- Research article
- Open access
- Published:
Association of phase angle with sarcopenia in chronic musculoskeletal pain patients: a retrospective study
Journal of Orthopaedic Surgery and Research volume 18, Article number: 87 (2023)
Abstract
Background
In chronic musculoskeletal pain patients, detection of sarcopenia is of significant clinical interest. Phase angle, which can be measured through bioelectrical impedance analysis (BIA), can detect sarcopenia; however, the evidence in chronic musculoskeletal pain patients is limited. This study aimed to assess the relationship between phase angle and sarcopenia in patients with chronic musculoskeletal pain. Our hypothesis was that phase angle would be a useful indicator to identify sarcopenia in patients with chronic musculoskeletal pain.
Methods
A total of 190 patients (51 men and 139 women) with chronic musculoskeletal pain were included in this retrospective cross-sectional study. Patient data of backgrounds, numeric rating scale score for pain, skeletal muscle index, and phase angle assessed using BIA were retrospectively reviewed. Sarcopenia was diagnosed using the Asian Working Group for Sarcopenia criteria 2019.
Results
A total of 51 patients (26.7%), including 10 men (19.6%) and 41 women (29.5%), were diagnosed with sarcopenia. Phase angle, sarcopenia-related factors, age, and body mass index (BMI) differed significantly in patients with and without sarcopenia. On multiple logistic regression analysis, the prevalence of sarcopenia was significantly correlated with phase angle and BMI. The areas under the curve exhibited high accuracy in discriminating sarcopenia in men and moderate accuracy in both sexes and in women.
Conclusions
Phase angle may be a valid discriminator of sarcopenia in patients with chronic musculoskeletal pain.
Background
Chronic pain, which affects 20% of the general population, is a global problem that decreases activities of daily living [1, 2]. A total of 30–50% of older adults suffer from chronic pain, most of which originates from the musculoskeletal system [3]. Furthermore, musculoskeletal conditions are the leading cause of physical disability and also have a large impact on many other aspects of older people’s health, such as low physical activity level, poor mobility, frailty, depression, cognitive impairment, and falls [4]. As a musculoskeletal problem, sarcopenia, which was proposed to be a progressive and generalized loss of skeletal muscles, is attracting attention [5,6,7,8,9]. Sarcopenia is associated with increased adverse outcomes, including falls, fractures, functional decline, and even mortality [10,11,12,13,14]. In patients with chronic musculoskeletal pain, physical function and activity are impaired from an early age and exacerbate further with pain, which was explained by the fear-avoidance model [15,16,17]. This model explains why some patients with musculoskeletal disorders develop chronic pain syndrome. In this model, pain experience causes fear of pain itself, which leads to avoidance behavior and eventually immobilization and disuse syndrome, and disuse syndrome exacerbates pain. Therefore, it is very important to detect musculoskeletal dysfunction and perform physical exercise to maintain daily activity for the treatment of chronic musculoskeletal pain [18,19,20]. While chronic musculoskeletal pain and sarcopenia may correlate with each other, and detection of sarcopenia is important in the patients with chronic pain, the evidence for the association between them is limited.
On the other hand, phase angle, which can be measured noninvasively by bioelectrical impedance analysis (BIA), is reported to reflect the quality of cells, and a lower phase angle suggests decreased cellular integrity [21,22,23]. Previous reports have suggested that phase angle correlated with nutritional status, muscle strength, and mortality [24,25,26]. Therefore, phase angle could be used for sarcopenia detection [27,28,29,30,31]. However, in chronic musculoskeletal pain patients, it is unclear how phase angle and sarcopenia are related and whether phase angle can effectively detect sarcopenia. Therefore, the purpose of this study was to assess the relationship between phase angle and sarcopenia in patients with chronic musculoskeletal pain. Our hypothesis was that phase angle would be a useful indicator to identify sarcopenia in patients with chronic musculoskeletal pain.
Methods
Study participants
This retrospective study was conducted at Okayama University Hospital. The participants included 190 patients (51 men, 139 women) with chronic musculoskeletal pain who visited our pain outpatient clinic between June 2019 and February 2021. The inclusion criteria for this study were age over 40 years, pain for longer than 3 months, and complete self-report questionnaires and physical examination. The exclusion criteria were as follows: in litigation, dementia, delirium, or other conditions that made completing questionnaires and physical examinations difficult (Fig. 1). Ethical approval was obtained from the hospital board of ethics, and the need for patient informed consent was waived due to the retrospective study design. This study was conducted in accordance with the Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans.
Assessment of sarcopenia-related factors
Diagnosis of sarcopenia
Diagnosis of sarcopenia was performed according to the Asian Working Group for Sarcopenia (AWGS) criteria 2019 [32]. Gait speed, grip strength, and muscle mass were measured in this study. The criterion for low muscle strength was handgrip strength < 28 kg for men and < 18 kg for women and that for low physical performance was walking speed at < 1.0 m/s for 6 m. The skeletal muscle index (SMI) was assessed using InBody 770 and S10 (InBody Japan, Tokyo, Japan), and low muscle mass was defined by an SMI of < 7.0 kg/m2 in men and < 5.7 kg/m2 in women in this study. Sarcopenia was defined by the presence of low muscle mass combined with either low muscle strength or low physical performance.
Assessment of phase angle
Phase angle was defined by the following equation using 50-kHz current:
Phase angle (degrees) = arctangent [reactance (Xc)/resistance (R)] × (180/π).
This calculation was performed automatically by the device, and we used the data obtained during SMI assessment. Diagnosis of sarcopenia and measurement of phase angle were performed by a same examiner.
Evaluation of pain-related factors
Pain intensity assessment
The numeric rating scale (NRS) was used for assessment of pain intensity. NRS scores range from 0 to 10, with 0 representing no pain and 10 representing the worst imaginable pain [33]. The average pain intensity in the past 1Â week was used in this study.
Statistical analyses
Descriptive statistics are presented as mean ± standard deviations (SDs) for continuous variables and as numbers and percentages for categorical variables. The Kolmogorov–Smirnov test was used to assess normality for continuous variables. We analyzed correlations of phase angle with each measured variable using Spearman’s rank correlation coefficient. Then, we performed the Mann–Whitney U test to compare the measured parameters in the patients with and without sarcopenia. In a subsequent analysis, we performed multiple logistic regression analysis to evaluate the factors and odds ratio (OR) associated with sarcopenia. The explanatory variables included phase angle, body mass index (BMI), NRS, age, and sex. Next, in order to evaluate the discrimination performance of phase angle, area under the curve (AUC) was calculated using a receiver operating characteristic curve (ROC) analysis. Then, the sensitivity and specificity were calculated using the best cutoff point of phase angle for both genders and each gender individually with the Youden index for the ROC, respectively. As a previous study reported that men and women had different cutoff values for the phase angle, evaluation was conducted in both genders, male and female. The sample size was set as 10 of event per variable in logistic regression analysis [34]. Since this study was designed five variables in the multiple logistic regression analysis, the number of events, i.e., the required number of sarcopenia participants, was determined to be 50. We reviewed retrospectively all cases in the period that met the number of events. For the statistical analyses, we used EZR software (Saitama Medical Center Jichi Medical University, Tochigi, Japan), which is a graphical user interface for R (The R Foundation for Statistical Computing). Results were considered significant at a level of p < 0.05.
Results
Participants’ characteristics
The characteristics of the patients are shown in Table 1. The mean age was 67.2 (SD: 13.5) years, and the mean NRS score was 5.2 (SD: 2.5) points. Sarcopenia was diagnosed in 51 (26.7%) patients, which included 10 (19.6%) men and 41 (29.5%) women. The mean phase angle was 4.7 (SD: 1.0) degrees. Pain site and other sarcopenia-related factors are also shown in Table 1.
We performed the following three analyses: 1. correlations among phase angle and measured variable, 2. comparison between with and without sarcopenia patients, and 3. the discrimination capacity of phase angle for sarcopenia.
Correlations among phase angle and measured variable
Table 2 shows the correlation among phase angle and other variables. Phase angle was significantly correlated with age (r = − 0.54, p < 0.001), BMI (r = 0.21, p = 0.003), grip power (r = 0.61, p < 0.001), gait speed (r = 0.42, p < 0.001), SMI (r = 0.71, p < 0.001), and NRS (r = − 0.19, p = 0.007).
Comparison between with and without sarcopenia patients
Table 3 shows the characteristics of patients with and without sarcopenia. All sarcopenia-related factors, phase angle, age, and BMI differed significantly in patients depending on the presence of sarcopenia. In a multiple logistic regression analysis, sarcopenia prevalence was significantly correlated with phase angle (OR = 0.09, p < 0.001) and BMI (OR = 0.80, p < 0.001) (Table 4).
The discrimination capacity of phase angle for sarcopenia
The discrimination value of phase angle for sarcopenia was assessed by the ROC curves (Fig. 2). The AUCs for both genders, men, and women were 0.851, 0.911, and 0.837, respectively. The cutoff values calculated by Youden index for both genders, men, and women were 4.2, 5.1, and 4.2, respectively (Table 5).
Discussion
Our findings showed that in chronic musculoskeletal pain patients, phase angle significantly correlated with age, BMI, grip power, gait speed, SMI, and NRS scores. Further, the phase angle was lower in patients with sarcopenia than in those without it. A lower phase angle was significantly correlated with sarcopenia and showed high accuracy in discriminating sarcopenia in men and moderate accuracy in both genders and women.
Previous reports suggested that phase angle was lower in individuals with sarcopenia, and several possible causes were reported to explain it. One of the most reported reasons was nutrition; patients with low phase angle were considered to be malnourished [27]. Previous studies that had taken BMI as a nutritional indicator reported that since patients with sarcopenia showed lower phase angle and BMI, they were considered to be malnourished [31]. In our study as well, with a multivariate analysis adjusted for age, gender, and degree of pain, a low phase angle and BMI were significantly correlated with sarcopenia prevalence. Given these, malnutrition could be factor in sarcopenia patients with chronic musculoskeletal pain, and therefore, nutrition therapy may be helpful in such patients. Though, in our study, nutritional status could only be assessed by BMI, further study would be needed to evaluate malnutrition in sarcopenia patients with chronic musculoskeletal pain. Another reason which should be considered is that phase angle correlates with functional status or muscle quality [28]. In our study, phase angle was significantly correlated with physical function and muscle strength, and we found that phase angle of patients with sarcopenia was lower than that of patients without it. Therefore, our results are compatible with those of previous reports.
As for the treatment of chronic musculoskeletal pain, our study suggests that detection and prevention of sarcopenia is of clinical significance in the management and treatment of musculoskeletal pain. Previous report suggested that phase angle was useful for detecting sarcopenia [27]. In addition, the AUC in ROC curves was 0.73 in kidney transplant recipients [31], 0.718 for men and 0.721 for women among community-dwelling individuals [28], and 0.85 in our study, which is similar to the results of previous studies. As for the cutoff point of phase angle, previous reports suggested that a value of 4.46 for kidney transplant recipients [31], 5.05 for cirrhosis patients [30], 4.55 for community-dwelling and hospitalized older adults [29], and 4.05 for men and 3.55 for women among community-dwelling individuals [28] could discriminate sarcopenia. Similarly, our results indicated that values of 4.2 for both genders, 5.1 for men, and 4.2 for women with chronic musculoskeletal pain were the best cutoff points to discriminate sarcopenia (Table 6). Thus, our study demonstrated that for chronic musculoskeletal pain patients, phase angle was useful in detecting sarcopenia.
Notwithstanding the contribution of this study, there were several limitations. First, as this study was conducted in Japanese patients and we used the AWGS 2019 criteria for sarcopenia diagnosis, the results may differ in the studies involving other populations and those using other sarcopenia criteria, such as those proposed by the European working group for sarcopenia in older people [35] or the international working group on sarcopenia [36]. Second, it is known that psychosocial factors are intricately intertwined in patients with chronic musculoskeletal pain, and such factors were not considered in this study. Third, as this study was a retrospective cross-sectional study, it was difficult to evaluate the chronological order or change in phase angle, sarcopenia, and chronic musculoskeletal pain. Considering these limitations, future studies would require a detailed assessment, and clinical data from other countries would be needed to explore the relationships between phase angle, sarcopenia, and chronic musculoskeletal pain in different populations.
Conclusion
Phase angle may be a valid discriminator of sarcopenia in patients with chronic musculoskeletal pain.
Availability of data and materials
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- AUC:
-
Area under the curve
- AWGS:
-
Asian Working Group for Sarcopenia
- BIA:
-
Bioelectrical impedance analysis
- BMI:
-
Body mass index
- NRS:
-
Numeric rating scale
- OR:
-
Odds ratio
- ROC:
-
Receiver operating characteristic
- SD:
-
Standard deviation
- SMI:
-
Skeletal muscle index
References
Blyth FM, March LM, Brnabic AJ, Jorm LR, Williamson M, Cousins MJ. Chronic pain in Australia: a prevalence study. Pain. 2001;89(2–3):127–34.
Breivik H, Collett B, Ventafridda V, Cohen R, Gallacher D. Survey of chronic pain in Europe: prevalence, impact on daily life, and treatment. European J Pain. 2006;10(4):287–333.
Dieppe P. Chronic musculoskeletal pain. BMJ (Clin Res ed). 2013;346: f3146.
Blyth FM, Noguchi N. Chronic musculoskeletal pain and its impact on older people. Best Pract Res Clin Rheumatol. 2017;31(2):160–8.
Evans WJ, Campbell WW. Sarcopenia and age-related changes in body composition and functional capacity. J Nutr. 1993;123(2 Suppl):465–8.
Rosenberg IH. Sarcopenia: origins and clinical relevance. J Nutr. 1997;127(5 Suppl):990s–1s.
Dos Santos L, Cyrino ES, Antunes M, Santos DA, Sardinha LB. Sarcopenia and physical independence in older adults: the independent and synergic role of muscle mass and muscle function. J Cachexia Sarcopenia Muscle. 2017;8(2):245–50.
Narici MV, Maffulli N. Sarcopenia: characteristics, mechanisms and functional significance. Br Med Bull. 2010;95:139–59.
Chen YP, Kuo YJ, Hung SW, Wen TW, Chien PC, Chiang MH, Maffulli N, Lin CY. Loss of skeletal muscle mass can be predicted by sarcopenia and reflects poor functional recovery at one year after surgery for geriatric hip fractures. Injury. 2021;52(11):3446–52.
Landi F, Liperoti R, Russo A, Giovannini S, Tosato M, Capoluongo E, Bernabei R, Onder G. Sarcopenia as a risk factor for falls in elderly individuals: results from the ilSIRENTE study. Clin Nutrit. 2012;31(5):652–8.
Wong RMY, Wong H, Zhang N, Chow SKH, Chau WW, Wang J, Chim YN, Leung KS, Cheung WH. The relationship between sarcopenia and fragility fracture-a systematic review. Osteoporosis Int J Establ Result Coop Between European Found Osteoporosis Natl Osteoporosis Found USA. 2019;30(3):541–53.
Zhang Y, Hao Q, Ge M, Dong B. Association of sarcopenia and fractures in community-dwelling older adults: a systematic review and meta-analysis of cohort studies. Osteoporosis Int J Establ Result Coop Between European Found Osteoporosis Natl Osteoporosis Found USA. 2018;29(6):1253–62.
Yeung SSY, Reijnierse EM, Pham VK, Trappenburg MC, Lim WK, Meskers CGM, Maier AB. Sarcopenia and its association with falls and fractures in older adults: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle. 2019;10(3):485–500.
Liu P, Hao Q, Hai S, Wang H, Cao L, Dong B. Sarcopenia as a predictor of all-cause mortality among community-dwelling older people: a systematic review and meta-analysis. Maturitas. 2017;103:16–22.
Vlaeyen JWS, Linton SJ. Fear-avoidance and its consequences in chronic musculoskeletal pain: a state of the art. Pain. 2000;85(3):317–32.
Asmundson GJ, Norton PJ, Norton GR. Beyond pain: the role of fear and avoidance in chronicity. Clin Psychol Rev. 1999;19(1):97–119.
Leeuw M, Goossens ME, Linton SJ, Crombez G, Boersma K, Vlaeyen JW. The fear-avoidance model of musculoskeletal pain: current state of scientific evidence. J Behav Med. 2007;30(1):77–94.
Booth J, Moseley GL, Schiltenwolf M, Cashin A, Davies M, Hübscher M. Exercise for chronic musculoskeletal pain: a biopsychosocial approach. Musculoskeletal Care. 2017;15(4):413–21.
O’Connor SR, Tully MA, Ryan B, Bleakley CM, Baxter GD, Bradley JM, McDonough SM. Walking exercise for chronic musculoskeletal pain: systematic review and meta-analysis. Arch Phys Med Rehabil. 2015;96(4):724-734.e723.
Tsuji H, Tetsunaga T, Tetsunaga T, Misawa H, Nishida K, Ozaki T. Cognitive factors associated with locomotive syndrome in chronic pain patients: a retrospective study. J Orthop Sci off J Japanese Orthopaedic Assoc. 2020. https://doi.org/10.1016/j.jos.2020.08.007.
De Lorenzo A, Andreoli A, Matthie J, Withers P. Predicting body cell mass with bioimpedance by using theoretical methods: a technological review. J Appl Physiol. 1997;82(5):1542–58.
Lukaski HC. Evolution of bioimpedance: a circuitous journey from estimation of physiological function to assessment of body composition and a return to clinical research. Eur J Clin Nutr. 2013;67(Suppl 1):S2-9.
Norman K, Stobäus N, Pirlich M, Bosy-Westphal A. Bioelectrical phase angle and impedance vector analysis–clinical relevance and applicability of impedance parameters. Clin Nutrit. 2012;31(6):854–61.
Lukaski HC, Kyle UG, Kondrup J. Assessment of adult malnutrition and prognosis with bioelectrical impedance analysis: phase angle and impedance ratio. Curr Opin Clin Nutr Metab Care. 2017;20(5):330–9.
de Blasio F, Santaniello MG, de Blasio F, Mazzarella G, Bianco A, Lionetti L, Franssen FME, Scalfi L. Raw BIA variables are predictors of muscle strength in patients with chronic obstructive pulmonary disease. Eur J Clin Nutr. 2017;71(11):1336–40.
Mundstock E, Amaral MA, Baptista RR, Sarria EE, Dos Santos RRG, Filho AD, Rodrigues CAS, Forte GC, Castro L, Padoin AV, et al. Association between phase angle from bioelectrical impedance analysis and level of physical activity: systematic review and meta-analysis. Clin Nutrit. 2019;38(4):1504–10.
Di Vincenzo O, Marra M, Di Gregorio A, Pasanisi F, Scalfi L. Bioelectrical impedance analysis (BIA)-derived phase angle in sarcopenia: a systematic review. Clin Nutrit. 2020. https://doi.org/10.1016/j.clnu.2020.10.048.
Yamada M, Kimura Y, Ishiyama D, Nishio N, Otobe Y, Tanaka T, Ohji S, Koyama S, Sato A, Suzuki M, et al. Phase angle is a useful indicator for muscle function in older adults. J Nutr Health Aging. 2019;23(3):251–5.
Kilic MK, Kizilarslanoglu MC, Arik G, Bolayir B, Kara O, Dogan Varan H, Sumer F, Kuyumcu ME, Halil M, Ulger Z. Association of bioelectrical impedance analysis-derived phase angle and sarcopenia in older adults. Nutrit Clin Pract Off Publ Am Soc Parenteral Enteral Nutrit. 2017;32(1):103–9.
Espirito Santo Silva DD, Waitzberg DL, Passos de Jesus R, Oliveira LPM, Torrinhas RS, Belarmino G. Phase angle as a marker for sarcopenia in cirrhosis. Clin Nutrit ESPEN. 2019;32:56–60.
Kosoku A, Uchida J, Nishide S, Kabei K, Shimada H, Iwai T, Maeda K, Hanayama Y, Ishihara T, Naganuma T, et al. Association of sarcopenia with phase angle and body mass index in kidney transplant recipients. Sci Rep. 2020;10(1):266.
Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY, Iijima K, Jang HC, Kang L, Kim M, Kim S, et al. Asian Working group for sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J Am Med Dir Assoc. 2020;21(3):300-307.e302.
Jensen MP, Karoly P, Braver S. The measurement of clinical pain intensity: a comparison of six methods. Pain. 1986;27(1):117–26.
Peduzzi P, Concato J, Kemper E, Holford TR, Feinstein AR. A simulation study of the number of events per variable in logistic regression analysis. J Clin Epidemiol. 1996;49(12):1373–9.
Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(1):16–31.
Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, Abellan van Kan G, Andrieu S, Bauer J, Breuille D, et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc. 2011;12(4):249–56.
Acknowledgements
The authors would like to thank all the medical staff who collaborated on this study.
Funding
This study was supported by JSPS KAKENHI Grant Number 17K16691.
Author information
Authors and Affiliations
Contributions
HT and TT contributed to conceptualization. HT and TT were involved in methodology. HT contributed to formal analysis and investigation. HT, TT, and HM were involved in writing—original draft preparation. TT contributed to funding acquisition. TT was involved in resources. KN and TO contributed to supervision. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
We obtained approval from the institutional review board of Okayama University Hospital (approval number 2104-035), and the need for patient informed consent was waived due to the retrospective study design.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
About this article
Cite this article
Tsuji, H., Tetsunaga, T., Misawa, H. et al. Association of phase angle with sarcopenia in chronic musculoskeletal pain patients: a retrospective study. J Orthop Surg Res 18, 87 (2023). https://doi.org/10.1186/s13018-023-03567-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1186/s13018-023-03567-1