1Unit of Reproductive Endocrinology, First Department of Obstetrics and Gynecology, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece; 2Department of Midwifery, Alexander Technological Educational Institute of Thessaloniki, Sindos, Greece
Basal metabolic rate (BMR) is one of the major components of total energy expenditure (TEE). It is affected by various factors, such as body weight, body composition, age, race/ethnicity, gender, biochemical parameters, physical activity, and health status. Gestational diabetes mellitus (GDM) is the most common metabolic disorder during pregnancy and it increases the risk for health complications, such as stillbirth, diabetes mellitus, and cardiovascular disease in later life. Both BMR and GDM have been linked with gestational weight gain (GWG), a fact suggesting a possible association between them. However, assessing BMR is a complex procedure, which becomes more complicated when additional parameters, such as pregnancy and GDM, are taken into consideration. The present review summarizes the current knowledge on factors affecting BMR and its regulation in relation to pregnancy and GDM. Future research addressing these associations should thoroughly consider other factors that affect BMI when designing such studies and/or discussing the BMR outcome results.
Affecting factors, Basal metabolic rate, Energy expenditure, Gestational diabetes mellitus, Pregnancy
The measurement of basal metabolic rate (BMR) is widely used for the assessment of metabolic activity in various groups and conditions. Gestational diabetes mellitus (GDM) is the most common metabolic disorder during pregnancy.1 Both BMR and GDM have been associated with the same factors,2,3 suggesting a link between BMR and GDM (Table 1). The most indicative factor seems to be gestational weight gain (GWG). GDM is increasing worldwide in parallel with overweight and obesity4 and several recent studies have identified GWG as an important and independent risk factor for GDM.5-7 Given that weight gain is principally regulated by the imbalance between energy intake and total energy expenditure (TEE) and BMR is a major component of TEE, BMR has also been associated with GWG.8-12
Several studies state that a low prepregnancy BMR is associated with increased GWG, which increases the risk for GDM (Figure 1a).13 Others claim that excessive GWG, in part due to increased maternal circulatory, respiratory and renal functions, is associated with increased risk for GDM.3 In this case, the higher BMR observed appears to be a mere epiphenomenon of the increased GWG (Figure 1b).
Figure 1. Hypotheses regarding the association between BMR and GDM: (a) Decreased prepregnancy BMR as a causative factor of GDM development, (b) Increased BMR as an epiphenomenon in GDM development. BMR: basal metabolic rate; GDM: gestational diabetes mellitus; GWG: gestational weight gain.
Although several studies have examined the relationship between BMR and GWG during normal pregnancy, to date there is no study describing this relationship in women with GDM. Therefore, the present review aims to present and critically appraise the current knowledge about the factors affecting BMR in normal pregnancy and in women with GDM in order to identify possible associations and suggest directions for future research.
BASAL METABOLIC RATE
BMR, defined as “the rate of energy expenditure (EE) in the post-absorptive state after 12-h overnight fast”, represents the minimum energy required to maintain all the vital activities and functions in the awake state.2 BMR is one of the three principal constituents of TEE, along with the thermic effect of food (TEF) and the EE of activity (activity thermogenesis),14 and is affected by such factors as age, gender, body composition, race/ethnicity, physical activity, nutrition, hormones, such as leptin, and health status.2 This section provides an overview of BMR measurement and describes the most significant factors affecting BMR.
Measurement of BMR
As BMR is affected by various factors, a significant variation occurs among individuals.15,16 Therefore, the measurement of BMR requires specific conditions to be met in order that accurate comparisons may be made. These standardized conditions include the time of the day (preferably between 06:00 and 09:00 h) and the environment (preferably thermoneutral at 22-26°C). Furthermore, the subjects should have slept at the site of the measurement overnight, have fasted for at least 10-12 h before measurement and be completely rested, awake, motionless, free from emotional stress, and in the supine position.2,14 The full description of complete methodology for BMR measurement is beyond the purpose of this paper.
As a principal component of TEE, BMR is used in various research projects. Nevertheless, due to practical issues, resting metabolic rate (RMR) is often used instead.2 The experimental conditions for BMR and RMR are similar; however, RMR is measured after at least 4 h fasting and factors, such as time of the day and physical activity, are not controlled.2 RMR is about 10% to 20% higher than BMR.2 Therefore, scientists need to take this difference into account when comparing RMR with BMR.
Body weight and composition
RMR and BMR have been proposed by some,17-19 but not all,20 researchers to be independent factors of weight gain, after adjustment for fat-free mass (FFM), fat mass (FM), age, and sex. Conversely, FFM is well-established as the principal predictor of BMR,10,15,21 while the contribution of FM to BMR seems more complex. FM is also positively associated with BMR,10,15,21 but this association appears to be exponential and dependent on the relation between FM and body weight.21 After weight loss, FFM and FM account for almost 50% of the Resting Energy Expenditure (REE) decrease.22 Furthermore, body mass index (BMI) is negatively associated with RMR/kg and, thus, BMR.23 In addition, both RMR/kg of body weight or RMR/kg FFM decrease with weight gain due to the decline of the relative contributions of the most metabolically active organs, such as the brain, liver, and heart.2 However, individual variation exists and other factors should also be evaluated. The associations of BMR with body weight parameters in pregnancy are discussed in sections 3.1 and 3.2.
TEE declines approximately 10 and 7 kcal/year for men and women, respectively,2 and BMR, as a significant component of TEE, declines by 1-2% per decade.24 However, the increased heterogeneity of the elder groups compared with the younger makes BMR prediction difficult.25 Although BMR in general declines,26 some subjects show in fact an increase with ageing.25 BMR reduction with age is partly explained by the loss of FFM and the gain of FM.26,27 FFM seems to account for most of the BMR variability (about 60%), but it is not the only factor involved.27,28 BMR is lower in older compared to younger adults, even when adjusted for FFM, with the reduction ranging across the studies from 4.6 to over 13%.29,30 In addition, the reduction in RMR due to age is greater than what can be attributed to FM or FFM.31 Recent evidence on REE indicates that BMR decline is also affected by decreases in: a) the contribution in organ and muscle masses to FFM and b) specific organ and tissue metabolic rates.32
Race and ethnicity
A number of studies report ethnicity as a factor affecting BMR levels,2 although factors such as methodology,33 physical activity, and nutrition34 might influence the reported ethnic differences. Caucasians seem to have higher BMR levels than non-Caucasians,35 while sub-Saharan Africans have been reported to have lower RMR levels.36 African-American adults37-40 and children41-44 have lower basal or resting energy expenditure levels, and thus BMR levels, than their white counterparts. However, this appears unlikely to account for weight gain in this population.45 Furthermore, African-American healthy adults seem to have a lower RMR than Caucasian independently of sleep duration.46 Moreover, a decline in REE, proportional to the amount of lost fat and lean mass, was reported for white but not for black women.47 Racial differences in BMR levels are also detected between indigenous and non-indigenous circumpolar groups, variations that are attributed to different thyroid responses to environmental stressors.48 Furthermore, total daily energy expenditure (TDEE) seems to be explained by variation in physical activity energy expenditure rather than REE in women49 or RMR in children.50 Gannon et al raise methodological concerns about the measurement of RMR with indirect calorimetry, the measurement of body composition and the menstrual cycle variation in RMR in studies examining RMR in African-Americans versus Caucasians.33 Further research, with particular focus on the experimental design and BMR affecting factors, would shed light on the detected racial RMR and BMR variance.
Gender differences in BMR levels are mostly attributable to differences in body composition and hormones.2 After adjustment for body composition, male adolescents seem to have higher BMR levels and energy expenditure than females,51-53 although not all researchers agree.54 However, even though obese male children and adolescents appear to have increased BMR levels compared to females, this difference was not detected in obese adults.27 In addition, it has been suggested that BMR variance depends on the menstrual cycle, with the follicular phase being 6-15% lower than the luteal phase.2 However, there are other studies that report no effect of the menstrual cycle on BMR.55 Despite this discrepancy, it is strongly recommended to record the menstrual cycle phase in studies examining BMR in women.
Thyroid hormones have been linked to BMR variation, but the literature is limited on this subject and presents contradicting reports. BMR and both triiodothyronine (T3) and the free T3 index seem to be positively associated after adjustment for body composition,56,57 but not all the studies agree.15,58 By contrast, thyroxine (T4) was both positively15 and negatively59 associated with BMR. Furthermore, T4 appears to have an effect on BMR levels in men, but not in women.15 Clearly, the effects of T4 on BMR require further investigation.
Leptin, adiponectin and resistin are members of the adipokine family. Leptin is linked with FM and body weight, but does not appear to be directly associated with BMR levels.15,60,61 The association of serum adiponectin with BMR is in dispute, as studies have found contradictory results describing a negative,62 a positive63 or no association.64 Circulating resistin has been connected with markers of obesity, insulin resistance and inflammation.65 However, we are not aware of any studies examining the association between resistin and BMR in humans.
Other hormones and cytokines, such as cortisol, fasting insulin, insulin-like growth factor 1 (IGF-1), C-reactive protein (CRP), and tumor necrosis factor-alpha (TNF-α), have been examined for their association with BMR. Despite the findings of a negative association between maternal cortisol levels and BMR, increases in maternal cortisol concentration levels were reported to determine 27.1% of the BMR variation during pregnancy,11 indicating a possible role of cortisol in GWG and a potential association with GDM. Furthermore, fasting insulin levels66,67 and IGF-110,67 have been positively associated with RMR or BMR, while the levels of fasting glucose seem to have a negative association with BMR.68 In contrast, the association between CRP and BMR is not yet clear, as the limited studies report conflicting findings.69-71 Finally, there is no apparent direct association between TNF-α and BMR.23
Physical activity is one of the most important components of TEE. Physical activity level (PAL), defined as the ratio of TEE / BEE, is “commonly used to describe typical physical activity levels”.2 However, the PAL approach used to calculate physical activity level has certain limitations and might produce errors in the estimation of both TEE and activity energy expenditure (AEE).72 The effects of physical activity on BMR are controversial and depend on specific parameters of physical activity, such as age, exercise volume,73 intensity, duration, frequency and type of exercise.74 Cross-sectional studies comparing endurance athletes with untrained control subjects report contradictory results with either no significant differences75,76 or an association pointing to higher levels in athletes.77 Longitudinal studies on physical activity effects exerted on BMR are also controversial. Endurance exercise training does not seem to affect RMR levels at normal altitudes78,79 but appears to affect it when performed at high altitudes.80 Although a 12-week endurance training program failed to induce changes in RMR, it prevented the decrease of RMR that was found in the non-training control group.81 Furthermore, physically active women seem to have a higher RMR than sedentary women.82
Type 2 diabetes mellitus (T2DM) has been positively associated with higher BMR levels in Pima Indians,83 Caucasians,84 and Japanese.85 Higher BMR levels in obese individuals with T2DM range from 5.2-7.1%, after adjustment for FFM, FM, age, and sex.84,85 In addition, a number of parameters have been identified as determinants of RMR in patients with T2DM: basal endogenous glucose output (3-3H-glucose), fasting insulin and free-fatty acid (FFA) concentrations, and glucose disposal.66 The association of BMR levels with GDM is discussed in section 5.
Several additional factors have been associated with BMR levels. Sleep restriction seems to decrease RMR levels,46,86 albeit not all studies are in agreement about this.87 Sympathomimetic medications have also been reported to increase RMR,88 while drugs, such as amphetamines, ephedrine, and some antidepressants, could increase BMR. In contrast, drugs, including propranolol, reserpine, and bethanidine, may reduce it.2 Although smoking seems to reduce 24-h EE,89 the effect of cigarette smoking on BMR remains unclear.2 Lower socioeconomic status appears to be associated with lower BMR levels.90,91
Pregnancy requires an additional amount of energy due to increased basal metabolism (BMR), the energy cost of physical activity and energy deposition for the development of maternal and fetal tissues,2 as well as for the woman’s gradual increase in cardiac output and respiratory rate.92 In addition, pregnancy is characterized by increased GWG due to higher demands for synthesis and maintenance of maternal tissue along with elevated fat deposition in order to support mother and fetus.93-95 Several factors have been proposed as being associated with BMR variation during pregnancy, including GWG, prepregnancy body fatness, IGF-1, thyroid hormones, and fetal size.10 This section briefly describes the factors of pregnancy that are linked or possibly associated with BMR and/or GDM. The association between BMR and GDM is described in section 5.
Normal pregnancy and BMR
BMR and its association with various factors in healthy and diabetic individuals were described in section 2. The relation of BMR with pregnancy is briefly described here.
A number of studies report increased BMR or RMR levels throughout pregnancy.3 The increases in BMR range from 124 to 157 MJ for the entire pregnancy,93 or from 8 to 35%.3 During late pregnancy, the fetus contribution to the BMR increase is about 50%.2 However, wide variability has been reported.10,93 Several factors have been implicated in the variability of BMR in pregnancy, including prepregnancy body weight and body fatness, lean body weight,96 reduced daily activity during pregnancy,95 changes in serum concentration of metabolism related-hormones,68 diabetes,96 and cardiac output changes.10 Nonetheless, controversy exists in regard to the magnitude of the contribution of each factor.
Gestational weight gain
The amount of GWG is critical, since it can have short- and long-term effects on both infant and maternal health.97 Within the recommended range, GWG is associated with improved birth outcome for both mother and fetus in regard to birth weight and perinatal complications.98 On the other hand, excessive GWG is independently associated with adverse maternal and neonatal outcomes, such as pre-eclampsia, cesarean delivery, perineal laceration, postpartum hemorrhage, macrosomia, large for gestational age (LGA) neonates, and neonatal intensive care unit (NICU) admission.99,100 Several lines of evidence support the association between excessive weight gain during pregnancy with increased birthweight,101-103 independently of genetic factors.102 Siega-Riz et al report an association between inadequate GWG and decreased birthweight.101 Furthermore, GWG is associated with postpartum body fat and weight retention104 and it has been identified as an independent risk factor for GDM,1,105,106 even though not all studies agree.107 GWG during the first trimester of pregnancy, but not during the second, was identified as an independent risk factor for GDM.99,108 Moreover, Morisset et al report that every kg of weight gain during the first trimester of pregnancy increased the risk for GDM by 25%.99
Physical activity in pregnancy
The controversial effects of physical activity in BMR levels are described in section 2.7. During pregnancy, physical activities require additional EE.2 Weight-bearing activities increase EE by about 19% after 25 weeks of gestation, while non-weight-bearing activities increase it by about 10%.94 Despite the additional energy required, possible reductions in PAL would counterbalance the effect of increased BMR levels and, thus, variation in TEE levels would remain low. Although the physical and mental benefits of exercise have been reported,109 physical activity effects on total EE of pregnant women are controversial due to variation of PAL and methodological issues.95 Most of the studies examining physical activity during pregnancy use methods of limited validity and reliability, questionnaires or interviews, which might inaccurately estimate physical activity levels.95 In addition, the majority of the studies examining the relation between recreational physical activity and two important pregnancy outcomes, birthweight and length of gestation, do not assess significant physical activity variables such as type, frequency, intensity, and duration.110
Nutrition is crucial to energy balance and thus to weight control. As described in section “Gestational weight gain”, insufficient or excessive GWG may lead to various negative outcomes. Nutritional interventions could reduce excessive GWG and improve outcomes for both mother and baby.111 Energy demands increase with pregnancy by 300 kcal/day on average, but there is variation between trimesters and among women.112 However, recommendations for a 240 kcal/day increase may support excessive weight gain and its negative outcomes.113 The requirements for the majority of nutrients also increase with pregnancy: proteins (by 25 g/d), iron, vitamins A, C, B group, as well as fiber and various minerals. In contrast, the recommendations for fluoride, calcium, and vitamins D, E, and K do not increase with pregnancy.112 Tanentsapf et al report lack of sufficient evidence to support the hypothesis that nutrition interventions could reduce the incidence of pre-eclampsia, macrosomia, and GDM.114 Nevertheless, more recent studies reveal associations between nutritional interventions and congenital anomalies, pre-eclampsia,115 and GDM116,117 and indicate the potential benefits of nutrition-specific and nutrition-sensitive interventions.
Pregnancy outcomes in pre-existing diabetes
Excess pregestational weight is significantly associated with cesarean delivery, gestational hypertension/pre-eclampsia, and GDM.118 Furthermore, women with pre-existing diabetes mellitus have higher risks for negative pregnancy outcomes than women with GDM.119 Women with pre-existing diabetes also have an increased rate of cesarean delivery than women with GDM,120,121 indicating a possible higher rate of macrosomia. This indication has been confirmed by the study of Wahabi et al in which the authors identified associations of pre-existing diabetes with increased risk for macrosomia, stillbirth, preterm delivery, and low APGAR scores at 5 min.121
GESTATIONAL DIABETES MELLITUS
GDM is the most common metabolic disorder during pregnancy.1 It is defined as “carbohydrate intolerance of varying degrees of severity with onset or first recognition during pregnancy”.122 The global prevalence of GDM rates ranges from 3 to 14%.123 GDM is associated with several health complications for both the mother and the infant, including metabolic and respiratory complications, cesarian section,124 cardiovascular disease, and development of T2DM for the mother125,126 and macrosomia (birth weight above 4 kg), low birth weight (<2.5 kg), and stillbirth for the infant.124,127
There are several non-modifiable and modifiable factors associated with GDM. Age, ethnicity, parity, and socioeconomic status are non-modifiable factors that affect the risk for GDM.128-130 Advanced maternal age is related to hypertension and GDM.131 The risk of GDM increases significantly and progressively from 2.1% in women aged below 25 years old to 7.0% in women aged 35 years or more.132 Moreover, the GMD recurrence rate is about 48%, with primiparous and Caucasian women having lower recurrence rates than multiparous and other ethnicities, respectively.133 The risk for development of GDM varies between different ethnic groups. Among the ethnic groups, Asians seem to have the highest risk for GDM development, followed by Middle Eastern, Caribbean, Central and South American, African-American, sub-Saharan African, Hispanic and Caucasian individuals.134-136 Finally, lower socioeconomic status, disadvantaged place of residence, multiple pregnancies, and marriage or partnership status are among the socioeconomic factors that increase the risk for developing GDM.129
Modifiable factors include excess prepregnancy weight,118 body composition, nutrition,120,137-140 physical activity, and excess GWG.99 BMI change141 and BMI gain between pregnancies142 are also important risk factors for GDM for multiparous women.142 A transition from obesity Class I (BMI 30-34.9 kg/m2) to class III (BMI >40 kg/m2) results in a two- to nine-fold increase of the risk for GDM.143 However, women with increased BMI but who are physically active during pregnancy have a 50% reduction in the risk of developing GDM.1 Moreover, FM and FFM have been associated with higher and lower risk for GDM development, respectively.141 The evidence for the protective effects of exercise on GDM risk is insufficient.144 A systematic review and meta-analysis by Russo et al identifies only a slight protective effect of physical activity against GDM.145 In contrast, Tobias et al report that women who have higher levels of physical activity seem to have significantly lower risk for GDM, while Sanabria-Martínez et al suggest that structured physical activity programs reduce the risk for the development of GDM.146-147
In addition to physiological and environmental factors, psychological stress appears to be linked with GDM. Stressful events were suggested as being an independent risk factor for the development of GDM.148 Nevertheless, Sit et al failed to discover significant variations in glucose challenge test responses between mothers with bipolar disorder (BD) or with current major depressive disorder and healthy mothers.149 Shorter sleep duration does not seem to have a significant effect on the risk for GDM development despite the reported higher fasting glucose levels after sleep restriction.150 Beta-adrenergic agents and corticosteroids appear to increase the risk for GDM development.151
Finally, a vast number of biomarkers have been examined for association with GDM, including fasting plasma glucose (FPG), insulin, and sex hormone binding globulin (SHBG). In early pregnancy, FPG levels lower than 80 mg/dl were negatively associated with GDM risk, while a 1.5-fold increase of GDM development risk was detected for every 5 mg/dl increase.152 Fasting plasma insulin, despite the positive association with GDM in the first two trimesters of pregnancy,153,154 and higher levels of insulin do not seem to predict GDM in all patients.155,156 In contrast, lower concentrations of SHBG before157 and during158 the first weeks of pregnancy are associated with the risk for developing GDM and appear to be a better GDM predictor than FPG.159 Of the various cytokines and inflammatory markers, only adiponectin, leptin,160 TNF-α and its ratio with interleukin-10 (TNF-α/IL-10)161 as well as the adipocyte fatty acid-binding protein (AFABP) seem to be related to the pathophysiology of GDM.162 Both TNF-α and AFABP are positively associated with GDM,161,162 Adiponectin levels show a negative association with GDM,162-164 even though not all studies agree.165 In contrast, leptin seems to be positively related and to predict GDM,164,166 but not all studies are in agreement.165,167 Also, high-sensitive C-reactive protein (hs-CRP) appears to predict GDM.158,168
IGF-1, cortisol, thyroid hormones (T3, T4), and iron status markers seem to have a possible role in the development of GMD. More specifically, an inverse association between GDM and both free IGF-1169 and IGFBP-1 was detected.169,170 Higher levels of cortisol have recently been correlated with hyperglycemia in ewes after daily cortisol infusions,171 but cortisol levels do not seem to be associated with GDM.152,168 Lower free triiodothyronine (T3) was suggested as an independent predictor of GDM,172 while thyroxine (T4) levels appear to decrease significantly in women with GDM, but only after the first trimester of pregnancy.172,173 Iron deficiency defined by serum ferritin and total body iron, but not by transferrin receptor, was recently associated with lower risk for GDM.174
BMR AND GDM
BMR and GDM have both been positively associated with body weight8,142 and GWG.7,107,141 However, a recent study showed no significant BMR variation between women with and without GDM.175 Weight gain is primarily regulated by the imbalance between the energy intake and the TEE8 and GWG is positively associated with increased risk for the development of GDM.1,108 Increased BMR is one of the major factors affecting elevated TEE and GWG during pregnancy, despite a partial compensation by a decrease in activity EE.68,97 Although a low prepregnancy BMR has been linked with a higher body weight6-8 and a higher GWG9 during pregnancy, the association between a low BMR and weight gain has been questioned as regards a typical Western population.20 However, crucial BMR-affecting factors, such as nutritional status and physical activity, were not evaluated in this study. In addition, there are physiological and metabolic differences between a typical Western population and women with GDM mainly caused by the development of maternal and fetal tissues as well as a gradual increase in cardiac output and respiratory rates.2 It has been reported that more than 60% of the variability in metabolic rate was explained by combining fetal weight and maternal weight gain.10
In addition to the relationship between prepregnancy BMR and GWG described above, there seems to be an association between GDM and BMR once GDM has been developed. Obesity affects many aspects of maternal metabolism, including insulin resistance and blood glucose metabolism.176 T2DM has been positively associated with higher BMR levels in various ethnicities after adjustment for FFM, FM, age, and sex,83-85 indicating a possible positive relation of BMR with GDM. However, to date no study has focused on the contribution of BMR among the risk factors for GDM development. This is an interesting field of research which requires further investigation.
BMR is one of the three principal components of TEE and is used in many research projects. The various factors affecting BMR can however generate inaccurate results and produce false interpretations when they are not appropriately considered. GDM is the most common metabolic disorder during pregnancy that increases the risk of several health complications for both mother and infant, such as metabolic, respiratory, and cardiovascular disease, and stillbirth. Several factors have been linked to GDM, including age, history of glucose intolerance, delivery of a child with macrosomia or LGA, race, overweight or obesity, GWG, lack of physical activity, insufficient or inadequate nutrition, and psychological factors. Most of these factors, especially GWG, also affect BMR, a fact that suggests a possible association of BMR with GDM. Since a) low prepregnancy BMR is negatively associated with GWG (Figure 1a), b) BMR increases during pregnancy in parallel with GWG, and c) GWG has been linked to GDM, we can assume that BMR might be associated with GDM, most likely through the increase of GWG (Figure 1b). This possible association should be taken into account in future GDM prognostic models. To date, there is not sufficient evidence for the relative contribution of BMR in GDM development. Future research could shed light on this association; until then, the factors affecting BMR should be thoroughly considered when the effect of BMR on GDM and GWG is examined.
E.T. wrote the first draft and edited the manuscript. D.S. (physical activity), E.T. (diet), P.P. (gestational diabetes) and G.M. (Endocrinology) made significant contributions in their areas of expertise. M.Z., D.V., B.C.T. and D.G.G. edited and revised the manuscript for important intellectual content.
CONFLICT OF INTERESTS / FINANCIAL DISCLOSURE
None for all authors.
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Address for correspondence:
Eleftheria Taousani, Unit of Reproductive Endocrinology, First Department of Obstetrics and Gynecology, Aristotle University of Thessaloniki, “Papageorgiou” General Hospital, Ring Road, 56403, Nea Efkarpia, Thessaloniki, Greece; Tel.: +30 2310 233468, E-mail: firstname.lastname@example.org, email@example.com
Received: 03-05-2017, Accepted: 24-09-2017