Type 2 diabetes and its correlates in a first nationwide study among Cypriot adults

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Contents lists available at ScienceDirect

Primary Care Diabetes journal homepage: http://www.elsevier.com/locate/pcd

Original research

Type 2 diabetes and its correlates in a first nationwide study among Cypriot adults Eleni Andreou a,b,∗ , Dimitrios Papandreou a,g , Photos Hajigeorgiou b , Katia Kyriakou a , Thalia Avraam a , Georgia Chappa a , Procopis Kallis a , Christalleni Lazarou a , Christiana Philippou a , Christoforos Christoforou c , Rebecca Kokkinofta d , Christos Dioghenous d , Savvas Savva a , Antony Kafatos e , Antonios Zampelas f a

Cyprus Dietetic and Nutrition Association, Cyprus Department of Life and Health Sciences, University of Nicosia, Cyprus c Cyprus Center for European and International Affairs, University of Nicosia, Cyprus d DNA Biomedical Science Lab, Cyprus e Department of Social Medicine, University of Crete Heraklion, Greece f Unit of Human Nutrition, Department of Food Science and Technology, Agricultural University of Athens, Greece g Zayed University Abu Dhabi, United Arab Emirates b

a r t i c l e

i n f o

a b s t r a c t

Article history:

Obesity rates in Cyprus are very high and epidemiological information on type 2 diabetes

Received 16 November 2016

mellitus is limited. The correlates of type 2 diabetes among adults remain unknown in the

Received in revised form

Cypriot population. Thus, the purpose of this study is to provide the first national estimate of

2 January 2017

the prevalence of type 2 diabetes and investigate its correlates. A randomly stratified nation-

Accepted 4 January 2017

ally sample of 1001 adults aged 18–80 participated in the study. Only 950 subjects completed

Available online xxx

the study. All subjects were free of any diseases (known diabetes, kidney, liver), medication

Keywords:

criteria was 9.2% and 16.3%, respectively. After adjusting for age, energy intake, smoking and

and supplementation. The overall prevalence of diabetes and pre-diabetes based on WHO Type 2 diabetes

physical activity participants with obesity (BMI) (OR = 2.00, P < 0.001), waist circumference

Prevalence

(WC) (OR = 2.08, P < 0.001), hypertension (HT) (OR = 1.99, P < 0.001) and hypercholesterolemia

Metabolic syndrome

(HC) (OR = 2.07, P < 0.007) were most likely to develop T2DM compared with the normal ones.

Cyprus

The odds of having diabetes were also found significant between subjects with high levels

Diet

of triglycerides (TG) (OR = 1.49, P < 0.007), compared with the normal ones and between subjects with low levels of HDL (OR = 1.44, P < 0.008) compared with the ones with high levels of HDL. The prevalence of type 2 diabetes in Cyprus is relatively medium–high. However, the pre-diabetes rates are very high showing a promising increase toward total rates of type 2 diabetes. Obesity, HT, WC, TG, HC and low HDL are all strong correlates of type 2 diabetes.

∗

Corresponding author at: Department of Life and Health Sciences, University of Nicosia, Nicosia, Cyprus. Fax: +357 22 452292. E-mail addresses: [email protected], [email protected] (E. Andreou). http://dx.doi.org/10.1016/j.pcd.2017.01.001 1751-9918/© 2017 Primary Care Diabetes Europe. Published by Elsevier Ltd. All rights reserved.

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Healthy education programs should be initiated for young and older-aged people and those with described abnormal risk factors. © 2017 Primary Care Diabetes Europe. Published by Elsevier Ltd. All rights reserved.

1.

Introduction

Overweight and obesity have reached epidemic proportions globally along with an adaptation of a westernized lifestyle which is characterized by a combination of excess food intake and inactivity [1,2]. In 2008, statistics from all over the world reported that around 1.5 billion of people were overweight (BMI > 25 kg/m2 ) while 508 million people were obese [3]. This dramatic rise in the prevalence of obesity has been accompanied by alarming increases in the incidence and prevalence of type 2 diabetes and metabolic syndrome (MS) [4], as well as atherosclerosis, hypertension and stroke [5]. The estimated global prevalence of type 2 diabetes is expected to increase overall 39%, from 4.6% in 2000 to 6.4% in 2030 [6]. Overall, the prevalence of diabetes is higher in men than in women, higher after the age of 40 years, while, on a country basis, India, China, USA, Indonesia and Japan are in the first line [6]. It is worthy to point out that in these countries, the adult diabetic population is estimated to be increased more than double by 2030. A recent review [7] that was published in Lancet analyzed the trends of diabetes since 1980 in a pooled analysis study of 751 populations with 4.4 million participants. In this review, the global age-standardized diabetes prevalence increased from 4.3% in 1980 to 9.0% in 2014 in men, and from 5.0% to 7.9% in women. In addition, the agestandardized adult diabetes prevalence in 2014 was lowest in northwestern Europe, and highest in Polynesia and Micronesia, at nearly 25%, followed by Melanesia and the Middle East and north Africa. Moreover, in 2014, American Samoa had the highest national prevalence of diabetes (>30% in both sexes), with age-standardized adult prevalence also higher than 25% in some other islands in Polynesia and Micronesia [7]. Findings from epidemiological studies have repeatedly confirmed the positive relation between obesity and developing type 2 diabetes [8,9]. Other factors related to hyperglycemia are abdominal/visceral adiposity, hyperinsulinemia and insulin resistance [10]. Type 2 diabetes remains a leading cause of cardiovascular disorders, blindness, end-stage renal failure, amputations and hospitalizations. It is also associated with increased risk of cancer, serious psychiatric illness, cognitive decline, chronic liver disease, accelerated arthritis and other disabling or deadly conditions [11]. Cyprus is a Greek island country in the Eastern Mediterranean Sea, off the coast of Syria and Turkey and east of Greece. Data (not full paper) from International Diabetes Federation (IDF) [12] reveal that the prevalence of type 2 diabetes is very high, 10.4% of the total population, while another 6.7% suffer from impaired glucose tolerance (pre-diabetes) [12]. This situation will deteriorate in the future, with an estimate of 15% of adult citizens with diabetes in 2030. Moreover, about one-third of all people with type 2 diabetes are unaware of their condition and remain untreated. This

means that one out of five people with type 2 diabetes are diagnosed too late, resulting in increased complications and costs [13]. Furthermore, Cyprus has one of the highest European incidence rates for obesity: almost one in two Cypriot men is overweight (46%) and one in four is obese (26,5%). One in three Cypriot women is overweight (34%) and one in five is obese (24%) [14]. A more recent study showed that the prevalence of OW and OB in Cyprus was 46.9% and 28.8% for males and 26% and 27% for females, respectively [15]. So far, information of the prevalence of type 2 diabetes is limited and there is no data available concerning diabetesrelated complications for the Cypriot population. Thus, the purpose of this study is to report on the prevalence of type 2 diabetes and to identify risk factors associated with, in a population-based study of healthy Cypriot adults.

2.

Methodology

The national survey took place during 2005–2009, and included 1001 Cypriot adults aged 18–80 (48.5% males/51.5% females). The figures of the subjects were adopted by the Cyprus Ministry of Health while the statistical error for the sample size was 3%. The sample was representative from all main cities and suburbs in Cyprus (Nicosia, Limassol, Pafos, Larnaka and Famagusta). The selection of the subjects was performed randomly using the 2005 telephone directory, and the total final sample was stratified and in full compliance with the demographics of the Republic of Cyprus. Out of the 1001 adults, after excluding missing data the final sample size was 950 subjects. Detail information of the whole procedure and any possible health risks was given to the subjects prior to any intervention and a consent form was signed by all subjects willing to participate. The study was also approved by the Cyprus National Bioethics Committee. Body weight and height was calculated using a scale with Stadiometer from Seca 700. BMI was calculated by dividing weight (kg) by height squared (m2 ). The categorization of the weight situation of the subjects according to the BMI was taken as follows: BMI 20–25 normal weight, BMI 25–30 overweight, and BMI >30 obese. Waist circumference (WC) was measured to the nearest 0.1 cm using a regular tape. Bioelectrical impedance analysis was used to measure body fat (BF) levels (Tanita TBF-215, England). Blood pressure was obtained in a relaxed supine position; three measurements were performed at intervals of 3 min, and the mean number of the three values was considered as the BP [16]. Blood cholesterol levels were considered “borderline high” if they were ≥200 mg/dL [17]. Information on socioeconomic status and dietary status such as energy intake, carbohydrate and fat intake as well as exercise and smoking information were collected from all par-

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Table 1 – Basic demographic, anthropometric and socioeconomic characteristics of the Cypriot population (n = 950). Anthropometric variables Age Subjects <40 years Subjects >40 years Sex M F BMI (kg/m2 ) WC (cm) FAT (%) FFM (%) SBP (mmHg) DBP (mmHg) Energy (kcal/day)

Normal

Pre-diabetes

Diabetes

P-value

239 470

28 60

93 62

0.006

410 297 27.2 ± 5.2a 91.7 ± 13.7a 23.3 ± 11.8a 50 ± 10.9b 118 ± 13.5a 79 ± 9 2150 ± 267

45 43 304 ± 5.7a 102.3 ± 10.8a 31 ± 18a 60 ± 9 123 ± 13a 83 ± 9 2650 ± 288

75 80 31.1 ± 4.1a 104 ± 11.3a 32 ± 19a 59 ± 21b 129 ± 12a 83.1 ± 9.4 2780 ± 280

0.519 0.001 0.001 0.001 0.004 0.002 0.681 0.001

Values are presented as mean ± SD. Mean values were significantly different between the pre-diabetic and normal group and between the diabetic and normal group; P < 0.05. Mean values were significantly different between the diabetic and normal group; P < 0.05. Abrev.: BMI: body mass index, WC: waist circumference, FFM: free fatty mass, SBP: systolic blood pressure, DBP: diastolic blood pressure. a Mean values were significantly different between the pre-diabetic and normal group and between the diabetic and normal group; P < 0.05. b Mean values were significantly different between the diabetic and normal group; P < 0.05.

ticipants in the study using a detailed questionnaire. A 24-h recall was used to record all dietary information. Laboratory examinations were obtained for all subjects (n = 950) who participated in the study after an overnight fasting of 12 h. The fasting plasma glucose was centrifuged immediately; total cholesterol (TC), triglyceride (TG), low-density lipoprotein cholesterol (LDL-C) and high density lipoprotein cholesterol (HDL-C) concentrations were all measured using Vitros 5600-Integrated Automatic Analyzer (Ortho-Clinical Diagnostics, NJ, USA). The method is performed using dry chemistry based on enzymatic methodology: after the dissociation of the TC/TG/LDL-C/HDL-C by using different enzymes and procedures such as hydrolysis/oxidation/catalysis a colored dye is generated that is measured by reflectance spectrophotometry, in the dedicated wavelength for each component based to the Vitros-5600 Protocols. The survey used the criteria from WHO [18] for the cut off point for measuring fasting plasma glucose. A person was considered to have diabetes if FPG was ≥126 mg/dL, while a value of 100–126 mg/dL was considered as pre-diabetes. Finally, a person with <100 mg/dL was considered normal. Similarly, we use WHO [18] that includes MS in its classification of diabetes (≥126 mg/dL) as the major abnormality plus two or more of the following: (a) elevated blood pressure (≥140/90 mmHg), (b) elevated plasma triglycerides (≥150 mg/dL), (c) high density lipoprotein (<35 mg/dL men; <39 mg/dL women) and (d) BMI >30 kg/m2 .

3.

Statistical analysis

The statistical package IBM SPSS Statistics 20.0 (IBM Corp.) was used for the statistical analysis of data. Data distribution was normal. Values were expressed as mean ± SD. One-way ANOVA was used to determine if there was a difference between the three groups. Pair wise comparison was evaluated by the Tukey–Krammer test. The correlates of diabetes

Fig. 1 – Metabolic syndrome related risk factors associated with diabetes (≥126 mg/dL).

among the adults were assessed by using multivariable logistic regression models. Odds ratios (OR) with 95% confidence intervals (CI) for correlates of diabetes were estimated. Statistical significance was considered for P < 0.05.

4.

Results

The prevalence of type 2 diabetes and pre-diabetes was 88/950 = 9.2% and 155/950 = 16.3%, respectively. Among the respondents 41.8% were male and 57.2% female. Respondents with age >40 years old, and higher levels of energy intake had higher percentages of having diabetes compared to the respondents with a younger age and lower energy intake (Table 1). The pre-diabetic and diabetic group had statistically significantly higher levels of weight, BMI, WC, % body FAT and SBP

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Table 2 – Biochemical characteristics of the Cypriot population between the three groups (n = 950).

TC (mg/dL) HDL (mg/dL) LDL (mg/dL) TG (mg/dl)

Normal

Pre-diabetes

Diabetes

P-value

214 ± 42a 54 ± 13a 91 ± 35 105 ± 61a

218 ± 49a 48 ± 11a 100 ± 36 166 ± 107a

239 ± 56a 46 ± 12a 98 ± 34 228 ± 129a

0.007 0.009 0.541 0.001

Values are presented as mean ± SD. Abrev.: TC: total cholesterol, HDL: high density lipoprotein, LDL: low density lipoprotein, TG: triglycerides. Mean values were significantly different between the diabetic and normal group; P < 0.05. a Mean values were significantly different between the pre-diabetic and normal group and between the diabetic and normal group; P < 0.05.

(Table 1) compared with the normal one. Out of the 88 subjects with type 2 diabetes 79 of them were obese (90%) (data not shown). Furthermore, in the diabetic group, 45% in total were presented with metabolic syndrome (Fig. 1). Table 2 represents the biochemical characteristics of the three groups. Both pre-diabetic and diabetes group had statistically significantly higher levels of serum TC, TG and significantly lower levels of HDL, compared with the normal group. After adjusting for smoking and physical activity, participants with increased age (OR = 1.5, P < 0.002) and energy intake (OR = 1.3, P < 0.043) were most likely to develop T2DM. Subjects with obesity (BMI), abdominal obesity (WC) hypertension and hypercholesterolemia had more than twice the chance (OR = 2.05, P < 0.001), (OR = 2.21, P < 0.001), (OR = 2.01, P < 0.001), (OR = 2.12, P < 0.007) of having diabetes compared with the normal ones. The odds of having diabetes were also found significant between subjects with high levels of TG compared

Table 3 – Odds ratio + CI at correlates of diabetes (≥126 mg/dL). ORa Age <40 years >40 years BMI Normal OW (>25 kg/m2 ) OB (>30 kg/m2 ) Hypertension No Yes (≥140 or 90) Abdominal obesity No Yes (WC >94 M or 80 W) Borderline high cholesterol No Yes (≥200 mg/dL) Hypertriglyceridemia No Yes (≥150 mg/dL) Low HDL No Yes (<35 M or <39 W) Energy (kcal) <2500 >2500 a

95% CI

P-value

1 1.5

0.76, 2.98

0.002

1 1.56 2.05

1.02, 1.71 1.64, 2.31

0.004 0.001

1 2.01

1.32, 2.45

0.001

1 2.21

1.92, 259

0.001

1 2.12

1.95, 2.55

0.007

1 1.52

1.10, 1.90

0.002

1 1.48

0.90, 1.80

0.005

1 1.5

0.60, 2.10

0.043

Adjusted for smoking and physical activity.

to ones with normal levels (OR = 1.52, P < 0.002) and between subjects with low level of HDL (OR = 1.48, P < 0.005) compared with the ones with high levels of HDL (Table 3). The odds ratio to develop type 2 DM still remained higher and significant in the subjects with OB (OR: 2.00, P < 0.001), HT (OR: 1.99, P < 0.001), WC (OR: 2.08, P < 0.001), hypercholesterolemia (OR: 2.07, P < 0.009), hypertriglyceridemia (OR: 1.49, P < 0.007) and low HDL (OR: 1.44, P < 0.008) even when the statistical model adjusted additionally for age and energy intake (Table 4).

5.

Discussion

Cyprus population is about 600,000 thousand people and this is the first well-known well-designed representative study that tried to estimate the prevalence of type 2 diabetes in Cyprus. We reported a prevalence rate of 9.2% and 16.3% of diabetes and pre-diabetes, respectively. The prevalence of diabetes was similar in females and males but it was significantly higher in ages over 40 years old. A recent paper [7] that included data from 751 populations, 4,372,000 adults in 200 countries, reported global age-standardized prevalence of diabetes 9% and 7.9% in men and women, respectively. The authors also

Table 4 – Odds ratio + CI at correlates of diabetes (≥126 mg/dL).

BMI Normal OW (>25 kg/m2 ) OB (>30 kg/m2 ) Hypertension No Yes (≥140 or 90) Abdominal obesity No Yes (WC >94 M or 80 W) Borderline high cholesterol No Yes (≥200 mg/dL) Hypertriglyceridemia No Yes (≥150 mg/dL) Low HDL No Yes (<35 M or <39 W) a

ORa

95% CI

1 1.38 2.00

1.00, 1.51 1.69, 2.18

0.009 0.001

1 1.99

1.42, 2.39

0.001

1 2.08

1.96, 2.63

0.001

1 2.07

1.89, 2.49

0.009

1 1.49

1.08, 1.77

0.007

1 1.44

0.88, 1.68

0.008

P-value

Adjusted for age, energy, smoking and physical activity.

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reported that the prevalence was higher in low-income and middle-income countries. Moreover, the highest prevalence’s rates were found to be in Oceania, Middle East and north Africa [7]. The results on the prevalence of diabetes type 2 from our study were lower compared to a similar study in Cyprus reported from IDF [12] (10.3), which was based on data (editorial letter) reported 12–14 years ago [19]. However, the data collection of this particular study did not included a representative sample of the whole population. Our results are also lower to neighbor countries such as Greece 13.5% [20] but higher than Turkey 7.4% [12]. Our results also showed that the prevalence of pre-diabetes was 16.3% which is much higher compared to Cyprus (6.7%), Greece (7.4%) and Turkey (8.9%) reported from IDF [12], respectively. In addition, 60% of subjects with pre-diabetes are in the age of <40 years old showing that young people are very closely to get type 2 DM. Above all that, it is worthy to point out that out of 88 diabetic subjects 21 (23.8%) of them did not know they had diabetes. Type 2 diabetes may remain undetected for many years, leading to severe complications and healthcare costs. Globally, 45.8%, or 174.8 million of all diabetes cases in adults are estimated to be undiagnosed, ranging from 24.1% to 75.1% across data regions. An estimated 83.8% of all cases of undiagnosed diabetes type 2 are in low- and middle-income countries. At a country level, Pacific Island nations have the highest prevalence of undiagnosed diabetes type 2 [21]. Another important finding of our study was that 90% of the diabetic subjects were obese. Furthermore, our study confirmed that being overweight and obese is a strong correlate of having T2DM. Obesity has been the one single factor that has been associated with diabetes in all population studies [22,23]. In fact, this association has been known since antiquity. In a recent epidemiological study that included data from 32 countries, overweight and obesity based on BMI and WC were highly associated to cardiovascular disease in T2DM [24]. Metabolic syndrome has been also a major predictor for T2DM for many years [25]. CV risk factors such as insulin resistance, low HDL and high blood pressure have been shown to have a high prediction on the development of T2DM [26]. In our study, 45% of the diabetic subjects were diagnosed with MS using the WHO definition. In a recent meta-analysis review in 2016 [27], the prevalence of MS in mainland of China was 24.5% in 226,000 Chinese subjects. Generally, the prevalence of metabolic syndrome is estimated to be between 10 and 30%, increasing sharply in older age-groups in most European countries [28]. Increased intra-abdominal fat accumulation, indicated by a large waist circumference, may have a direct intermediary role in the development of the metabolic syndrome [7]. WC has been recommended by many researchers as an excellent indicator of abdominal obesity and a very good predictor of T2DM [8,29]. Our results indicated a strong relation between WC and development of T2DM increasing this way the risk of metabolic complications to these patients. The prevalence of hypertension in the diabetic population is 1.5–3 times higher than that of non-diabetic subjects [30]. In our study, T2DM was found to be associated with hyper-

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tension. These finding are consistent with other extensive epidemiological studies [23,31]. High triglyceride and low HDL cholesterol levels are core components of the metabolic syndrome and type 2 DM. In our study, subjects with lower levels of HDL were most likely to develop T2DM. Extensive epidemiological studies have reported that HDL is commonly found in diabetic patients and it is best known as a predictor of CVD [32,33]. T2D and its associated vascular complications have been found to be partially linked to dyslipidemia. A diabetic dyslipidemia resulting from lipotoxicity is a state characterized by changes in the lipid profile including increases in triglycerides, and cholesterol [34]. Insulin resistance together with obesity and overeating seem to contribute to this mechanism [35]. The risk of cholesterol and TG in our study were double in patients having T2DM. Our study though has its limitations. We did not examine the genetic predisposition of the population due to the lack of financing. Additionally, we did not evaluate in depth the dietary, physical activity and socioeconomic factors of the subjects. Nevertheless, our study provides evidence of the correlates of T2DM using a nationally representative sample. Most importantly, all subjects were unware of their high blood glucose levels which makes it more valuable to the community and reduces possible future complications for the subjects. To our knowledge, this the first well-design study in Cyprus that collected information on adult population. Therefore, the findings are more representative compared to other previous data.

6.

Conclusions

The prevalence of T2DM is medium–high in Cyprus while the pre-diabetes levels are very high, showing a future increase in the total prevalence of type 2DM. However, our findings are consistent with the literature, that there is a wide range of factors, which are significantly related with diabetes. The findings demonstrate that excessive weight, hypertension, high serum total cholesterol, hypertriglyceridemia and low HDL levels may have a strong influence on the odds of T2DM. Additionally, old age and high energy intake may also increase the odds of having type 2 diabetes. Preventive strategies that focus on the correlates of T2DM should be initiated and implemented to build the awareness of the disease. Healthy dieting, promotion of exercise as well as behavioral programs should be promoted through public interventions.

Conflict of Interest The authors state that they have no conflict of interest.

Funding The study was funded by research grant—HEALTH/1104/21 by Cyprus Research Promotion Foundation and also from external sponsors, Flora Pro-Active, Zorpas Bakery, Lanitis Ltd., Costas Papaellinas, and Nestlé Ltd. All the above funders had no role in the design, analysis or writing of this article.

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Authorship [10]

DP and EA wrote the paper. EA designed the study and is the guarantor of this work for its accuracy and integrity. PH, SS, AK and AZ contributed on the concept of the study as well as advisors of the whole project. KK, TA, GCH, PK, CL and CP participated in the collection of data. CC and MC conducted the statistical analysis of the data. RK and CC participated in the laboratory analysis of data.

[11]

[12]

Acknowledgments The authors wish to thank all the volunteer clinical dietitians for their efforts, namely, C. Andreou, X. Averkiou, K. Christofi, E. Constantinou, M. Gabrielidou, P. Koulapi, S. Kountouri, N. Michaelidou, P. Michaelidou, K. Milidoni, Jean-Philippe Ricau, A. Stavrou, C. Schou, Y. Tsokkou, M. Yiannaki, M. Charalambous, C. Constantinou, C. Constantinou, M. Economou, C. Economidou, A. Erodotou, C. Koni, C. Kontos, C. Kompou, P. Lappa, K. Michael, O. Nicola, A. Nicolaou, A .Panayidou, A. Pahita, V. Piki, P. Prodromos, I. Savva, N. Stylianou, and V. Xenopoulou. Finally, we wish to thank the Cyprus Ministry of Health, the Cyprus Registration Board for Food Scientists, Food Technologists and Dietitians, and the Cyprus Parliamentary Committee on Health for their interest in and support of this study.

[13]

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[15]

[16]

[17]

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