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Saudi Journal of Kidney Diseases and Transplantation
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Table of Contents   
ORIGINAL ARTICLE  
Year : 2019  |  Volume : 30  |  Issue : 1  |  Page : 24-32
Evaluation of the anthropometric clinical measurements and Vitamin D status in kidney transplant recipients: Comparison between sexes


1 Department of Medicine, Santa Casa de Sao Paulo School of Medical Sciences, São Paulo, SP, Brazil
2 Department of Nephrology, Santa Casa de Sao Paulo School of Medical Sciences, São Paulo, SP, Brazil

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Date of Submission06-Nov-2017
Date of Decision29-Jan-2018
Date of Acceptance02-Feb-2018
Date of Web Publication26-Feb-2019
 

   Abstract 


Anthropometric clinical indexes have been used to verify the association of obesity with Vitamin D status; however, different reports have yielded conflicting results. The aim of this study was to evaluate the relationship between anthropometric clinical indexes and Vitamin D status in kidney transplant recipients (KTR), comparing by sex. Eighty-five KTR were selected and demographic, clinical, and laboratory data were collected. Anthropometric evaluation using clinical indexes and body composition by bioelectrical impedance analysis were determined, and the patients compared by sex. No differences of serum 1,25-dihy-droxyvitamin D (25(OH)D) values between males and females were found. Females had higher abdominal obesity observed by waist/height ratio and waist/weight ratio, and also higher body fat%, than males. No correlation was found among the 25(OH)D levels and anthropometric data in both sexes. Since serum 25(OH)D concentrations could be influenced by body weight, we also analyzed the 25(OH)D/weight ratio, and this showed an inverse correlation with body mass index (BMI), waist circumference (WC), WC/height ratio, index, conicity index, and body fat%, in females. Moreover, the comparison of the 25(OH)D values among patients classified by BMI showed no differences between sexes. However, the 25(OH)D/weight ratio revealed lower values in overweight and obese patients compared with the normal BMI group, and progressively decreased as the BMI increased, mainly in females. The study suggests that KTR with higher abdominal obesity may need higher Vitamin D intake to obtain adequate serum 25(OH)D status, notably in females.

How to cite this article:
B. Argentino AC, Souza JF, dos Santos Sens YA. Evaluation of the anthropometric clinical measurements and Vitamin D status in kidney transplant recipients: Comparison between sexes. Saudi J Kidney Dis Transpl 2019;30:24-32

How to cite this URL:
B. Argentino AC, Souza JF, dos Santos Sens YA. Evaluation of the anthropometric clinical measurements and Vitamin D status in kidney transplant recipients: Comparison between sexes. Saudi J Kidney Dis Transpl [serial online] 2019 [cited 2019 Jul 20];30:24-32. Available from: http://www.sjkdt.org/text.asp?2019/30/1/24/252919



   Introduction Top


The active form of Vitamin D, 1,25-dihydroxy-vitamin D (1,25(OH)D) exerts its multiple actions through the widely distributed Vitamin D receptors (VDR) in tissues and cells.[1] Recent studies have demonstrated that VDR and Vitamin D metabolizing enzymes are expressed in adipocytes. The VDR expression in adipose tissue is related to obesity and might be regulated by 25(OH)D.[2] The direct effect of Vitamin D deficiency on atherogenic dyslipidemia is still debated.[3],[4] A specific lipid pattern, characterized by low high-density lipoprotein cholesterol (HDL-C), increased low-density lipoprotein cholesterol (LDL-C), and increased levels of triglycerides (TGs) is associated with increased atherogenic risk, and the Vitamin D deficiency is also associated with this lipid pattern.[5] The prevalence of abdominal adiposity among US women and overweight men has increased, irrespective of the body mass index (BMI) categories.[6] This trend in body fat distribution suggests a need for alternative approaches to anthropometry in clinical and epidemiologic settings. Rather than concentrating on total body weight, examiners could focus on external measurements of the abdomen. These considerations support the logic of quantifying dysfunctional adiposity primarily through an external, inexpensive estimate of intra-abdominal adipose tissue accumulation. The waist circumference (WC) has been employed as an approximate measure of abdominal adipose tissue, although the WC/height ratio may represent an anthropometric improvement because it roughly controls variation in the adult stature.[7],[8] Neither WC nor WC/height ratio distinguishes between abdominal adipose tissue accumulated into the visceral or subcutaneous compartment.[9] Other anthropometric indexes have been utilized, such as the lipid accumulation product (LAP) index, an easy parameter for the calculation of dysfunctional adiposity, and it is proposed as a powerful marker for metabolic syndrome (MS) and insulin resistance. The LAP index was created to describe the metabolic interplay between accumulated visceral fat and impaired TG metabolism.[10] The TG to HDL-C ratio is also considered as a marker for dyslipidemia and insulin resistance.[11],[12] The conicity index (CI) incorporates three measures, including the WC, weight and height, which are common to the other indexes. The theoretical range of the CI is between 1.00 and 1.73 and this ratio increases with the accumulation of abdominal fat.[13],[14] The magnitude of lipid accumulation in abdominal ectopic sites, however, cannot be estimated directly except by costly imaging technologies. High prevalence of obesity and hypovitaminosis D has been observed after kidney transplantation; also, the MS and cardiovascular disease have been associated with kidney transplantation outcomes.[15],[16] Sex differences have been suggested for Vitamin D status. However, few studies have evaluated the differences in 25(OH)D levels according to sex in chronic diseases.[17] The factors frequently associated with hypovitaminosis D include reduced sun exposure, a diet low in calcium and Vitamin D, nutritional status, and decreased renal function. In addition, many other factors may contribute to the Vitamin D insufficiency in kidney transplant recipients (KTR) including: the recommendation to avoid sun exposure and to use sunscreen for prevention of skin cancer, allograft dysfunction, use of immunosuppressive drugs (especially corticosteroids), and elevated fibroblast growth factor 23 a phosphatonin that suppresses 25(OH)D after kidney transplantation.[18] Anthropometric indexes have been used to verify the association of obesity with Vitamin D status, however, different reports have yielded conflicting results. Some authors related the controversy to race, gender, or age differences.[19] In addition, there are anthropometric indexes which are less known and less used in clinical practice and some of them have not been previously tested in KTR. The objective of this study was to evaluate the relationship between anthropometric clinical indexes and Vitamin D status in KTR and comparing them by sexes.


   Methods Top


This is an observational and transversal study of the KTR attending the nephrology clinic in a hospital in Sao Paulo, Brazil. A total of 147 patients who had a minimum of two years posttransplantation and glomerular filtration rate (GFR) ≥15 mL/min were enrolled for the study; 58 were excluded since they did not meet the inclusion criteria, four refused to participate, and the remaining 85 were eligible for additional analysis. The patients with a history of endocrine diseases, diabetes, alcohol abuse, liver diseases, acute infection, pregnant or lactating, or receiving calcium or Vitamin D supplements were excluded. All patients were receiving immunosuppressive therapy, which consisted of combination of calcineurin inhibitors (tacrolimus or cyclosporine), mycophenolate or azathioprine and prednisolone. The study was approved by the Ethical Committee of the Institution No. 608418, and the participants were informed and signed consent forms were obtained to participate in the study. Demographic and clinical data were obtained from the medical records and during the regular visits to the outpatient at the Hospital in a low latitude city (23.5°/South latitude) in Brazil, between September and December, 2014 (spring season). Blood pressure levels (mean of three measurements) were recorded. Blood samples for fasting glucose, creatinine, 25-hydroxyvitamin D, parathyroid hormone (PTH), and lipid profile with total cholesterol, HDL-C, LDL-C, and TGs were collected. The estimate GFR (eGFR) was obtained using the chronic kidney disease (CKD) epidemiology collaboration formula.[20] Serum glucose, creatinine, and lipids were determined by automated methods (Beckman Instruments, Brea, USA). Serum 25(OH)D and intact PTH were measured using chemiluminescense immuno-assay. Vitamin D values were defined as normal if serum 25(OH)D levels were ≥30 ng/mL, insufficient when between 15 and 30 ng/mL and deficient if <15 ng/mL.[21] All the blood samples were collected on the same occasion and bio-electrical impedance analysis was performed. The MS was diagnosed according to the revised NCEP-ATP III criteria.[22]

Anthropometric data

All patients were subjected to an anthro-pometric evaluation and body composition assessment through bioelectrical impedance analysis. Body weight was determined using a portable, digital scale (Tanita® Corp., model UM080, USA) with capacity up to 150 kg. Height was assessed using a portable stadio-meterscale (Sanny®, model ES 2060, Brazil). BMI was calculated using the formula: weight (kg) divided by height squared (m2). The BMI classified the patients according to the WHO definition.[23] Body composition was estimated by bioelectrical impedance analysis, and was performed with a portable device (Maltron®, Body Composition Analyzer model BF-907, United Kingdom); the software provided by the manufacturer calculated the percentage of body fat (between 20% and 25% considered normal). Central obesity was assessed by WC in standing subjects (measured midway between the lower costal margin and the iliac crest, using an inelastic measuring tape), by WC/height ratio, and WC/weight ratio. The LAP index was obtained by the formulas: for males, LAP = [WC (cm)–65] χ [TG concentration (mmol/L)], and for females, LAP = [WC (cm)–5] × [TG concentration (mmol/ L)].[24] The CI was obtained by the formula: CI = WC (m)/0.109 × [square root of (Weight (kg)/ Height (m)].[13],[14] The TGs/HDL-C ratio was also calculated.


   Statistical Analysis Top


The data were expressed as mean ± standard deviation or frequencies. The patients were divided into two groups based on sex. Differences between groups were examined using unpaired Student's t-test if the data presented a normal curve distribution, otherwise, Mann–Whitney U-test was used. To compare proportions, Chi-square test was used. Pearson's correlation coefficients between serum 25(OH)D values or 25(OH)D/weight ratio with anthropometric indexes were determined. To compare differences among categories of BMI, Kruskal–Wallis complemented by Dunn test were performed. Differences with P <0.05 were considered significant. Statistical analyses were performed using Statistical Package for Social Science (SPSS) software version 13.0 (SPSS Inc., Chicago, IL, USA).


   Results Top


Of the 85 KTR studied, 37 (43.5%) were females and 48 (56.4%) were male, the mean age was 38.1 ± 13.5 years (18–60 years). The median posttransplant period was eight years (2–36 years). The most common cause of CKD in this group was hypertensive nephrosclerosis (46.1%) followed by chronic glomerulopathy (36.3%) and others (16.5%). Sixty-five percent of the patients received renal grafts from living donors. For analysis, the patients were divided into two groups based on sex. The comparison of the demographic, biochemical and anthropometric data between sexes of the study patients are shown in [Table 1]. There was no significant difference between the sexes in age, race, and presence of arterial hypertension, PTH and eGFR. Males had higher fasting glucose and females had higher HDL-cholesterol values. No significant differences were found between males and females in the 25(OH)D values, which varied from 5.1 to 55.0 ng/mL. However, when Vitamin D values were adjusted according to body weight [25(OH)D/weight ratio], females had higher levels. Females also had higher abdominal obesity, as observed by WC/height ratio, WC/body weight ratio, and higher body fat%. The MS was diagnosed in 51.3% (19/37) of females and in 50% (24/48) of males (P = NS). No significant differences were observed in the other data between females and males.
Table 1: Demographic, biochemical, and anthropometric data of the 85 kidney transplant recipients, according to sex.

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Since the serum 25(OH)D concentration is affected by the amount of body fat, we also analyzed the 25(OH)D/weight ratio. [Table 2] shows the correlations between 25(OH)D values and the 25(OH)D/weight ratio with anthropometric data. No significant correlation was found in the 25(OH)D values and anthropometric data in females or males. However, the 25(OH)D/weight ratio showed a significant inverse correlation with BMI,WC, WC/height, body fat%, LAP index, and CI, in females only. Among males, no significant correlation was observed. Moreover, no significant correlations were found between TG/ HDL-C and 25(OH)D or the 25(OH)D/weight ratio, in both sexes. Furthermore, no significant difference was obtained when we examined the correlation between 25(OH)D or the 25(OH)D/ weight ratio and eGFR or PTH, in both females (eGFR: r = 0.28, P = 0.09 and r = 0.30, P = 0.07; PTH: r = −0.34, P = 0.05-and r = −0.21, P = 0.23, respectively) and males (eGFR: r = –0.03, P = 0.83 and r = 0.09, P = 0.52; PTH: r =0.10, P = 0.47, and r = −0.0, P = 0.74, respectively).
Table 2: Pearson's correlation coefficients between 25(OH)D levels and 25(OH)D/weight ratio with anthropometric data in kidney transplant recipients.

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[Table 3] shows the patients stratified based on BMI categories and sex. Among females, 29.5% were normal, 40.5% were overweight, and 29.7% were obese; among males, 41.6% were normal, 45.8% were overweight, and 12.5% were obese. When Vitamin D values were compared among categories of BMI, we observed no significant differences among females. However, the 25(OH)D/weight ratio was found to be significantly lower in overweight and obese patients compared to those with BMI <25, especially in females. We observed that the values of serum 25(OH)D/ weight ratio progressively decreased as the BMI increased. Among males, no significant difference was found among any of the BMI categories, although there was a tendency toward a lower 25 (OH)D/weight ratio in obese patients.

The comparison of body fat% between sexes in different categories of BMI showed that the body fat% was higher in females than in males [Table 4].
Table 3: Comparison among patients of different categories of body mass index with Vitamin D values and Vitamin D/weight ratio according to sex.

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Table 4: Comparison of body fat% between sexes, in different categories of body mass index.

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   Discussion Top


The study evaluated the relationship between the anthropometric clinical indexes and serum 25(OH)D values in KTR. Overall, it was demonstrated that the Vitamin D/weight ratio had good correlation with anthropometric data to identify the Vitamin D status than the values of 25(OH)D only, in females. The 25(OH) D/weight ratio showed an inverse correlation with BMI, WC, WC/height, body fat%, LAP index, and CI. The study also found the known association of obesity with hypovitaminosis D. Cheng et al[25] in the Framingham cohort showed that Vitamin D deficiency was highly correlated with adiposity measures assessed by computerized tomography, and more prevalent in patients with high visceral and low subcutaneous fat, although no analysis of sex differences was reported. Adults from the Caribbean with higher BMI, WC, and waist/ hip ratio had a lower Vitamin D status.[26] However, conflicting data from different populations have been reported, because the correlation between 25(OH)D and anthropometric indexes can be influenced by the age, gender, race, the body weight, and height of the patients. In the HELENA study in European male and female adolescents, no significant correlation was found between Vitamin D level and BMI.[27] In healthy African-American and Caucasian women from the US, it was observed that the serum Vitamin D level was not correlated with the BMI, although it was inversely associated with body fat%.[28] The BMI is only an indirect index of overall fat mass and it is influenced by other components, such as muscle and bone mass. The GFR and PTH values can be related to Vitamin D levels, but in the present study no significant differences were obtained when the correlation between 25(OH)D or 25(OH) D/weight ratio and eGFR or PTH was examined, in both sexes. The LAP index is expressed by the association of the WC and hypertriglyceridemia, which increases with age for males than for females.[25] In the present study, the LAP index in females was inversely associated with 25(OH)D/weight ratio, but not with 25(OH)D. Patients with type II diabetes with higher LAP indexes exhibit a high risk of 25(OH)D deficiency, suggesting that adiposity is a worsening factor for hypovitaminosis D and occurs to a greater extent in males than in females.[29] Roriz et al[8] evaluated the accuracy of anthropometric clinical indicators, using computerized tomography as the gold standard, in adults and elderly of both sexes. The LAP index, as well as the CI and WC/height ratio had high accuracy in determination of abdominal obesity among individuals with different measurements of body weight and height. Another study determined the clinical utility of visceral adipose tissue (VAT) measured by computerized tomography compared with measures of total fat mass, body fat%, WC and BMI, in white and African–American adults. The authors concluded that the VAT was not any better than the WC, and recommended the use of WC for the identification of adults with elevated cardiometabolic risk factors.[30] In the present study, there was an inverse correlation between the CI and the 25(OH)D/weight ratio, but not with 25(OH)D, although to our knowledge, no study has evaluated the CI in KTR, making it impossible to compare with our results. The comparison among patients from different categories of BMI with 25(OH)D values did not show a difference in either sex. However, the 25(OH) D/weight ratio showed a significant and progressive reduction in overweight and obese patients compared to those with a BMI <25, especially in females [Table 3]. In addition, the comparison of body fat% between genders, in different categories of BMI, showed that the body fat% is higher in females than in males [Table 4]. Conversely, in the adult Korean population, Kim and Kim[31] found that the 25(OH)D level was significantly higher in males than in females, and an inverse association between serum 25(OH)D with body fat% was found, after adjustment for age. Our findings are consistent with other studies reporting an inverse relationship between Vitamin D levels and obesity in women.[32],[33] Al Asoom[33] demonstrated that the 25(OH)D/ weight ratio was negatively associated with WC and WC/height ratio in young females, and considered that the relative value of Vitamin D to body weight is a better indicator of Vitamin D status, particularly in obese patients. The gonadal hormone, such as estrogen may play a role in these sex differences because it has a favorable effect on insulin and glucose homeostasis, adipose tissue distribution, and pro-inflammatory markers.[34] Up to menopause, females tend to accrue adipose tissue preferentially in the subcutaneous tissue due to its greater storage capacity, and men accrue adipose tissue preferentially in the visceral area. Menopause is followed by redistribution of adipose tissue to the visceral area.[35] The diversity of Vitamin D receptor polymorphism in different racial groups could also be involved and comparison could be difficult because the studies used different measurements for adiposity in different ethnic groups.[36] In Brazil, hypovitaminosis D (serum 25 Vitamin D <30 ng/mL) was present in 77.4% of the healthy Brazilian population and a study on KTR of both sexes indicated an independent and inverse association of body fat with 25(OH) D levels.[37],[38] Another study on KTR found that females had higher body adiposity values, abdominal obesity and diabetes prevalence than males, but the association with 25(OH)D levels was not studied.[39] The present study shows that in KTR, lower levels of Vitamin D were observed in females with higher WC, BMI, and other anthropometric indexes. These associations can be found in specific populations, who are characterized by elevated levels of abdominal fat accumulation and often exhibit MS, as observed in approximately half of the KTR in this study. While the serum 25(OH)D concentration is affected by the volume of body fat, it seems reasonable to analyze the status of Vitamin D adjusted to body weight.

The limitations of this study include the small sample size from a single center, the seasonal variation that may occur on Vitamin D values and the cross-sectional design of the study permits examination of association, but not causal or temporal relationships.

In conclusion, the study suggests that KTR with higher abdominal obesity may need higher Vitamin D intake to obtain adequate serum 25(OH)D status, notably in females. The measure of the Vitamin D/weight ratio as an indicator to evaluate the Vitamin D status requires other studies.


   Ethical Approval Top


All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee at which the studies were conducted (No. 608.418) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.


   Informed Consent Top


Informed consent was obtained from all individual participants included in the study.


   Acknowledgment Top


The authors are grateful to the CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior); Statistics service; and to the Support Center for Scientific Publications of Santa Casa de Sao Paulo School of Medical Sciences.

Conflict of interest:

None declared.



 
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Nicoletto BB, Fonseca NK, Manfro RC, et al. Effects of obesity on kidney transplantation outcomes: A systematic review and meta-analysis. Transplantation 2014;98:167-76.  Back to cited text no. 16
    
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Correspondence Address:
Yvoty Alves dos Santos Sens
Department of Medicine, Santa Casa de Sao Paulo School of Medical Sciences, São Paulo, SP
Brazil
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DOI: 10.4103/1319-2442.252919

PMID: 30804263

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