru024

Predisposing factors associated with uncomplicated type 2 diabetes among adults in a diabetic clinic, Enugu State, Nigeria Thomas Nubilaa,*, Ernest O. Ukaejiofoa, Samuel O. Ikeb, Elvis N. Shuc, Nkoyo I. Nubilac, Chioli P. Chijiokec, Ayodele C. Ukaejiofod, Eghosa E. Iyaree, Chukwubuzor U. Okwosaf and Onyinye V. Okwuowulua Departments of aMedical Laboratory Sciences; bMedicine; cPharmacology and Therapeutics; dMedical Rehabilitation; e Physiology; College of Medicine, University of Nigeria, Enugu Campus (UNEC); f Oral and Maxillofacial Surgery, University of Nigeria Teaching Hospital, Ituku-Ozalla, Enugu State, Nigeria

Received 6 July 2013; revised 14 January 2014; accepted 22 January 2014 Background: The role of micronutrients and other predisposing factors associated with the aetiology of type 2 diabetes in Nigeria is not well established. The objectives of this study were to investigate predisposing factors associated with uncomplicated type 2 diabetes among a Nigerian adult population. Methods: Predisposing factors associated with uncomplicated type 2 diabetes were investigated in 60 Igbo (a major tribe in Eastern Nigeria) adults aged 30–90 years. This study was carried out at the Diabetic Clinic, University of Nigeria Teaching Hospital (UNTH) Ituku-Ozalla, Enugu. Packed cell volume (PCV), serum ferrtin and some anthropometric parameters were measured alongside fasting blood sugar (FBS). Results: PCV recorded a statistically significant lower (p,0.001) mean value at 32.94+0.61% in the patients when compared with the control group with a mean value of 39.06+1.02%. Serum ferritin revealed a statistically significant higher (p,0.01; 110.20+15.17 ng/ml) mean value in the patients when compared with the control group (20.4+5.64 ng/ml). However, PCV (32.00+0.88%) and body mass index (BMI) (31.99+1.12 Kg/m2) recorded a statistically significant lower (p,0.05) mean value in female patients when compared with their corresponding males. There was no significant correlation (p.0.05) between serum iron ferritin, FBS and all other anthropometric predictors of incidence of type 2 diabetes. Conclusion: Type 2 diabetes is not associated with elevated levels of serum iron ferritin. Hence, serum ferritin may not be a better predictor of type 2 diabetes, especially in uncomplicated cases. Keywords: Nigeria, Risk factors, Serum ferritin, Type 2 diabetes

Introduction Diabetes mellitus receives more attention than other related diseases both clinically and in public.1 Diet and lifestyle play a major role in the development of type 2 diabetes.2 The quality and quantity of macro-nutrients (especially fat and carbohydrate) are known to have an impact on the risk of type 2 diabetes. 3 However, the role of micronutrients is not well established.4 Several studies have suggested a possible role of minerals such as magnesium,5,6 chromium,7,8 calcium9 and iron10 in insulin resistance on diabetes. In addition, a prospective epidemiological study showed that increased abdominal fat accumulation11,12 is an independent risk factor for cardiovascular disease and as measured by waistheight ratio (WHtR) may be a better predictor of type 2 diabetes compared to body mass index (BMI).13

Iron is a transitional metal and potential catalyst in many cellular reactions that produce reactive oxygen species. Such relations contribute to tissue damage and increase oxidative stress, thereby potentially altering the risk of type 2 diabetes.14 Several studies have suggested a possible link between high body iron stores and metabolic parameters15,16 as well as hypertension,15,17 dyslipidemia15,18,19 and obesity.15,20 Furthermore, epidemiological studies have reported an association between high iron stores and increased risk of cardiovascular disease,21 metabolic syndrome,16,22,23 gestational diabetes24,25 and type 2 diabetes.26–29 The major source of body iron is either heme (derived from meat and meat products) or non-heme iron. In two recent prospective cohort studies,28,30 intake of total or non-heme iron was not associated with the risk of type 2 diabetes, but heme iron was associated with elevated risk.

# The Author 2014. Published by Oxford University Press on behalf of Royal Society of Tropical Medicine and Hygiene. All rights reserved. For permissions, please e-mail: [email protected].

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*Corresponding author: Tel: +234 803 582 3127; E-mail: [email protected]

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Materials and methods Sixty persons with uncomplicated type 2 diabetes mellitus aged .30 years and with ≥1 year of diabetes evolution, as diagnosed and controlled by the diabetic clinic of University of Nigeria Teaching Hospital (UNTH), Ituku-Ozalla and 30 age and sex matched non-diabetic or related volunteers with no apparent medical or family history of diabetes participated in the study. They were recruited between March and May 2009. A complete review of medical history of all participants was recorded before the beginning of the study. Informed consent was obtained from all participants, after which a structured health and lifestyle questionnaire was administered to obtain information on general lifestyle, eating habits and health status. Ethical approval was obtained from the Ethics Committee of UNTH. All procedures followed were in accordance with Ethical Standards of the responsible Committee on Human experimentation (Regional) and with the Helsinki Declaration of 1975, as revised in 2000.34

Smoking and drinking Smoking was assessed by asking the frequency and/or number of daily cigarette intake. Drinking was assessed by asking the frequency and amount of alcohol/wine intake.

Height, weight and blood pressure At the clinic, health workers measured the height, weight and blood pressure as described by Fayzeh et al.36 Blood pressure was measured using standardised mercury sphygmomanometer on the right upper arm of the subject, who was seated for 5 mins before the measurement. Blood pressure was measured twice, and the mean of these two measurements was used in the analysis.37 Hypertension was defined as systolic blood pressure greater than 140 mmHg and/or diastolic blood pressure greater than 90 mmHg. Height was measured without shoes and weight was measured with light clothing. BMI was calculated as weight in kilograms divided by the square of height in metres. Family history of diabetes was defined as the presence of known family members with type 2 diabetes in any of the three generations (siblings, parents or grandparents). Education was recorded into three categories: low, medium and high. Low, medium and high levels of education equates to low: illiteracy, primary school; medium: secondary school; and high: high school and above.

Blood sample collection and analysis Venous blood samples (4 mls) were collected aseptically from all the subjects after a 12 h overnight fast. Three ml was centrifuged after clot retraction and the expressed serum stored frozen at 2208C for serum iron ferritin determination, while the remaining 1 ml was emptied into a tripotassium (K3) EDTA anticoagulant container bottle and mixed immediately by gentle inversion for the estimation of PCV using standard haematological manual methods as described by Dacie and Lewis.35 All samples were processed within 2 h of collection.

Measurements and interviews Participants were interviewed at the diabetic clinic using a precoded, research structured and pilot-tested interview questionnaire. It covered information on: sociodemographic variables (age, gender, family history, level of education, smoking and drinking status) and clinical information about history and duration of diabetes.

Statistical analysis

Packed cell volume, serum iron ferritin and fasting blood glucose

Results

The entire participant’s fasting blood glucose was determined by thumb pricking using a glucometer (Ultra Quick, Lifescan, USA). PCV was measured by microhaematocrit method as described by Dacie and Lewis,35 while serum iron ferritin was determined by the Enzyme Immuno Assay Test Kit-Genway, (Genway Biotech Inc, San Diego, CA, USA) following the manufacturer’s guidelines. Anaemia was defined as PCV less than 36% for males and less than 30% for females. Diabetes was defined as fasting blood glucose greater than 7.0 mmol/l.

Statistical analysis was carried out using Statistical Package for Social Science (SPSS Inc., Chicago, IL, USA) version 14. One–way analysis of variance (ANOVA) was adopted for comparison. The data were expressed as mean+SE; p,0.05 was considered significant.

From the result of the present study, the comparison of some of the predisposing factors to diabetes between the male and female patients, PCV and BMI revealed a statistically significant lower (p,0.05) mean value while a statistically significant higher (p,0.05) mean value in blood pressure was observed in the male patients. The prevalence of hypertension was higher, 29% (7/24), in men than in women, 24% (6/25). Similarly, anaemia recorded a higher prevalence 91% (20/22) in the male and 89% (25/28) in the female patients. In addition, a higher prevalence of family history of diabetes was recorded in the males, 48% (14/29) than the

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Susceptibility to type 2 diabetes mellitus is determined by multiple genetic and environmental factors and their interactions.31 Non insulin-dependent diabetes mellitus is a common complication of iron overload diseases such as haemochromatosis; 53–80% of persons with haemochromatosis develop diabetes. It has been observed that the development of diabetes in persons with haemochromatosis is related to the magnitude of iron excess.32 However, it is not clear whether moderately elevated iron stores are associated with the risk of type 2 diabetes in a healthy person.29 Furthermore, the mechanisms that determine whether iron promotes the development of diabetes are unknown and, therefore, further in-depth studies are warranted.33 This study was designed to determine the association between serum ferritin, packed cell volume (PCV), and some anthropometric predictors of incident type 2 diabetes in adult Igbos in Enugu urban, Enugu State Nigeria.

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Table 1. Comparison of some of the predisposing factors to diabetes between the male and female subjects Parameter

Males (n¼29) Mean+SE

Age (years) Packed cell volume (%) Serum Ferritin (mg/l) Body mass index (kg/m2) Fasting blood sugar (mg/l) Blood pressure

58.11+2.68 34.14+0.78 131.9+24.99 34.94+0.07 197.8+17.43 130/76.50 + 21.16/13.19

55.03+2.49 32.0+0.88 89.18+17.06 31.97+1.01 173.90+17.37 137.60/83.60 + 21.85/13.19

t-test p-value

,0.05 .0.05 ,0.05 .0.05 ,0.05

Frequency (%)

Frequency (%)

7 (29) 17 (70)

6 (24) 19 (76)

NA

20 (91) 2 (9)

25 (89) 3 (11)

NA

14 (48) 15 (52)

14 (47) 16 (53)

NA

14 (50) 14 (50)

8 (28) 21 (72)

NA

12 (41) 8 (28) 9 (31)

17 (57) 6 (20) 7 (23)

NA

10 (35) 8 (28) 11 (38)

20 (71) 3 (11) 5 (18)

NA

NA: not applicable.

Table 2. Comparison of packed cell volume, serum ferritin and fasting blood sugar between patients and controls Parameter

Patients Mean+SE

Controls Mean+SE

p value

Packed cell volume (%) Serum ferritin (mg/l) Fasting blood sugar (mg/l)

32.94+0.61 110.2+15.17 185.9+12.30

39.06+1.02 20.47+5.64 88.29+3.25

,0.001 ,0.01 ,0.001

females 47% (14/31). Also the male patients recorded a higher prevalence of smoking, snuffing and drinking, 50% (14/28), than their female counterparts 28% (8/29). Furthermore, the female patients revealed a higher prevalence in low educational level, 57% (17/30) as opposed to their male counterparts who showed a higher prevalence in the medium 28% (8/29) and higher 31%

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(9/29) levels of education. Finally, a higher prevalence in the duration of diabetes was demonstrated at 6–10 years, 28% (8/29) and .10 years 38% (11/29) in the male patients when compared to their female counterpart, while the females recorded a higher prevalence 71% (20/28) at 0–5 years (Table 1). In the comparison of the mean+SE PCV, serum iron ferritin and FBS mean values between the patients and control group, PCV recorded a statistically significant lower mean (p,0.01) value in the patients when compared with the control group. However, serum ferritin revealed a statistically significant higher mean value in the patients (p,0.01) when compared with the control group. Similarly, FBS mean (+SE) values revealed a significant higher (p,0.001) mean value in the patients when compared with the control group (Table 2). There was no correlation between serum ferritin and all the other parameters investigated (p.0.05) (Figures 1A–1E). Similarly, there was no association between serum ferritin, smoking, educational level, hypertension and duration of diabetes in the parameters (p.0.05) studied (Figures 2A–2D).

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Hypertension Yes No Anemia Yes No Family History of diabetes Yes No Smoking/drinking Yes No Education Low (Primary school) Medium (Secondary school) High (High school and above) Duration of diabetes (years) 0–5 6–10 .10

Females (n¼31) Mean+SE

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Discussion Diabetes mellitus receives more attention than other related diseases both clinically and in public health.1 There is an increasing concern about the relationship between iron status and type 2 diabetes.28–30 The result of this pilot study among uncomplicated type 2 diabetic subjects revealed that PCV showed a statistically significant lower (p,0.001) mean value in the patients with diabetes when compared with the control group. This might be due to the higher prevalence of anaemia in the developing countries, more especially Nigeria, which are mostly linked to iron deficiency as reported by WHO.38 One assumption could be that this might also be an indicator of general nutritional deficiency as reported by Zumin et al.37 In addition, high rates of microbial infections

and the inheritance of haemoglobin disorders such as sickle cell anaemia could also be a contributing factor. However, serum ferritin mean value recorded a statistically significant higher (p,0.01) mean value in the patients when compared with the control group. The result of this present study was in line with other previous studies in which elevated serum iron ferritin levels were associated with increased diabetes mellitus risk among healthy individuals.33,39–41 Furthermore, this high level of serum iron ferritin might indicate that increase above normal of plasma glucose level may have an adverse (inhibitory) effect on iron metabolism. This could also be due to latent chronic inflammatory diseases which are common among type 2 diabetic patients as reported by Zumin et al.37 Surprisingly, there was no correlation between serum iron ferritin, PCV, fasting blood sugar,

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Figure 1. Correlation between serum ferritin with (A) age, (B) Body Mass Index (BMI), (C) duration of diabetes, (D) Fasting Blood Sugar (FBS) and (E) Packed Cell Volume (PCV) (p.0.05) in the patients studied.

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and all other anthropometric and some non-anthropometric predictors of incidence of type 2 diabetes mellitus. This might be attributable to the fact that except for a minor decrease in PCV and a slightly elevated fasting blood sugar, all other parameters investigated were within the normal reference ranges. This could also be explained by the fact that the patients studied were uncomplicated cases of type 2 diabetes, apparently healthy, and were all responding to treatment. Interestingly, the correlation result in this present study agreed with a more recent prospective study where no association between ferritin levels and risk of type 2 diabetes mellitus in multivariate-adjusted models was recorded.42 However, the association results revealed in our study were in contrast to other recent literature in which higher heme iron intake and higher body iron stores were significantly associated with a greater risk of type 2 diabetes mellitus.33,43 This conflicting result could be attributed most probably to nutritional, genetic or racial ethnic differences in the population studied.

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Ideally, type 2 diabetes patients who are ‘newly’ diagnosed and not on treatment should have been studied. Also, their nutritional status and other factors most likely to influence serum iron ferritin and blood sugar levels should also have been investigated. These are some of the limitations of our study. In conclusion, type 2 diabetes is not associated with elevated levels of serum iron ferritin. Hence, serum ferritin levels may not be a better predictor of type 2 diabetes, especially in uncomplicated or on treatment cases. However, a larger number of diabetic patients at different stages of the disease and/or untreated should be investigated.

Authors’ contributions: TN and EOU conceived the study; SOI and CUO carried out the clinical assessment; ENS and EEI designed the protocol; NIN analysed and interpreted the data; CPC critically revised the

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Figure 2. Association between serum ferritin and (A) smoking, (B) educational level, (C) hypertension and (D) duration of diabetes in the patients studied (p.0.05).

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manuscript for intellectual content; ACU drafted the manuscript; OVO collected and analysed samples. All authors read and approved the final manuscript. NT is guarantor of the paper. Funding: None. Competing interests: None declared. Ethical approval: Ethical approval was obtained from the Ethics Committee of UNTH. All procedures followed were in accordance with Ethical Standards of the responsible Committee on Human experimentation (Regional) and with the Helsinki Declaration of 1975, as revised in 2000.34

17 Piperno A, Trombini P, Gelosa M et al. Increased serum ferritin is common in men with essential hypertension. J Hypertens 2002;20:1513–8. 18 Halle M, Ko¨nig D, Berg A et al. Relationship of serum ferritin concentrations with metabolic cardiovascular risk factors in men without evidence for coronary artery disease. Atherosclerosis 1997;120:235–40. 19 Williams MJ, Poulton R, Williams S. Relationship of serum ferritin with cardiovascular risk factors and inflammation in young men and women. Atherosclerosis 2002;165:179–84. 20 Gillum RF. Association of serum ferritin and indices of body fat distribution and obesity in Mexican American men: the third National Health and Nutrition Examination Survey. Int J Obes Relat Metab Disord 2001;25:639–45.

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38 WHO. Iron deficiency anaemia: assessment, prevention and control. A guide for programme managers. Geneva: World Health Organization; 2001. 39 Rajpathak S, Ma J, Manson J et al. Iron intake and the risk of type 2 diabetes in women: a prospective cohort study. Diabetes Care 2006;29:1370–6. 40 Kaye TB, Guay AT, Simonson DCC. Non-insulin-dependent diabetes mellitus and elevated serum ferritin level. J Diabetes Complicat 1993;17:246–9.

41 Ford ES, Cogswell ME. Diabetes and serum ferritin concentration among U.S. adults. Diabetes Care 1999;22:1978–83. 42 Jehn ML, Guallar E, Clark JM et al. A prospective study of plasma ferritin level and incident diabetes. The Atherosclerosis Risk in Communities (ARIC) study. Am J Epidemiol 2007;165:1047–54. 43 Zhoa Z, Li S, Liu G et al. Body iron stores and heme-iron intake in relation to risk of type 2 diabetes: a systematic review and meta-analysis. PLos ONE 7(7):e41641. doi:10.1371/journal.pone. 0041641

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Predisposing factors associated with uncomplicated type 2 diabetes among adults in a diabetic clinic, Enugu State, Nigeria.

The role of micronutrients and other predisposing factors associated with the aetiology of type 2 diabetes in Nigeria is not well established. The obj...
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