Ava i l ab l e on l i ne a t www.sc i enced i r ec t . com

ScienceDirect

Journal of Crohn's and Colitis (2013) xx, xxx–xxx

CROHNS-00884; No of Pages 7

Lower extremity mobility limitation and impairedmuscle function in women withulcerative colitis☆,☆☆

Cyrla Zaltmana,⁎, Valeria Bender Brauliob, Rosângela Outeiral c,Tiago Nunesd, Carmen Lucia Natividade de Castroe

a Division of Gastroenterology of the University Hospital of the Federal University of Rio de Janeiro (UFRJ),Department of Internal Medicine, Rio de Janeiro, Brazilb Division of Nutrition and Metabolism of the University Hospital of the Federal University of Rio de Janeiro (UFRJ),Department of Internal Medicine, Rio de Janeiro, Brazilc Division of Nutrition of the University Hospital of the Federal University of Rio de Janeiro (UFRJ), Department ofInternal Medicine, Rio de Janeiro, Brazild Nutrition and Immunology Chair, ZIEL Research Center for Nutrition and Food Sciences, Technical University of Munich,Freising-Weihenstephan, Germanye Division of Physical Medicine and Rehabilitation of the University Hospital of the Federal University of Rio de Janeiro(UFRJ), Department of Internal Medicine, Rio de Janeiro, Brazil

Received 19 September 2013; received in revised form 6 November 2013; accepted 8 November 2013

☆ Author contributions: Cyrla ZaltmValeria Bender Braulio made all statistall human materials and made the phystudy. Tiago Nunes made a critical rev☆☆ Supported by: Fundação de Amp

⁎ Corresponding author at: ServiçoPaulo Rocco 255, Ilha do Fundão, Rio d

E-mail address: c.zaltman@gmai

1873-9946/$ - see front matter © 2013http://dx.doi.org/10.1016/j.crohns.20

Please cite this article as: Zaltman C, eJ Crohns Colitis (2013), http://dx.doi

KEYWORDSUlcerative colitis;Muscle function;Physical performance;Body composition

Abstract

Background and aim: Fatigue, weakness and musculoskeletal manifestations are associatedwith IBD. An impaired nutritional status and a reduced physical activity can contribute to theseclinical outcomes, impacting quality of life and increasing disability. This study aims to assessmuscle strength and lower limb physical performance in female UC patients, taking into

consideration disease activity, body composition and habitual physical activity.Methods: A case-control study was performed including 23 UC female outpatients and 23 age-and BMI-matched healthy women as controls. Quadriceps strength (QS), handgrip strength(HGS), physical performance based measures (five repetitions sit-up test and 4 meter gait speedtest), body composition (bioelectrical impedance analysis, anthropometry), and habitualphysical activity (HPA) levels were assessed.

an was involved in study design, editing the manuscript and provided financial support for this work.ical analyses and was involved in editing the manuscript. Rosângela Outeiral provided the collection ofsical evaluation. Carmen Lúcia Natividade de Castro was involved in coordinating and designing of theiew of the manuscript and was involved in writing the final draft.aro a Pesquisa do Estado do Rio de Janeiro — FAPERJ.de Gastroenterologia, 4° andar, Hospital Universitário Clementino Fraga Filho, Rua Prof. Rodolphoe Janeiro 21941-913, RJ, Brazil. Tel./fax: +55 21 2562 2326.l.com (C. Zaltman).

European Crohn's and Colitis Organisation. Published by Elsevier B.V. All rights reserved.13.11.006

t al, Lower extremitymobility limitation and impairedmuscle function in womenwith ulcerative colitis,.org/10.1016/j.crohns.2013.11.006

2 C. Zaltman et al.

Please cite this article as: Zaltman C, eJ Crohns Colitis (2013), http://dx.doi

Results: UC group had decreased QS (−6%; P = 0.012), slower sit-up test (−32%; P = 0.000),slower gait speed (−17% P = 0.002) and decreased HPA level (−30%, P = 0.001) compared withcontrols. No difference in HGS was observed between groups. Logistic regression showed that UCwas an independent factor for decreased QS and slower sit-up test, while HPA was a protectivefactor for impaired gait speed. Multivariate linear regression showed that BMI was independentlyassociated with an improved QS and slower sit-up test in the UC group.Conclusion: Women with UC had decreased lower limb strength and mobility limitations, whichwere associated with BMI and the level of physical activity. Early evaluation of nutritional statusand performance of the lower limbs could identify UC patients with pre-clinical disability whomay benefit from earlier health lifestyle modifications.© 2013 European Crohn's and Colitis Organisation. Published by Elsevier B.V. All rights reserved.

t al, Lower extremitymobility l.org/10.1016/j.crohns.2013.11

1. Introduction

Ulcerative colitis (UC) is a chronic inflammatory bowel diseasethat affects segments of colonic and rectal mucosa in acontinuous pattern. UC has an intermittent disease coursewith periods of exacerbated symptoms, and periods that arerelatively symptom-free.1 The clinical presentation dependson the extent and severity of the intestinal involvement andthe presence of extra-intestinal manifestations.2

Even though, UC patients often complain of musculoskel-etal symptoms,muscleweakness is one of the least understoodextra-intestinal manifestations associated with inflammatorybowel diseases (IBD). In this regard, very few studies haveinvestigated the involvement of peripheral muscle function inIBD patients. Most of the available data, however, showcontradictory results. Geerling et al.,3 for instance, examinedthe lower limb muscle strength in 30 UC patients of bothgenders and reported no significant differences in hamstringsor quadriceps strength in comparison with age- and sex-matched controls. In contrast, Valentini et al.1 foundsignificant reduction in handgrip strength (HGS) in 50 UCpatients compared with controls. More recently, Werkstetteret al.4 detected preserved HGS, but only in female UCpatients. Importantly, even though upper and lower limbfunctions are both central components of daily living tasks,there are currently no studies evaluating the physicalperformance of the lower limbs in patients with UC.

The present study, therefore, aims to reassess the upper andlower limb muscle strength in patients with UC compared withage, gender and body mass index (BMI)-matched healthyindividuals. In addition, performance-based measures of mobil-ity and the overall physical activity were also evaluated.

2. Subjects and methods

2.1. Ethical considerations

The study protocol was approved by the Ethical Committeeof the University Hospital of the Federal University of Rio deJaneiro (HUCFF-UFRJ), and informed consents were obtain-ed from all subjects.

2.1.1. Study design and the studied populationA case-control study including UC female patients and BMIand age-matched healthy women was designed. Patients and

imit.006

controls were recruited at the gastroenterology outpatientclinic of the HUCFF-UFRJ. UC Patients had an establisheddiagnosis by standard clinical, radiological, histological, andendoscopic criteria.5,6 The matched controls were recruitedamong healthy patient's relatives and hospital staff.

All subjects were above 18 and below 65 years of age,non-smokers and had a sedentary life style, which wasdefined as the absence of a programmed physical activity(≥30 min) on most days of the week.7 Patients and controlswith any chronic disease (even under medical treatment),previous total colectomy or ileostomy, current pregnancy orbreastfeeding, and those with muscle and joint abnormali-ties (which could limit the practice of physical activity) wereexcluded. Subjects with less than 3 years of school or thosewho were, for any reason, unable to read, understand, oranswer questionnaires were also excluded. A complete bloodanalysis was performed in all subjects and the presence ofhemoglobin levels below 12 g/dL was also considered anexclusion criterion. All subjects exhibited normal plasmaalbumin levels (4.2 ± 3.4 g/dL).

Disease activity was assessed according to the partialMayo score.8 Disease location, phenotype and age of diseasediagnosis were determined according to the MontrealClassification.9

2.2. Body composition

Body composition was assessed using anthropometry andbioelectrical impedance analysis (BIA). Subjects were studiedat least 4 h after their last meal, and had emptied theirbladders before their body weight and height were recorded.BIAwas undertakenwith a tetrapolar bioanalyzer device (Model310, Biodynamics Corp, Seattle, WA-USA). Measurements wereundertaken as previously described.10 BMI was calculated asweight (kg) divided by squared height (meters). Subjects wereclassified as underweight (BMI b 18.50 kg/m2), normal weight(BMI = 18.50–24.99 kg/m2), overweight (BMI ≥ 25.00 kg/m2)or obese (BMI ≥ 30.00 kg/m2), according to the World HealthOrganization.11 Fat-free mass (FFM) and fat mass (FM) werecalculated from the measurements of resistance made at50 kHz using the formula provided by the instrument manufac-turer. In addition, the resistance directly read from theimpedance device was considered along with height, weight,and age in the obesity-specific equation published by Segal etal.12 The FFM index (FFMI) was derived as FFM (kg) divided byheight (m) squared (kg/m2).

ation and impairedmuscle function in womenwith ulcerative colitis,

3Lower extremity performance and ulcerative colitis

2.2.1. Muscle strengthMaximum non-dominant handgrip strength (HGS) was evaluat-ed using the JAMAR hand dynamometer (Preston, Jackson, MI,USA). The subjects performed the test while sitting comfort-ably with the arm extended along the body.13 Maximalquadriceps strength (QS) was measured in the non-dominantleg with an electro-mechanic chair dynamometer (IsoTesteKroman-Trigher, Brazil). Subjects were asked to seat uprightwith arms crossed in front of the chest. Velcro straps wereapplied tightly across the pelvis. The dynamometer lever armconnected to the strain gaugewas adjusted just proximal to themalleoli.14 The force values were shown at a digital display. Forboth HGS and QS assessments, subjects performed 3 trials, andeach trial was separated by a 1 minute interval. The meanforce was kept. Values below 18.9 kgf were considereddecreased HGS and values below 35.6 kgf were considereddecreased QS according to our sex and age-matched data base(n = 120). For eachmeasurement, the subjects were instructedby a certified physical trainer to perform a maximal isometriccontraction. The trainer was responsible for the test supervi-sion and the maintenance of motivation.

2.2.2. Assessment of physical performanceLower-extremity functional performance was assessed bymeasures of ability to rise from a chair and walking velocitywith the assistance of the same certified physical trainer. Bothtests were measured to the nearest 0.01 s. A digital chronom-eter (Chronometer Kenko Sport Timer, model CR8010, Brazil)was used to measure the time spent on each of the two tests.

2.3. Sit-up test (ST)

To test the ability to rise from a chair, a straight-backedchair was placed next to a wall; participants were asked tofold their arms across their chest and to stand up from thechair one time. If successful, participants were asked tostand up and sit down five times as quickly as possible, andwere timed from the initial sitting position to the finalstanding position at the end of the fifth stand.15 Valuesabove 11.4 s indicate poor performance.16

2.4. Gait speed (GS)

To test walking speed at normal pace, a test track area of4-meter walking course with an additional 2-meter at eitherend was set up. Subjects were instructed to walk at acomfortable pace. Two trials were conducted. In order toavoid interference from the acceleration and decelerationphases of the gait trials, only the data obtained from 2 to 6 mwere considered for statistical analysis. Results are reportedas the mean of the two trials in seconds/4 m or in m/s.17 Avalue below 0.8 m/s indicates walking impairment.18

2.4.1. Habitual physical activity level (HPA)The Brazilian validated version19 of the Baecke question-naire20 was used to evaluate the HPA level and encompassesthree distinct dimensions which are physical activity at work,sport during leisure-time, and other physical activity duringleisure-time excluding sport. It consists of 16 questionsinvolving the three HPA scores related to the previous12 months: (1) occupational physical activity, consisting of

Please cite this article as: Zaltman C, et al, Lower extremitymobility limitJ Crohns Colitis (2013), http://dx.doi.org/10.1016/j.crohns.2013.11.006

eight questions, (2) physical exercise in leisure, consisting offour questions, and (3) leisure and locomotion activities,consisting of four questions. The total score for HPA (rangingfrom 3 to 15 [minimum to maximum value]) is obtained byadding the three scores of the specific groupings of activities.Higher scores indicate more physically active subjects.

2.4.2. Statistical analysisData are presented as mean ± standard deviation (SD),number of subjects, percentage, and as odds ratio (OR)with 95% confidence intervals (95% CI). Statistical analyseswere performed using Package for the Social Sciences(SPSS) for Windows version 16.0 (SPSS, Inc., Chicago, IL).The Kolmogorov– Smirnov test was used to evaluate thenormal distribution of datasets. Student's t-test or Mann–Whitney U test compared data among subjects. Binarylogistic regressions were used to study potential predictorsassociated with muscle strength and physical performancein the sample. Input variables were the presence of UC inthe sample, age, BMI, and habitual physical activity.Multiple linear regression analysis was conducted to assessindependent factors associated with muscle strength andphysical performance in the UC group. Statistical signifi-cance was considered when P b 0.05.

3. Results

3.1. Clinical characteristics and bodycomposition parameters

Table 1 shows the clinical characteristics for the UC subjectsand controls. There were no significant differences in age,body composition and nutritional status between both groups.Sixty-five percent of the UC group had active disease. Of these,93% hadmild tomoderate activity. A high prevalence of obesityplus overweight was found in the recruited UC subjects (61%)and only one patient was underweight (BMI = 16.9 kg/m2) andhad low FFMI (13.2 kg/m2). This patient was in clinicalremission.

3.2. Univariate comparison of muscle strength,physical performance tests and habitual physicalactivity between UC patients and controls

The results for HGS, QS, ST, GS and the HPA evaluation forUC patients and controls are summarized in Fig. 1. QS wassignificantly decreased in UC patients compared withcontrols (−6%). UC patients were significantly slower thancontrols at the ST (−32%) and at the GS test (−17%). Inaddition, HPA levels were significantly decreased in UCpatients compared with controls (−30%). There was nosignificant difference in HGS between both groups.

3.3. Predictors for impaired muscle strength andpoorer physical performance

Multivariate binary logistic regression results evaluating pre-dictors for decreased muscle strength and impaired physicalperformance can be found in Table 2. In this analysis, in thetotal population of UC patients and controls, having the

ation and impairedmuscle function in womenwith ulcerative colitis,

Table 1 Clinical characteristics of the UC group and controls.

Characteristics UC Group (N = 23) Control group (N = 23) P

Age, year, mean ± SDTotal 43.9 ± 10.0 43.9 ± 8.5 1.000Active disease (N = 15) 43.7 ± 11.4Remission (N = 8) 44.2 ± 8.2

Disease activity, N (%)Mild 9(39)Moderate 5(22)Severe 1(4)Remission 8(35)

Disease extension, N (%)Proctitis 12(52)Extensive colitis 7(30)Distal colitis 4(18)

Disease duration, year, median (range)Disease activity (N = 8) 6(0.12–18)Disease remission (N = 15) 12.6(0.12–23)Total (N = 23) 9(0.12–23)

Medication use, N (%), dose5 ASA 19(83), (0.8–4 g/day)Prednisone 9(39), (10–40 mg/day)Azathioprine 4(18), (2–2.5 mg/kg/day)No Medication 1(4)

Body compositionBody mass index, kg/m2 28.0 ± 6.8 29.5 ± 6.6 0.445Free-fat mass, kg 45.2 ± 6.30 44.8 ± 3.5 0.805Fat mass, kg 24.3 ± 12.3 28.6 ± 13.2 0.257

Nutritional status, mean ± SD kg/m2, (%)Underweight 16.9, (4) –, (0) –Normal weight 22.6 ± 1.8, (39) 21.6 ± 0.7 (35) 0.157Overweight 27.5 ± 1.4 (17) 27.15 ± 2.3 (13) 0.838Obesity 34.1 ± 3.7 (39) 35.3 ± 1.9 (52) 0.338

4 C. Zaltman et al.

diagnosis of UC was independently associated with a decreasedQS and a slower ST. No factor was independently associatedwith decreased HGS and HPA was found to be protectiveagainst an impaired GS.

3.4. Multiple linear regression to assess theassociation between disease activity and musclestrength and physical performance in UC patients

Multivariate linear regression results in the UC group can befound in Table 3. Disease activity in this cohort was notcorrelated to changes in muscle strength and physical perfor-mance. In this analysis, BMI was the only factor independentlycorrelated to any outcome (QS and ST). In this regard, forinstance, holding all the other independent variables constant,a gain of one unit of BMI might lead to an average increase of0.3 kgf in QS. In relation to the ST, BMI had the opposite effect,i.e., increases in BMI were directly associated with a slowersit-up test.

4. Discussion

The chronic systemic inflammation that takes place in UChas been previously suggested to affect the muscular

Please cite this article as: Zaltman C, et al, Lower extremitymobility limitJ Crohns Colitis (2013), http://dx.doi.org/10.1016/j.crohns.2013.11.006

performance of patients. Although no direct link betweenIBD-related inflammation and muscle impairment has beendemonstrated, studies on other inflammatory conditionshave shown that higher levels of chronic inflammationmarkers, including interleukin-1,21 interleukin-6,21,22 tumornecrosis factor-alpha22 or CRP21,23 are associated withdecreased muscle strength, lower muscle mass,22 and disabil-ity.21,23 Some mechanisms have been proposed to explain therole of systemic inflammation on muscle function and limitedmobility.24 A possible explanation could be the direct effect ofincreasing levels of IL-6 or TNF-α on skeletal muscle proteinbreakdown with simultaneous decrease in the rate of proteinsynthesis.25,26 Other mechanismmight be the negative impactthat chronic inflammation has on endothelial integrity. A lossof endothelial integrity might promote a reduction in gapjunction communication impacting the coordinated vasodila-tor response required to increase blood flow to deliver oxygenand nutrients for muscle activity.27

In the present study, UC seems to impact mobility andmuscle performance, with women with UC having mild tomoderate mobility limitations compared with gender, ageand BMI-matched healthy controls. These patients haddecreased lower limb strength with normal upper limbperformance. This impairment in physical performance wasevaluated by the gait speed test and the chair stand test,

ation and impairedmuscle function in womenwith ulcerative colitis,

Fig. 1 Handgrip strength (A) and quadriceps strength (B) in kilogram-force, sit-up test in seconds (C), gait velocity in meters persecond (D) and the habitual physical activity score results (E) are presented in the graphics. Groups of patients are shown in differentbars corresponding to controls (CON) and UC patients (UC). Statistical significance was considered when P b 0.05.

5Lower extremity performance and ulcerative colitis

two components of the Short Physical Performance Batterywhich is a widely used tool that measures physicalperformance of the lower limbs. A reduction in mobilityevaluated by these measurements can detect pre-clinicallimitations and predict future disability in non-disabledpeople.17 The detected alterations in physical performancesuggest that UC patients might be under a higher risk todevelop difficulties in the performance of common dailyliving activities.28 In line with these findings, in our cohort,UC patients had lower physical activity levels than controls,which is in agreement with previous work that foundreduced physical activity in UC children and adolescentwith quiescent disease.4

Our results are in accordance with those of Werkstetter etal.4 who also observed preserved upper limb strength in

Table 2 Binary logistic regression to assess predictors for impair

Outcome Variable B

Decreased handgrip strength Presence of UCAge −BMI −Habitual physical activity

Decreased quadriceps strength Presence of UCAge −BMI −Habitual physical activity −

Impaired sit-up test Presence of UCAgeBMIHabitual physical activity

Impaired gait speed Presence of UCAgeBMIHabitual physical activity −

Please cite this article as: Zaltman C, et al, Lower extremitymobility limitJ Crohns Colitis (2013), http://dx.doi.org/10.1016/j.crohns.2013.11.006

female children and adolescents with mild UC with shortdisease duration. In contrast, Valentini et al.1 describedreduced HGS in a group of female adults with UC in remission,but these patients had longer disease duration. Since thedisease duration in our cohort was similar to the latter study,the discrepancy between results may be due to the higherprevalence of malnutrition (40%) in the study by Valentini etal. as it has been shown that grip strength is a sensitivemethodfor detecting nutritional changes.29 Concerning lower limbstrength, our results contradict those of Geerling et al.3 whoshowed similar QS in UC patients compared with healthycontrols. In their study, however, the sample includedpatients with recent UC diagnosis which could indicate thatmuscle strength is not yet affected in early stages of thedisease.

ed muscle strength or mobility (n = 46).

S.E. Odds ratio 95% CI P value

1.234 0.950 3.434 0.534 22.097 0.1940.047 0.041 0.954 0.880 1.035 0.2580.028 0.064 0.972 0.858 1.102 0.6590.092 0.256 1.097 0.663 1.813 0.7192.729 1.155 15.312 1.592 147.269 0.0180.012 0.047 0.989 0.902 1.083 0.8050.161 0.084 0.851 0.722 1.004 0.0560.205 0.256 0.815 0.494 1.345 0.4242.000 0.697 7.389 1.887 28.939 0.0040.030 0.041 1.030 0.950 1.117 0.4680.057 0.059 1.059 0.944 1.188 0.3280.018 0.229 1.018 0.651 1.594 0.9371.368 0.861 3.927 0.726 21.225 0.1120.005 0.040 1.005 0.928 1.087 0.9090.077 0.060 1.080 0.961 1.215 0.1980.305 0.243 0.591 0.392 0.890 0.012

ation and impairedmuscle function in womenwith ulcerative colitis,

Table 3 Multiple linear regression to assess independent factors associated with muscle strength and physical performanceresults in the UC group.

Outcome Variable B SE R2 P

Handgrip strength (kgf) Disease activity −1.519 3.170 −0.107 0.637Age 0.264 0.177 0.374 0.154Body mass index −0.080 0.257 −0.077 0.759Habitual physical activity 0.173 0.853 0.047 0.842

Quadriceps strength (kgf) Disease activity −2.828 1.738 −0.319 0.121Age −0.003 0.097 −0.007 0.975Body mass index 0.301 0.141 0.463 0.045Habitual physical activity 0.378 0.468 0.164 0.430

Sit-up (S) Disease activity 0.825 0.997 0.165 0.419Age 0.012 0.056 0.049 0.830Body mass index 0.188 0.081 0.514 0.030Habitual physical activity 0.127 0.268 0.098 0.642

Gait speed (M/S) Disease activity −0.078 0.088 −0.191 0.388Age 0.000 0.005 0.006 0.982Body mass index 0.002 0.007 0.069 0.776Habitual physical activity 0.039 0.024 0.365 0.120

6 C. Zaltman et al.

The multivariate analysis identified the diagnosis of UCand obesity as two independent factors influencing QS.These factors, however, exert different effects on muscleperformance. In this regard, the presence of UC decreasedmuscle strength and obesity contributed to its increase.When the UC group was analyzed separately, obesity was thesole independent factor associated with QS (protection),regardless of disease activity and HPA. These findings are inline with the study by Hulens et al.30 who found increased QSin obese compared with lean healthy women age- andphysical activity-matched. According to these authors, aplausible explanation for the stronger quadriceps muscle inobese subjects is the training effect of the weight bearingactivities. Regarding the ST, however, increased BMI led tothe opposite effect, and our data show that BMI was stronglyassociated with an impaired ST independently of age,disease activity and physical activity. In fact, mobilitydifficulties commonly described in old age are increasingamong middle-life population, probably also related toincreased rates of obesity.31

Preserved upper limb and reduced lower limb capacitiesare a pattern of progressive disuse of leg muscles becauseupper muscles are more often used in daily living activities. Inthis study, patients with UC seem to have this pattern ofdisuse, which was also observed by Wiroth et al. in adults withCD.32 Nevertheless, there is a lack of studies evaluating thetherapeutic impact of physical exercise on muscle strengthand physical performance in UC patients. To date, only onestudy evaluated the effect of moderate exercise for 10 weeksin UC patients in remission. The authors concluded that therewas a significant improvement in quality of life, without anyrelapse.33 Although there is no clear evidence that exercisehas any effect on the clinical course of IBD, current researchsuggest that low-intensity physical activity has no detrimentaleffect on disease activity and may contribute to a betterquality of life and the prevention of osteoporosis.34

The presentwork has limitations that should be addressed byfuture studies on the topic. First, owing to its cross-sectionaldesign, any causal relationship cannot be definitely established.In this regard, it is known that mobility impairment is a common

Please cite this article as: Zaltman C, et al, Lower extremitymobility limitJ Crohns Colitis (2013), http://dx.doi.org/10.1016/j.crohns.2013.11.006

early stage of disability, but not all functional limitations areexpected to lead to this outcome. Therefore, the relationshipbetweenmuscle function, mobility, disease activity and obesityin UC should be further addressed by large prospective studies.Second, symptoms causing mobility impairment in middle-agedpopulation35 (as lower limb pain and shortness of breath) whichcould function as confounding factors were not collected in thisstudy. Third, the inclusion of only female patients and therelatively small sample size allow the evaluation of factorsassociated with different outcomes but restrict the generaliza-tion of these findings and prevent an accurate determination ofthe magnitude of the risk, given the large confidence intervalsobserved. In this regard, it is important to stress, however, thatthe control group was pair-matched by gender, age and BMI,controlling for themain factors impactingmobility impairment.

In conclusion, our results suggest that female UC patientshave poorer lower limb performance and impaired musclestrength when compared with matched controls. An earlyclinical evaluation of body composition, nutritional statusand physical performance of the lower limbs, therefore, mayidentify UC patients with a pre-clinical stage of disabilitywho may benefit from earlier healthy lifestyle interventions,such as body weight control and a personalized exerciseregimen.

Conflict of interest

No conflict of interest.

References

1. Valentini L, Schaper L, Buning C, Hengstermann S, Koernicke T,Tillinger W, et al. Malnutrition and impaired muscle strength inpatients with Crohn's disease and ulcerative colitis in remission.Nutrition 2008;24:694–702.

2. Mijac DD, Jankovic GL, Jorga J, Krstic MN. Nutritional status inpatients with active inflammatory bowel disease: prevalence ofmalnutrition and methods for routine nutritional assessment.Eur J Intern Med 2010;21:315–9.

ation and impairedmuscle function in womenwith ulcerative colitis,

7Lower extremity performance and ulcerative colitis

3. Geerling BJ, Badart-Smook A, Stockbrugger RW, Brummer RJ.Comprehensive nutritional status in recently diagnosed patientswith inflammatory bowel disease compared with populationcontrols. Eur J Clin Nutr 2000;54:514–21.

4. Werkstetter KJ, Ullrich J, Schatz SB, Prell C, Koletzko B,Koletzko S. Lean body mass, physical activity and quality of lifein paediatric patients with inflammatory bowel disease and inhealthy controls. J Crohns Colitis 2012;6:665–73.

5. Schaap LA, Pluijm SM, Deeg DJ, Harris TB, Kritchevsky SB,Newman AB, et al. Higher inflammatory marker levels inolder persons: associations with 5-year change in muscle massand muscle strength. J Gerontol A Biol Sci Med Sci 2009;64:1183–9.

6. Stange EF, Travis SP, Vermeire S, Beglinger C, Kupcinkas L,Geboes K, et al. European evidence based consensus on thediagnosis and management of Crohn's disease: definitions anddiagnosis. Gut 2006;55(Suppl 1):i1–i15.

7. Varo JJ, Martinez-Gonzalez MA, De Irala-Estevez J, Kearney J,Gibney M, Martinez JA. Distribution and determinants of sedentarylifestyles in the European Union. Int J Epidemiol 2003;32:138–46.

8. Lichtiger S, Present DH. Preliminary report: cyclosporin intreatment of severe active ulcerative colitis. Lancet 1990;336:16–9.

9. Satsangi J, Silverberg MS, Vermeire S, Colombel JF. The Montrealclassification of inflammatory bowel disease: controversies,consensus, and implications. Gut 2006;55:749–53.

10. Braulio VB, Furtado VC, Silveira MG, Fonseca MH, Oliveira JE.Comparison of body composition methods in overweight andobese Brazilian women. Arq Bras Endocrinol Metabol 2010;54:398–405.

11. WHO. The WHO Global Database on Body Mass Index. 22-09-2012ed: World Health Organization; 2012.

12. Segal KR, Van Loan M, Fitzgerald PI, Hodgdon JA, Van ItallieTB. Lean body mass estimation by bioelectrical impedanceanalysis: a four-site cross-validation study. Am J Clin Nutr1988;47:7–14.

13. Da Nobrega AC, Vaisman M, De Araujo CG. Skeletal musclefunction and body composition of patients with hyperthyroid-ism. Med Sci Sports Exerc 1997;29:175–80.

14. Reuters VS, Buescu A, Reis FA, Almeida CP, Teixeira PF, CostaAJ, et al. [Clinical and muscular evaluation in patients withsubclinical hypothyroidism]. Arq Bras Endocrinol Metabol2006;50:523–31.

15. Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF,Blazer DG, et al. A short physical performance battery assessinglower extremity function: association with self-reported dis-ability and prediction of mortality and nursing home admission.J Gerontol 1994;49:M85–94.

16. Bohannon RW. Reference values for the five-repetition sit-to-standtest: a descriptive meta-analysis of data from elders. Percept MotSkills 2006;103:215–22.

17. Guralnik JM, Ferrucci L, Pieper CF, Leveille SG, Markides KS, OstirGV, et al. Lower extremity function and subsequent disability:consistency across studies, predictive models, and value of gaitspeed alone compared with the short physical performancebattery. J Gerontol A Biol Sci Med Sci 2000;55:M221–31.

18. Lauretani F, Russo CR, Bandinelli S, Bartali B, Cavazzini C, DiIorio A, et al. Age-associated changes in skeletal muscles andtheir effect on mobility: an operational diagnosis of sarcopenia.J Appl Physiol 2003;95:1851–60.

Please cite this article as: Zaltman C, et al, Lower extremitymobility limitJ Crohns Colitis (2013), http://dx.doi.org/10.1016/j.crohns.2013.11.006

19. Florindo AA. Latorre Mdo R, Jaime PC, Tanaka T, Zerbini CA.[Methodology to evaluation the habitual physical activity in menaged 50 years or more]. Rev Saude Publica 2004;38:307–14.

20. Baecke JA, Burema J, Frijters JE. A short questionnaire for themeasurement of habitual physical activity in epidemiologicalstudies. Am J Clin Nutr 1982;36:936–42.

21. Cesari M, Penninx BW, Pahor M, Lauretani F, Corsi AM, RhysWilliams G, et al. Inflammatory markers and physical perfor-mance in older persons: the InCHIANTI study. J Gerontol A BiolSci Med Sci 2004;59:242–8.

22. Visser M, Pahor M, Taaffe DR, Goodpaster BH, Simonsick EM,Newman AB, et al. Relationship of interleukin-6 and tumor necrosisfactor-alpha with muscle mass and muscle strength in elderly menand women: the Health ABC Study. J Gerontol A Biol Sci Med Sci2002;57:M326–32.

23. Kuo HK, Bean JF, Yen CJ, Leveille SG. Linking C-reactive protein tolate-life disability in the National Health and Nutrition Examina-tion Survey (NHANES) 1999-2002. J Gerontol A Biol Sci Med Sci2006;61:380–7.

24. Rantanen T, Guralnik JM, Foley D, Masaki K, Leveille S, Curb JD,et al. Midlife hand grip strength as a predictor of old age disability.JAMA 1999;281:558–60.

25. Goodman MN. Tumor necrosis factor induces skeletal muscleprotein breakdown in rats. Am J Physiol 1991;260:E727–30.

26. Garcia-Martinez C, Lopez-Soriano FJ, Argiles JM. Acute treatmentwith tumour necrosis factor-alpha induces changes in proteinmetabolism in rat skeletal muscle. Mol Cell Biochem 1993;125:11–8.

27. Payne GW. Effect of inflammation on the aging microcircula-tion: impact on skeletal muscle blood flow control. Microcircu-lation 2006;13:343–52.

28. Wennie Huang WN, Perera S, VanSwearingen J, Studenski S.Performance measures predict onset of activity of daily livingdifficulty in community-dwelling older adults. J Am Geriatr Soc2010;58:844–52.

29. Bin CM, Flores C, Alvares-da-Silva MR, Francesconi CF. Compar-ison between handgrip strength, subjective global assessment,anthropometry, and biochemical markers in assessing nutrition-al status of patients with Crohn's disease in clinical remission.Dig Dis Sci 2010;55:137–44.

30. Hulens M, Vansant G, Lysens R, Claessens AL, Muls E, BrumagneS. Study of differences in peripheral muscle strength of leanversus obese women: an allometric approach. Int J Obes RelatMetab Disord 2001;25:676–81.

31. Institute ofMedicine (US) Committee on Disability in America; FieldMJ JA, editors. The Future of Disability in America. 2010/07/30 ed.Washington (DC): National Academies Press (US); Available from:http://www.ncbi.nlm.nih.gov/books/NBK11434/, 2007.

32. Wiroth JB, Filippi J, Schneider SM, Al-Jaouni R, Horvais N, GavarryO, et al. Muscle performance in patients with Crohn's disease inclinical remission. Inflamm Bowel Dis 2005;11:296–303.

33. Elsenbruch S, Langhorst J, Popkirowa K, Muller T, Luedtke R,Franken U, et al. Effects of mind-body therapy on quality of lifeand neuroendocrine and cellular immune functions in patientswith ulcerative colitis. Psychother Psychosom 2005;74:277–87.

34. Narula N, Fedorak RN. Exercise and inflammatory boweldisease. Can J Gastroenterol 2008;22:497–504.

35. Gardener EA, Huppert FA, Guralnik JM, Melzer D. Middle-aged andmobility-limited: prevalence of disability and symptom attribu-tions in a national survey. J Gen Intern Med 2006;21:1091–6.

ation and impairedmuscle function in womenwith ulcerative colitis,