Are there any differences between women with long term gastric bypasses and non-operated matched controls in body composition, muscular strength and physical performance?

doi:10.21203/rs.3.rs-4863214/v1

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Are there any differences between women with long term gastric bypasses and non-operated matched controls in body composition, muscular strength and physical performance?

https://doi.org/10.21203/rs.3.rs-4863214/v1

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Introduction:

There is concern about an excessive loss of fat-free mass (FFM), and its consequences in the long term after bariatric surgery. The aim of this study was to evaluate body composition, muscle strength and physical performance in a group of women who underwent Roux-en-Y Gastric Bypass (RYGB-G) more than 2 years ago, and had stable weight, not significant weight regain, using micronutrient supplementation and compare them with a non-operated control group (CG).

Methods

We assessed body composition by DEXA, handgrip strength (HGS) and physical performance through sit-to-stand tests in the RYGB-G (n = 13) and in a CG (n = 13) matched by age, body mass index, skin phototype and physical activity level. Dietary intake, sun exposure, nutritional, biochemical and hormonal assessments were done in both groups.

Results

The RYGB-G had a mean follow-up of 6.7 ± 2.8 years and had a greater FFM (42.3 ± 4.9 vs 38.4 ± 4.5kg, p = 0.049), FFM% (60.7 ± 5.1 vs 56.1 ± 5.1%, p = 0.027) and FFM/Fat Mass (1.72 ± 0.43 vs 1.39 ± 0.30kg, p = 0.033) than the CG. The CG had a higher fat mass percentage (FM% 36.4 ± 5.2 vs 41.1 ± 5.3%, p = 0.029). There were no differences between the groups for HGS or physical performance tests. The average energy intake was significantly higher in the CG 1021.5 (957.5-1278.7) vs 1498.6 (1310.7-1767.7) kcal/day p = 0.002.

Conclusion

Women with a long term RYGB (BMI 27.5 ± 3.4 kg/m²) and regular use of micronutrients supplementation had a higher FFM, FFM%, FFM/FM and lower FM% compared to a CG, without differences in HGS or physical performance tests.

Women with long term RYGB had better body composition than a control group
Women with long term RYGB don’t have less strength than a control group
Women with long term RYGB have similar physical performance than a control group

During the first year of bariatric surgery (BS), the decrease in weight is mainly due to a reduction in fat mass (FM) accompanied by a significant loss of fat-free mass (FFM) that can vary between 33 and 35% [1–5]. In this period of time the loss of FFM is mainly at the expense of muscle mass, which could have negative consequences on metabolism, muscle strength, physical performance and resting energy expenditure [6–9]. However, after the first year of BS, weight reduction would continue in a physiological way, bringing bariatric patients to a body composition (BC) similar to non-operated controls (10–17].

The degree of loss of FFM is variable among patients undergoing BS and is influenced by type of surgery, gender, age, body mass index (BMI), FM, FFM, and muscular strength prior to surgery [18–22]. In the postoperative period, some factors can counteract this loss of FFM and allow adequate muscle function, e.g.: level of physical activity, protein intake and some micronutrients such as iron, calcium, phosphorus, zinc, vitamin B₁₂ and vitamin D which are essential for proper energy metabolism, DNA synthesis, oxygen transport and the functioning of the neuro-muscular unit [23–26].

Few studies have been published evaluating muscular strength and functional capacity in patients with more than two years of BS; most have been carried out during the first postoperative year and with a wide variety of methodologies. Most studies show that physical performance improves after the first year of BS [27].

The objective of this study was to evaluate BC, muscle strength and physical performance in a group of women who underwent Roux-en-Y Gastric Bypass (RYGB-G) more than 2 years prior, with stable weight, without significant weight regain and compare them with a non-operated control group (CG).

Patients

13 women submitted to RYGB at least 2 years prior and current stable weight were evaluated. They were matched by BMI, age, physical activity level and skin phototype with 13 controls at the time of evaluation. The exclusion criteria were: weight regain ≥ 15% with respect to the nadir, revisional surgery, pregnancy, kidney or liver disease; lack of micronutrient supplementation and use of medications that affect nutritional status. All the volunteers completed all exams and functional tests.

This study was approved by the Ethics Committee for Human Research of the Faculty of Medicine of the University of Chile and informed consent was obtained from all individual participants included in the study.

Measurements

Anthropometry and body composition

Weight and height were measured using a Seca® digital weight (Vogel & Halke GmbH & Co, Germany). BC analysis was performed using DEXA (Lunar Prodigy Advance, General Electric Medical Systems, Madison, Wi, USA. Software v15 SP2). The results were used to determine FM, FM percentage (FM%), non-bone fat-free mass (FFM), FFM percentage (FFM%), upper limb FFM (FFM-UL) lower limbs FFM (FFM-LL) and appendicular skeletal muscle mass (ASMM).

Muscular strength.

Handgrip strength dynamometry

Handgrip strength (HGS) was evaluated with dynamometry performed with a Jamar® hydraulic dynamometer, following the measurement technique recommended by the American Society of Hand Therapists [28]. Three measurements with the dominant hand and non-dominant hand were done with one minute of rest between each attempt.

Physical performance tests.

Sit-to-stand test in 5 repetitions (5-STS) and for 30 seconds (STS-30s)

Lower extremity muscle functional capacity was measured by sit-to-stand tests. 5-STS was described by Bohanon R [29]. After a 10-minute break, the STS-30s was performed in which, after giving the signal, the volunteers sat and stood up again for 30 seconds.

Level of physical activity, skin phototype and sun exposure

The International Physical Activity Questionnaire (IPAQ) was applied. The skin phototype was identified through the phototype evaluation test [30]and the level of sun exposure with the sun exposure score [31].

Dietary Intake Evaluation

Dietary intake was assessed using a 24-hour recall test and food frequency questionnaire, and all participants were asked about their use of vitamin or mineral supplements [32–34]. Questionnaire results were analyzed with the Food Processor II software (ESHA Research, Salem, OR, USA), which uses a nutritional database for North American and Chilean foods [35]. These results were then used to analyze adequacy of nutrient intake according to standards published by the Food and Nutritional Board of the Institute of Medicine in association with Health Canada [36].

Hematological and biochemical evaluation

Hemoglobin and mean corpuscular volume were measured using a Coulter cell counter (CELL-DYN 1700; Abbott Diagnostics, Abbott Park, IL, USA). Basal glucose, calcium, phosphorus and urinary urea nitrogen were measured using dry chemistry (Vitros 4600). Basal insulin and ferritin were measured using chemiluminescence. Glycosylated hemoglobin was measured through HPLC. A 24-hour urine collection was done the day before the evaluation, to measure urinary urea nitrogen and calculate the nitrogen balance: (ingested protein (g)/6.25) - (24-hour urinary urea nitrogen + 4).

Assessment of vitamins, minerals and hormones

Vitamin B₁₂ was measured by chemiluminescence and 25(OH) vitamin D by ELISA. Plasma zinc was measured using the method described by Smith et al. [37] and Ruz et al. [38] with a PerkinElmer Analyst 100 atomic absorption spectrophotometer (PerkinElmer Corp. Waltham, MA, USA). Thyroid stimulating hormone and parathyroid hormone were measured through chemiluminescence.

Statistics

Considering the CG would have a 10% higher value of HGS compared to the RYGB-G [39], with an alpha error of 5% and power of 80%, a sample size of 13 individuals per group was estimated (Stata 12.1 program). The Shapiro Wilk Test was used to assess normal distribution. The results were expressed as mean ± standard deviation or median (p25-p75). Mann-Whitney test and independent two-sampleT-test were applied as appropriate. Correlations were made through the Pearson or Spearman test. Significance was considered with p-value < 0.05. SPSS 22.0 program was used for data analysis.

General

Thirteen patients submitted to RYGB 6.7 (4.9–7.7) years prior were evaluated. The median of weight regain was 7.3% (1.6–11.6%). Table 1 shows the preoperative BMI, preoperative complications prevalence and their prevalence on the day of the study. Also shows descriptive statistics of patients and highlights significantly higher triceps skin fold in the CG.

Table 1

Descriptive statistics of subjects
Parameter^a	RYGB		Controls	P value*
	Pre-surgery	Present time
Age (years)	44.5 ± 10.1	50.2 ± 9.7	50.4 ± 8.4	0.958
T2DM n (%)	4 (30.7)	1(7.7)	0 (0.0)
HTN n (%)	6 (46.1)	3 (23.0)	0 (0.0)
Dyslipidemia n (%)	7 (53,8)	0 (0.0)	0 (0.0)
Arthropathy n (%)	9 (69.2)	2 (15.4)	0 (0.0)
OSAHS n (%)	1 (7.7)	0 (0.0)	0 (0.0)
Weight (kg)	105.6 ± 13.4	69.8 ± 8.0	69.3 ± 10.8	0.894
Height (m)	1.6 ± 0.1	1.6 ± 0.1	1.57 ± 0.07	0.381
BMI (kg/m²)	41.6 ± 5.6	27.5 ± 3.4	28.0 ± 3.9	0.726
WC (cm)		86.2 ± 9.1	89.0 ± 9.9	0.463
BC (cm)		31.0 ± 3.7	31.3 ± 3.1	0.813
TSF (mm)		19.0 (15.0-20.8)	25.0 (20.5–25.0)	0.016
AMA (cm²)		44.4 ± 12.7	40.6 ± 9.2	0.390
Physical activity level (METS)		792.0 (342.8-1,996.5)	1,318.0 (181.5-2 027.3)	0.840
Skin phototypes 2 n (%) 3 n (%) 4 n (%)		1 (7.7) 10 (76.9) 2 (15.4)	3 (23.1) 8 (61.5) 2 (15.4)	0.543
RYGB Roux-en-Y gastric bypass, T2DM type 2 diabetes mellitus, HTN hypertension, OSAHS Obstructive sleep apnea-hypopnea syndrome, BMI body mass index, METS metabolic equivalent of task, BC Brachial circumference, AMA arm muscle área, TSF triceps skin fold, WC waist circumference.
^a Values are expressed as mean ± SD or median (25th-75th percentile).
* P values were obtained from the independent two-sampleT-test or Mann-Whitney test or chi square test to indicate statistical significance for between-group differences. Differ significantly between groups at P < 0.05.
.

Energy, macronutrient and micronutrient intake

Estimated energy and macronutrient intake are shown in Table 2.

Table 2

Energy and macronutrient intake determined by using a food frequency questionnaire
Parameter^a	RYGB	Controls	P value*
Energy (kcal/day)	1201 (957–1278)	1498 (1310–1767)	0.002
Carbohydrate (g/day) %TCV	154.1 (127.0-177.0) 47.0%	181 (153.0-203.0) 46.5%	0.080
Protein (g/day) %TCV	52.5(37.0–64.0) 19.0%	59.7 (52.0–76.0) 17.0%	0.100
Fats (g/day) %TCV	41.7 (24.0–48.0) 34.0%	51.6 (43.0–83.0) 36.0%	0.047
Saturated fat (g/day)	11.3 (5.8–17.5)	17.7 (11.7–27.5)	0.047
Monoinsaturated fat (g/day)	7.4 (4.0-13.4)	1307 (10.4–21.7)	0.063
Polyunsaturated fat (g/day)	3.9 (2.8–7.4)	6.5 (4.6–13.8)	0.063
Cholesterol (mg/day)	113.5 (61.7-309.4)	257.9 (139.4-378.2)	0.100
Fiber (g/day)	12.8 (10.9–16.6)	13.1 (10.2–21.7)	0.800
RYGB Roux-en-Y gastric bypass, TCV total caloric value.
^a Values are expressed as median (25th-75th percentile).
Thus, the P values were obtained from the Mann-Whitney test to indicate statistical significance for between-group differences. Differ significantly between groups at *P < 0.05.
.

The distribution of CHO and protein intake was within the recommended range in both groups, but the percentage of fats intake was above the recommendation in the CG (p = 0.047). The average intake of energy, total and saturated fat intake were significantly higher in the CG. There was wide variability in protein intake without significant differences between the groups. The nitrogen balance in the RYGB-G was − 5.55 (-7.97 - -4.91) and in the control group it was − 2.07 (-7.35 - +0.35) with no

differences between the groups.

As shown in Table 3, the dietary micronutrients intake presents a low percentage of adequacies to their recommended dietary allowance (RDA), in both groups. This is reversed with the use of supplements in the RYGB-G.

Table 3

Micronutrient intake and adequacy determined by using a food frequency questionnaire.
Micronutrient	RDA	RYGB			Controls		P value*
		Median (p25-p75)	Diet Adequacy (%)	Diet + Supplement Adequacy (%)	Median (p25-p75)	Diet Adequacy (%)
Iron (mg/day)	18	6.3 (4.0-10.7)	35.0	234	8.9 (7.3–13.3)	49.4	0.000
Calcium (mg/day)	1000	224.2 (120.6-706.2)	22.4	137	534.9 (343.9-691.5)	53.5	0.004
Phosphorus (mg/day)	700	363.9 (150.2-727.3)	51.9	87	688.1 (453.2-1,007.2)	98.3	0.500
Zinc (mg/day)	8	3.0 (1.2–5.4)	37.5	140	5.0 (3.3–7.7)	62.5	0.001
Vitamin B12 (µg/day)	2.4	1.23 (0.09–2.4)	51.3	207	1.7 (1.03–3.70)	69.5	0.002
Vitamin D (IU/day)	600	16.4 (2.1-107.7)	2.7	103	26.5 (3.0-79.5)	4.4	0.000
p25-75 25th-75th percentile, RDA recommended dietary allowance, RYGB Roux-en-Y gastric bypass. Thus, the P values were obtained from the independent two-sampleT-test or Mann-Whitney test to indicate statistical significance for compares diet + supplement adequacy in RYGB vs diet adequacy in control group. Differ significantly at *P < 0.05.
.

Micronutrient nutritional status

The CG had significantly higher ferritin concentrations and hematocrit than RYGB-G. Despite the fact that the CG had a higher sun exposure, the RYGB-G had a higher plasma level of 25-OH vitamin D (Table 4).

Table 4

Biochemical variables, vitamins levels and sun exposure
Parameter^a	RYGB	Controls	P value*
Glucose (mg/dL)	90.0(84.5–96.0)	94.0 (89.0-96.5)	0.287
Insulin (mIU/mL)	7.1(4.6–9.6)	9.7 (5.7–14.8)	0.064
HbA1c (%)	5.5(5.4–5.9)	5.4 (5.2–5.9)	0.418
Hemoglobin (g/dL)	11.9 ± 1.7	13.1 ± 1.2	0.058
Hematocrit (%)	36.3 ± 3.9	39.3 ± 3.2	0.041
MCV (fL)	84.4 ± 10.2	90.9 ± 4.6	0.052
CHCM	32.8 ± 1.4	33.1 ± 1.0	0.447
Ferritin (ng/mL)	18.3(5.2–51.9)	76.8 (18.2-146.6)	0.039
Calcium (mg/dL)	9.4(9.3–9.6)	9.1(8.9–9.5)	0.125
Phosphorous (mg/dL)	4.2 ± 0.4	3.8 ± 0.5	0.081
Plasma zinc (mg/dL)	79.3(73.2–86.0)	80.7(77.6–83.0)	0.960
Vitamin B12 (pg/mL)	326.0 (253.0-603.0)	312.0 (210.5- 428.0)	0.153
25-OH vitamin D (ng/mL)	18.7 ± 4.3	15.0 ± 4.1	0.033
PTH (pg/mL)	50.5(33.2–78.6)	45.1(33.7–50.9)	0.650
TSH (uUI/ml)	2.5(1.3-3.0)	2.4 (1.4–3.5)	0.614
UUN in 24 hours (g/24 hrs)	9.7(7.9–11.8)	8.3(7.2–14.7)	0.614
Total sun exposure score	4.0 (1.0–7.0)	9.0 (7.0-17.5)	0.002
RYGB Roux-en-Y gastric bypass, HbA1c glycated hemoglobin, MCV mean corpuscular volume, PTH parathyroid hormone, UUN urine urea nitrogen.
^a Values are expressed as mean ± SD or median (25th-75th percentile).
Thus, the P values were obtained from the independent two-sampleT-test or Mann-Whitney test to indicate statistical significance for between-group differences. Differ significantly between groups at *P < 0.05.

Body composition

The BC analysis showed that the RYGB-G had a greater amount of FFM, a higher FFM% and a greater amount of FFM adjusted for FM than the CG.

Additionally, the CG had a higher FM% and a higher percentage of trunk fat mass compared to the RYGB-G (Table 5).

Table 5

Body composition
Parameter^a	RYGB	Controls	P value*
FFM (kg)	42.3 ± 4.9	38.4 ± 4.5	0.049
FM (kg)	25.7 ± 5.5	28.9 ± 7.4	0.213
FFM/FM (kg)	1.72 ± 0.43	1.39 ± 0.30	0.033
FFM (%)	60.7 ± 5.1	56.1 ± 5.1	0.027
FM (%)	36.4 ± 5.2	41.1 ± 5.3	0.029
FM trunk (%)	36.5 ± 7.5	44.1 ± 6.0	0.009
FFM-UL (kg)	4.30 ± 0.45	4.17 ± 0.58	0.537
FFM-LL (kg)	14.2 ± 2.2	13.5 ± 1.9	0.409
AFFM (kg)	18.5 ± 2.6	17.7 ± 2.3	0.415
AFFM/height² (kg/m²)	7.31 (7.16–7.63)	7.09 (6.71–7.52)	0.223
RYGB Roux-en-Y gastric bypass, FFM non-bone fat free mass, FM fat mass, FFM% percent fat-free mass, FM% percent fat mass, FFM-UL fat-free mass upper limbs, FFM-LL fat-free mass lower limbs, AFFM appendicular fat-free mass.
^a Values are expressed as mean ± SD or median (25th-75th percentile).
Thus, the P values were obtained from the independent two-sampleT-test or Mann-Whitney test to indicate statistical significance for between-group differences. Differ significantly between groups at *P < 0.05.

Muscle strength and physical performance

There were no statistically significant differences between the groups for HGS or in the 5-STS and STS-30s physical performance tests (Fig. 1a, b and c).

This study shows that a group of women who underwent a long term RYGB (BMI 27.5 ± 3.4 kg/m²), with stable weight, regular use of micronutrients supplementation and without significant weight regain, in a follow-up of 6.7 ± 2.8 years, had a higher FFM, FFM%, FFM/FM ratio and lower FM% compared to a CG matched by age, BMI, skin phototype and level of physical activity, without differences in HGS or physical performance tests.

Although during the first 6 to 12 months after BS there is a significant reduction in FFM [3,8,9], most of the studies that have been developed in patients more than one year after surgery [10–13], are consistent and show that patients do not have a massive FFM loss, but rather a weight reduction with a “physiological change in the body composition” in which the patients reach FM and FFM values similar to the non-operated controls [10–16]. Indeed, a systematic review and meta-analysis found that bariatric surgeries, especially RYGB, might be effective for a decrease in FM and maintenance of FFM in patients with extreme obesity in over 1 year [17]. Notably, in our study we found a higher FFM% and a lower FM% in the RYGB-G vs CG. In a similar way to our study, Heshka et al found that in patients with RYGB five years after surgery, an interesting pattern of increased FFM and decreased skeletal muscle compared to the CG, due to the fact that the patients with RYGB had higher mass intra-abdominal organs [16]. Also, obesity produces alterations in the body fluids distribution secondary to excess of adiposity: people with obesity have a high extracellular water/intracellular water ratio (ECW/ICW) compared to lean individuals [40–44]. This expansion of the ECW does not seem to be totally corrected after significant weight reductions even up to 9 years after BS, which could be another factor that helps to explain the higher FFM in the RYGB-G [45,46].

In our study, even though the RYGB-G had significantly higher FFM and higher plasma concentrations of 25-OH vitamin D, we did not find differences in HGS or physical performance tests when compared to CG. There are few studies that evaluate muscle strength and functionality after BS, and most have been carried out during the first postoperative year. Most of these studies report a decrease in absolute muscle strength, with preservation of muscle strength relative to BMI or ASMM [25,47,48]. A review indicates that physical performance improves after BS, but it is not possible to conclude whether this improvement is the result of surgery-induced changes in BC or an indirect result of an increase in the level of physical activity and other factors [27]. The biomechanical changes induced by the reduction of weight after surgery and a lower infiltration of muscle fat translates in the long term into an improvement in muscle quality that is expressed with the maintenance of strength and physical performance in physiological values and similar to those of the CG [47,49]. On the contrary, Cole et al found a persistent decrease in FFM and HGS at 9 years after RYGB [46], but included only 5 patients who never reached a post-operative BMI lower than 30 kg/m² and also had weight regain at the expense of FM, which would translate into sarcopenic obesity, a condition that is associated with greater loss of functionality [50,51].

The magnitude of changes in BC and muscle functionality after BS weight loss are influenced also by nutritional factors such as protein and micronutrient intake, which may have deficit states even before BS, as we have previously described [12,21,52]. Notably the RYGB-G had a healthier diet and reaching the RDA for the micronutrients studied through the use of supplementation (except phosphorus). Despite this, in the RYGB-G, several patients had micronutrients deficiencies, as we have described in other studies [53,54]. These findings confirm the importance of the permanent use of micronutrient supplements in bariatric patients since their importance on the proper functioning of the neuro-muscular unit [26].

Both groups had a similar protein intake, which is within the range suggested by the latest American clinical practice guidelines [55]. Despite this, the 24-hour urinary urea nitrogen in both groups was in the range of mild catabolism and the nitrogen balance was negative, without a negative impact on the strength and physical performance tests in the groups. These data suggest that this group of patients may require a higher protein intake of around 86–93 g/day on average (1.2–1.3 g/kg/day) to reach a neutral nitrogen balance.

Although both groups had low concentrations of 25-OH vitamin D, its values were significantly higher in the RYGB-G, even though the CG had a significantly higher sun exposure. This could be explained by the vitamin D supplementation used by the RYGB-G that allowed them to achieve the RDA. 25-OH vitamin D deficiency is common in Santiago, Chile, because its southern location [56,57].

Our study has some limitations. The age range goes from 40 to 60 years, but it was done to avoid the effect of aging on changes in BC and because this is the age range where the largest number of bariatric surgeries are performed. Additionally, in the older population it was more difficult to find healthy controls. Also, we only included women, because it is the main group submitted to BS; it is possible that changes in BC may present differently in men, however in studies where men have been included, no significant differences were found between the groups. The cross-sectional nature of the study and the sample size do not allow us to generalize or find causality; however, monitoring for more than 6 years in large cohorts of bariatric patients is problematic and challenging since several study groups have shown that adherence to controls decreases over time.

Our study also has strengths. The postoperative follow-up of our patients was more than six years and only patients without significant weight regain and with micronutrient supplementation were included, which allowed us to study the changes in BC, muscle strength and functionality that occur with successful BS in the long term. We evaluate several factors that can affect FFM%. We use DEXA as the research reference method to evaluate the FFM, and we use HGS, 5-STS and STS-30s tests to study upper and lower limbs simultaneously which allow us to obtain objective values of BC, muscle strength, physical performance and extrapolate the level of functionality and independence.

Women between 40–60 years with a follow-up of 6.7 ± 2.8 years after RYGB, with stable weight, regular use of micronutrients and without weight regain, had a higher FFM, FFM%, FFM/FM ratio and lower FM% compared to a control group matched by age, BMI, skin phototype and level of physical activity.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Conflict of Interest

The authors declare that they have no conflict of interest.

Funding statement

This study was funded by ACHINUMET (Asociación Chilena de Nutrición Clínica, Obesidad y Metabolismo). ACHINUMET was not involved in study design, data analysis, interpretation of results or writing of the manuscript.

Author Contribution

A.S.: Conceptualization; methodology; investigation, writing – original draft; visualization; supervision; project administration; funding acquisition. K.B: Formal analysis; investigation; data curation; writing - review& editing; supervision. Inostroza J: Validation, methodology; investigation; data curation. G. C.: investigation, writing - review& editing. Sambra V: investigation; writing - review& editing. J. C. : Validation; investigation, resources. P. R.: Conceptualization; methodology; investigation; formal analysis; data curation; writing - review& editing; visualization; funding acquisition. All authors reviewed the manuscript.

Data Availability

The data that support the findings of this study are not openly available due to reasons of sensitivity and are available from the corresponding author upon reasonable request.

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Are there any differences between women with long term gastric bypasses and non-operated matched controls in body composition, muscular strength and physical performance?

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Abstract

Introduction:

Methods

Results

Conclusion

Figures

Key Points

Introduction

Material and Methods

Patients

Measurements

Anthropometry and body composition

Handgrip strength dynamometry

Sit-to-stand test in 5 repetitions (5-STS) and for 30 seconds (STS-30s)

Level of physical activity, skin phototype and sun exposure

Dietary Intake Evaluation

Hematological and biochemical evaluation

Assessment of vitamins, minerals and hormones

Statistics

Results

General

Energy, macronutrient and micronutrient intake

Micronutrient nutritional status

Body composition

Muscle strength and physical performance

Discussion

Conclusion

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Ethical Approval

Conflict of Interest

Funding statement

Author Contribution

Data Availability

References

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