DOI: 10.1111/eci.12201

ORIGINAL ARTICLE Recovery of upper limb muscle function in chronic fatigue syndrome with and without fibromyalgia Kelly Ickmans*,†,‡, Mira Meeus†,§,¶, Margot De Kooning*,‡,**, Luc Lambrecht†† and Jo Nijs*,‡ *

Pain in Motion Research Group, Department of Human Physiology and Physiotherapy, Faculty of Physical Education & Physiotherapy, Vrije Universiteit Brussel, Brussel, †Pain in Motion Research Group, Division of Musculoskeletal Physiotherapy, Department of Health Care Sciences, Artesis University College Antwerp, Antwerp, ‡Pain in Motion Research Group, Department of Physical Medicine and Physiotherapy, University Hospital Brussels, Brussels, §Rehabilitation Sciences and Physiotherapy, Faculty of Medicine & Health Sciences, Ghent University, Gent, ¶Pain in Motion Research Group, Department of Rehabilitation Sciences and Physiotherapy, Faculty of Medicine & Health Sciences, Antwerp, **Department of Neurology, Faculty of Medicine, University of Antwerp (UA), Antwerp, ††Private practice for internal medicine, Ghent, Belgium

ABSTRACT Background Chronic fatigue syndrome (CFS) patients frequently complain of muscle fatigue and abnormally slow recovery, especially of the upper limb muscles during and after activities of daily living. Furthermore, disease heterogeneity has not yet been studied in relation to recovery of muscle function in CFS. Here, we examine recovery of upper limb muscle function from a fatiguing exercise in CFS patients with (CFS+FM) and without (CFS-only) comorbid fibromyalgia and compare their results with a matched inactive control group. Design In this case–control study, 18 CFS-only patients, 30 CFS+FM patients and 30 healthy inactive controls performed a fatiguing upper limb exercise test with subsequent recovery measures. Results There was no significant difference among the three groups for maximal handgrip strength of the nondominant hand. A significant worse recovery of upper limb muscle function was found in the CFS+FM, but not in de CFS-only group compared with the controls (P < 005). Conclusions This study reveals, for the first time, delayed recovery of upper limb muscle function in CFS+FM, but not in CFS-only patients. The results underline that CFS is a heterogeneous disorder suggesting that reducing the heterogeneity of the disorder in future research is important to make progress towards a better understanding and uncovering of mechanisms regarding the nature of divers impairments in these patients. Keywords Chronic fatigue syndrome, handgrip strength, maximal voluntary contraction, muscle fatigue, muscle recovery. Eur J Clin Invest 2014; 44 (2): 153–159

Introduction Chronic fatigue syndrome (CFS) is a debilitating and complex clinical problem, characterized by extreme fatigue. In addition to the chronic fatigue, the majority of patients with CFS experience widespread and persistent pain [1]. Chronic widespread musculoskeletal pain is the hallmark symptom of fibromyalgia (FM), another chronic debilitating condition. In addition, cooccurring symptoms such as fatigue, sleep disturbances, cognitive dysfunction and mood disturbances are often seen in patients with FM as well [2–5]. Indeed, a substantial overlap exists between FM and CFS and it has been reported that 43–70% of CFS patients also meet the diagnostic criteria for fibromyalgia [2–6]. An increasing amount

of scientific evidence indicates that overlapping conditions such as CFS and FM are bound by a common pathophysiological mechanism of central sensitization [7–10]. Central sensitization is defined as an increased responsiveness of neurons within the central nervous system to nociceptive and nonnociceptive stimuli inducing hyperalgesia and allodynia [11]. In other words, the clinical outcome of central sensitization is an increased responsiveness to various peripheral stimuli including mechanical pressure, chemical substances, light, sound, cold, heat and electrical stimuli [9]. In this regard, muscle metabolites causing muscle fatigue can also act as peripheral stimuli, maintaining – whether not

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together with several other stimuli – the process of central sensitization [12]. Indeed, the presence of abnormalities in peripheral muscles has been demonstrated both in patients with CFS [13] and FM [12]. Our clinical experience indicates that CFS patients (with or without comorbid FM) are more rapidly exhausted than healthy people and many of them complain of muscle fatigue and abnormally slow recovery, especially of the upper limb muscles during and after activities of daily living such as combing and washing hair, ironing, cooking and cleaning (windows) among others. This has important implications for maintaining independence in these patients. Nevertheless, upper limb muscle recovery has never been subjected to research in these patients. Furthermore, disease heterogeneity and the effect of comorbid illnesses such as FM have not yet been studied in relation to recovery of muscle function in CFS. Previous research on the lower limbs has shown delayed muscle recovery following exercise in patients with CFS [14] but normal recovery in patients with FM [15]. Therefore, in this study, we examine recovery of upper limb muscle function from a fatiguing exercise in CFS patients with and without comorbid FM and compare their results with a healthy age-, body mass index- and gender-matched inactive control group. We hypothesized that both CFS patients with and without FM would present with delayed upper limb muscle recovery compared with the control group.

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Participants and assessments

sis of FM was identified using a questionnaire to determine whether they fulfilled the American College of Rheumatology (ACR) 2010 criteria for fibromyalgia [17]. Healthy [pain-free and without any (chronic) disease] inactive control persons were relatives, friends or acquaintances of researchers, students, university personnel or patients participating in the study. ‘Inactive’ was defined as working in an occupation that did not require moderate to intense physical labour and performing a maximum of 3 h of moderate physical activity/week. Moderate physical activity is defined as activity demanding at least the threefold of the energy spent passively [18]. In order to preclude confounding factors, participants could not be pregnant or until 1 year postnatal. Furthermore, all participants, if applicable, were asked to stop anti-depressive, anti-epileptic and opioid pain-medication 2 weeks prior to study participation and were asked not to undertake physical exertion, and to refrain from taking analgesics and consuming caffeine, alcohol or nicotine on the morning of the assessments. An a priori sample size calculation was performed with the program G*Power 3.1.5 (Kiel, Germany) [19] based on the results of a study by Paul et al. [14] on peripheral muscle recovery of the quadriceps muscle group in CFS patients. The a priori calculation revealed that a total sample size of at least nine subjects would provide a 97% power with a = 005 to detect a statistically significant difference in upper limb muscle recovery between the three groups. The post hoc power analysis indicated a power of > 99% (total n = 78 and a = 005). All assessments were performed by the same researchers who were blinded to whether participants were patients or controls. After collecting personal characteristics (age, gender, disease duration and FM criteria) and checking for the presence of possible confounders participants’ height and weight were measured. Next, they performed a fatiguing exercise test and subsequent recovery measures. During the recovery period participants filled out the Tampa Scale for Kinesiophobia (TSK). Finally, at the end of the assessment session, the success of assessor blinding was examined by asking whether the assessor thought the participant belonged to the patient (CFS or CFS+FM) or control group.

The study sample consisted of patients with a diagnosis of CFS who were split up into a group of patients with and without comorbid FM (CFS+FM and CFS respectively) and a group of healthy inactive control persons. Each study participant had to be Dutch speaking and aged between 18 and 65 years. Patients with CFS were recruited via a private practice for internal medicine and through advertisements placed in the newsletter of a local patient support group, and calls during patient information sessions. Written confirmation of a CFS diagnosis as defined by the United States Centres for Disease Control and Prevention (CDC) 1994 criteria for CFS [16] was required from each patient’s physician. The comorbid diagno-

Fatiguing exercise test and recovery measurements. Recovery from fatiguing exercise was measured using a hydraulic hand dynamometer (Saehan Corporation, Masan, Japan) which is supplied with an adjustable handle and an analogous reproduction of the delivered power in kilogram-force (kgf). Participants were asked to sit on a chair while holding the dynamometer in their non-dominant hand with the elbow flexed at 90° and the forearm in neutral position. First, participants were instructed to grip the instrument as hard as possible [isometric maximum voluntary contraction (MVC)] in three consecutive attempts. They were verbally

Methods Study design and setting This study was designed as a blinded case–control study in line with the STROBE Statement (http://www.strobe-statement. org/). All assessments took place at the Pain in Motion research lab of the Artesis University College Antwerp and the Vrije Universiteit Brussel between February 2011 and December 2012. The study protocol was approved by the ethics committees of the University Hospital Brussels/Vrije Universiteit Brussel and the University Hospital Antwerp.

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encouraged in a standardized way during each contraction to promote maximal contractions. The highest peak force of three attempts was stored for subsequent analysis (baseline MVC). Next, every participant performed a fatiguing exercise test consisting of 18 maximum contractions using a 50% duty cycle (5 s contraction, 5 s rest). After the fatiguing exercise test (recovery phase), participants were instructed to make single 5 s isometric MVCs at time intervals of 0, 5, 10, 15, 20, 30 and 45 min post-exercise. These values were converted into percentages of baseline MVC with the latter being taken as 100%. For statistical analyses, the recovery data were split into three sections. MVCstart equals the MVC at time interval 0 min postexercise, MVCmid equals the mean of the MVCs at time interval 5–30 min post-exercise, and MVCend equals the MVC at time interval 45 min post-exercise. Self-reported questionnaire. The TSK-Dutch version was used to assess the fear of (re)injury due to movement [20]. The TSKDutch version was found to be reliable and valid [21–23].

Statistical analysis Data analyses were performed using the Statistical Package for Social Sciences 20.0 for Windows (SPSS Inc., Chicago, IL, USA). Normality of the variables was tested using the Kolmogorov– Smirnov goodness of fit test and through visual inspection of the histograms and distribution graphs. Comparability of the groups was studied with a Pearson Chi-Square test for gender and with a one-way independent analysis of variance (ANOVA) for age, body mass, height, body mass index and disease duration. Recovery of upper limb muscle function was compared between the groups with a 3 9 3 mixed factorial ANOVA with group (CFS, CFS+FM, and CON) and time (MVCstart, MVCmid, and MVCend) being the between- and within-subjects factor respectively. Bonferroni corrected post hoc comparisons were performed when a main effect for group was found. When a main effect for time was found, a post hoc one-way repeated measures ANOVA with time as within-subjects factor was performed for every group separately. Furthermore, group 9 time interaction effects were examined. A one-way independent ANOVA was performed to compare baseline MVC and percentage of baseline MVC at min 0 post-exercise among the groups. To examine the fatigability of the exercise, the difference between baseline MVC and MVC immediately postexercise was analysed in every group with a Paired-Samples ttest. To examine possible lack of effort due to kinesiophobia, a Pearson’s correlation analysis was performed between participant’s score on the TSK and all MVC-values. For all comparisons, a two-sided P < 005 was considered statistically significant. Data are reported as means  SD

within the text and the tables, and as means  SEM in the figures.

Results Group characteristics Thirty CFS+FM patients, 18 CFS-only patients and 30 healthy inactive controls were included, meaning that 625% of the included CFS patients also met the ACR 2010 criteria for FM. Demographic data of the three study samples are listed in Table 1. The groups were comparable for gender distribution, age, body weight and body mass index (P > 005), but not for body height [F(2,75) = 469, P=0012]. Disease duration was not significantly different (P = 10) between both patient groups.

Maximum voluntary contraction in the chronic fatigue syndrome, CFS+FM and control group The mean MVC baseline was 2893 ( 774) kgf for the CFS+FM, 3283 ( 703) kgf for the CFS, and 3370 ( 1005) kgf for the control group. There was no significant difference [F (2,75) = 254, P = 0086] among the groups for baseline MVC. Immediately after the fatiguing exercise mean MVCs were 1460 ( 521) kgf for the CFS+FM, 1778 ( 588) kgf for the CFS, and 2020 ( 617) kgf for the control group. This decline

Table 1 Demographic data of the study samples CFS (n = 18)

CFS+FM (n = 30)

CON (n = 30)

Age (years)†

4056  1246

4017  1067

3727  1454

Gender (% female)‡

9444

9767

8333

Body mass (kg)†

7061  1528

6837  1273

7060  1569

Height (cm)†

16794  579

16600  515

17060  647*

Body mass index†

2505  532

2478  430

2416  466

15406  18651

13497  10353

Disease duration (months)†

000  000**

CFS, patients with chronic fatigue syndrome; CFS+FM, patients with chronic fatigue syndrome + fibromyalgia; CON, healthy inactive controls. Values are means  SD or numbers. * Significant difference between CFS+FM and CON (P < 001). ** Significant difference between both CFS+FM and CFS vs. CON (P < 0001). † Statistical analyses were performed using a one-way independent analysis of variance. ‡ Pearson’s Chi-Square test.

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in maximal force was significant in the three groups [t (29) = 1202, P < 0001; t(17) = 1091, P < 0001; and t (29) = 1085, P < 0001 respectively]. When expressed as percentages of baseline MVC, mean MVC-values immediately post-exercise were 5050 ( 1513)% for the CFS+FM, 5433 ( 1449)% for the CFS and 6077 ( 1316)% for the control group. Comparing these values among the three groups led to a significant difference between the CFS+FM and the control group (P = 002). There were no other statistically significant differences among the groups (P > 005).

Upper limb recovery from fatiguing exercise in the chronic fatigue syndrome, CFS+FM and control group Figure 1 depicts the recovery capacity and pattern of upper limb muscle function of the non-dominant hand in the CFS+FM, CFS and control group. The analyses revealed significant main effects for group [F(2,75) = 902, P < 0001] and time [F(136,10177) = 32241, P < 0001], but no significant group 9 time interaction effect [F(271,10177) = 169, P = 0178] was found. Post hoc analyses indicated a significant difference in recovery capacity between the CFS+FM and the control group (P < 0001). No significant differences were observed between the CFS and the control group (P = 05), nor among both patient groups (P = 0081). A post hoc oneway repeated measures ANOVA that was carried out in the three groups separately to get a better view on the recovery pattern, confirmed the significant main effect for time

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(P < 0001) in each group. Post hoc Bonferroni corrected multiple comparisons revealed a significant difference between MVCstart and MVCmid (P < 0001), MVCstart and MVCend (P < 0001), and MVCmid and MVCend (P = 0013) in the CFS+FM group. In the CFS-only and control group, significant differences were found between MVCstart and MVCmid (P < 0001 in both groups), and MVCstart and MVCend (P < 0001 in both groups), but not between MVCmid and MVCend (P = 0066 and P = 0268 in the CFS and control group respectively). Correlations between participants’ score on the TSK and all MVC-values were examined to investigate if a lack of effort due to kinesiophobia was present. No significant correlations were found in any of the three groups (P > 005).

Success of assessor blinding In the CFS group (CFS+FM and CFS-only) the assessors assumption regarding disease status was correct in 625% of the cases (30 of 48). In the control group, the assessor guessed correctly in 90% of the cases (27 of 30).

Discussion In this study, upper limb muscle recovery following a fatiguing exercise was investigated for the first time in CFS patients. In addition, as CFS patients were subgrouped into CFS-only and CFS+FM patients, these findings underline the importance of disease heterogeneity in CFS. We found no significant difference among the three groups (CFS, CFS+FM and controls) for baseline MVC of the nondominant hand. Interestingly, a significant worse recovery of upper limb muscle function from the fatiguing exercise was found in the CFS+FM group compared with the control group, but no difference was found between the CFS-only and the control group.

Maximum voluntary contraction

Figure 1 Recovery capacity and pattern of upper limb muscle function of the non-dominant hand in chronic fatigue syndrome (CFS) patients (n = 18), CFS+FM patients (n = 30) and healthy controls (n = 30). Values are means  SEM. CFS = patients with chronic fatigue syndrome; CFS+FM = patients with chronic fatigue syndrome + fibromyalgia; CON = healthy inactive controls.

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Several studies have examined MVC in individuals with CFS [14,24–31]. The results of the present study demonstrate no significant difference in maximum voluntary muscle (nondominant handgrip) strength between patients with CFS, patients with CFS+FM, and healthy controls. Although there is controversy in the literature about MVC in CFS patients compared with healthy controls, the results of this study are consistent with most studies that examined this parameter in these patients [24,27–31]. The few conflicting results that are found in literature may be due to disease heterogeneity (including the presence of comorbid FM and the use of different diagnostic criteria for CFS), measurement of different muscle groups (significant differences among patients and controls were primarily found when the quadriceps muscle group was tested

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[14,26]), composition of the control group (inactive vs. active) and test side (dominant vs. non-dominant side).

Recovery of upper limb muscle function Regarding recovery of peripheral muscle function, the results demonstrate that patients with CFS+FM fail to recover properly from a fatiguing exercise of the upper extremity. Recovery was significantly delayed in this patient group, whereas in patients with CFS-only there was no difference compared with the inactive control group. In a previous study, Paul et al. [14] also showed a significant recovery delay of the quadriceps muscle group in CFS patients, while recently Srikuea et al. [15] found no difference in post-exercise MVCs between FM patients and controls. The difference in tested muscle group (knee extensors vs. finger flexors) and limb (lower vs. upper) and the disease heterogeneity (CFS+FM, CFS-only, FM-only) may (partly) account for the difference in results with our study. Several mechanisms may cause or contribute to the delayed recovery of muscle function seen in the CFS+FM group. First, these patients began the recovery phase at a lower per cent of their baseline MVC compared to the CFS and control group. This suggests that a worse muscle endurance during exercise might be a contributing factor. Furthermore, in patients with CFS, the presence of impaired function of transporter mechanisms that remove intracellular acid following exercise is presumed [13,32]. This acid transporter dysfunction is possibly related to autonomic dysfunctions that are frequently seen in CFS patients [13], thus also suggesting the involvement of a vascular phenomenon. Similarly, in patients with FM altered microcirculation (reduced capillary density and permeability and structural changes in the capillary endothelium) is observed, which impacts upon the muscles ability to remove waste products [15]. In addition, mitochondrial oxidative function may be affected in FM [15], whereas in patients with CFS this has been found to be comparable with matched controls in different muscles [13,33–36]. It is possible that this mitochondrial (dys)function accounts (partly) for the difference in recovery of muscle function observed in CFS patients with and without comorbid FM. Besides these peripheral mechanisms it is likely that central mechanisms are involved as well. Ciubotariu et al. [37] showed that experimental muscle pain decreases the motor activity of both the painful and other active synergistic muscles during the recovery period of a fatiguing isometric exercise. A pain-related inhibitory mechanism controlling the motor neurons might form the basis of this disadvantageous pain-fatigue interaction. Our results suggest that CFS patients should sufficiently alternate between physically and mentally demanding tasks in their activities of daily living. Furthermore, they should make sure not to perform the same physically demanding task for

extended periods, thus avoiding the task becomes to exhaustive. These recommendations might be respected by health professionals working with all CFS patients since our results underline the presence of a major heterogeneity in this disease and the presence of comorbidities is not always known.

Study strengths and limitations This study has several strengths as well as a few study limitations which require being mentioned. First, we only tested 45 min into the recovery phase. In the CFS+FM group, a significant increase in recovery was found during the last part of the recovery phase (between MVCmid and MVCend) which was not significant in the other groups. It is possibly that if we would have tested further into the recovery phase, we would have seen the CFS+FM patients catching up with the other groups. Second, the results of this study represent changes in voluntary muscle contraction. It is possible that if we would have used electrical stimulation to look at what extent the upper limb is able to recover, we would have found other results. However, this would mean that results would have been less translatable to daily activities because voluntary force production is the only force that patients can rely on during everyday situations. In addition, after the fatiguing exercise both patients and controls showed a significant decline in the force produced by MVC. This suggests that both patient groups produced MVCs. Moreover, no significant correlations were found between the score on the TSK and all MVC-values in any of the three groups. This ensures that no lack of effort due to kinesiophobia was present and thus further supports the assumption that patients produced maximal contractions. Besides these limitations, this study also has several strengths. The most important one is that our control group was matched to both patient groups for age, gender and body mass index. Both CFS groups were also matched for disease duration. Healthy control persons had to be inactive because CFS patients are known to have a more sedentary lifestyle. This way, observed differences could not be due to better trained muscles or a higher activity level of the control persons. Other important strengths of this study were that it seemed sufficiently powered and that we reduced the heterogeneity of the disease by including CFS patients according to the same strict diagnostic criteria and in addition dividing this group based on FM comorbidity. Furthermore, we also anticipated sources of bias like pregnancy; use of medication, caffeine, alcohol and nicotine; and execution of physical exertion on the days of the assessments. Finally, we attempted to blind the assessor regarding participants’ disease status. However, blinding was only successful in 375% of the patients and in 10% of the controls. In summary, maximal handgrip strength at the non-dominant side was not different among CFS patients (with and

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without FM) and controls. However, the results demonstrate that CFS+FM but not CFS-only patients fail to recover properly from a fatiguing exercise of the upper limb. We conclude that CFS is a heterogeneous disorder suggesting that reducing the heterogeneity of the disorder in future research is important to make progress towards a better understanding and uncovering of mechanisms regarding the nature of divers impairments in these patients. Acknowledgements The study was funded by ME Research UK, a national charity funding biomedical research into Myalgic Encephalomyelitis/ Chronic Fatigue Syndrome. Mira Meeus is awardee of the 2012 early research career grant of the International Association for the Study of Pain (IASP), funded by the Scan│Design Foundation by INGER & JENS BRUUN. Jo Nijs is holder of the Chair ‘Exercise immunology and chronic fatigue in health and disease’ funded by the European College for Decongestive Lymphatic Therapy, the Netherlands. Kelly Ickmans is a research fellow of ME Research UK. The authors thank Tinne Boey and Laura van Weijnen for their aid in the data input. None of the authors has any conflict of interest. Authors’ contributions Kelly Ickmans: acquisition of data, analysed data, drafted and wrote manuscript. Mira Meeus: designed study, revised the manuscript critically. Margot De Kooning: acquisition of data, revised the manuscript critically. Luc Lambrecht: acquisition of data, revised the manuscript critically. Jo Nijs: designed study, drafted paper, revised the manuscript critically. Address Pain in Motion Research Group, Department of Human Physiology and Physiotherapy, Faculty of Physical Education & Physiotherapy, Vrije Universiteit Brussel, Building L, Pleinlaan 2, B-1050 Brussel, Belgium (K. Ickmans, M. De Kooning, J. Nijs); Pain in Motion Research Group, Division of Musculoskeletal Physiotherapy, Department of Health Care Sciences, Artesis University College Antwerp, Van Aertselaerstraat 31, B-2170 Antwerp, Belgium (K. Ickmans, M. Meeus); Pain in Motion Research Group, Department of Physical Medicine and Physiotherapy, University Hospital Brussels, Laarbeeklaan 101, B-1090 Brussels, Belgium (K. Ickmans, M. De Kooning, J. Nijs); Rehabilitation Sciences and Physiotherapy, Faculty of Medicine & Health Sciences, Ghent University, Campus Heymans, De Pintelaan 185, B-9000 Gent, Belgium (M. Meeus); Pain in Motion Research Group, Department of Rehabilitation Sciences and Physiotherapy, Faculty of Medicine & Health Sciences, University of Antwerp, Campus Drie Eiken, Universiteitsplein 1, B-2610 Antwerp, Belgium (M. Meeus); Department of Neurology, Faculty of Medicine, University of Antwerp (UA), Campus

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Drie Eiken, Universiteitsplein 1, B-2610 Antwerp, Belgium (M. De Kooning); Private practice for internal medicine, Koning Albertlaan 101, B-9000 Ghent, Belgium (L. Lambrecht). Correspondence to: Jo Nijs, Faculty of Physical Education & Physiotherapy, Vrije Universiteit Brussel, Medical Campus Jette, Building F-Kine, Laarbeeklaan 103, BE-1090 Brussels, Belgium. Tel.: +3224774489; fax +3226292876; e-mail [email protected] Received 25 July 2013; accepted 5 November 2013 References 1 Meeus M, Nijs J, De Meirleir KD. Chronic musculoskeletal pain in patients with the chronic fatigue syndrome: a systematic review. Eur J Pain 2007;11:377–86. 2 Ciccone DS, Natelson BH. Comorbid illness in women with chronic fatigue syndrome: a test of the single syndrome hypothesis. Psychosom Med 2003;65:268–75. 3 Goldenberg DL, Simms RW, Geiger A, Komaroff AL. High frequency of fibromyalgia in patients with chronic fatigue seen in a primary care practice. Arthritis Rheum 1990;33:381–7. 4 Mease P, Arnold LM, Choy EH, Clauw DJ, Crofford LJ, Glass JM, et al. Fibromyalgia syndrome module at OMERACT 9: domain construct. J Rheumatol 2009;36:2318–29. 5 Fitzcharles MA, Ste-Marie PA, Pereira JX. Fibromyalgia: evolving concepts over the past 2 decades. CMAJ 2013;185:645–51. 6 Bradley LA, McKendree-Smith NL, Alarcon GS. Pain complaints in patients with fibromyalgia versus chronic fatigue syndrome. Curr Rev Pain 2000;4:148–57. 7 Banic B, Petersen-Felix S, Andersen OK, Radanov BP, Villiger PM, Arendt-Nielsen L, et al. Evidence for spinal cord hypersensitivity in chronic pain after whiplash injury and in fibromyalgia. Pain 2004;107:7–15. 8 Meeus M, Nijs J. Central sensitization: a biopsychosocial explanation for chronic widespread pain in patients with fibromyalgia and chronic fatigue syndrome. Clin Rheumatol 2007;26:465–73. 9 Nijs J, Van Houdenhove B, Oostendorp RA. Recognition of central sensitization in patients with musculoskeletal pain: application of pain neurophysiology in manual therapy practice. Man Ther 2010;15:135–41. 10 Yunus MB. Fibromyalgia and overlapping disorders: the unifying concept of central sensitivity syndromes. Semin Arthritis Rheum 2007;36:339–56. 11 Meyer RA, Campbell IT, Raja SN. Peripheral neural mechanisms of nociception. In: Wall PD, Melzack R, editors. Textbook of Pain. Edinburgh: Churchill Livingstone; 1995: pp 13–44. 12 Vierck CJ Jr. Mechanisms underlying development of spatially distributed chronic pain (fibromyalgia). Pain 2006;124:242–63. 13 Jones DE, Hollingsworth KG, Taylor R, Blamire AM, Newton JL. Abnormalities in pH handling by peripheral muscle and potential regulation by the autonomic nervous system in chronic fatigue syndrome. J Intern Med 2010;267:394–401. 14 Paul L, Wood L, Behan WM, Maclaren WM. Demonstration of delayed recovery from fatiguing exercise in chronic fatigue syndrome. Eur J Neurol 1999;6:63–9. 15 Srikuea R, Symons TB, Long DE, Lee JD, Shang Y, Chomentowski PJ, et al. Association of fibromyalgia with altered skeletal muscle

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16

17

18

19

20 21

22

23

24

25

26

characteristics which may contribute to postexertional fatigue in postmenopausal women. Arthritis Rheum 2013;65:519–28. Fukuda K, Straus SE, Hickie I, Sharpe MC, Dobbins JG, Komaroff A. The chronic fatigue syndrome: a comprehensive approach to its definition and study. International Chronic Fatigue Syndrome Study Group. Ann Intern Med 1994;121:953–9. Wolfe F, Clauw DJ, Fitzcharles MA, Goldenberg DL, Katz RS, Mease P, et al. The American College of Rheumatology preliminary diagnostic criteria for fibromyalgia and measurement of symptom severity. Arthritis Care Res (Hoboken) 2010;62:600–10. Bernstein MS, Morabia A, Sloutskis D. Definition and prevalence of sedentarism in an urban population. Am J Public Health 1999;89: 862–7. Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 2007;39:175–91. Kori SH, Miller RP, Todd DD. Kinesiophobia: a new view of chronic pain behavior. Pain Manage 1990;1990:35–43. Crombez G, Vlaeyen JW, Heuts PH, Lysens R. Pain-related fear is more disabling than pain itself: evidence on the role of pain-related fear in chronic back pain disability. Pain 1999;80:329–39. Goubert L, Crombez G, Van Damme S, Vlaeyen JWS, Bijttebier P, Roelofs J. Confirmatory factor analysis of the Tampa scale, for Kinesiophobia - Invariant two-factor model across low back pain patients and fibromyalgia patients. Clin J Pain 2004;20:103–10. Vlaeyen JW, Kole-Snijders AM, Boeren RG, van Eek H. Fear of movement/(re)injury in chronic low back pain and its relation to behavioral performance. Pain 1995;62:363–72. Gibson H, Carroll N, Clague JE, Edwards RH. Exercise performance and fatiguability in patients with chronic fatigue syndrome. J Neurol Neurosurg Psychiatry 1993;56:993–8. Kent-Braun JA, Sharma KR, Weiner MW, Massie B, Miller RG. Central basis of muscle fatigue in chronic fatigue syndrome. Neurology 1993;43:125–31. Fulcher KY, White PD. Strength and physiological response to exercise in patients with chronic fatigue syndrome. J Neurol Neurosurg Psychiatry 2000;69:302–7.

27 Lloyd AR, Hales JP, Gandevia SC. Muscle strength, endurance and recovery in the post-infection fatigue syndrome. J Neurol Neurosurg Psychiatry 1988;51:1316–22. 28 Lloyd AR, Gandevia SC, Hales JP. Muscle performance, voluntary activation, twitch properties and perceived effort in normal subjects and patients with the chronic fatigue syndrome. Brain 1991;114 (Pt 1A):85–98. 29 Rutherford OM, White PD. Human quadriceps strength and fatiguability in patients with post viral fatigue. J Neurol Neurosurg Psychiatry 1991;54:961–4. 30 Sacco P, Hope PA, Thickbroom GW, Byrnes ML, Mastaglia FL. Corticomotor excitability and perception of effort during sustained exercise in the chronic fatigue syndrome. Clin Neurophysiol 1999;110:1883–91. 31 Samii A, Wassermann EM, Ikoma K, Mercuri B, George MS, O’Fallon A, et al. Decreased postexercise facilitation of motor evoked potentials in patients with chronic fatigue syndrome or depression. Neurology 1996;47:1410–4. 32 Jones DE, Hollingsworth KG, Jakovljevic DG, Fattakhova G, Pairman J, Blamire AM, et al. Loss of capacity to recover from acidosis on repeat exercise in chronic fatigue syndrome: a case– control study. Eur J Clin Invest 2012;42:186–94. 33 Lane RJ, Barrett MC, Taylor DJ, Kemp GJ, Lodi R. Heterogeneity in chronic fatigue syndrome: evidence from magnetic resonance spectroscopy of muscle. Neuromuscul Disord 1998;8:204–9. 34 Wong R, Lopaschuk G, Zhu G, Walker D, Catellier D, Burton D, et al. Skeletal muscle metabolism in the chronic fatigue syndrome. In vivo assessment by 31P nuclear magnetic resonance spectroscopy. Chest 1992;102:1716–22. 35 McCully KK, Smith S, Rajaei S, Leigh JS Jr, Natelson BH. Blood flow and muscle metabolism in chronic fatigue syndrome. Clin Sci (Lond) 2003;104:641–7. 36 Barnes PR, Taylor DJ, Kemp GJ, Radda GK. Skeletal muscle bioenergetics in the chronic fatigue syndrome. J Neurol Neurosurg Psychiatry 1993;56:679–83. 37 Ciubotariu A, Arendt-Nielsen L, Graven-Nielsen T. Localized muscle pain causes prolonged recovery after fatiguing isometric contractions. Exp Brain Res 2007;181:147–58.

European Journal of Clinical Investigation Vol 44

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Recovery of upper limb muscle function in chronic fatigue syndrome with and without fibromyalgia.

Chronic fatigue syndrome (CFS) patients frequently complain of muscle fatigue and abnormally slow recovery, especially of the upper limb muscles durin...
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