Is Skin Thinning a Natural Consequence of Aging or a Result of Sarcopenia? A Case-Control Study

doi:10.21203/rs.3.rs-3990883/v1

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Is Skin Thinning a Natural Consequence of Aging or a Result of Sarcopenia? A Case-Control Study

https://doi.org/10.21203/rs.3.rs-3990883/v1

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Background: It is widely accepted that skin thickness decreases and fragility increases with aging. However, the relationship between skin thickness and sarcopenia, a common condition in the elderly associated with an increased risk of fragility, remains unknown.

Objective: We aimed to investigate the presence of skin thinning in sarcopenia patients and explore the relationship between age, sarcopenia, and skin thickness.

Methods: This case-control study included a total of 66 individuals (33 individuals with sarcopenia, 33 healthy controls) aged 40 to 80 years. In all patients, total skin (epidermal + dermal) thickness was measured using ultrasound (US) at the leg, hand, forearm, and upper arm.

Results: Skin thickness in all regions was significantly lower in patients with sarcopenia compared to controls (all p < 0.05). Controlling for potential confounders, including age, sex, and body mass index, revealed a significant relationship between sarcopenia and skin thickness.

Conclusion: Sarcopenia was found to be associated with skin thinning in all regions and BMI is positively correlated only with leg skin thickness. However, age and gender were not found to be associated with skin thickness.

Skin thickness

Skin fragility

Aging

Sarcopenia

Hand Grip Strength

Aging is a complex process influenced by a multitude of factors such as chronic inflammation, changes in metabolic pathways, and alterations in stress adaptation. It affects numerous organs and systems and serves as a risk factor for geriatric diseases.^{1, 2}

Sarcopenia is a multifactorial disease characterized by the progressive loss of muscle mass and function, which increases in prevalence with age. ³ Sarcopenia prevalence was reported to vary between 8% and 36% in individuals younger than 60 years and between 10% and 27% in individuals aged 60 or older, according to a meta-analysis.⁴ It has also been reported to reach 50% in individuals aged 80 and above.⁵ It is one of the most significant health issues in elderly adults and is associated with heightened frailty, increased risk of falls, morbidity and mortality.⁶

Aging is also linked to increased epidermal fragility, which is associated with an elevated risk of skin disorders. This epidermal fragility is believed to be related to the thinning of the epidermis.^{7, 8}

Despite the widespread belief that skin thickness decreases with age, research findings on this topic are contradictory and subject to ongoing debates ^8–14.

Environmental factors, climate, gender, skin phototypes, and ethnic background have been reported to influence skin thickness, but it has been indicated that the thinning of the skin, particularly in sun-protected areas with aging, cannot be solely attributed to environmental factors and the effects of sunlight exposure^{8, 13, 14}.

The conflicting results in the literature regarding the relationship between aging and skin thickness may stem from the lack of investigation into the presence of sarcopenia. The increasing prevalence of sarcopenia during the aging process could potentially lead to two distinct outcomes: skin thinning and the same mechanisms may be involved in both phenomena. Additionally, skin thinning might even be a consequence of sarcopenia. As far as we have been able to ascertain, we have not come across a study in the literature that explores the connection between sarcopenia and skin thickness.

Therefore, we investigated the hypothesis that "the reduction in skin thickness with aging is not a natural consequence of aging but rather a result of sarcopenia, and the risk factor for decreased skin thickness is sarcopenia, not aging." We aimed to explore the relationship between skin thickness measured using ultrasound (US) and sarcopenia, aging, gender, and BMI in individuals with and without sarcopenia among healthy adults.

Study population:

This cross-sectional study included a total of 66 individuals (33 individuals with sarcopenia, 33 healthy controls) aged 40 to 80 years, who presented to our Physical Medicine and Rehabilitation outpatient clinic, between February 2023 and September 2023. Individuals with any inflammatory rheumatic diseases, skin disorders, malignancies, neurological diseases, and those using corticosteroids were excluded from the study.

A control group similar to the sarcopenia group in terms of age, gender, BMI, and skin color was formed. A control was obtained for each sarcopenia case. Case and control groups were formed from the same area and wearing the same style in terms of exposure to sunlight, which could potentially be biased.

The diagnosis of sarcopenia was established based on the revised diagnostic criteria of the European Working Group on Sarcopenia in Older People (EWGSOP2)⁵ According to these criteria;

In women;

1) Hand Grip Strength (HGS) < 16N = > Presarcopenia,

2) Presarcopenia and Appendicular Skeletal Muscle Mass (ASMM) < 15kg = > Sarcopenia,

3) Sarcopenia and gait speed ≤ 0.8 m/s = > Severe Sarcopenia.

In men;

1) HGS < 27N = > Presarcopenia,

2) Presarcopenia and ASMM < 20 kg = > Sarcopenia,

3) Sarcopenia and gait speed ≤ 0.8 m/s = > Severe Sarcopenia.

HGS measurements were conducted using the Jamar hand dynamometer (Lafayette Instrument, Lafayette, IN, USA).Three measurements were taken from the dominant hand, and the average was calculated. Bioelectrical impedance analysis (BIA) was evaluated using the Tanita Body Composition Analyzer, model BC-418, (Tanita Corp, Tokyo, Japan). ASMM was calculated by summing the muscle mass of the right and left arm and leg.

Due to the lack of significant differences in skin thickness among sarcopenia, sarcopenia, and severe sarcopenia, as well as the inadequate number of participants in each group, patients with pre-sarcopenia, sarcopenia, and severe sarcopenia were all considered as part of the sarcopenia group.

Measurements:

The skin thickness measurements were conducted using a MyLab 70X US (Esaote, Genova, Italy). The measurements were taken for all patients while they were in a supine position. For proximal leg skin thickness. (Leg-ST), The leg extensor surface was measured from the midpoint between the proximal patella and the posterior superior iliac crest. For dorsal hand skin thickness (Hand-ST), measurements were taken from 3rd metatarsal midpoint on the back of the hand. For dorsal forearm skin thickness. (Forearm-ST), measurements were taken from the midpoint between the medial aspect of the elbow crease and the wrist crease on the dorsal forearm extensor surface. Lastly, for upper arm skin thickness. (Upper arm-ST), measurements were taken on the upper arm flexor surface, from the midpoint between the axilla and the elbow crease. Because the ultrasound used was not of high frequency, it was unable to distinguish between the epidermis- dermiş boundary in some patients. Therefore, total skin thickness was measured. The total thickness of the epidermis and dermis was measured using B-mode ultrasound by the same ultrasound specialist. (Fig. 1)

Statistical analysis:

A power analysis was conducted using G Power 3.1.¹⁵ As the closest available study, we determined approximate values for total skin thickness using upper arm flexion epidermis and dermis thickness data from the study by Wang S et al. ¹³ to be around 1.130 ± 0.147 and 0.99 ± 0.16. The effect size calculated according to the paired t-test for the difference between skin thicknesses (Cohen's d = 0.911) the margin of error of 0.05 (α = 0.05), and the power of 0.95, and the minimum number of samples planned to be included in the study, totaln = 66 ( 33 + 33) was calculated.

Statistical analyses were performed using the SPSS 21 program. Independent-sample T-tests were used for normally distributed data (as assessed by the Shapiro-Wilk test) for two independent groups' differences, and Mann-Whitney U tests were used for non-normally distributed data. The correlation between skin thickness, HGS, age, and Body Mass Index. (BMI) was examined. In the current study, multiple linear regression was employed to explore the potential impacts of BMI, gender, group, and age on skin thickness. A total of 66 participants were included in the analysis.

A Receiver Operating Characteristic (ROC) analysis was conducted to evaluate the performance of skin thickness predictive models in different body parts (Leg-ST, Hand-ST, Forearm-ST, Upper arm-ST) for diagnosing sarcopenia.

Ethics statement:

This study protocol was reviewed and approved by the ethics committee of Akdeniz University Faculty of Medicine( 2012-KAEK-20). It was conducted by the ethical standards of the 2000 Declaration of Helsinki. All subjects were informed about the study and their written informed consent was obtained.

We used the STROBE case-control checklist when writing our report.¹⁶

The mean age of a total of 66 patients. (46 females and 20 males)

was 62.94 ± 8.01. Demographic and clinical characteristics of the patients are given in Table 1. Skin thickness in all regions was significantly lower in patients with sarcopenia compared to controls. (all p < 0.05). The post-hoc Effect Sizes(ES) in our study ranged from moderate to high. The highest power and ES were observed for upper arm skin thickness (Cohen's d = 1.079, 99% power). (Table 1)

When comparing skin thickness between the control group, presarcopenia, sarcopenia, and severe sarcopenia groups, it was observed that the control group had significantly thicker skin in all regions compared to all sarcopenia groups (all p > 0.05). There was no significant difference in skin thickness among the sarcopenia groups (all p > 0.05).

Correlations between skin thickness, HGS, age, and BMI were examined for all patients. No correlation was found between age and skin thickness.(Leg-ST p = 0.894, Hand-ST p = 0.846, Forearm-ST p = 0.561, Upper arm-ST p = 0.810) Positive significant correlations were observed between HGS and skin thickness in all regions.(Leg-ST r = 0.434, Hand-ST r = 0.316, Forearm-ST r = 0.467, Upper arm-ST r = 0.507) Only a positive correlation was found between BMI and Leg-ST.(r = 0.320)

When considering all subjects, there were no significant differences between females and males in terms of age, BMI, and skin thickness. (p ≥ 0.05) Hand_ST

Multiple linear regression models: Leg-ST: The regression model was significant. F(4, 61) = 4.384, p = 0.004, and accounted for approximately 22,3% of the variance ( R² = 0.223). Hand-ST: The regression model was not significant. F(4,61) = 1.823, p = 0.136, and explained approximately 10.7% of the variance in the dependent variable ( R² = 0.107, adjusted R² = 0.048).Forearm-ST: The regression model was significant. F(4,61) = 4.490, p = 0.003 and accounted for approximately 22.7% of the variance ( R² = 0.227) Upper arm-ST: The regression model was significant Hand-ST F(4, 61) = 5.813, p < 0.001 and accounted for approximately 27.6% of the variance ( R² = 0.276). (Table 2)

The ROC curve analysis revealed that all the models were significant in their ability to distinguish sarcopenia. (Table 3)

In this study, where we investigated the hypothesis that skin thinning with aging is not a natural consequence of aging but rather a result of sarcopenia, our findings support our hypothesis. The results demonstrated that individuals with sarcopenia exhibit reduced skin thickness. Moreover, there was no correlation found between age and skin thickness, suggesting that the relationship between skin thinning and aging might be mediated by factors such as sarcopenia. Furthermore, the study suggests that skin thinning could serve as a potential parameter for diagnosing sarcopenia. Although no significant relationship was observed between gender and skin thickness, a connection was identified between BMI and leg skin thickness.

Skin thickness measurements can be conducted using various methods including histology, optical coherence tomography, laser scanning microscopy, and high-frequency ultrasound (HFUS). Among these methods, the US has been recommended as a cost-effective, non-invasive, and practical tool. ¹⁴ (14)¹⁴ For skin imaging, the use of High-Frequency Ultrasound (HFUS) in the frequency range of 20–75 MHz is recommended.¹⁴

The limitations of our study include the lack of utilization of high-frequency US due to resource constraints and the absence of an investigation into skin fragility. We used a 6 to 18 Hz B mode US. In our study, the number of patients with sarcopenia and severe sarcopenia was low. To avoid potential bias, individuals with skin conditions were excluded from this study, as it is the first study examining the relationship between sarcopenia and skin thickness in the literature. Skin thinning has been associated with an increased risk of skin fragility, which is characterized by an increased risk of skin disorders. The exclusion of individuals with skin conditions may have resulted in a lower number of sarcopenia and severe sarcopenia cases. In the realm of skin thickness research, there is a need for more comprehensive studies that also delve into examining skin fragility and elasticity. Furthermore, investigations focusing on sarcopenia in individuals with skin conditions, particularly in the elderly population, could offer valuable insights into this field.

Many studies in the literature investigating the relationship between aging and skin thickness have shown a decrease in epidermal thickness, particularly in elderly individuals.^{8, 9, 13, 17}. It has also been reported that the dermis thins by approximately 20% with aging and becomes more acellular and avascular.¹⁷ However, some studies contradict the belief that epidermal thickness changes with age. Some studies have even suggested that epidermal thickness remains unchanged with age or even thickens, especially in sun-exposed areas.¹⁸ Generally, it is widely accepted that both dermis and epidermis thin with aging.

While many studies in the literature demonstrate a thinning of skin thickness with aging, the presence of studies showing no change in skin thickness might stem from the omission of considering sarcopenia in those studies. In our study, the fact that sarcopenia affects skin thickness, but no relationship was found between age and skin thickness, supports our hypothesis.

A meta-analysis has suggested that the increased risk of skin diseases and the development of epidermal fragility with aging could be related to the reduction in epidermal thickness, impairment of the epidermal barrier function, and alterations in viscoelastic properties.⁸ Epidermal fragility, which is associated with an increased risk of skin diseases, is defined as susceptibility to trauma and skin injuries. Fragility, despite lacking a universally accepted precise definition, is a syndrome characterized by heightened vulnerability to stressors and reduced resistance due to an age-related progressive decline in various physiological systems.^19–21 Sarcopenia is a significant component of frailty.^{20, 21} Therefore, the thinning of the skin associated with skin fragility in older adults is likely to be related to sarcopenia as well. Indeed, our study results support this relationship.

While there are studies in the literature demonstrating that skin thickness is greater in males compared to females, there are also studies indicating no significant gender differences in skin thickness.^{8, 22} In our study, there was no relationship found between gender and skin thickness. However, when we compared females and males within the groups, we observed that skin thickness had decreased more in sarcopenic females compared to sarcopenic males. This finding suggests that sarcopenia might lead to a greater degree of skin thinning in females. Moreover, considering the higher prevalence of sarcopenia in women, the varying results in different studies regarding differences in skin thickness between men and women could also be attributed to the presence of sarcopenia and differences in the distribution of male and female participants among the study subjects. In this regard, our findings are not contradictory to the literature; in fact, they explain the diverse results observed in previous studies.

Skin thickness has generally been reported to be associated with BMI in the literature.⁸ In our study, we also found a positive correlation between BMI and leg skin thickness, which is consistent with the literature. Considering that BMI and ASMM are related parameters, and given that sarcopenia is characterized by a decrease in ASMM, there may be complex relationships between these findings as well.

The fact that our data consists of data such as age, gender, and BMI is positive in terms of generalizing our results. Although factors such as sun exposure and race are negative factors, we still predict that sarcopenia patients will have skin thinning compared to similar controls.

The results of our study demonstrate that sarcopenia is associated with a decrease in skin thickness across all examined body regions and that BMI is positively correlated only with leg skin thickness. However, age and gender were not found to be associated with skin thickness. These findings support the idea that sarcopenia could be a risk factor for skin thinning. Moreover, it suggests that skin thinning could potentially serve as an indicator of sarcopenia.

Based on our results, we recommend that the possibility of sarcopenia in older individuals should also be taken into consideration, both in future studies investigating skin thickness, fragility, and quality and in clinical practice.

Funding sources: None

Conflicts of Interest: None

Data availability statement: The data that support the findings of this study are available from the corresponding author upon reasonable request.

Ethics statement: Reviewed and approved by Akdeniz University Ethics Committee; approval (2012-KAEK-20) The patients in this manuscript have given written 24informed consent to publication of their case details.

Author Contribution

ST performed the researchSE designed the research studyST contributed essential reagents or toolsSE analysed the dataST and SE wrote the paperAll authors have read and approved the final manuscript.

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Table 1

Demographic and clinical data of sarcopenia and control groups
			Total (66)	Sarcopenia Group (33)	Control Group (33)	p	Cohen's d
Sex n (%)		Female	46 (70%)	24 (73%)	22 (67%)	0,789
Sex n (%)		Male	20 (30%)	9 (27%)	11 (33%)	0,789
Age (mean ± std)			62,94 ± 8,01	63,15 ± 9,69	62,73 ± 6,02	0,832_a
BMI (mean ± std)			27,23 ± 4,12	27 ± 3,9	27,46 ± 4,37	0,650_a
HGS (Median(Q1-Q3))			21,39 ± 7,44	16,15 ± 4,01	26,64 ± 6,29	< 0,001**_b
ASMM (Median(Q1-Q3))			20,17 ± 4,61	18,84 ± 3,97	21,49 ± 4,87	0,021*_b
Gait speed (Median(Q1-Q3))			0,81 ± 0,33	0,79 ± 0,43	0,83 ± 0,2	0,038*_b
Sarcopenia	Presarcopenia		20 (61)	20 (61)	0
n (%)	Sarcopenia		6 (18)	6 (18)	0
	Severe sarcopenia		7 (21)	7 (21)	0
Leg-ST (mean ± std)			1,83 ± 0,35	1,72 ± 0,37	1,94 ± 0,28	0,008*_a	0,671
Hand-ST (mean ± std)			1,13 ± 0,26	1,06 ± 0,29	1,21 ± 0,19	0,013*_a	0,612
Forearm-ST (mean ± std)			1,34 ± 0,28	1,22 ± 0,27	1,46 ± 0,24	< 0,001**_a	0,940
Upper arm-ST (mean ± std)			1,11 ± 0,28	0,98 ± 0,26	1,24 ± 0,22	< 0,001**_a	1,080

*: p<0,05

**: p<0,001

_a: Independent-sample T-test

_b: Mann-Whitney U test

HGS: Hand Grip Strength

ASMM: Appendicular Skeletal Muscle Mass

Leg-ST: Proximal leg skin thickness

Hand-ST: Dorsal hand skin thickness

Forearm-ST: Dorsal forearm skin thickness

Upper arm-ST: Upper arm skin thickness

Table 2

Linear Regression Analysis for Skin Thickness and Group, Age, Sex, and BMI
Model		B(SE)	p-value	95%CI
Leg-ST	Intercept	0,999(0,397)	0,014*	0,205 to 1,793
	Group	-0,204(0,078)	0,011*	-0,36 to -0,049
	Sex	0,116(0,085)	0,178	-0,054 to 0,287
	Age	0,002(0,005)	0,728	-0,008 to 0,012
	BMI	0,025(0,01)	0,012*	0,006 to 0,044
Leg-ST = 0,999–0,204Group (0 = control,1 = sarcopenia) + 0,025BMI
Hand-ST	Intercept	1,095(0,319)	0,001*	0,457 to 1,733
	Group	-0,151(0,063)	0,019*	-0,276 to -0,026
	Sex	0,063(0,069)	0,363	-0,074 to 0,2
	Age	-0,001(0,004)	0,859	-0,009 to 0,007
	BMI	0,003(0,008)	0,714	-0,013 to 0,018
Hand-ST = 1,095 − 0,151*Group (0 = control,1 = sarcopenia)
Forearm-ST	Intercept	1,14(0,316)	0,001*	0,508 to 1,773
	Group	-0,227(0,062)	0,001**	-0,351 to -0,102
	Sex	0,091(0,068)	0,189	-0,046 to 0,227
	Age	-0,001(0,004)	0,829	-0,009 to 0,007
	BMI	0,009(0,008)	0,236	-0,006 to 0,024
Forearm-ST = 1,14 − 0,227*Group (0 = control,1 = sarcopenia)
Upper arm-ST	Intercept	0,902(0,303)	0,004*	0,297 to 1,508
	Group	-0,259(0,059)	< 0,001**	-0,378 to -0,14
	Sex	0,083(0,065)	0,209	-0,048 to 0,213
	Age	0,005(0,004)	0,201	-0,003 to 0,012
	BMI	-0,003(0,007)	0,707	-0,017 to 0,012
Upper arm-ST = 0,902-0,259*Group (0 = control,1 = sarcopenia)

*: p < 0,05

**: p< 0,01

B: Unstandardized coefficient,

CI: Confidence interval,

SE: Standard Error.

Leg-ST: Proximal leg skin thickness

Hand-ST: Dorsal hand skin thickness

Forearm-ST: Dorsal forearm skin thickness

Upper arm-ST: Upper arm skin thickness

Table 3

ROC analysis for sarcopenia and skin thickness
	AUC (SE)	p	95%CI	Cut-Off	Sensiv.	Spesif.
Leg-ST	0,692(0,066)	0,007*	0,563 to 0,821	1,85	70%	64%
Hand-ST	0,706(0,065)	0,004*	0,578 to 0,833	1,15	64%	67%
Forearm-ST	0,745(0,06)	0,001*	0,628 to 0,863	1,35	73%	61%
Upper arm-ST	0,778(0,057)	0,000*	0,667 to 0,89	1,05	76%	64%

*: p<0,01

AUC: Area Under Curve

SE: Standard error

CI: Confidence interval

Leg-ST: Proximal leg skin thickness

Hand-ST: Dorsal hand skin thickness

Forearm-ST: Dorsal forearm skin thickness

Upper arm-ST: Upper arm skin thickness

No competing interests reported.

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Is Skin Thinning a Natural Consequence of Aging or a Result of Sarcopenia? A Case-Control Study

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