Is upper extremity pain an important cause of sleep problems in patients with multiple sclerosis?

Abstract

AimIn this study, we aimed to examine the localization of pain in multiple sclerosis (MS) patients and to determine the relationship of pain localization with quality of life, sleep and depression level.MethodsEighty-six MS patients (19 males, 67 females, age: 18-65 years, Expanded Disability Status Scale (EDSS) Level 1-8) were included in the study. The pain was evaluated with the Short Form Mc-Gill Pain Questionnaire (SF-MPQ), quality of life (QoL) with the Nottingham Health Profile (NHP), sleep quality with the Pittsburg Sleep Quality Index (PSQI) and mood of depression with the Beck Depression Inventory (BDI).ResultsThe percentage of patients with pain was 55.8. Patients complained of the neck (4.2%), upper extremity (25%), headache (14.5%), low back pain (47.9%), upper back pain (5%) and lower extremity pain (58.3%). NHP scores (total: p=0.033, pain: p=0.001, sleep: p=0.0033) and sleep quality (p=0.014) were better in patients without pain. In addition, there was a weak to moderate correlation between several PSQI scores (sleep quality: rho=0.498, p=0.001, sleep latency: rho=0.440, p=0.002, sleep efficiency: rho=0.343, p=0.017 and total: rho=0.379, p=0.008) and upper extremity pain.ConclusionUpper extremity pain affects sleep quality and therefore QoL in patients with MS. For this reason, when examining the pain of MS patients with sleep problems, especially questioning this region and adding modalities to the program to relieve upper extremity pain may contribute to the sleep quality that it affects. Thus, the quality of life can be positively affected in many ways. Further studies are required to obtain exact conclusions.

Keywords

Introduction

Pain is a common problem in multiple sclerosis (MS) patients and ranges from 29% to 86%.¹ Pain in MS has been classified in different ways according to its etiology, type, and localization in pain studies. It is seen that the etiology of pain is attributed to spinal injuries,² lesions in the central motor pathways and sensorial pathways, nociceptive stimuli due to motor disorders, drugs, etc.³ Pain in MS is categorized in different ways such as nociceptive, central, peripheral neuropathic, spasticity-related pain, psychogenic, idiopathic, and mixed pain.^3-4 Pains such as migraine, trigeminal neuralgia, L’hermitte sign, dysesthetic pain, back pain, visceral pain, and extremity pain are considered in different categories in some studies^3,5 and are sometimes excluded from studies.^4,6 When pain complaints of MS patients are examined, it has been reported that pain is felt in forms such as stinging, numbness, electrical currents, tightness, burning, squeezing, pressing, painful dysesthesias, aching, pinching, tingling, cramping, throbbing, stabbing, smarting, cutting.^2,4,6 Patients have reported pain in many localizations from head to feet, including the face and around the eyes.^3-4
Pain has been associated with high EDSS scores, age, education level, gender, disease duration, spinal lesions, progressive MS, and multiple attacks.^2,5 Pain in MS occurs in many different parts of the body depending on different mechanisms and etiology and has a multidimensional negative effect on the lives of patients. Previously, the negative impact of pain on the activity of daily living, social performance, mental health, mood, and quality of life has been reported in many studies.^7-8 Many of these studies provided information on the type and duration of pain in MS. However, although it has been shown in the literature that pain localization is associated with sleep, general activity level, enjoying life, mood, and walking ability,⁹ no study has been conducted on the effect of pain localization in MS. Our study aims to examine the localization of pain in MS patients and to determine the relationship of pain localization with quality of life, sleep, and depression level.

Materials and Methods

This cross-sectional study was conducted at Hacettepe University, Ankara, Turkey. Hacettepe University Non-Interventional Ethical Committee approved the study (GO16/462-44). Eighty-six MS patients (EDSS 1–8) who were administered Neurology department were recruited. The inclusion criteria were as follows: age between 18–65 years, diagnosed with definite MS by neurologists, Standardized Mini-Mental Status Examination score above 24, no relapse within 1 month, having any other chronic disease. Patients with hearing or visual impairments and cooperation problems were excluded from the study.AssessmentsAll patients signed a written informed consent form, and then the following assessments were applied to the patients who accepted to participate in the study. Patients’ demographic data and information about the course of the disease were recorded before performing clinical assessments.
Disability level: The patient’s disability level was determined by Expanded Disability Status Scale (EDSS). The EDSS is between 0 to 10. Lower scores indicate a minimal disability level.¹⁰PainPatients who have pain were given detailed information about how they fulfill the Turkish version of the Short Form Mc-Gill Pain Questionnaire (SF-MPQ). The SF-major MPQ’s component comprises 15 descriptive words for the pain experience (11 sensorial and 4 emotional), which the patient rates on a point scale based on their intensity (0 = none, 1 = mild, 2 = moderate, and 3 = severe). The intensity rank values of the words selected for the sensory, affective, and overall descriptors are added to provide three pain scores. Sensory and emotional intensity values are added to determine the sensory and affective scores. The intensity levels add up to the final score. The visual analogue scale and the evaluative total pain intensity index are two additional ways that the SF-MPQ measures pain intensity.¹¹ Physical therapists interviewed the patients face-to-face and in a silent room for making an accurate pain assessment.Quality of LifeThe Turkish version of the Nottingham Health Profile (NHP) was used for the assessment of QoL. The Turkish version of the Nottingham Health Profile (NSP) is a self-reported general health questionnaire. It includes 38 items and 6 sub-parameters such as energy level (EL), emotional reactions (ER), physical activity (PA), pain (P), sleep (S) and social isolation (SI). The answers to the questions are given as “yes” and “no” according to the current situation perception. The total score is between 0 and 600, and the perception of high quality of life related to health is inversely proportional to the score obtained.¹²Sleep QualityThe seven-component Pittsburg Sleep Quality Index (PSQI) was used to assess the quality of sleep. The Turkish validity and reliability study of the scale was performed by Hisli et al. Each component assesses various elements of sleep (sleep quality, sleep latency, sleep duration, habitual sleep efficiency, sleep disturbances, use of sleeping medication, and daytime dysfunction). The overall score ranges from 0 to 21, with the highest values indicating poor sleep.¹³Mood of DepressionBeck Depression Inventory (BDI), the Turkish version of which was developed by Hisli et al.¹⁴ measures the physical, emotional, motivational, and cognitive symptoms of depression. The BDI consists of 21 items and each item is scored between 0–3 points. The total score ranges from 0 to 63. High scores indicate increased severity of depression. The BDI was administered in a silent room and gave patients adequate time.Statistical AnalysisData analysis was performed with SPSS 20.0 (SPSS Inc., Chicago, Illinois, USA). The normality was checked by the Kolmogorov-Smirnov test. The homogeneity of group variances was checked by the Levene test. To determine the direction and strength of the relationship between the two variables, Pearson’s correlation analyses were used in a normal distribution, and Spearman’s correlation analyses were used in non-normal distribution. Point biserial correlation was used for analyzing the correlation between categorical variables and dichotomous variables. Correlation values were considered weak correlation for r values up to 0.39, moderate for values between 0.40 and 0.69, and strong for values equal to or greater than 0.70.¹⁵ Student t-test was used to compare two independent variables with normal distribution and the Mann Whitney-U Test with non-normal distribution. p<0.05 was considered statistically significant.

Results

77.9% of the 86 patients included in our study were female, 22.1% were male, and the mean age was 34.97 ± 5.16 years. 55.8% of patients complained of pain, while 44.2% of the patients had no pain complaints. When the painful areas of the patients with pain were questioned, it was seen that 4.2% complained of neck pain, 25% of upper extremity pain, 14.5% of headache, 47.9% of low back pain, 5% of upper back pain and 58.3% of lower extremity pain. The socio-demographic characteristics and clinical course of the disease are shown in Table 1.
In addition, it was determined that NHP was affected in patients with pain in terms of pain, sleep and total score compared to patients without pain. Similarly, sleep quality was found to decrease in patients with pain (Table 2).
Analysis of the relationship between pain region and sleep quality showed that there was a weak to moderate correlation between the total sleep quality score and the subgroup scores of upper extremity pain, excluding sleep duration and sleeping pill intake. In addition, it was determined that back pain was weakly correlated with subjective sleep quality in patients (Table 3).

Discussion

Our study is the first to show the relationship between pain localization and sleep in MS patients. The results determined that upper extremity pain affects sleep differently from other pain localizations.
In our study population, it was determined that more than half of the patients complained of pain in at least one body region and the incidence of pain was 55.8%. When the prevalence of pain in MS patients is examined in the literature, it is seen that there are different results. However, Foley et al. reported that the prevalence of pain ranged from 55% to 70% in a meta-analysis they conducted.¹⁶ Our patient group is similar to other studies in terms of the incidence of pain.
It is seen that our patients mostly suffer from lower extremity and back pain. In studies on pain in MS, it has been shown that the most frequently reported pain after a headache is back pain and lower extremity pain.¹⁷ In terms of pain distribution, our patient population showed similar characteristics to the populations of other studies in the literature.
The relationship between pain, disease severity, depression level, sleep, and quality of life has been investigated in many studies on MS patients. Comparing the MS group with and without pain in our study showed that the groups were similar in terms of disease severity and depression level, but different in terms of sleep quality and quality of life. The prevalence of pain increased with higher EDSS values in MS according to previous studies.^2,5,18 In addition, age, disease duration, and MS type were also associated with pain in these studies. Since the groups were not different in terms of these variables interacting with EDSS, the EDSS scores of the groups may have been similar. Comparably, although many studies have shown the relationship between depression and pain,¹⁷ there was no difference in depression levels between the pain group and the pain-free group in our study. Day et al.¹⁹ contend, however, that the correlation between pain and depression has been overstated in earlier studies because when the severity of MS symptoms is reduced, the association between pain and depression becomes controllable. The homogeneity of the groups in terms of disease severity in our study may have caused this result.
The relationship between sleep and pain in MS patients was determined in previous studies.^18,20 Furthermore, Amtman et al. reported that pain affects sleep more than sleep affects pain.²¹ In our study, we determined that the painful group and the pain-free group were different in terms of sleep quality as in the literature. Additionally, the quality of life varied between groups in the subsections related to pain and sleep. This outcome appears to illustrate how pain and sleep interact.
In contrast to the literature, the impact of pain localization on the quality of sleep was also examined in our study. Global sleep quality, subjective sleep quality, sleep latency, and habitual sleep efficiency were all shown to be impaired by upper extremity pain; other pain localizations did not have any effects other than habitual sleep efficiency. There are various articles in the literature that might imply a connection between upper extremity pain and sleep. Kezele et al.²² determined that combined upper extremity and respiratory exercises reduced the overall pain intensity in patients with MS patients with pain in general. Peters et al.²³ stated in their study that practices aimed at reducing pain might affect sleep disorders in patients with different upper extremities problems. Tajika et al.²⁴ showed that there is a relationship between upper extremity pain and sleep disturbance in the general elderly population. In light of this information, we think that upper extremity pain may be a key point for sleep. There could be several reasons for this. Primarily, the upper extremity is widely represented in the motor and sensory homunculus.²⁵ This suggests that there may be an unproven connection between upper extremity pain and sleep. The upper extremity plays a crucial role in a person’s daily life activities, and the slightest disruption in these activities may change the person’s perception of disability and be reflected in their sleep from a biopsychosocial perspective. In addition, the fact that the upper extremity is constantly in the visual field may alter the person’s awareness and pain perception indirectly and indirectly affect sleep. Even though it is clear that all of these points are debatable and that further study is required, we believe that upper extremity pain should be assessed independently in sleep difficulties in MS patients.
The present study has several limitations. The small sample size and the lack of assessment of fatigue in MS patients are important limitations. In addition, the exclusion of pain types such as nociceptive, musculoskeletal, and neural pain can be considered a limitation.

Conclusion

We determined that pain, especially upper extremity pain, affects sleep and therefore quality of life in patients with MS. For this reason when examining the pain of MS patients with sleep problems, especially questioning the upper extremities and adding modalities to the program to relieve pain for this localization may contribute to the improvement of the pain and therefore the sleep quality it affects. Thus, the quality of life can be positively affected in many ways. Studies in a larger patient population with characteristics such as pain types and MS subtypes, pain duration, fatigue, anxiety, and comprehensive psychosocial assessments may reveal the relationship between sleep and upper extremity pain in detail.

References

1. O’Connor AB, Schwid SR, Herrmann DN, Markman JD, Dworkin RH. Pain associated with multiple sclerosis: systematic review and proposed classification. Pain. 2008;137(1):96-111. doi:10.1016/j.pain.2007.08.024
   Article · PubMed · Google Scholar
2. Grau-López L, Sierra S, Martínez-Cáceres E, Ramo-Tello C. Analysis of the pain in multiple sclerosis patients. Neurologia (Engl Ed). 2011;26(4):208-213. doi:10.1016/s2173-5808(11)70043-8
   Article · PubMed · Google Scholar
3. Truini A, Barbanti P, Pozzilli C, Cruccu G. A mechanism-based classification of pain in multiple sclerosis. J Neurol. 2013;260(2):351-367. doi:10.1007/s00415-012-6579-2
   Article · PubMed · Google Scholar
4. Osterberg A, Boivie J, Thuomas KA. Central pain in multiple sclerosis: prevalence and clinical characteristics. Eur J Pain. 2005;9(5):531-542.
   PubMed · Google Scholar
5. Solaro C, Brichetto G, Amato M, et al. The prevalence of pain in multiple sclerosis: a multicenter cross-sectional study. Neurology. 2004;63(5):919-921. doi:10.1212/01.wnl.0000137047.85868.d6
   Article · PubMed · Google Scholar
6. Srotova I, Kocica J, Vollert J, et al. Sensory and pain modulation profiles of ongoing central neuropathic extremity pain in multiple sclerosis. Eur J Pain. 2021;25(3):573-594. doi:10.1002/ejp.1695
   Article · PubMed · Google Scholar
7. Amtmann D, Askew RL, Kim J, et al. Pain affects depression through anxiety, fatigue, and sleep in multiple sclerosis. Rehabil Psychol. 2015;60(1):81-90. doi:10.1037/rep0000027
   Article · PubMed · Google Scholar
8. Ehde DM, Gibbons LE, Chwastiak L, Bombardier CH, Sullivan MD, Kraft GH. Chronic pain in a large community sample of persons with multiple sclerosis. Mult Scler. 2003;9(6):605-611. doi:10.1191/1352458503ms939oa
   Article · PubMed · Google Scholar
9. Bortsov AV, Platts-Mills TF, Peak DA, et al. Effect of pain location and duration on life function in the year after motor vehicle collision. Pain. 2014;155(9):1836-1845. doi:10.1016/j.pain.2014.06.013
   Article · PubMed · Google Scholar
10. Meyer-Moock S, Feng YS, Maeurer M, Dippel FW, Kohlmann T. Systematic literature review and validity evaluation of the Expanded Disability Status Scale and the Multiple Sclerosis Functional Composite in patients with multiple sclerosis. BMC Neurol. 2014;14:58. doi:10.1186/1471-2377-14-58
    Article · PubMed · Google Scholar
11. Yakut Y, Yakut E, Bayar K, Uygur F. Reliability and validity of the Turkish version short-form McGill Pain Questionnaire in patients with rheumatoid arthritis. Clin Rheumatol. 2007;26(7):1083-1087. doi:10.1007/s10067-006-0452-6
    Article · PubMed · Google Scholar
12. Kucukdeveci AA, McKenna SP, Kutlay S, Gursel Y, Whalley D, Arasil T. The development and psychometric assessment of the Turkish version of the Nottingham Health Profile. Int J Rehabil Res. 2000;23(1):31-38.
    PubMed · Google Scholar
13. Ağargün MY, Kara H, Anlar O. The validity and reliability of the Pittsburgh Sleep Quality Index. Turk Psikiyatri Derg. 1996;7(2):107-115.
    PubMed · Google Scholar
14. Hisli N. Beck depresyon envanterinin universite ogrencileri icin gecerliligi, guvenilirligi (a reliability and validity study of Beck Depression Inventory in a university student sample). J Psychol. 1989;7:3-13.
    PubMed · Google Scholar
15. Schober P, Boer C, Schwarte LA. Correlation coefficients: appropriate use and interpretation. Anesth Analg. 2018;126(5):1763-1768. doi:10.1213/ane.0000000000002864
    Article · PubMed · Google Scholar
16. Foley PL, Vesterinen HM, Laird BJ, et al. Prevalence and natural history of pain in adults with multiple sclerosis: systematic review and meta-analysis. Pain. 2013;154(5):632-642. doi:10.1016/j.pain.2012.12.002
    Article · PubMed · Google Scholar
17. Yilmazer C, Lamers I, Solaro C, Feys P. Clinical perspective on pain in multiple sclerosis. Mult Scler. 2022;28(4):502-511. doi:10.1177/1352458520952015
    Article · PubMed · Google Scholar
18. Ehde DM, Osborne TL, Hanley MA, Jensen MP, Kraft GH. The scope and nature of pain in persons with multiple sclerosis. Mult Scler. 2006;12(5):629-638. doi:10.1177/1352458506071346
    Article · PubMed · Google Scholar
19. Day MA, Ehde DM, Ward LC, et al. An empirical investigation of a biopsychosocial model of pain in multiple sclerosis. Clin J Pain. 2016;32(2):155-163. doi:10.1097/ajp.0000000000000240
    Article · PubMed · Google Scholar
20. Boe Lunde HM, Aae TF, Indrevag W, et al. Poor sleep in patients with multiple sclerosis. PLoS One. 2012;7(11).
    PubMed · Google Scholar
21. Amtmann D, Bamer AM, Askew R, Jensen MP. Cross-lagged longitudinal analysis of pain intensity and sleep disturbance. Disabil Health J. 2020;13(3):100908. doi:10.1016/j.dhjo.2020.100908
    Article · PubMed · Google Scholar
22. Grubic Kezele T, Babic M, Kauzlaric-Zivkovic T, Gulic T. Combined upper limb and breathing exercise programme for pain management in ambulatory and non-ambulatory multiple sclerosis individuals: part II analyses from feasibility study. Neurol Sci. 2020;41(1):65-74.
    PubMed · Google Scholar
23. Peters RM, Menendez ME, Mellema JJ, Ring D, Vranceanu AM. Sleep disturbance and upper-extremity disability. Arch Bone Jt Surg. 2016;4(1):35-40.
    PubMed · Google Scholar
24. Tajika T, Kuboi T, Endo F, et al. Association between upper extremity dysfunction and sleep disturbance in an elderly general population. SAGE Open Med. 2020;8:2050312120901584. doi:10.1177/2050312120901584
    Article · PubMed · Google Scholar
25. Matias CM. Edwin Boldrey and Wilder Penfield’s homunculus: from past to present. World Neurosurg. 2020;135:14-15. doi:10.1016/j.wneu.2019.11.144
    Article · PubMed · Google Scholar

Tables