Review on Weight Loss Interventions that Can Prevent Muscle Mass Loss in Sarcopenic Obesity

Min-jeong Park; Young-Woo Lim; Eunjoo Kim; Park, Min-jeong; Lim, Young-Woo; Kim, Eunjoo

doi:10.13048/jkm.24005

JKM > Volume 45(1); 2024 > Article

Park, Lim, and Kim: Review on Weight Loss Interventions that Can Prevent Muscle Mass Loss in Sarcopenic Obesity

Original Article

The Journal of Korean Medicine 2024; 45(1): 79-98.

Published online: March 1, 2024

DOI: https://doi.org/10.13048/jkm.24005

Review on Weight Loss Interventions that Can Prevent Muscle Mass Loss in Sarcopenic Obesity

Min-jeong Park¹

, Young-Woo Lim¹^{, 2}

, Eunjoo Kim¹^{, 2}^{, *}

¹Nubebe Obesity Research Institute

²Nubebe Korean Medical Clinic Bundang Center

Correspondence to: Eunjoo Kim, Nubebe Obesity Research Institute, 7F, 130, Seochojungang-ro, Seocho-gu, Seoul, Republic of Korea, Tel: +82-70-5148-7650, Fax: +82-2-566-2252, E-mail: boggil82@gmail.com

Received November 24, 2023 Accepted February 16, 2024

Abstract

Objectives

The objective of this study was to review clinical studies conducted over the last ten years that investigated weight or fat loss interventions that can preserve muscle or fat-free mass in Sarcopenic obesity

Methods

PubMed, Embase, Cochrane Central Register of Controlled Trials (CENTRAL), Research Information Sharing Service (RISS) and Korea Studies Information Service (KISS) were searched for Randomized clinical trials that had investigated all-type of interventions on the management of sarcopenic obesity from October 2013 to September 2023.

Results

A total of 14 studies met all the inclusion criteria. Interventions that increase muscle mass while reducing body fat at the same time included resistance training (including using elastic bands) and whole-body electromyostimulation(WB-EMS) in exercise intervention and Hypocaloric high-protein diet in nutritional intervention, exercise and nutritional combined intervention, and combination intervention of electrical acupuncture and amino acid supplementation. Among them, the most positive method of changing the body composition in sarcopenic obesity was the electric acupuncture and amino acid supplements.

Conclusion

Varying diagnostic criteria and management interventions for sarcopenic obesity in the included studies made it hard to maintain homogeneity across the studies. Well-defined criteria for diagnostic sarcopenic obesity should be considered. In addition, since all of the interventions examined did not show sufficient clinical effectiveness, follow-up studies are needed to confirm effective interventions for sarcopenic obesity patients in the future.

Keywords: Sarcopenic obesity, Resistance training, Nutrition, Electrical acupuncture

Fig. 1

Flow chart of the literature search process

Table 1

Characteristics of Studies Included in the Review

Author, Year, country	Mean age	Sex	Intervention category	Intervention	Sample size	Intervention duration	Adherence	Outcomes
Balachandran, 2014¹²⁾ USA	Power circuit(HSC): 71.6 ± 7.8 Hypertrophy (SH): 71 ± 8.2	HSC: F (100%) SH: F (88%)	Exercise (2 arms)	HSC: 3 sets of 10–12 repetitions(no recovery between sets) 2x/wk for 40–45 min/session SH: 3 sets of 10–12 repetitions(1–2min recovery between sets) 70% of 1RM 2x/wk for 55–60 min/session	N=21 1. 11 2. 10	15 weeks	1. 81% 2. 85%	SPPB, lower body and upper body power and strength, IADL, RPE, PBF, SMI, HG
Gadelha, 2016¹³⁾ Brazil	67.0 ± 5.2	F (100%)	Exercise (2 arms)	Resistance training: 3 sets of each machine(1min recovery) 3x/wk 60% of 1RM for 4wks, 70% of 1RM for 4wks, 80% of 1RM for 16wks Control: maintain their usual activities	N=133 1. 69 2. 64	24 weeks	100%	Weight, BMI, Body Fat, TFFM, relative TFFM, AFFM, knee extensor isokinetic peak torque
Chen, 2017¹⁴⁾ Taiwan	68.8 ± 3.3	F (80%)	Exercise (4 arms)	Aerobic training: 2x/wk for 60 min/session Resistance training: 60%–70% of 1RM 2x/wk for 60min/session Combination training: 1x/wk Aerobic + resistance Control: prohibited from engaging in any exercises	N=93 1. 22 2. 24 3. 25 4. 22	8 weeks	64.5%	Weight, SMM, ASM, BFM, BMI, PBF, VFA, HG, Maximum Back Extensor Strength, Maximum Knee Extensor Muscle Strength, IGF-1
Park, 2017¹⁵⁾ Korea	74.1 ± 6.1	F(100%)	Exercise (2arms)	Aerobic & resistance group: 5x/wk for 50–80/min, resistance exercise(elastic band exercise) 3x/wk + Aerobic(various walking activities) 5x/wk Control: health and family life education twice	N=50 1. 25 2. 25	24weeks	100%	PBF, ASM, WC, HG, 30-s chair stand-up test, sit-and-reach test, Maximum walking speed, IPAQ, CIMT, CLD, PSV, EDV
Huang, 2017¹⁶⁾ Taiwan	69.2 ± 5.0	F(100%)	Exercise (2arms)	Elastic resistance: progressive (20%) elastic band resistance training program, 3x/wk for 55min Control: a 40-min course about home exercise for sarcopenic obesity	N=35 1. 18 2. 17	12 weeks	100%	BW, BMI, SMI, PBF, Laboratory data, Total BMD, T-score, Z-score
Liao, 2018¹⁷⁾ Taiwan	67.3 ± 5.2	F(100%)	Exercise (2arms)	Elastic resistance: moderate-intensity 3x/wk for 55 min Control: no intervention	N=56 1. 33 2. 23	12 weeks	89.2%	PBF, TSM, ALM, LMI, AMI, SMI, HG, maximal isometric quadriceps strength, Physical capacity
Muscariello, 2016¹⁸⁾ Italy	66.7 ± 4.9	F(100%)	Nutrition (2arms)	Normal protein intake hypocaloric diet: 0.8 g/kg DBW/day of proteins High protein intake hypocaloric diet: 1.2 g/kg DBW/day of proteins	N=104 1. 50 2. 54	12 weeks	N/A	MMI, BMI, WC, PFM, FMI, HG, IPAQ-SF
Sammarco, 2017¹⁹⁾ Italy	55.0 ± 9.6	F(100%)	Nutrition (2arms)	Hypocaloric high-protein diet: 1.2–1.4 g/kg body weight reference/day obtained with the addition of 15 g daily of protein supplement, basal metabolic rate – 10% according to calorimetry Hypocaloric + placebo: 0.8–1 g/kg body weight reference/day, basal metabolic rate – 10% according to calorimetry	N=18 1. 9 2. 9	16 weeks	100%	BMI, FM, FFM, HG, SPPB, REE
Yin, 2023²⁰⁾ China	68.13 ± 6.12	F(70%)	Nutrition (2arms)	Dietary behaviour change: A Moderate hypocaloric diet (12% reduction in calories from the estimated daily energy expenditure) + a dose of 1.2–1.5 g/kg body weight/day of protein intake+ BCTs(HAPA model) Control: regular health talks	N=60 1. 30 2. 30	15 weeks	83.3%	Feasibility and Acceptability of the intervention, BW, BFM, BMI, PBF, SMI, WC, HG, 6-m gait speed, SPPB, HAPA Nutrition Self efficacy Scale: DQI-I, Food diary MNA, SF-36
Kemmmler, 2016²¹⁾ Germany	77.0 ± 4.3	F (100%)	Exercise Nutrition Combined (3arms)	WB-EMS: 1x/wk for 20 min + vitamin-D 800 IU/day WB-EMS&Protein: WB-EMS + 40 g/day (21g whey protein) Control: Vitamin-D 800 IU/day	N=75 1. 25 2. 25 3. 25	26 weeks	89.3%	Sarcopenia Z-Score, SMI, HG, gait speed
Kemmmler, 2017²²⁾ Germany	77.4 ± 4.8	M (100%)	Exercise Nutrition Combined (3arms)	WB-EMS&Protein: 1or2 sets of 8 repetitions, 1.5x/wk for 20 min + Protein + Vitamin-D Protein: 1.7–1.8 g/kg day protein(whey protein) + Vitamin-D 800 IU/day Control: Vitamin-D 800 IU/day	N=100 1. 33 2. 33 3. 34	16 weeks	92%	Sarcopenia Z-Score, TBF, SMI, HG
Kim, 2016²³⁾ Japan	81.1 ± 4.6	F (100%)	Exercise Nutrition Combine (4arms)	Exercise + Nutrition Exercise: 2x/wk for 60 min Resistance + Aerobic Nutrition: EAA 30 g + Vitamin-D 20 μg + 540 g catechin Health education: once every 2wk, Total 6 times, only health education, no exercise or nutrition	N=139 1. 36 2. 35 3. 34 4. 34	12 weeks	98.6%	Muscle mass, BFM, PBF, SMI, HG, Peak isometric force, walking speed
Nubuco, 2019²⁴⁾ Brazil	69.1 ± 4.1	F(100%)	Exercise Nutrition combined (2arms)	Whey protein + RT: 35 g whey protein, resistance training: 3x/wk Placebo+ RT: mixed with non-caloric sugar-free drinks, resistance training: 3x/wk	N=26 1. 13 2. 13	16 weeks	100%	BW, height, WC, HP, ALST, lower LST, total LST, total BFM, PBF, TFM, 1RM tests, 10MW, RSP
Zhou, 2018²⁵⁾ China	69.5 ± 5.2	M(100%)	Electrical acupuncture (2arms)	Electrical acupuncture + Nutrition: electrical acupuncture using the LI14 and LI11 pair, and the ST31 and ST34 pair for 20 min with a frequency of 5 Hz, wave duration of 1 ms, and strength of 1.5 mA, every 3 days for 12 weeks. + EAAs orally twice per day (20 g in total) for 28 weeks Nutrition: EAAs orally twice per day (20 g in total) for 28 weeks	N=48 1. 23 2. 25	28weeks	100%	ASM/Height², PBF

RM: repetition maximum, SPPB: Short Physical Performance Battery, IADL: instrumental activities of daily living, RPE: ratings of perceived exertion, PBF: percentage of body fat, SMI: skeletal muscle index, HG: Hand grip, BMI: body mass index, TFFM: total fat free mass, AFFM: appendicular fat free mass, SMM: skeletal muscle mass, ASM: appendicular skeletal muscle, BFM: body fat mass, VFA: visceral fat area, IGF-1: insulin like growth factor-1, WC: waist circumference, IPAQ: international physical activity questionnaire CIMT: carotid intima-media thickness CLD: carotid artery luminal diameter, PSV: peak systolic flow velocity, EDV: end diastolic flow velocity, BMD: bone mineral density, TSM: total skeletal muscle mass, ALM: appendicular lean body mass, LMI: Lean body mass index, AMI: appendicular lean body mass index, MMI: muscle mass index, PFM: percentage of fat mass, FMI: fat mass index, IPAQ-SF: International Physical Activity Questionnaire–Short Form, DBW: desirable body weight, FM: fat mass, FFM: fat free mass, REE: resting energy expenditure, BCT: behavior change techniques, HAPA: health action process approach, DQI-I: Dietary Quality Index-International, MNA: Mini Nutritional Assessment, SF-36: 36-item short form health survey, WB-EMS: Whole-body electromyostimulation TBF: total body fat, EAA: essential amino acid, RT: resistance training, HP: hip circumference, ALST: appendicular lean soft tissue, LST: lean soft tissue, 10MW: 10m walk test, RSP: rising from sitting position test

Table 2

Diagnostic Criteria for Sarcopenic Obesity Used in the Included Studies

Author, year	Measurement of Body composition	Diagnostic criteria for sarcopenia				Diagnostic criteria for obesity
		Reference	Muscle mass		Other criteria	BMI (kg/m²)	PBF (%)
		Reference	Adjusted by weight (%)	Adjusted by height² (kg/m²)	Other criteria	BMI (kg/m²)	PBF (%)
Balachandran, 2014¹²⁾	BIA (single-frequency)	EWGSOP, 2010²⁶⁾		SMI M <10.76 kg/m² F <6.76 kg/m²		>30
Gadelha, 2016¹³⁾	DXA	Newman, 2003²⁷⁾			Lowest 20th percentile of residuals (obtained from linear regression of appendicular lean mass (kg) on height (meters) and fat mass (kg)) and the ratio (aLM/ht²) of aLM (kg) and height squared (m²)	≥30
Chen, 2017¹⁴⁾	BIA (multifrequency)	Chang, 2013²⁸⁾	ASM/weight M ≤32.5% F ≤25.7%			≥25
Park, 2017¹⁵⁾	BIA (multifrequency)	Lim, 2010²⁹⁾	ASM/weight F <25.1%			≥25
Huang, 2017¹⁶⁾	BIA during the screening (multifrequency) DXA during the trial	Janssen, 2002³⁰⁾	TSM/weight F <27.6%				>30
Liao, 2018¹⁷⁾	BIA (multifrequency)	Janssen, 2002³⁰⁾	TSM/weight F <27.6%				>30
Muscariello, 2016¹⁸⁾	BIA (single-frequency)	N/A		MMI F <7.3 kg/m²		≥30
Kemmmler, 2016²¹⁾	BIA during the screening (multifrequency) DXA during the trial	EWGSOP, 2010²⁶⁾		SMI F <5.75 kg/m²			>35
Kemmmler, 2017²²⁾	BIA (multifrequency)	FNIH, 2014³²⁾			ASMM/BMI M <0.789		>27
Kim, 2016²³⁾	DXA	N/A		SMMI F< 5.67 kg/m²			>32
Nubuco, 2019²⁴⁾	DXA	FNIH, 2014³²⁾			Appendicular lean soft tissue <15.02 kg		>35
Zhou, 2018²⁵⁾	BIA (Multifrequency)	ASWG, 2014³³⁾		ASM M ≤7.0 kg/m²			≥25
Sammarco, 2017¹⁹⁾	BIA (single-frequency)	N/A			Lean body mass was <90% of the subject’s ideal fat free mass		>34.8
Yin, 2023²⁰⁾	BIA (Multifrequency)	ASWG, 2019³¹⁾			Low handgrip strength M <28 kg, F <18 kg or low physical performance in the 5-time chair stand test of 12s	≥28

MI: body mass index, PBF: percentage of body fat, BIA: Bioelectrical Impedance Analysis, EWGSOP: European Working Group on Sarcopenia in Older people, SMI: skeletal muscle index, DXA: Dual Energy X-ray Absorptiometry, ASM: appendicular skeletal muscle, TSM: total skeletal muscle, MMI: muscle mass index, ASWG: Asian Working Group for Sarcopenia, FNIH: The Foundation for the National Institutes of Health, ASMM: appendicular skeletal muscle mass, SMMI: skeletal muscle mass index

Table 3

Absolute Muscle Mass or Fat-Free Mass and Body Fat Percentage Changes Following Interventions

Author, year	Interventions	Absolute muscle mass (kg)							PBF (%)

		(T)FFM			Other muscle mass parameters

		Baseline	After	Mean difference	Parameters	Baseline	After	Mean difference	Baseline	After	Mean Difference
Gadelha, 2016¹³⁾	RT	36.39±4.16		0.60±0.15^*†	AFFM	13.80±1.86		0.29±0.11^*†	39.85±6.27		−0.88±0.33

Chen, 2017¹⁴⁾	RT					22.9±4.0	23.0±4.1^†		39.7±5.6	38.7±6.4^†
	AT				SMM	20.0±3.3	20.2±3.2^†		40.0±4.4	39.0±4.6^†
	RT + AT					20.7±4.0	21.4±3.7^†		39.7±5.8	37.4±5.3^†

Park, 2017¹⁵⁾	RT + AT				ASM	14.1±1.8	14.5±1.9		41.0±3.6	39.0±3.9^*

Sammarco, 2017¹⁹⁾	LCD	47.7±3.34	48.0±2.83						55.4±4.46	53.2±4.8^*
Sammarco, 2017¹⁹⁾	LC-HPD	47.6±2.45	48.7±2.11^*						51.4±4.52	48.0±6.1^*

Nubuco, 2019²⁴⁾	Whey protein + RT				ALST	13.9±0.9	14.7±1.1^*†		40.9±4.1	39.7±4.1^*†
Nubuco, 2019²⁴⁾	RT					13.9±0.8	14.2±0.8^*		39.6±4.4	39.5±4.9^*

(T)FFM: (total) fat free mass, PBF: percentage of body fat, RT: resistance training, AFFM: appendicular fat free mass, AT: aerobic training, SMM: skeletal muscle mass, ASM: appendicular skeletal muscle, LCD: low caloric diet, LC-HPD: low caloric-high protein diet, ALST: appendicular lean soft tissue

* Significant difference from baseline value (P < 0.05)

† Significant difference from control or placebo (P <0.05)

Baseline and After Data presented as mean±standard deviation, Mean difference presented as mean±standard error

Table 4

Relative Muscle Mass or Fat-Free Mass and Body Fat Percentage Changes Following Interventions

Author, year	Intervention	Relative muscle mass								PUFF (%)

		Adjusted by height² (kg/m²)				Adjusted by weight (%)

		Index	Baseline	After	Mean difference	Index	Baseline	After	Mean Difference	Baseline	After	Mean difference
Balachandran, 2014¹²⁾	HSC	SMI	6.5±0.66	6.6±0.59						45.2±4.7	44.5±4.5
Balachandran, 2014¹²⁾	SH	SMI	6.7±0.45	6.8±0.42						43.8±6.5	43.4±5.9

Gadelha, 2016¹³⁾	RT	Relative TFFM			0.27±0.07^*^†							−0.88±0.33

Chen, 2017¹⁴⁾	RT						24.1±2.4	24.3±2.6^†		39.7±5.6	38.7±6.4^†
	AT					ASM	23.0±2.0	23.4±2.1^†		40.0±4.4	39.0±4.6^†
	RT+AT						23.7±2.7	24.4±2.4^†		39.7±5.8	37.4±5.3^†

Author, year	Intervention	Relative muscle mass								PBF(%)

		Adjusted by BMI (kg/(kg/m²))

		Index	Baseline		After			Mean difference		Baseline	After	Mean difference
Huang, 2017¹⁶⁾	ER					SMM	22.37±2.14	22.47±2.45		41.66±7.65	37.68±5.36^*

Liao, 2018¹⁷⁾	ER	AMI	6.09±0.83	6.37±0.76	0.33^† (0.13, 0.52)	SMI	29.94±2.80	30.15±3.16	0.28^† (−0.50, 1.06)	41.65±4.02	40.89±3.77	−2.17^† (−4.13, 0.21) ^†

Yin, 2023²⁰⁾	DBC	SMI	7.31±0.16	7.23±0.19		SMM	33.31±0.65	33.02±0.79		39.35±1.09	39.83±1.25^*

Kemmmler 2016²¹⁾	WB-EMS	SMI	5.67 (5.50, 5.83)		0.14 (0.08, 0.21)^*					37.3 (35.6, 39.0)		−0.34 (−0.78, 0.10)
Kemmmler 2016²¹⁾	WB-EMS +P	SMI	5.66 (5.48, 5.83)		0.11 (0.04, 0.19)^*					37.5 (36.2, 38.7)		−0.52 (−0.98, 0.06)

Kim, 2016²³⁾	E+N	SMI			1.1±0.5					38.1±4.3		−4.0±0.9
	E				0.1±0.7					37.0±4.1		−3.9±0.8
	N				0.6±0.6					37.8±3.3		−3.0±0.7
	HE				1.2±0.8					38.5±4.9		−3.0±0.7

Zhou, 2018²⁵⁾	EA+AA	AMI	6.04±0.50	6.19±0.52^*						33.17±2.66	27.30±1.96^*
Zhou, 2018²⁵⁾	AA	AMI	5.94±0.49	5.96±0.48						31.80±2.83	30.16±2.84^*

Kemmler, 2017²²⁾	WB-EMS +P	(ASMM/BMI)	0.709 (0.695, 0.734)					0.018 (0.011, 0.026)^*		31.6 (30.5, 32.9)		−2.05^* (−1.40, −2.68)
Kemmler, 2017²²⁾	P	(ASMM/BMI)	0.703 (0.681, 0.723)					0.008 (0.001, 0.015)^*		31.4 (30.4, 32.4)		−1.13^* (0.48, −1.78)

PBF: percentage of body fat, HSC: power circuit, SH: hypertrophy, SMI: skeletal muscle index, RT: resistance training, TFFM: total fat free mass, AT: aerobic training, ASM: appendicular skeletal muscle, ER: elastic band resistance exercise, SMM: skeletal muscle mass, DBC: dietary behavior change, WB-EMS: whole body electromyostimulation, P: protein, E: exercise, N:nutrition, HE: health education, EA: electrical acupuncture, AA: amino acid, AMI: appendicular muscle index, BMI: body mass index, ASMM: appendicular skeletal muscle mass

* Significant difference from baseline value (P < 0.05)

† Significant difference from control or placebo (P <0.05)

Baseline and After Data presented as mean±standard deviation or mean(95% CI), Mean difference presented as mean±standard error or mean(95% CI)

참고문헌

1. Cruz-Jentoft A. J., Sayer A. A.2019; Sarcopenia. Lancet. 393:2636–2646. https://doi.org/10.1016/S0140-6736(19)31138-9

2. Baek J. Y., Lee E., Jung H. W., Jang I. Y.2021; Geriatrics fact sheet in Korea. Ann Geriatr Med Res. 25:65–71. https://doi.org/10.4235/agmr.21.0063

3. Donini L. M., Busetto L., Bischoff S. C., Tommy C., Maria D. B., John A. B., Rocco B.2022; Definition and diagnostic criteria for sarcopenic obesity: ESPEN and EASO consensus statement. Obes Fact. 15:3. 321–335. https://doi.org/10.1159/000521241

4. Hong S. H., Choi K. M.2020; Sarcopenic Obesity, Insulin Resistance, and Their Implications in Cardiovascular and Metabolic Consequences. Int J Mol Sci. 21:2. 494 https://doi.org/10.3390/ijms21020494

5. Zhang X., Xie X., Dou Q., Liu C., Zhang W., Yang Y., Andy S. K.2019; Association of sarcopenic obesity with the risk of all-cause mortality among adult over a broad range of different settings: a updated meta-analysis. BMC Geriatr. 19:1. 183 https://doi.org/10.1186/s12877-019-1195-y

6. Chaoran L., Pui Y. W., Yik L. C., Simon K. C., Wing H. C., Sheung W. L., Ronald M. Y.2023; Deciphering the “obesity pardox” in the elderly: A systematic review and meta-analysis of sarcopenic obesity. Obes Rev. 24:2. e13534 https://doi.org/10.1111/obr.13534

7. Goisser S., Kemmler W., Porzel S., Volkert D., Sieber C. C., Bollheimer L. C., Freiberger E.(2015) Sarcopenic obesity and complex interventions with nutrition and exercise incommunity-dwelling older persons–a narrative review. Clin Interv Aging. 10:1267 https://doi.org/10.2147/CIA.S82454

8. Poggiogalle E., Migliaccio S., Lenzi A., Donini L.2014; Treatment of body composition changes in obese and overweight older adults: insight into the phenotype of sarcopenic obesity. Endocrine. 47:3. 699–716. https://doi.org/10.1007/s12020-014-0315-x

9. Hit-contreras F. H., Bueno-Notivol J., Martínez-Amat A., Cruz-Díaz D., Hernadez A. V., Pérez-López F. R.2018; Effect of exercise alone or combined with dietary supplements on anthropometric and physical performance measures in community-dwelling elderly people with sarcopenic obesity: a meta-analysis of randomized controlled trials. Maturitas. 116:24–35. https://doi.org/10.1016/j.maturitas.2018.07.007

10. Eglseer D., Traxler M., Schoufour J. D., Weijs P. J., Voortman T., Boirie Y., Bouer S.; SO-NUT Consortium. 2023; Nutritional and exercise interventions in individuals with sarcopenic obesity around retirement age: a systematic review and meta-analysis. Nutr Rev. 81:9. 1077–1090. https://doi.org/10.1093/nutrit/nuad007

11. Bosy W. A., Muller M. J.2014; Measuring the impact of weight cycling on body composition: a methodological challenge. Curr Opin Clin Nutr Metab Care. 17:396–400. https://doi.org/10.1097/MCO.0000000000000092

12. Balachandran A., Krawczyk S. N., Potiaumpai M., Signorile J. F.2014; High-speed circuit training vs hypertrophy training to improve physical function in sarcopenic obese adults: a randomized controlled trial. Exp Gerontol. 60:64–71. https://doi.org/10.1016/j.exger.2014.09.016

13. Gadelha A. B., Paiva F. M., Gauche R., de Oliveira R. J., Lima R. M.2016; Effects of resistance training on sarcopenic obesity index in older women: a randomized controlled trial. Arch Gerontol Geriatr. 65:168–173. https://doi.org/10.1016/j.archger.2016.03.017

14. Chen H. T., Chung Y. C., Chen Y. J., Ho S. Y., Wu H. J.2017; Effects of different types of exercise on body composition, muscle strength, and IGF-1 in the elderly with sarcopenic obesity. J. Am. Geriatr. Soc. 65:4. 827832 https://doi.org/10.1111/jgs.14722

15. Park J., Kwon Y., Park H.2017; Effects of 24-week aerobic and resistance training on carotid artery intima-media thickness and flow velocity in elderly women with sarcopenic obesity. J. Atheroscler. Thromb. 24:11. 1117–1124. https://doi.org/10.5551/jat.39065

16. Huang S. W., Ku J. W., Lin L. F., Liao C. D., Chou L. C., Liou T. H.2017; Body composition influenced by progressive elastic band resistance exercise of sarcopenic obesity elderly women: a pilot randomized controlled trial. European Journal of Physical and Rehabilitation Medicine. 53:4. 556–563. https://doi.org/10.23736/S1973-9087.17.04443-4

17. Liao C. D., Tsauo J. Y., Lin L. F., Huang S. W., Ku J. W., Chou L. C., Liou T. H.2017; Effects of elastic resistance exercise on body composition and physical capacity in older women with sarcopenic obesity: a CONSORT-compliant prospective randomized controlled trial. Medicine. 96:23 https://doi.org/10.1097/MD.0000000000007115

18. Muscariello E., Nasti G., Siervo M., Di Maro M., Lapi D., D’Addio G., Colantuoni A.2016; Dietary protein intake in sarcopenic obese older women.(ORIGINAL RESEARCH). Clin. Interv. Aging. 11:133 https://doi.org/10.2147/CIA.S96017

19. Sammarco R., Marra M., Di Guglielmo M., Naccarato M., Contaldo F., Poggiogalle E., Pasanisi F.2017; Evaluation of hypocaloric diet with protein supplementation in middle-aged sarcopenic obese women: a pilot study. Obes. Facts. 10:3. 160–167. https://doi.org/10.1159/000468153

20. Yin Y. H., Liu J. Y., Välimäki M.2023; Dietary behaviour change intervention for managing sarcopenic obesity among community-dwelling older people: a pilot randomised controlled trial. BMC Geriatrics. 23:597 https://doi.org/10.1186/s12877-023-04327-w

21. Kemmler W., Teschler M., Weissenfels A., Bebenek M., Stengel S., Kohl M., Engelke K.2016; Whole-body electromyostimulation to fight sarcopenic obesity in community-dwelling older women at risk. Results of the randomized controlled FORMOsA-sarcopenic obesity study. Osteoporos. Int. 27:11. 3261–3270. https://doi.org/10.1007/s00198-016-3662-z

22. Kemmler W., Weissenfels A., Teschler M., Willert S., Bebenek M., Shojaa M., von Stengel S.2017; Whole-body electromyostimulation and protein supplementation favorably affect sarcopenic obesity in community-dwelling older men at risk: the randomized controlled FranSO study. (ORIGINAL RESEARCH) (Report). Clin Interv Aging. 12:1503 https://doi.org/10.2147/CIA.S137987

23. Kim H., Kim M., Kojima N., Fujino K., Hosoi E., Kobayashi H., Yoshida H.2016; Exercise and nutritional supplementation on community-dwelling elderly Japanese women with sarcopenic obesity: a randomized controlled trial. J Am Med Dir Assoc. 17:11. 1011–1019. https://doi.org/10.1016/j.jamda.2016.06.016

24. Nabuco H. C., Tomeleri C. M., Fernandes R. R., Junior P. S., Cavalcante E. F., Cunha P. M., Barbosa D. S.2019; Effect of whey protein supplementation combined with resistance training on body composition, muscular strength, functional capacity, and plasma-metabolism biomarkers in older women with sarcopenic obesity: a randomized, double-blind, placebo-controlled trial. Clinical Nutrition ESPEN. 32:88–95. https://doi.org/10.1016/j.clnesp.2019.04.007

25. Zhou X., Xing B., He G., Lyu X., Zeng Y.2018; The effects of electrical acupuncture and essential amino acid supplementation on sarcopenic obesity in male older adults: a randomized control study. Obes. Facts. 11:4. 327–334. https://doi.org/10.1159/000491797

26. Cruz-Jentoft A. J., Baeyens J. P., Bauer J. M., Boirie Y., Cederholm T., Landi F., Zamboni M.; European Working Group on Sarcopenia in Older People. 2010; Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing. 39:412–423. https://doi.org/10.1093/ageing/afq034

27. Newman A. B., Kupelian V., Visser M., Simonsick E., Goodpaster B., Nevitt M., Harris T. B.; Health ABC Study Inverstigators. 2003; Sarcopenia: alternative definitions and associations with lower extremity function. Journal of the American Geriatrics Society. 51:1602–1609. https://doi.org/10.1046/j.1532-5415.2003.51534.x

28. Chung J. Y., Kang H. T., Lee D. C., Lee H. R., Lee Y. J.2013; Body composition and its association with cardiometabolic risk factors in the elderly: A focus on sarcopenic obesity. Arch Gerontol Geriatr. 56:270–278. https://doi.org/10.1016/j.archger.2012.09.007

29. Lim S., Kim J. H., Yonn J. W., kang S. M., Choi S. H., Park Y. J., Jang H. C.2010; Sarcopenic obesity: Prevalence and association with metabolic syndrome in the Korean longitudinal study on health and aging(klosha). Diabetes Care. 33:1652–1654. https://doi.org/10.2337/dc10-0107

30. Janssen I., Heymsfield S. B., Ross R.2002; Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc. 50:889–896. https://doi.org/10.1046/j.1532-5415.2002.50216.x

31. Chen L. K., Woo J., Assantachai P., Auyeung T. W., Chou M. Y., Iijima K., Arai H.2020; Asian Working Group for Sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J Am Med Dir Assoc. 21:300–307.e2. https://doi.org/10.1016/j.jamda.2019.12.012

32. Studenski S. A., Peters K. W., Alley D. E., Cawthon P. M., McLean R. R., Harris T. B., Vassileva M. T.2014; The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci. 69:547–558. https://doi.org/10.1093/gerona/glu010

33. Chen L. K., Liu L. K., Woo J., Assantachai P., Auyeung T. W., Bahyah K. S., Arai H.2014; Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc. 15:95–101. https://doi.org/10.1016/j.jamda.2013.11.025

34. Ling C. H., de Craen A. J., Slagboom P. E., Gunn D. A., Stokkel M. P., Westendorp R. G., Maier A. B.2011; Accuracy of direct segmental multi-frequency bioimpedance analysis in the assessment of total body and segmental body composition in middle-aged adult population. Clin Nutr. 30:610–615. https://doi.org/10.1016/j.clnu.2011.04.001

35. Ji Yeon Baek J. Y., Jung H. W., Kim K. M., Kim M., Park Y. C., Lee K. P., Lim J. Y.2023; Korean Working Group on Sarcopenia Guideline. Expert Consensus on Sarcopenia Screening and Diagnosis by the Korean Society of Sarcopenia, the Korean Society for Bone and Mineral Research, and the Korean Geriatrics Society. Ann Geriatr Med Res. 27:1. 9–21. https://doi.org/10.4235/agmr.23.0009

36. Kim K. K., Haam J. H., Kim B. T., Kim E. M., Park J. H., Rhee S. Y., Lee C. B.; Committee of Clinical Parctice guidelines, Korean Society for the Study of Obestiy (KSSO). 2023; Evaluation and Treatment of Obesity and Its Comorbidities: 2022 Update of Clinical Practice Guidelines for Obesity by the Korean Society for the Study of Obesity. J Obes Metab Syndr. 32:1. 1–24. https://doi.org/10.7570/jomes23016

37. Ryan D. H., Yockey S. R.2017; Weight loss and improvement in comorbidity: differences at 5%, 10%, 15%, and over. Curr Obes Rep. 6:187–194. https://doi.org/10.1007/s13679-017-0262-y

38. Garber C. E., Blissmer B., Deschenes M. R., Franklin B. A., Lamonte M. J., Lee I. M., Swain D. P.; American College of Sports Medicine. 2011; American college of sports medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: Guidance for prescribing exercise. Med Sci Sports Exerc. 43:1334–1359. https://doi.org/10.1249/MSS.0b013e318213fefb

39. Schulte J. N., Yarasheski K. E.2001; Effects of resistance training on the rate of muscle protein synthesis in frail elderly people. Int J Sport Nutr Exerc Metab. 11:Suppl. S111–118. https://doi.org/10.1123/ijsnem.11.s1.s111

40. Fry A. C.2004; The role of resistance exercise intensity on muscle fibre adaptations. Sports Med. 34:663–79. https://doi.org/10.2165/00007256-200434100-00004

41. Hunter G. R., Wetztein C. J., Mclafferty C. L., Zuckerman P. A., Landers K. A., Bamman M. M.2001; High-resistance versus variable-resistance training in older adults. Med Sci Sports Exerc. 33:1759–1764. https://doi.org/10.1097/00005768-200110000-00022

42. Guang J. W., Hossein A. M., Wei B. Z.2010; Meridian studies in China: a systematic review. J Acupunct Meridian Stud. 3:1–9. https://doi.org/10.1016/S2005-2901(10)60001-5

43. Cho J. K., Kang H. S., Yoon J. H.2013; Increased Dietary intake of proteins for the prevention and Treatment of sarcopenic obesity in the Elderly. Korean J obes. 22:77–82. https://doi.org/10.7570/kjo.2013.22.2.77

44. Morton R. W., Murphy K. T., McKellar S. R., Schoenfeld B. J., Henselmans M., Helms E., Phillips S. M.2017; A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults. Br J Sports Med. 52:6. 376–384. https://doi.org/10.1136/bjsports-2017-097608

45. Sandberg M., Lundeberg T., Lindberg L. G., Gerdle B.2003; Effects of acupuncture on skin and muscle blood flow in healthy subjects. Eur J Appl Physiol. 90:114–119. https://doi.org/10.1007/s00421-003-0825-3

46. Shinbara H., Okubo M., Kimura K., Mizunuma K., Sumiya E.2015; Contributions of nitric oxide and prostaglandins to the local increase in muscle blood flow following manual acupuncture in rats. Acupunct Med. 33:65–71. https://doi.org/10.1136/acupmed-2014-010634

47. Zamboni M., Mazzali G., Zoico E., Harris T. B., Meigs J. B., Di Francesco V., Bosello O.2005; Health consequences of obesity in the elderly: a review of four unresolved questions. Int J Obes (Lond). 29:9. 1011–1029. https://doi.org/10.1038/sj.ijo.0803005