Effectiveness of massage and range of motion exercises on muscle strength and intensive care unit-acquired weakness in Iranian patients with COVID-19: a randomized parallel-controlled

Mohammad Ali Zakeri; Adnan Rashid Aziz; Elham Rahiminezhad; Mahlagha Dehghan

doi:10.4266/acc.2023.00416

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Original Article Nursing Effectiveness of massage and range of motion exercises on muscle strength and intensive care unit-acquired weakness in Iranian patients with COVID-19: a randomized parallel-controlled trial: Mohammad Ali Zakeri^1,2, Adnan Rashid Aziz³, Elham Rahiminezhad⁴, Mahlagha Dehghan^5,6; Acute and Critical Care 2024;39(1):78-90.
DOI: https://doi.org/10.4266/acc.2023.00416
Published online: December 13, 2023

¹Pistachio Safety Research Center, Rafsanjan University of Medical Sciences, Rafsanjan, Iran

²Clinical Research Development Unit, Ali-Ibn Abi-Talib Hospital, Rafsanjan University of Medical Sciences, Rafsanjan, Iran

³College of Nursing, Al-Kitab University, Kirkuk, Iraq

⁴Student Research Committee, Razi Faculty of Nursing and Midwifery, Kerman University of Medical Sciences, Kerman, Iran

⁵Nursing Research Center, Kerman University of Medical Sciences, Kerman, Iran

⁶Department of Critical Care, Faculty of Nursing and Midwifery, Kerman University of Medical Sciences, Kerman, Iran

Corresponding author: Mahlagha Dehghan Nursing Research Center, Kerman University of Medical Sciences, Kerman 7616913555, Iran Tel: +98-34-3132-5192, Fax: +98-76-1691-3555, Email: m_dehghan@kmu.ac.ir

• Received: February 20, 2023 • Revised: August 13, 2023 • Accepted: August 14, 2023

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Abstract
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
KEY MESSAGES
NOTES
Acknowledgments
SUPPLEMENTARY MATERIALS
REFERENCES

Abstract

Background
Muscle weakness is prevalent in intensive care patients. This study focused on comparing the effects of massage and range of motion (ROM) exercises on muscle strength and intensive care unit-acquired weakness (ICU-AW) among patients with coronavirus disease 2019 (COVID-19).
Methods
This study was a randomized clinical trial that recruited patients (n=45) with COVID-19 admitted to the ICU and divided them into three groups (ROM exercises, massage, and control). We evaluated muscle strength and ICU-AW in the arms and legs using a hand dynamometer. The Medical Research Council sum score was determined before and after the intervention.
Results
The study findings were that 0%, 20%, and 100% of the participants in the ROM exercises, massage, and control groups had ICU-AW on the 7th day of ICU admission. The ROM exercise group had greater muscle strength in the hands and legs than the masscage and control groups, and the massage group had greater muscle strength than the control group.
Conclusions
Massage and ROM exercises could improve muscle strength and reduce ICU-AW in COVID-19 patients admitted to the ICU.
Keywords: COVID-19; massage; muscle strength; muscle weakness; range of motion

INTRODUCTION

The epidemic of coronavirus disease 2019 (COVID-19) has become a great threat to human society in the last 2 years [1-5]. The COVID-19 disease has affected individuals of all communities worldwide [6-10]. Many COVID-19 patients require 1–2 weeks of admission and mechanical ventilation, and their ICU mortality rate was 26% [11]. Neuromuscular complications, mental health disorders and muscle atrophy are complications of long-term hospitalization of patients in the ICU [12-16].

Muscle weakness has been predicted to occur in many COVID-19 patients [17], which is more likely in COVID-19 patients where muscle weakness is a direct consequence of critical illness. Intensive care unit acquired weakness (ICU-AW) is a critical neuromuscular disorder in critical patients, the cause of which is only critical illness [14,18,19]. ICU-AW can cause problems in weaning patients from the ventilator, prolong stay in the ICU, and increase patient mortality [20]. One million patients worldwide may develop ICU-AW syndrome [21].

Some studies have pointed to the long-term effects of ICU-AW on ICU survivors. Wieske et al. [22] showed that ICU-AW was associated with increased post-ICU mortality and decreased physical function 6 months after ICU discharge. Some other systematic review studies have emphasized the use of interventions and methods, such as muscle stimulation to maintain patients' muscle strength, implement rehabilitation, and reduce ICU-AW. Therefore, it seems necessary to focus on strategies and interventions, such as electrical muscle stimulation, touch, massage, exercise, range of motion (ROM) exercises to reduce complications in COVID-19 patients [12,13,23-25]. Muscle stimulation has been considered in the prevention or improvement of ICU-AW. It has been found that an intensive physical therapy protocol, including postural changes, breathing and active exercises, can facilitate the initial recovery process of patients with ICU-AW [26].

ROM is a technique in an intervention program that includes active ROM, passive ROM, and assisted active ROM to reduce the effects of immobilization [27,28]. Wollersheim et al. [29] also found that the whole body vibration could stimulate muscle and improve muscle metabolism. Therefore, muscle stimulation and ROM may prevent or treat ICU-AW. However, neuromuscular electrical stimulation and personalized physiotherapy, including transfer training, balance exercises and deambulation did not improve muscle strength [30]. These findings highlight the need for further research in this regard. Massage also stimulates the muscles, which have been recognized as an essential part of health [31]. Massage can reduce muscle spasm, nervous excitability and sympathetic activity and increase blood circulation [32,33]. Swedish massage is a type of massage that uses stroking, exfoliation, vibration, and kneading movements to reduce sympathetic responses [34,35].

Existing studies have investigated the effects of vibration, ROM exercises, and electrical neuromuscular stimulation on the prevention and treatment of ICU-AW in non-COVID-19 patients and it have not considered COVID-19 patients [26,29,30]. The literature unequivocally supports the view that early intervention for ICU management of patients with acute respiratory distress syndrome (ARDS) secondary to COVID-19 needs to focus on reducing contributors to impaired long-term function, with direct attention paid to preventing or managing ICU-AW [36]. Many of COVID-19 patients have severe damages to one or more organs, suggesting that certain patients will need rehabilitation care in a follow-care and rehabilitation service [37]. However, the ICU-AW is higher in the COVID-19 patients who have to stay in the ICU compared to the non-COVID-19 patients [38].

Therefore, considering the importance and consequences of ICU-AW in patients admitted to ICU, which are also probable for COVID-19 patients [17], more effective interventions are required to clinically improve muscle strength and prevent ICU-AW in COVID-19 patients. The aim of the present study was to compare the effect of ROM exercises and massage on muscle strength and ICU-AW in COVID-19 patients.

MATERIALS AND METHODS

We followed the methods of Rahiminezhad et al. [39]. The study by Rahiminezhad et al. [39] was a randomized controlled trial that was conducted to investigate the effect of massage and ROM exercises on 90 patients admitted to the ICU in Kerman, Iran.

Study Design, Setting, and Ethical Consideration

This parallel single-blinded randomized controlled clinical trial study in ICU, which was conducted on hospitalized conscious patients with COVID-19. Afzalipour Hospital has two COVID-19 ICUs with 19 beds. This study was performed after the acquisition of the code of ethics of IR.KMU.REC.1398.558 and the code of clinical trial (IRCT20200203046358N1). The participants in this study were alert because individuals needed the cooperation of Medical Research Council (MRC) to measure. The patients underwent a high-flow device and simple oxygen mask, mask without inhalation of exhaled air or invasive mechanical ventilation. Our study began a few hours after the patient was admitted. Considering that the patients were fully conscious and they were stable, consent was obtained from the patients.

Sample Size and Sampling

The convenience sampling method was used to select the participants (June 2020 and ended in November 2020). The patients were divided into three groups by stratified block randomization (stratum: sex, age, and block size: 6). Groups were assigned labels A=massage, B=control, and C=ROM exercises. The randomization list was generated by using free online software (https://www.sealedenvelope.com/simple-randomiser/v1/lists). The third author (Elham Rahiminezhad) generated the randomization list and the first author (Mohammad Ali Zakeri) enrolled the participants and assigned them to the three groups. Massage and other forms of touch are not routine in our clinical setting. Male and female patients appear to have varying perceptions of massage and touch [40]. As a result of the possibility of confounding variables, we chose to include sex as a stratum in randomization in order to match the three groups on gender.

An infectious disease specialist initially diagnosed the COVID-19 based on symptoms (respiratory, gastrointestinal, neurological, etc.) and then with positive results of the tests [41-44]. The polymerase chain reaction test result was negative for some participants, but lung involvement was evident on computed tomography. We checked the patients' diagnosis in consultation with their infectious disease specialist.

Inclusion criteria were patients aged ≥18 years, non-invasive mechanically ventilated patients, and not mechanically ventilated patients), with Full Outline of Unresponsiveness (FOUR) score ≥14 [14], and patients in need of complete bed rest position and those who were predicted to be in ICU for at least 7 days. For this study, we needed patients to be awake and collaborative for assessing muscle strength, as our two assessment tools, the MRC and hand dynamometer, were not self-administered. Therefore, we did not need patients’ verbal communication; all we needed for them was to obey our commends while we assessed their muscle strength. As a result, one of the main criteria was FOUR scores ≥14, and patients on invasive mechanical ventilation who could collaborate with us were not excluded.

In addition, the criteria for admission to the ICU in our setting were based on the doctor's order and the patients' condition, such as diagnosis, the severity of the illness, coexisting disease, prognosis, availability of suitable treatment, and recent cardiopulmonary arrest. Power analysis calculations with G*Power software (power=80%, P=0.05, groups number=3) showed that 42 participants were needed (effect size of 0.5). A total of 62 eligible participants were evaluated, of which 51 eligible participants were divided into three groups.

Patients were followed for 7 days [39]. Six patients did not finish the study: three patients in the control group (two patients hospitalized for less than 7 days in the ICU and one patient with a decreased level of consciousness), two patients in the ROM group and one patient in the massage group (decline to participate) (Figure 1).

Data Collection Tools

In the present study, a demographic and background information questionnaire (Table 1) was used to assess the variables [45].

Hand-Held Dynamometer

A hand-held dynamometer was used to evaluate muscle strength. Target muscles was the upper extremities and lower extremities (Supplementary Material 1). To determine the reliability, the rater was trained how to work with the dynamometer under the supervision of a trained physiotherapist (an assistant professor, Department of Physical Therapy, Kerman University of Medical Sciences, Kerman, Iran, with more than 6 years of educational and clinical experiences) during three 2-hour sessions and performed the rating after approval. The rater evaluated 15 patients admitted to the ICU of Afzalipour Hospital twice (with an interval of 2 hours). A single person (ER) performed all evaluations in each of the measurements.

Medical Research Council Sum Score

This study used Medical Research Council sum score (MRC-SS) to assess muscle strength only in patients who were aware of the time and place and need cooperation [26]. A manual muscle test was used in MRC-SS to assess muscle strength in the upper and lower extremities. The strength score was obtained according to the force applied to the resistance: grade 0: no visible contraction, 1: vibration or low amount of contraction, 2: movement of the limb but not against gravity, 3: the movement against gravity, 4: the movement against gravity and resistance, 5: normal strength. Sixty is a perfect score, with scores less than 48 reflecting ICU-AW [23,46]. The score of 60 is given by the sum of the scores obtained for the four limbs. The physiotherapist trained the rater how to measure MRC during three 2-hour sessions. Then, the rater performed the rating after the approval of an expert.

Data Collection and Interventions

The researcher referred to the ICUs and completed the demographic and background information of the patients before the intervention. Using the MRC scale and a hand-held dynamometer, a single rater evaluated the muscle strengths of the upper and lower extremities on the first (before intervention) and 7th days (after intervention) of admission to the ICU at 8 pm. The intervention was performed in the ROM and massage groups once a day for 7 consecutive days. In all three groups (control, massage, and ROM), patients, who were transferred to the ward within the first 7 days of their hospitalization, were excluded from the study.

ROM exercise group

ROM exercises were performed once a day for 7 consecutive days. ROM exercises of the upper extremity and ROM exercises of the lower extremity were performed rhythmically in 10 repetitions [47]. ROM exercises lasted 30–60 minutes (Supplementary Material 2). ROM exercises were done at 3–7 pm. In case of intolerance, ROM exercises were postponed until the patient's condition became stable. The physiotherapist trained the second researcher and her colleague (ER and MD) how to do ROM exercises within three sessions (6 hours) and they started the intervention after their approval. The second researcher did ROM exercises for female participants while her colleague did ROM exercises for male participants.

Massage group

The upper/lower extremities, back, and chest were massaged with Swedish massage once a day for 7 consecutive days. An absorbent pad was placed to protect the patient's mattress from leaking oil. The patient was in a supine position, with the head at an angle of 30°–45°. Then the researcher used Swedish massage using olive oil (about 20 ml) to make the area slippery to massage [48]. The upper/lower extremities, back, chest were massaged continuously during 30–60 minutes. A physiotherapist trained the second researcher and her colleague (ER and MD) how to massage within three sessions (6 hours).

Control group

The patients in the control group have the same condition as patients in the intervention groups. The control group only received routine care (Supplementary Material 2).

Data Analysis

Descriptive statistic was used to describe the demographic characteristics and clinical history of patients using IBM SPSS 24 (IBM Corp.) [49-52]. Chi-square, Fisher's exact, one-way analysis of variance were used to evaluate the homogeneity study variables between the three groups. Paired t-test was used to compare muscle strength scores within the three groups at different times. In addition, first, analysis of variance test used to compare muscle strength scores between the three groups at different times. As there were significant different between three groups regarding Acute Physiology and Chronic Health Evaluation (APACHE) II score and in some cases the muscle strength scores were different before the intervention, analysis of covariance (ANCOVA) were used for controlling the covariates. Bonferroni post hoc test used for multiple comparison. Kruskal-Wallis test and Wilcoxon test were used for comparison of MRC score between and within the three groups.

RESULTS

The mean ages of the participants in the ROM exercise, the massage, and the control groups were 41.33±13.50, 52.33±14.22, and 52.0±16.30, respectively. All the groups were homogenous in terms of gender (P=0.924), length of stay in hospital before ICU admission (P=0.123), and history of addiction (P=0.481), ICU admission (P>0.99), and using renal replacement therapy (P=0.373). The mean scores of APACHE II in the ROM exercise, the massage, and the control groups were 5.73±2.15, 6.80±2.54, and 9.27±3.41, respectively (P=0.003). No significant difference in receiving respiratory support (comparison between invasive ventilation, simple mask, mask without inhalation of exhaled air, and high flow device) (P=0.371). In the massage (n=9) and control (n=8) groups, most patients used the high flow device. In the ROM exercises group (n=8), most patients used mask without inhalation of exhaled air (Table 1).

According to Table 2, the muscle strength in the right and left hands increased in ROM exercise and massage groups after the intervention while it significantly decreased in the control group (P<0.001). In addition, Bonferroni test showed that the muscle strengths in right- hand (right deltoid, right biceps, and right wrist) in the ROM exercise group were more than that of the massage group and control group, and the right- and left-hand muscle strengths in the massage group were more than that of the control group (P<0.05).

According to Table 3, the muscle strength in the right and left legs increased in ROM exercise and massage groups after the intervention while it significantly decreased in the control group (P<0.001). In addition, Bonferroni test showed that the muscle strengths of right rectus and left rectus and left tibialis in the ROM exercise group were more than that of the massage group and control group, and the right rectus, left rectus and left tibialis muscle strengths in the massage group were more than that of the control group (P<0.05). The muscle strengths in the right tibialis, right quadriceps and left quadriceps in the ROM exercise group were not more than that of the massage group, but were more than that of control group, and the right tibialis, right quadriceps and left quadriceps muscle strengths in the massage group were more than that of the control group (P<0.001).

The MRC score increased in ROM exercise and massage groups after the intervention while it significantly decreased in the control group (P<0.001) (Table 4). ΔMRC scores in the three groups were different. On the other hand, the ΔMRC score in the ROM exercise group was more than that of the massage group and control group (P<0.001), and the ΔMRC score in the massage group was more than that of the control group (P<0.001). Before the intervention, the frequency of ICU-AW in ROM exercise, massage, and control groups was 12 (80%), 11 (73.3%), and 10 (66.7%), respectively, but after the intervention, the frequency of ICU-AW in ROM exercise, massage, and control groups was 0 (0%), 3 (20%), and 15 (100%), respectively (Table 5).

DISCUSSION

Early mobilization improves the physical function of ICU patients, enhances their muscle strength, improves their ability to walk independently, reduces the incidence of ICU-AW, and does not increase in-hospital mortality [53]. This study aimed to compare the effects of ROM exercises and massage on muscle strength and ICU-AW in patients with COVID-19. The findings of the present study showed that the muscle strength in hands and legs of the ROM exercise group was higher than that of the other groups. Disser et al. [54] emphasized that rehabilitation programs with aerobic and resistance training reduced fatigue and increased strength of skeletal muscle, bone, joints, a connective tissue in patients with COVID-19.

Early mobilization and exercise are essential for the treatment of critically ill COVID-19 patients. The guideline of the international professional team has recommended early exercise for physiotherapy management for COVID-19 in the acute hospital setting [55]. Exercise training programs have improved musculoskeletal function in patients with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). A randomized controlled trial showed that a progressive aerobic and resistance training program for 6 weeks could be effective in improving musculoskeletal strength and function of the patients with SARS-CoV-2 [56].

Studies on non–COVID-19 patients have also recommended the effect of training programs on improving muscle strength and reducing ICU-AW. Verceles et al. [57] also found that a multimodal rehabilitation program improved strength, physical function, and mobilization in long-term acute care hospital patients with ICU-AW compared with conventional physiotherapy and it was more successful in weaning and discharging patients. The results of the above studies in both COVID-19 and non–COVID-19 patients confirm the results of the present study. The hypothesis proposed to describe the mechanisms of ROM exercises is that active and passive ROM exercises reactivate nerve connections and cause new connections and axonal regeneration [58].

Baroni et al. [59] showed that the use of full ROM could lead to muscle damage in addition to muscle recovery. Therefore, ROM-based interventions should be performed based on (1) specific goals such as increasing muscle strength, (2) type of training programs such as the number of sessions per week and the interval between sessions, and (3) cases of muscle damage. Therefore, ROM interventions should be considered in a long recovery period and in large muscle groups to improve muscle condition. According to the present study, MRC scores in the massage group were higher than that of the control group. It is believed that massage has many benefits for the body, including increased blood circulation, reduced muscle tension, and nerve irritability. Massage can increase muscle adaptation by mechanical pressure and thus increase joint movement, reduce passive stiffness and active stiffness [60]. Imtiyaz et al. [32] showed that massage was effective in preventing delayed onset muscle soreness and restoration of concentric strength. we used 30 to 60 minutes of massage. No specific time for massage has been established in studies [40], and it is unknown what the minimum effective dose of massage is; more studies are needed in this area.

However, Best et al. [61] indicated that massage was not effective in most studies evaluating its effectiveness in regenerating skeletal muscle after intense exercise, and that the use of massage to help muscle recovery or function required further studies. In our study, the effect of massage was less than that of ROM stimulation. However, we did not find any study to confirm this finding. In addition, a review of the literature did not reveal studies on the effects of massage on muscle recovery or function, and longitudinal studies are needed to perform massage therapy in clinical settings.

According to the results of the present study, the frequency of ICU-AW in the ROM exercise, the massage, and control groups was 0%, 20%, and 100% after the intervention, respectively. A review of the literature showed no study comparing the frequency of ICU-AW among COVID-19 patients in the ROM exercise, massage, and control groups. ROM may result in better traction tolerance due to acute reduction in muscle and tendon stiffness or nerve adaptation. Increasing the ROM can reduce muscle damage by considering small to medium changes immediately after stretching [62].

As the intense isometric contraction phase promotes Ib muscle afferent activity, the great performance of proprioceptive neuromuscular facilitation to improve ROM has been traditionally attributed to autogenic inhibition [63]. This activity may hyperpolarize the dendritic ends of spinal α-motoneurons of the stretched muscle, reduce or eliminate the impact of reflexive activity mediated by stretch-induced type Ia [64], and allow for further increases in ROM.

ICU-AW can reduce muscle protein synthesis, increase muscle catabolism, and decrease muscle mass by reducing force generation. ICU-AW may be associated with polyneuropathy and myopathy as well as axonal nerve degeneration and critical complications in patients [65,66]. Preliminary studies have shown significant musculoskeletal disorders in some critically ill patients due to the widespread involvement of COVID-19. Studies have reported various problems, such as rhabdomyolysis, myalgias, and myopathy [67-70]. These findings may indicate that given the severity of COVID-19 disease, ICU-AW, and significant dysfunction may be expected in COVID-19 patients who have stayed in ICUs for a long time. Bakhru et al. [71] showed physical dysfunction in survivors of critical illness. Thirty-five percent of the patients were readmitted to a hospital after discharge, and Short Physical Performance Battery (SPPB) scores had a significant correlation with mortality and readmission. In addition, the SPPB scores of ICU survivors were significantly lower than that of other populations with chronic illness. Paying attention to clinical ICU-AW outcomes can affect patients’ performance. Health managers can use knowledge about ICU-AW and muscle conditions to improve patients' conditions in hospitals and prevent unnecessary use of health care resources [72]. Therefore, health managers should consider the importance and improvement of the ICU-AW-prone patients admitted to ICUs. One effective measure is to recognize and implement effective interventions to reduce these complications.

COVID-19 can adversely affect a patient’s survival and quality of life even after ICU discharge and lead to dysfunction. Critically ill COVID-19 patients should receive special attention to prevent ICU-AW, and medical management and rehabilitation should be performed timely after observation of the clinical features of ICU-AW [17]. COVID-19 patients are in critical condition, and clinical examinations and interventions are hardly feasible due to disease-related problems and the high probability of infection in these patients. In response to this knowledge gap, the results of the present study emphasized rehabilitation measures for COVID-19 patients with interventions such as ROM exercises to improve muscle strength and reduce ICU-AW.

We needed patients to be awake and collaborative and to obey our commends while assessing their muscle strength. As a result, one of the main criteria was FOUR scores ≥14, and patients on invasive mechanical ventilation, who could collaborate with us, were not excluded. However, because of the inclusion criteria, our results are more applicable to critically ill patients without severe ARDS, which may be a very different population than a general COVID-19 ICU population with mechanically ventilated patients requiring prolonged ICU stay. Additionally, the mean SOFA score at inclusion was 2, indicating that the patients were critically ill but did not have severe organ dysfunction or multiple organ dysfunction. Another limitation is the lack of follow-up. We have observed and reported ROM exercises and massage only for a few days because the specific conditions of COVID-19 patients and our limited resources did not allow us for further investigation. As we had limited resources and we did not receive funding for conducting the study, we had to choose a large effect size (i.e., 0.5) for participants size estimation. Therefore, further studies should conduct with a larger participants size. We did not use a sweat gauge to determine how much sweat the patient produced as a result of these movements, which is presented as a limitation of the present study. While it was impossible to have physiotherapists permanently present in the critical area team during the study period, this limitation lays the foundations for further studies in which the team is implemented with the physiotherapist present to allow for assessments of the quality of movement and functional outcome. Muscle strength before intervention and APACHE score were different in most muscles. We used ANCOVA to control the effect and interaction of these variables. Despite controlling the effect of covariates, one should be careful in interpreting the results. Due to a lack of previously published studies on COVID-19, we could not compare our findings with other studies and generalize our hypotheses to other communities. Therefore, future research should be considered in this regard.

ROM exercises and massage could improve muscle strength and reduce ICU-AW in critically ill COVID-19 patients. Despite the limitations of the current study, running a ROM and massage program during an ICU stay can be a convenient, safe, feasible, and inexpensive treatment option. Health managers should recognize and implement effective interventions to reduce ICU-AW. Experimental studies and future research can help us understand the effectiveness of ROM exercises and massage in critically ill patients with ICU-AW. The authors will want to articulate that this study is exploratory and no conclusive evidence exists that massage or ROM can prevent ICU-AW.

KEY MESSAGES

▪ The muscular strength of coronavirus disease 2019 (COVID-19) patients can be increased by performing interventions such as range of motion exercises and massage.

▪ These interventions have had a positive effect on the rehabilitation of COVID-19 patients and the prevention of complications such as intensive care unit acquired weakness.

NOTES

CONFLICT OF INTEREST

No potential conflict of interest relevant to this article was reported.

FUNDING

None.

AUTHOR CONTRIBUTIONS

Conceptualization: ER, MD. Methodology: ER, MD. Formal analysis: MD. Data curation: ER. Project administration: ER, MD. Writing–original draft: MAZ. Writing–review & editing: MAZ, MD, ARA.

Acknowledgments

The authors would like to express their sincerest gratitude to the Kerman University of Medical Sciences for supporting the research.

SUPPLEMENTARY MATERIALS

Supplementary materials can be found via https://doi.org/10.4266/acc.2023.00416.

Supplementary Material 1.

Hand-Held Dynamometer (HHD) assessment

acc-2023-00416-Supplementary-1.pdf

Supplementary Material 2.

Data collection and interventions

acc-2023-00416-Supplementary-2.pdf

Figure 1.

The flow diagram of the study. ROM: range of motion; ICU: intensive care unit.

Table 1.

Comparison of demographic and clinical characteristics of participants in three groups of massage, ROM exercises, and control

Variable	ROM exercise group (n=15)	Massage group (n=15)	Control group (n=15)	Test statistic	P-value
Age (yr)	41±14	52±14	52±16	F=2.71	0.081
Glascow coma scale score	15	15	15	-	-
FOUR score	14.5±0.5	14.4±0.6	14.9±0.4	F=2.13	0.132
APACHE II score	5.7±2.2	6.8±2.5	9.3±3.4	F=6.50	0.003
SOFA score	1.7±1.3	2.3±1.3	2.1±1.5	F=0.64	0.533
Sex				χ²=0.18	0.924
Male	7 (46.7)	7 (46.7)	8 (53.3)
Female	8 (53.3)	8 (53.3)	7 (46.7)
Length of hospital stay before ICU admission (day)				Fisher’s exact test=8.19	0.123
1	8 (53.3)	11 (73.3)	5 (33.3)
2	6 (40.0)	3 (20.0)	9 (60.0)
3	1 (6.7)	1 (6.7)	-
4	-	-	1 (6.7)
History of addiction				χ²=1.45	0.481
Yes	3 (20.0)	5 (33.3)	6 (40.0)
No	12 (80.0)	10 (66.7)	9 (60.0)
History of ICU admission				Fisher’s exact test=1.86	>0.99
Yes	-	-	1 (6.7)
No	15 (100)	15 (100)	14 (93.3)
Use of renal replacement therapy				Fisher’s exact test=2.81	0.323
Yes	-	-	2 (13.3)
No	15 (100)	15 (100)	13 (86.7)
Respiratory support				Fisher’s exact test=6.30	0.371
Simple mask	-	-	1 (6.7)
Mask without inhalation of exhaled air	8 (53.3)	5 (33.3)	3 (20.0)
Invasive mechanical ventilation	2 (13.3)	1 (6.7)	3 (20.0)
High flow device	5 (33.3)	9 (60.0)	8 (53.3)

Values are presented as mean±standard deviation or number (%).

ROM: range of motion; FOUR: Full Outline of Unresponsiveness; APACHE: Acute Physiology and Chronic Health Evaluation; SOFA: Sequential Organ Failure Assessment; ICU: intensive care unit.

Table 2.

Comparison of muscle strength in right and left hand between the three groups

Muscle group		ROM exercise group (n=15, a)	Massage group (n=15, b)	Control group (n=15, c)	Between P-value	ANCOVA F (P-value), effect size post-hoc
Right deltoid	Pre	11.6±2.8	8.7±3.3	11.5±1.7	0.007
	Post	12.4±2.7	9.1±3.2	10.7±1.9	0.007
	Difference	0.8±0.3	0.4±0.3	–0.8±0.5		37.37 (<0.001)
	t	11.3	4.6	–5.8		0.65
	P-value	<0.001	<0.001	<0.001		a>b>c
Left deltoid	Pre	11.5±2.8	8.6±3.3	11.4±1.7	0.006
	Post	12.3±2.8	9.0±3.2	10.7±1.9	0.008
	Difference	0.8±0.2	0.5±0.4	–0.7±0.5		36.06 (<0.001)
	t	12.9	5	–5.5		0.64
	P-value	<0.001	<0.001	<0.001		a>b>c
Right wrist	Pre	6.7±1.1	5.6±1.4	6.4±1.1	0.040
	Post	7.4±1.1	6.0±1.3	6.1±1.1	0.003
	Difference	0.6±0.2	0.4±0.3	–0.3±0.3		33.19 (<0.001)
	t	10.0	5.2	–3.6		0.62
	P-value	<0.001	<0.001	0.003		a>b>c
Left wrist	Pre	6.7±1.1	5.5±1.4	6.4±1.0	0.020
	Post	7.3±1.1	5.9±1.3	6.0±1.0	0.003
	Difference	0.6±0.2	0.4±0.3	–0.4±0.3		29.21 (<0.001)
	t	9.2	4.6	–4.1		0.59
	P-value	<0.001	<0.001	0.001		a>b>c
Right biceps	Pre	12.9±2.3	9.5±3.3	11.6±2.1	0.003
	Post	13.6±2.2	9.8±3.3	11.0±2.1	0.001
	Difference	0.7±0.2	0.3±0.3	–0.6±0.4		48.34 (<0.001)
	t	11.8	4.5	–6.1		0.71
	P-value	<0.001	<0.001	<0.001		a>b>c
Left biceps	Pre	12.8±2.3	9.3±3.4	11.7±2.0	0.002
	Post	13.5±2.4	9.7±3.3	11.0±2.1	0.001
	Difference	0.7±0.3	0.4±0.3	–0.7±0.4		42.88 (<0.001)
	t	9.0	5.0	–6.3		0.68
	P-value	<0.001	<0.001	<0.001		a>b>c

Values are presented as mean±standard deviation. Control variables of ANCOVA: pre-muscle strength, Acute Physiology and Chronic Health Evaluation II score.

ROM: range of motion; ANCOVA: analysis of covariance.

Table 3.

Comparison of muscle strength in right and left leg between the three groups

Muscle group		ROM exercise group (n=15, a)	Massage group (n=15, b)	Control group (n=15, c)	Between P-value	ANCOVA F (P-value), effect size post-hoc
Right recuts	Pre	14.9±1.6	12.6±2.7	12.1±1.2	0.001
	Post	15.5±1.5	13.0±2.6	11.2±1.5	<0.001
	Difference	0.7±0.3	0.4±0.3	–0.9±0.5		57.71 (<0.001)
	t	7.67	5.42	–6.89		0.74
	P-value	<0.001	<0.001	<0.001		a>b>c
Left rectus	Pre	14.8±1.6	12.6±2.6	12.2±1.3	0.001
	Post	15.4±1.6	12.9±2.6	11.2±1.5	<0.001
	Difference	0.7±0.3	0.3±0.3	–1.0±0.4		63.77 (<0.001)
	t	8.11	4.63	–8.77		0.76
	P-value	<0.001	<0.001	<0.001		a>b>c
Right tibialis	Pre	7.0±1.5	6.47±1.2	7.1±1.6	0.036
	Post	7.6±1.5	6.7±1.4	6.5±1.8	0.11
	Difference	0.6±0.2	0.3±0.3	–0.6±0.4		48.94 (<0.001)
	t	11.44	4.79	–5.76		0.71
	P-value	<0.001	<0.001	<0.001		a>b>c
Left tibialis	Pre	7.0±1.5	6.2±1.3	7.0±1.5	0.28
	Post	7.6±1.4	6.6±1.4	6.4±1.8	0.07
	Difference	0.6±0.3	0.3±0.3	–0.6±0.5		29.96 (<0.001)
	t	9.60	4.07	–5.06		0.6
	P-value	<0.001	0.001	<0.001		a>b>c
Right quadriceps	Pre	15.2±1.5	13.4±2.9	12.3±1.9	0.003
	Post	15.8±1.5	13.6±2.9	11.4±2.07	<0.001
	Difference	0.6±0.3	0.3±0.2	–0.9±0.5		55.52 (<0.001)
	t	8.37	6.37	–7.14		0.74
	P-value	<0.001	<0.001	<0.001		a>b>c
Left quadriceps	Pre	15.2±1.5	13.4±2.8	12.4±1.8	0.003
	Post	15.8±1.6	13.6±3.0	11.5±2.0	<0.001
	Difference	0.6±0.2	0.2±0.3	–0.9±0.4		72.01 (<0.001)
	t	13.14	3.3	–9.13		0.78
	P-value	<0.001	0.005	<0.001		a>b>c

Values are presented as mean±standard deviation. Control variables of ANCOVA: pre-muscle strength, Acute Physiology and Chronic Health Evaluation II score.

ROM: range of motion; ANCOVA: analysis of covariance.

Table 4.

Comparison of MRC score between the three groups of ROM exercise, massage, and control

Variable	ROM exercise group	Massage group	Control group	Kruskal-Wallis test	P-value	Effect size
MRC score before intervention	45.9±4.0	46.8±4.8	50.0±3.3	5.86	0.053	1.77
MRC score after intervention	45.9±4.1	46.8±4.8	50.0±3.3	31.84	<0.001	6.86
Wilcoxon test (P-value)	–3.44 (0.001)	–3.42 (0.001)	–3.44 (0.001)	-	-	-
Mean difference	12.0±2.3	6.3±3.0	–8.5±2.4	37.62	<0.001	8.62

Values are presented as mean±standard deviation unless otherwise indicated.

MRC: Medical Research Council; ROM: range of motion.

Table 5.

Comparison of frequency of ICU-AW between the three groups of ROM exercise, massage, and control

Variable	ROM exercise group	Massage group	Control group	Chi-square test	P-value
ICU-AW before intervention				0.68	0.71
YES	12 (80.0)	11 (73.3)	10 (66.7)
NO	3 (20.0)	4 (26.7)	5 (33.3)
ICU-AW after intervention				35.00^a)	<0.001
YES	0	3 (20.0)	15 (100.0)
NO	15 (100.0)	12 (80.0)	0
McNemar's test	20.00	8.57	6.00
P-value	<0.001	0.009	0.042

Values are presented as number (%).

ICU-AW: intensive care unit acquired weakness; ROM: range of motion.

^a)Fisher's exact test.

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Effectiveness of massage and range of motion exercises on muscle strength and intensive care unit-acquired weakness in Iranian patients with COVID-19: a randomized parallel-controlled trial

Acute Crit Care. 2024;39(1):78-90. Published online December 13, 2023

DOI: https://doi.org/10.4266/acc.2023.00416

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Effectiveness of massage and range of motion exercises on muscle strength and intensive care unit-acquired weakness in Iranian patients with COVID-19: a randomized parallel-controlled trial

Figure 1. The flow diagram of the study. ROM: range of motion; ICU: intensive care unit.

Figure 1.

Effectiveness of massage and range of motion exercises on muscle strength and intensive care unit-acquired weakness in Iranian patients with COVID-19: a randomized parallel-controlled trial

Variable	ROM exercise group (n=15)	Massage group (n=15)	Control group (n=15)	Test statistic	P-value
Age (yr)	41±14	52±14	52±16	F=2.71	0.081
Glascow coma scale score	15	15	15	-	-
FOUR score	14.5±0.5	14.4±0.6	14.9±0.4	F=2.13	0.132
APACHE II score	5.7±2.2	6.8±2.5	9.3±3.4	F=6.50	0.003
SOFA score	1.7±1.3	2.3±1.3	2.1±1.5	F=0.64	0.533
Sex				χ²=0.18	0.924
Male	7 (46.7)	7 (46.7)	8 (53.3)
Female	8 (53.3)	8 (53.3)	7 (46.7)
Length of hospital stay before ICU admission (day)				Fisher’s exact test=8.19	0.123
1	8 (53.3)	11 (73.3)	5 (33.3)
2	6 (40.0)	3 (20.0)	9 (60.0)
3	1 (6.7)	1 (6.7)	-
4	-	-	1 (6.7)
History of addiction				χ²=1.45	0.481
Yes	3 (20.0)	5 (33.3)	6 (40.0)
No	12 (80.0)	10 (66.7)	9 (60.0)
History of ICU admission				Fisher’s exact test=1.86	>0.99
Yes	-	-	1 (6.7)
No	15 (100)	15 (100)	14 (93.3)
Use of renal replacement therapy				Fisher’s exact test=2.81	0.323
Yes	-	-	2 (13.3)
No	15 (100)	15 (100)	13 (86.7)
Respiratory support				Fisher’s exact test=6.30	0.371
Simple mask	-	-	1 (6.7)
Mask without inhalation of exhaled air	8 (53.3)	5 (33.3)	3 (20.0)
Invasive mechanical ventilation	2 (13.3)	1 (6.7)	3 (20.0)
High flow device	5 (33.3)	9 (60.0)	8 (53.3)

Muscle group		ROM exercise group (n=15, a)	Massage group (n=15, b)	Control group (n=15, c)	Between P-value	ANCOVA F (P-value), effect size post-hoc
Right deltoid	Pre	11.6±2.8	8.7±3.3	11.5±1.7	0.007
	Post	12.4±2.7	9.1±3.2	10.7±1.9	0.007
	Difference	0.8±0.3	0.4±0.3	–0.8±0.5		37.37 (<0.001)
	t	11.3	4.6	–5.8		0.65
	P-value	<0.001	<0.001	<0.001		a>b>c
Left deltoid	Pre	11.5±2.8	8.6±3.3	11.4±1.7	0.006
	Post	12.3±2.8	9.0±3.2	10.7±1.9	0.008
	Difference	0.8±0.2	0.5±0.4	–0.7±0.5		36.06 (<0.001)
	t	12.9	5	–5.5		0.64
	P-value	<0.001	<0.001	<0.001		a>b>c
Right wrist	Pre	6.7±1.1	5.6±1.4	6.4±1.1	0.040
	Post	7.4±1.1	6.0±1.3	6.1±1.1	0.003
	Difference	0.6±0.2	0.4±0.3	–0.3±0.3		33.19 (<0.001)
	t	10.0	5.2	–3.6		0.62
	P-value	<0.001	<0.001	0.003		a>b>c
Left wrist	Pre	6.7±1.1	5.5±1.4	6.4±1.0	0.020
	Post	7.3±1.1	5.9±1.3	6.0±1.0	0.003
	Difference	0.6±0.2	0.4±0.3	–0.4±0.3		29.21 (<0.001)
	t	9.2	4.6	–4.1		0.59
	P-value	<0.001	<0.001	0.001		a>b>c
Right biceps	Pre	12.9±2.3	9.5±3.3	11.6±2.1	0.003
	Post	13.6±2.2	9.8±3.3	11.0±2.1	0.001
	Difference	0.7±0.2	0.3±0.3	–0.6±0.4		48.34 (<0.001)
	t	11.8	4.5	–6.1		0.71
	P-value	<0.001	<0.001	<0.001		a>b>c
Left biceps	Pre	12.8±2.3	9.3±3.4	11.7±2.0	0.002
	Post	13.5±2.4	9.7±3.3	11.0±2.1	0.001
	Difference	0.7±0.3	0.4±0.3	–0.7±0.4		42.88 (<0.001)
	t	9.0	5.0	–6.3		0.68
	P-value	<0.001	<0.001	<0.001		a>b>c

Muscle group		ROM exercise group (n=15, a)	Massage group (n=15, b)	Control group (n=15, c)	Between P-value	ANCOVA F (P-value), effect size post-hoc
Right recuts	Pre	14.9±1.6	12.6±2.7	12.1±1.2	0.001
	Post	15.5±1.5	13.0±2.6	11.2±1.5	<0.001
	Difference	0.7±0.3	0.4±0.3	–0.9±0.5		57.71 (<0.001)
	t	7.67	5.42	–6.89		0.74
	P-value	<0.001	<0.001	<0.001		a>b>c
Left rectus	Pre	14.8±1.6	12.6±2.6	12.2±1.3	0.001
	Post	15.4±1.6	12.9±2.6	11.2±1.5	<0.001
	Difference	0.7±0.3	0.3±0.3	–1.0±0.4		63.77 (<0.001)
	t	8.11	4.63	–8.77		0.76
	P-value	<0.001	<0.001	<0.001		a>b>c
Right tibialis	Pre	7.0±1.5	6.47±1.2	7.1±1.6	0.036
	Post	7.6±1.5	6.7±1.4	6.5±1.8	0.11
	Difference	0.6±0.2	0.3±0.3	–0.6±0.4		48.94 (<0.001)
	t	11.44	4.79	–5.76		0.71
	P-value	<0.001	<0.001	<0.001		a>b>c
Left tibialis	Pre	7.0±1.5	6.2±1.3	7.0±1.5	0.28
	Post	7.6±1.4	6.6±1.4	6.4±1.8	0.07
	Difference	0.6±0.3	0.3±0.3	–0.6±0.5		29.96 (<0.001)
	t	9.60	4.07	–5.06		0.6
	P-value	<0.001	0.001	<0.001		a>b>c
Right quadriceps	Pre	15.2±1.5	13.4±2.9	12.3±1.9	0.003
	Post	15.8±1.5	13.6±2.9	11.4±2.07	<0.001
	Difference	0.6±0.3	0.3±0.2	–0.9±0.5		55.52 (<0.001)
	t	8.37	6.37	–7.14		0.74
	P-value	<0.001	<0.001	<0.001		a>b>c
Left quadriceps	Pre	15.2±1.5	13.4±2.8	12.4±1.8	0.003
	Post	15.8±1.6	13.6±3.0	11.5±2.0	<0.001
	Difference	0.6±0.2	0.2±0.3	–0.9±0.4		72.01 (<0.001)
	t	13.14	3.3	–9.13		0.78
	P-value	<0.001	0.005	<0.001		a>b>c

Variable	ROM exercise group	Massage group	Control group	Kruskal-Wallis test	P-value	Effect size
MRC score before intervention	45.9±4.0	46.8±4.8	50.0±3.3	5.86	0.053	1.77
MRC score after intervention	45.9±4.1	46.8±4.8	50.0±3.3	31.84	<0.001	6.86
Wilcoxon test (P-value)	–3.44 (0.001)	–3.42 (0.001)	–3.44 (0.001)	-	-	-
Mean difference	12.0±2.3	6.3±3.0	–8.5±2.4	37.62	<0.001	8.62

Variable	ROM exercise group	Massage group	Control group	Chi-square test	P-value
ICU-AW before intervention				0.68	0.71
YES	12 (80.0)	11 (73.3)	10 (66.7)
NO	3 (20.0)	4 (26.7)	5 (33.3)
ICU-AW after intervention				35.00^a)	<0.001
YES	0	3 (20.0)	15 (100.0)
NO	15 (100.0)	12 (80.0)	0
McNemar's test	20.00	8.57	6.00
P-value	<0.001	0.009	0.042

Table 1. Comparison of demographic and clinical characteristics of participants in three groups of massage, ROM exercises, and control

Values are presented as mean±standard deviation or number (%).

ROM: range of motion; FOUR: Full Outline of Unresponsiveness; APACHE: Acute Physiology and Chronic Health Evaluation; SOFA: Sequential Organ Failure Assessment; ICU: intensive care unit.

Table 2. Comparison of muscle strength in right and left hand between the three groups

Values are presented as mean±standard deviation. Control variables of ANCOVA: pre-muscle strength, Acute Physiology and Chronic Health Evaluation II score.

ROM: range of motion; ANCOVA: analysis of covariance.

Table 3. Comparison of muscle strength in right and left leg between the three groups

Values are presented as mean±standard deviation. Control variables of ANCOVA: pre-muscle strength, Acute Physiology and Chronic Health Evaluation II score.

ROM: range of motion; ANCOVA: analysis of covariance.

Table 4. Comparison of MRC score between the three groups of ROM exercise, massage, and control

Values are presented as mean±standard deviation unless otherwise indicated.

MRC: Medical Research Council; ROM: range of motion.

Table 5. Comparison of frequency of ICU-AW between the three groups of ROM exercise, massage, and control