Influence of sex on functional capacity, and muscle strength and fine motor skills of upper limbs in patients with multiple sclerosis

Abstract

Introduction

Multiple Sclerosis (MS) is a neurodegenerative disease characterized by damage to the myelin sheath that covers neurons, and which shows differences between men and women in terms of susceptibility and disease progression related in turn to functional ability and quality of life.

Objectives

To know the differences based on gender, assessing the functional capacity, muscle strength and fine motor skills of the upper extremities of patients with MS.

Material and methods

A quantitativede, scriptive, cross-sectional study was conducted with a sample of 51 MS patients, that were assessed for functional capacity (DASH scale); static and dynamic balance (Berg scale), perceived balance (ABC); strenght (Jamar and dynamometer); and fine motor skills (NHPT).

Results

The sample consisted of 15 men and 36 women, with a mean age of 47 ± 12 años. No differences were observed in functional capacity DASH (p = 0.616). In addition, men showed greater pincer strength (p < 0.001) and greater triceps strength (p < 0.05) in both arms. Regarding fine motor skills, it was better in women in both the dominant and non-dominant hands (p < 0.05).

Conclusions

Despite not observing functional differences by sex, there are differences in the parameters of pincer and triceps strength, which is higher in men; and in manual dexterity of both hands, which is better in women.

Resumen

Introducción

La esclerosis múltiple (EM) es una enfermedad neurodegenerativa caracterizada por daños en la vaina de mielina que recubre las neuronas, y que muestra diferencias entre hombres y mujeres en cuanto a la susceptibilidad y progresión de la enfermedad relacionada a su vez con la capacidad funcional y calidad de vida.

Objetivos

Conocerlas diferencias en función del género, valorando la capacidad funcional, y fuerza muscular y motricidad fina de las extremidades superiores de pacientes con EM.

Material y métodos

Estudio cuantitativo, descriptivo de carácter transversal que contó con una muestra poblacional de 51 pacientes diagnosticados de EM, a los que se valoró la capacidad funcional (escala DASH), el equilibrio estático, dinámico (escala Berg) y percibido (escala ABC); fuerza (Jamar y dinamómetro); y la motricidad fina de las manos (NHPT).

Resultados

La muestra consistió en 15 hombres y 36 mujeres, con una edad media de 47 ± 12 años. no se observan diferencias en la capacidad funcional DASH (p = .616), Además, se observó en los hombres mayor fuerza en pinza (p < .001) y mayor fuerza en tríceps (p < .05), de ambos brazos. En cuanto a la motricidad fina, esta fue mejor en las mujeres tanto en la mano dominante como no dominante (p < .05).

Conclusiones

A pesar de no observarse diferencias funcionales por sexo, si existen diferencias en los parámetros de fuerza en pinza y fuerza en el tríceps, que es mayor en hombres; y en destreza manual de ambas manos, que es mejor en las mujeres.

Introduction

Multiple sclerosis (MS) is a neurodegenerative disease that causes progressive muscle atrophy¹. Anatomically, the disease manifests damage to the myelin sheath that covers neurons, which will have a drastic effect on axonal activity². This neuronal damage in the cortical area, primarily in the grey matter, is linked to the characteristic functional disability of the disease^3,4, which, in turn, has been related to balance and muscle strength in other diseases⁵. In this regard, loss of muscle mass and strength in MS patients has been mainly reported to affect the lower limbs⁶, implying that most of the physical exercise-based interventions were aimed at improving lower limb function^7,8. However, during the course of the disease, approximately three out of every four patients with MS develop upper limb dysfunction⁹ that may occur bilaterally. Consequently, a considerable number of these patients suffer adverse effects on important activities of daily living (ADLs) such as eating and toileting¹⁰, which has a devastating influence on their degree of dependency and quality of life¹¹.

Moreover and with respect to the upper extremities, proprioception and light touch or fine motor skills have a significant impact on functionality¹². It is estimated that 80% of patients exhibit sensory impairments and a large proportion of them experience problems with coordination and fine hand dexterity in the upper extremities, which also directly influences the performance of ADLs^13,14.

On the other hand, there is a clear preponderance of women who are affected by a variety of autoimmune diseases, such as systemic lupus erythematosus or rheumatoid arthritis. In this same sense, it should also be noted that the prevalence of MS is higher in women, with three women affected for every man, particularly adult women^15–17.

Additionally, there are gender-dependent differences in the development of lesions in the grey matter and white matter¹⁸ and in the progression of the disease¹⁹. In terms of progression, it has been shown that males are more likely to progress from relapsing remitting MS (RRMS) to secondary progressive MS (SPMS)^20,21. Moreover, it is worth noting that disease progression is linked to functional impairment, which, in turn, has a bearing on ADLs and, hence, on quality of life^22,23. However, being male has been correlated with better quality of life among MS patients²⁴. In this respect, other authors have demonstrated that women suffer a higher rate of flare-ups than men, with more relapses^25,26. Furthermore, females have been seen to exhibit greater fatigue and anxiety, and are also less able to walk²⁷.

Despite these findings, there are no studies in the scientific literature that evaluate differences in upper limb functionality in relation to sex. Therefore, given the importance of upper limb disability in ADLs and in view of the clinical differences in other functions, it is hypothesised that there are also differences between the sexes in terms of functional capacity, muscle strength, and fine motor skills of the upper limbs.

The objectives of this study are to determine possible differences in functional capacity, muscle strength, and fine motor skills of the upper limbs, as a function of the sex of patients with MS.

Material and methods

This is a quantitative, descriptive, cross-sectional study.

Study sample

The sample was obtained by contacting the MS associations of the Community of Valencia (ACVEM) and the Community of Murcia (AMDEM), who informed their members about the nature of the research. After a few months of recruitment, the following selection criteria were applied to the 67 people interested in participating in the study:

Inclusion criteria: Individuals over the age of 18 years diagnosed with MS at least 6 months prior to the study and treated with glatiramer acetate and interferon beta (common treatment for the disease).

Exclusion criteria: Physiological or pathological causes were applied, related to metabolic alterations that could affect predominantly functional activity, altering the results and thus keeping the study's objectives from being met. Therefore, pregnant or breastfeeding women; patients with tracheotomy, stoma, or short bowel syndrome; patients with dementia, alcohol, or drug abuse; patients who had suffered myocardial infarction, heart failure, cardiac arrhythmia, angina, or other cardiac condition; patients with renal problems with creatinine levels two times higher than normal; patients with elevated liver markers three times higher than normal or with chronic liver disease, and those with hyperthyroidism, with acromegaly, polycystic ovary syndrome, or MS patients included in other studies with experimental drugs or treatments were excluded.

After applying the inclusion and exclusion criteria, 51 patients diagnosed with MS were enrolled in the study. Each patient was then coded in order to maintain the anonymity and confidentiality of their data, and finally, they were referred to their corresponding associations for the stipulated measurements to be performed.

Statistical analysis

SPSS v.23 (IBM Corporation, Armonk, NY, USA) was used for all analyses. Descriptive mean (M) and standard deviation (SD) data were obtained. Qualitative variables were compared using chi-square. For quantitative variables, groups were tested for normality using the Shapiro-Wilk test, after which significant differences between males and females were analysed using the Student's t-test for independent samples in cases of normal data and the Mann-Whitney U test for non-normal data. To compare right and left, the Student's t-test for dependent samples or the Wilcoxon test was used, depending on whether the variables were normal or non-normal. The level of statistical significance was p < 0.05 in all cases.

Measurements

This section describes all the measurements that were performed under the same conditions and by the same researcher assigned at the beginning of the study. The questionnaires or scales were provided to the participants as hard copies:

Berg Balance Scale: This scale was used to measure dynamic and static balance; it consists of 14 items that are scored from 0–4 and added together for a total score ranging from 0−56. The higher the final score, the better the person’s balance²⁸.

Balance Confidence Scale (ABC): This scale quantifies how confident the patient feels that he/she will not lose their balance when carrying out ADLs. Scores range from 0−10. The higher the score, the better the perceived balance²⁹.

DASH Questionnaire: Used for global assessment of the upper extremity, developed jointly by the Institute for Work and Health and the American Academy of Orthopedic Surgeons (AAOS). It consists of 30 questions that are scored from 1−5. The final score ranges from 0–100; the higher the score, the greater the disability, and those who score more than 10 points are regarded as clinically significant variations³⁰.

Jamar: Used to gauge grip strength, it records the maximum strength achieved in each hand³¹.

Dynamometer: NedDFM/IBV (Instituto de Biomecánica de Valencia, Spain) makes it possible to determine the degree of weakness present in muscle groups in different planes of movement³².

9-Hole Peg Test (9-HPT): This is a test that assesses the fine dexterity of the upper extremity of both hands. The patient must be comfortably seated, place and remove the 9 pegs with one hand as quickly as possible, keeping time and repeating the test twice with each hand³³.

Ethical aspects

The study was conducted in accordance with the Declaration of Helsinki following protocol approval by the Human Research Committee of the Experimental Research Ethics Committee (procedure number: H1512345043343).

Likewise, all personal data obtained from the subjects participating in the trial will be processed in accordance with the provisions of Organic Law 3/2018 dated 5 December regarding Personal Data Protection, the European Directive on Data Privacy, and General Data Protection Regulation (GDPR) 679/2016, specifically with regard to consent. The data obtained in this trial will be used solely for the purpose of reaching scientific conclusions.

Results

Fifty-one patients who met the selection criteria were analysed, of whom 15 were male and 36 were female. The socio-demographic characteristics of the study sample are displayed in Table 1, in which no statistically significant differences can be distinguished between the group of men and women, in terms of ALS types and age.

Table 1.

Sociodemographic characteristics of the study sample (N total = 51).

	Global	Males	Femaless
	Count (%)	Count (%)	Count (%)	p		df
Relapsing-remitting MS	32 (63)	8 (25)	24 (75)	0.658	2.267^c	2
Secondary progressive MS	17 (33)	7 (41)	10 (52)
Primary progressive MS	2 (4)	0	2 (100)

	M ± SD	M ± SD	M ± SD	p	z	df
Age	47 ± 12	48 ± 12	46 ± 12	0.606	−0.516	50

SD: standard deviation; df: degrees of freedom; M: mean; p: statistical significance, z: z calculated for Mann-Whitney U (not normal data).

c

chi-square value.

Table 2 reports the mean values (± SD) of the variables analysed for the entire study sample (51 MS patients).

Table 2.

Mean values (±SD) of all the variables for the study sample: functional capacity (DASH, Berg, and ABC), muscle strength (Jamar and dynamometer tests), and fine motor skills (NHPT test).

	M ± SD
DASH	27.86 ± 21.7
Berg	46.4 ± 12.7
ABC	65.04 ± 28.4
Jamar R (kg)	23.1 ± 8.85
Jamar L (kg)	20.9 ± 7.98
Din BB-R (N)	7.23 ± 2.17
Din BB-L (N)	8.13 ± 2.54
Din TB-R (N)	6.1 ± 2.69
Din TB-L (N)	6.07 ± 2.51
NHPT Dom (s)	23.1 ± 13.5
NHPT No Dom (s)	24.1 ± 12.8

BB: biceps muscle; R: right; SD: standard deviation; Dyn: dynamometer test; Dom: dominant; L: left; M: mean; N: Newtons; No Dom: non-dominant; NHPT: Nine Hole Peg Test; kg: kilograms; s: seconds; TB: triceps muscle.

As for the variables analysed, Table 3 reveals that there were no statistically significant differences between male and female MS patients with respect to functional capacity on any of the three tests performed (DASH, Berg. and ABC).

Table 3.

Comparison of functional capacity between men and women (DASH, Berg, and ABC).

	Males(M ± SD)	Females(M ± SD)	P	z	df
DASH	29.2 ± 21.8	27.2 ± 22.1	0.6166	−0.5006	46
ABC	65.2 ± 25.9	65 ± 30.1	0.8063	−0.2452	48
BERG	47.2 ± 8.4	46 ± 14.2	0.5227	−0.6392	46

SD: standard deviation; df: degrees of freedom; M: mean; p: statistical significance, z: z calculated for Mann-Whitney U (non-normal data).

Nevertheless, for the variables related to muscle strength and fine motor skills, statistically significant differences can be noted between men and women (Table 4, Fig. 1). To be more specific, the parameters of grip strength in both hands (JAMAR R - JAMAR L and strength, as quantified with the triceps dynamometer in both arms (Din TB-R - Din TB-L), men displayed greater strength than women. As for fine motor skills, men were found to take the same amount of time to complete the NHPT test with the dominant and non-dominant hand; however, women were significantly faster than men in completing the test with both the dominant and non-dominant hand.

Table 4.

Comparison of muscle strength and fine motor skills variables in upper limbs between men and women.

	Males(M ± SD)	Females(M ± SD)	p	t/z	df
Jamar R (kg)	28.9 ± 7.6	19.9 ± 6.6	<0.001*	4.322^a	49
Jamar L (kg)	26.3 ± 9	18 ± 6.6	<0.001*	3.739^a	49
Din BB-R (N)	6.99 ± 1.5	7.28 ± 2.44	0.673	−0.425^a	48
Din BB-L (N)	8.54 ± 2.35	8.05 ± 2.7	0.529	0.634^a	49
Din TB-R (N)	7.57 ± 3.07	5.43 ± 2.54	0.011*	2.613^a	49
Din TB-L (N)	7.02 ± 2.9	5.63 ± 2.38	0.046*	2.340^a	49
NHPT Dom (s)	30.2 ± 10.1	22.5 ± 5.2	0.006*	−2.688^b	44
NHPT No Dom (s)	32.5 ± 11.2	25.7 ± 8.1	0.028*	−2.178^b	45

BB: biceps muscle; R: right; SD: standard deviation; Dyn: dynamometer test; Dom: dominant; df: degrees of freedom; L:left; kg: kilograms; M: mean; N: Newtons; No Dom: non-dominant; NHPT: Nine Hole Peg Test; p: statistical significance; s: seconds; t: estadístico t calculado; TB: triceps muscle; z: z calculated for Mann-Whitney U.

a

Student’s t-test for independent samples (normal data).

b

Mann-Whitney U test (not normal data).

*

Statistically significant differences p < 0.05.

Figure 1.

Comparison of muscle strength and fine motor skills variables in upper limbs between men and women. BB: bíceps muscle; R: right; Dyn: dynamometer test; Dom: dominant; L: left; NHPT: Nine Hole Peg Test; No Dom: non-dominant; TB: triceps muscle.

* Statistically significant differences p < 0.05.

Right/dominant and left/non-dominant hand strength and motor skills were also compared separately for males and females (Table 5, Fig. 2). Grip strength (JAMAR) displayed no statistically significant differences between the right and left hand for either sex. Triceps brachii strength (Din TB) also failed to present statistically significant differences between the right and left arm in either sex. However, statistically significant differences were found between the right and left arms in biceps strength (Din BB) for both males and females; in both cases, the left arm was stronger. As for fine motor skills (NHPT), there were only statistically significant differences between the dominant and non-dominant hand among females, in whom it took longer to complete the task when using the non-dominant hand.

Table 5.

Comparison of strength measures (JAMAR y Dinamómetro) and fine motor skills (NHPT) in right and left hands between men and women. Mean data ± standard deviation for both hands are presented.

	Males		Females
	R	L	R	L
JAMAR	28.9 ± 7.6	26.3 ± 9	19.9 ± 6.6	18 ± 6.6
	t(20) = 1.816; p = 0.084	t(48) = 1.798; p = 0.078
Din BB	6.99 ± 1.5	8.54 ± 2.35	7.28 ± 2.44	8.05 ± 2.7
	t(19) = −3.295; p = 0.004*	t(46) = −2.462; p = 0.018*
Din TB	7.57 ± 3.07	7.02 ± 2.9	5.43 ± 2.54	5.63 ± 2.38
	t(20) = .157; p = 0.877	t(47) = .049; p = 0.961

	Dom	No Dom	Dom	No Dom
NHPT	30.2 ± 10.1	32.5 ± 11.2	22.5 ± 5.2	25.7 ± 8.1
	t(17) = −.994; p = 0.334	z(37) = −2.028; p = 0.043*

Student’s test (t) for dependent samples was performed for normal variables and Wilcoxon’s test (z) for non-normal variables.

BB: biceps muscle; R: right; Dyn: dynamometer test; Dom: dominant; L:left; No Dom: non-dominant; NHPT: Nine Hole Peg Test; TB: triceps muscle.

*

Statistically significant differences p < 0.05.

Figure 2.

Comparison of muscle strength and fine motor skills variables between men and women in both hands. Din BB: biceps dynamometer test; Din TB: triceps dynamometer test; NHPT: Nine Hole Peg Test.

* Statistically significant differences p < 0.05.

Discussion

With the aim of contributing greater knowledge to the current literature on the existing differences between men and women with MS, which will allow, among other things, different therapeutic approaches to the disease to be considered based on sex, in the present study we compared the functional capacity, as well as muscle strength and fine motor skills of the upper extremities, between two populations of men and women with MS. With regard to functional capacity, and bearing in mind that most people with MS suffer upper limb dysfunction, such as tremor, coordination deficits, and muscle weakness,³⁴ no differences were detected between the sexes in our study, neither at the quantitative level, with the DASH and Berg questionnaire and scale, respectively, nor in the perception of balance assessed by means of the ABC scale.

The possibility of performing ADLs correlates with quality of life and, in turn, both are conditioned by functional capacity, especially by the strength of the upper extremities,¹¹ which is diminished by more than 50% in this population. With this premise, an attempt was made to assess the possible influence of sex in our study. After applying the Jamar and dynamometer tests, respectively, greater grip strength and greater triceps strength in both arms were observed in men, which is to be expected given the physical differences between both; nevertheless, it should be noted that no differences were observed between the left and right biceps muscles, which could indicate less atrophy in women in these muscles in particular.

In turn, Guclu-Gunduz et al. (2012) demonstrated that not only upper extremity strengthening, but also sensory hand training can contribute to upper extremity function in MS patients.¹⁴ In fact, there is a correlation between sensory and motor functions for the same limb.^35–37 In this regard, it is also noteworthy how MS patients had a 67% loss of fine motor movements and a 56% decrease in writing ability.³⁸ In fact, the most difficult movements for MS patients are those related to cutting their nails, using a hammer, peeling fruits and vegetables, buttoning, shuffling and dealing cards.³⁹ Therefore, given the relevance of these activities for the subjects in our study, we also attempted to determine possible differences in fine motor skills by gender; in this case, despite the fact that there are no functional differences between the sexes and that men display greater strength in the triceps, women exhibited better fine motor skills in both hands. In this sense, there is an earlier study that determined differences between healthy women and men when performing the test. Specifically, it was observed that women performed it faster with both hands, given that the healthy adult males completed the NHPT test in 19.0 ± 3.2 seconds with the right hand and in 20.6 ± 3.9 with the left hand, while women completed it in 17.9 ± 2.8 seconds with the right hand and 19.6 ± 3.4 with the left hand.⁴⁰ These differences, approximately 1 second per hand, do not appear to be significant, whereas in the MS patients in our study it is (with differences of approximately 7 seconds in the performance of the test for each hand). This is why the disease appear to increase the already existing differences between healthy men and women; since, in addition, our results coincide with those obtained in the only study we found of this nature, which also revealed that this manual function was statistically more impaired in men (80.7%) than in women (64.8%) with MS.⁴¹ Therefore, the results of our study in the NHPT test lead us to believe that perhaps the activity of the biceps muscle (which seems to be less atrophied in women) may be related precisely to fine motor skills in the hands.Finally, in an attempt to probe deeper into the analysis of the differences in these variables according to sex, our assessment also demonstrated that, regardless of the dominant hand, the strength of the biceps in the left arm is greater for both men and women; while the dominant hand only displays better fine motor skills than the non-dominant hand in women. These results could not be contrasted with others, given that to date, no published works of this type have been identified.

Our results, in addition to probing more deeply into the analysis of the clinical differences of the disease by sex, may also help in the therapeutic management of patients depending on whether they are male or female, trying to increase the strength of the triceps muscles especially in women and fine motor skills in men, while taking into account the differences observed within each sample (men or women).

Therefore, the conclusions of our study, responding to the proposed objectives, are that, despite failing to identify functional differences according to gender, differences do exsist between men and women in the parameters of grip strength of both hands (JAMAR D/I), strength in the TB of both arms (Din TB D/I), which is greater in men, and in manual dexterity of both hands (NHPT Dom/No Dom), which is better in women.

This means that these indicators should be taken into account in future studies in which changes in some of these variables are assessed by sex; for example, after some type of intervention. However, and despite the conclusions reached, the study has important limitations. Among these, it is perhaps worth mentioning that clinical parameters of the population related to the stages of the disease have not been taken into account, which would have been useful to establish the degree of involvement of the study population. Furthermore, factoring in the fact that the population was divided into males and females and women in order to reach the objectives set, it should be noted that the sample size is small. It is mainly because of these two aspects that, despite the interest of the results obtained, the study should be replicated with a larger population. Furthermore, when comparing by sex, it would be of interest to take the type of MS or age of the patients into account.

Funding

The authors received funding from the Fundación Universidad Católica de Valencia San Vicente Mártir (sponsorship code 2018-203-001), Spain.

Conflict of interest

The authors have no conflict of interests to declare.