Gender differences in Intra Limb Coordination while walking in older people

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1 Iranan Rehabltaton Journal, Vol. 12, No. 21, September 2014 Orgnal Artcle Gender dfferences n Intra Lmb Coordnaton whle walkng n older people Tabassom Ghanavat; Noureddn Karm * ; Mahyar Salavat Unversty of Socal Welfare and Rehabltaton Scences, Tehran, Iran Hossen Negahban; Mohammad Mehravar; Masumeh Hessam Ahvaz Jundshapur Unversty of Medcal Scences, Ahvaz, Iran Ismal Ebrahm Takamjan Iran Unversty of Medcal Scences, Tehran, Iran Objectves: Knowledge about gender dfferences n ntra-lmb coordnaton durng walkng provdes nsght nto the adaptablty of central nervous system for controllng gat n older adults. We assessed the varablty and phase dynamc of the ntra-lmb coordnaton n older men and women durng walkng. Methods: Twenty two older people, 11 female and 11 male, partcpated n ths study. They were asked to perform walk on a treadmll at ther preferred speed. Devaton phase and mean absolute relatve phase values -ndcators of varablty and phase dynamc of ntra-lmb coordnaton, respectvely- were calculated usng the data collected by a moton capture system. We used ndependent sample t-test for statstcal analyss. Results: The results showed that women had a sgnfcant hgher devaton phase n pelvs-thgh ntersegmental relatonshps on both sdes. Addtonally, the mean absolute relatve phase of left pelvs-thgh, thgh-shank and shank-foot were sgnfcantly dfferent between men and women. Dscusson: Whle women showed a lower mean absolute relatve phase n pelvs-thgh, men had a lower mean absolute relatve phase n shank-thgh nter-segmental relatonshps. We suggest that gender could affect the ntra-lmb coordnaton varablty and phase dynamc durng walkng n older people. Ths may be a reflecton of the great adaptablty of neuromuscular system to modfy control strateges for walkng n older women/ men. Key words: Intra-lmb coordnaton, Contnuous relatve phase, gat, gender, elderly Submtted: 14 May 2014 Accepted: 25 August 2014 Introducton Falls and ther possble consequences such as fractures, hosptalzatons, fear of fallng and loss of ndependence are mportant publc health concerns among elderly people. In addton they may mpose hgh costs on publc health and socal servces (1-6). Falls are more prevalent n older women than men (7,8). Women report hgher functonal lmtatons and fear of fallng and have lower levels of physcal capablty as compared wth men (9). However, the unntentonal consequences of fallng dffer between men and women. Adjusted for age, mortalty of falls are lower among women (10). Therefore, knowledge about the factors contrbutng to falls and explorng the factors that may dffer between women and men could be crtcal to fall preventon and nterventon. More than 50% of falls n older people happen durng walkng (10). Examnng gat, partcularly gat dfferences between women and men, may provde nformaton about dfferent mechansms of fallng contrbutng n fall-related njures and mortalty of falls among older women and men. Gat and moblty dfferences between men and women are well reported (11-17). Accordng to the fndngs of prevous studes, women generally walk wth shorter strdes and hgher cadences than men (11,15). Moreover, t has been shown that men experence greater decreases n maxmum and comfortable gat veloctes as they are aged over 65 years. Addtonally, compared to women, men have a stronger relatonshp between the lower lmb strength and gat velocty (18-20). Furthermore, All correspondences to: Noureddn Karm, emal: <karm@uswr.ac.r> 6 Vol. 12, No. 21, September. 2014

2 durng dual task walkng, men walked wth greater Varablty n walkng speed than dd women (21). Whle several studes have focused on comparng spatal and/or temporal gat parameters n men and women, hgher order parameters e.g. ntra-lmb coordnaton (ILC) s not consdered nto account yet. ILC s defned as the ablty to assemble and mantan a seres of proper relatons between jonts (nter-jont) or segments (nter-segment) wthn a lmb, organzed n a tmed and sequental manner, to produce a functonal movement (22,23). It s a fundamental ssue n human gat control especally for controlng a precse foot trajectory. By relatng motons of two segments, ILC provdes nformaton on how the neuromuscular skeletal system controls the redundant degrees of freedom (DF) of the jonts for achevng an effcent, smooth and accurate movement (23-28) Explorng ILC whle walkng provdes nsght nto the manner n whch CNS controls human gat. Partcularly, ILC varablty ndcates the adaptablty of the neuromuscular system to changng walkng condtons (22,23,25-27,29,30). Accordng to the above revew, the am of the present study was to address the gender dfferences n ILC of lower extremtes durng walkng n older adults. We hypothessed that older women may show hgher ILC varablty n pelvs-thgh ILC compared to older men. Methods Partcpants- Eleven older women and eleven older men (age 27.03±4.42) took part n the study. All partcpants had no hstory of orthopaedc, neurologcal, cardopulmonary, rheumatologc dsorders or hstory of lmb jont surgery or vertgo. The Human Research Ethcs Commttee of the relevant unversty approved the study and all of the tests were conducted n the Musculoskeletal Rehabltaton Research Center. A wrtten nformed consent was obtaned from each partcpant pror to partcpaton. Walkng tasks- Partcpants were asked to walk on treadmll wth ther preferred speed. The preferred speed of walkng was determned for each partcpant pror to the man testng by askng the partcpant to walk on the treadmll commencng at 1 km/h wth speed ncreased by 0.5 km/h ncrements untl they reported preferred or comfortable pace. When the partcpant frst ndcated hs/her preferred speed the treadmll velocty was agan ncreased and decreased n 0.5 km/h ntervals and the ndvdual asked to reconfrm the speed preference (31). The use of a self-selected comfortable pace ensured that any potental dscomfort that could have been ntroduced by usng a pre-determned speed for all subjects was mnmzed. For each walkng condton, the data were collected durng a 90- second perod of walkng. Data collecton- After each partcpant became famlar wth the laboratory settng wth several practce trals, data collecton started. Twenty-four nfrared-retroreflectve markers were placed on the wrst, lateral humeral epcondyle, acromon process, tempromandbular jonts, posteror superor lac spne, greater trochanter, lateral femoral epcondyle, head of fbula, lateral malleolus, 5th metatarsal base and heel, blaterally, and two addtonal markers on 7th cervcal and 12th thoracc vertebrae. Knematc data were measured by 7-camera moton capturng system (Qualsys, Inc.) at a samplng rate of 100 Hz. Intra-lmb coordnaton analyss- All knematc data were fltered usng a bdrectonal, fourth-order, low pass Butterworth flter. Optmal cut off frequences for each marker and tral data were determned usng resdual analyss method. The events of heel strke and toe-off were detected by examnng the poston of the foot durng the test. Snce changes due to walkng speed n lower extremty knematcs are mostly domnant n the sagttal plane (27,30), we only examned the sagttal plane ILC relatonshps. A custom-wrtten MatLab (MathWorks Inc.) program was used to flter the data and calculate the contnuous relatve phase (CRP) values. Snce t has been reported that asymmetres are more readly detected by usng segmental angles compared wth jont angles (27), we used the ILC relatonshps between segments rather than jonts to calculate CRP values. Sagttal plane segment angles (relatve to horzon) of lower extremtes were calculated blaterally for foot, shank, thgh and pelvs segments. Due to mssng markers n some trals, output varables could not be determned for all gat cycles. Therefore, 15 successve and complete gat cycles n the mddle of the test tme were used for all CRP analyss. Sagttal plane segment angles were truncated on a strde-by-strde bass and nterpolated to 100 ponts across the tme of each complete gat cycle. To confrm the applcaton of phase planes and dynamc system assumptons, that requre the tme seres to be lke snusod sgnals, an emprcal mode decomposton algorthm was appled (26). Segment angles were frst decomposed nto emprcal modes (snusod sgnals) wth dfferent frequences. Then Iranan Rehabltaton Journal 7

3 the tme seres data were reconstructed usng all emprcal modes except the lowest frequency whch was not assumed satsfactory wth the snusod assumpton. Segment angular veloctes were calculated usng a central dfference method. CRP was calculated by frst generatng phase portrats normalzed to the maxmum velocty. Normalzaton was conducted on a strde-per-strde bass. Angular poston and veloctes n each gat cycle were frst normalzed usng the followng equatons: _ normal mn( ) 1, max( ) mn( ) _ normal max( abs( )) Eq. 1. Where and are the angular poston and veloctes for each of 100 nterpolated data ponts durng a complete gat cycle. Eq. 1 normalzes phase portrats to 1 along the poston axs and to +1 or - 1 along the velocty axs, dependng on where the absolute maxmum velocty occurs. The normalzaton would mnmze ndvdual dfferences n ampltude and frequency (24) and centers the phase plot about an orgn. Then, phase 1 angles ( ) were calculated as tan ( / ) for each data pont over a gat cycle and unwrapped to correct dscontnutes occurred durng angle calculaton (29,32). The CRP n pont of normalzed gat cycle was calculated by subtractng the phase angle of dstal segment from that of proxmal segment φ pelvs-thgh, φ thgh-shank, φ shank-foot n that pont. The magntude and varablty of ILC were assessed wth mean absolute relatve phase (MARP) and devaton phase (DP). MARP and DP are the average values of all mean and standard devatons, respectvely, calculated for each data pont over a gat cycle from all 15 CRP curves. MARP accounts for the amount of ntra-lmb coordnaton. A low MARP value ndcates that the oscllatng segments have a more n-phase relatonshp whle a hgh MARP value ndcates that the oscllatng segments have a more out-o-phase relatonshp. DP represents the strde to strde varablty and compares the systemc knematc level coordnaton characterstcs over a gat cycle. So, hgher DP ndcates more changeable coordnaton between two adjacent jonts (29). Statstcal analyss- All varables were examned for normalty. We used ndependent sample t-tests to compare the measured values between men and women. All statstcal analyses were performed wth the SPSS 19.0 (SPSS Inc., Chcago, IL). Results Descrptve statstcs of the partcpants ncludng age, heght, weght, and BMI are shown n table (1). Table 1. Descrptve characterstcs of partcpants Characterstcs Mean±SD Female (n=11) Male (n=11) Age (years) ± ± 5.83 Heght (m) 1.55 ± ± 0.05 Weght (kg) ± ± BMI (kg/m 2 ) ± ± 3.41 * N: number of people; SD: standard devaton; BMI: Body Mass Index. Results of ndependent sample t-test showed sgnfcant dfferences n mean of DP n rght and left pelvs-thgh ILC between men and women (p=0.007 and p=0.002, respectvely). Fgure (1) presents the comparson of mean dfferences of DP n rght (A) and left (B) pelvs-thgh ILCs n between men and women. 8 Vol. 12, No. 21, September. 2014

4 Fg 1. Comparng the means of devaton phase (DP) n rght pelvs-thgh (A) and left pelvs-thgh (B) Moreover, the MARP n left pelvs-thgh, thghshank and shank-foot ILC between men and women (p= 0.016, p= and p= 0.025, respectvely). The comparsons of mean dfferences of MARP n the aforementoned ILCs are shown n Fgure (2). Fg 2. Comparng the means of mean absolute relatve phase (MARP) n left shank-foot (A), thgh-shank (B) and pelvs-thgh (C). Dscusson In ths study we nvestgated the gender dfferences n varablty and phase dynamcs of ILC of lower extremtes n older people durng walkng at preferred speeds. We hypotheszed that the varablty of ILC durng walkng wll be affected by gender and our results support ths hypothess. Novel to our study, we found that the varablty of ILC for pelvs-thgh nter-segmental relatonshp s hgher n women than men. Snce decreased ILC varablty reflects lmted degrees of freedom durng a motor task (26, 29), t may be a possble rsk when people confront perturbatons durng actvtes of daly lvng. It s especally mportant for older adults who commonly rely on hp strategy rather that ankle strategy when they are perturbed (28, 32). Thus restrcted pelvs-thgh ILC varablty n older man compared to women may put older male adults at a hgher rsk for fallng durng actvtes of daly lvng. Furthermore, our results showed that there are unlateral MARP dfferences between women and men. Interestngly men showed lower MARP values at shank-foot nter-segmental relatonshp whle women showed lower MARP values n pelvs-thgh. Lower MARP ndcates a more n-phase behavour of these nter-segmental relatonshps (33). The nphase dynamc of ILC reduces the control effort necessary for motor control (29). Thus, may be because of the more varable coordnaton n pelvsthgh, women reduce ther control effort by changng the phase dynamc of pelvs-thgh whle men reduce the effort by alterng shank-foot phase dynamcs. In order to analyse CRP, we needed numerous contnuous gat cycles (33). Accordng to our laboratory facltates t was only possble by askng the partcpants to walk on a motorzed treadmll. Another advantage of usng the treadmll was that we could control the speed durng cogntve task and observe the net effect of smultaneous cogntve task on gat parameters. On the other hand, t was also a Iranan Rehabltaton Journal 9

5 potental lmtaton of our study snce treadmll strctly enforced walkng speed and may artfcally change the natural varablty and attentonal demands of gat, compared to over-ground walkng (34). However, all partcpants were tested under the same expermental condtons and relatve to ther own cogntve load and walkng speeds. Therefore, over-ground walkng may yeld slghtly dfferent values for the quantfed measures. Secondly, we only assessed the ILC n the sagttal plane, because ths s the prmary plane of moton n whch the ILC s expected to be controlled durng gat. We suggest that the future studes evaluate the effects of dfferent fall preventve and nterventonal strateges consderng gender dfferences found n ILC of lower extremtes. Concluson Ths study demonstrated that n elderly people, gender can sgnfcantly alter the varablty and phase dynamcs of ILC of lower extremtes durng walkng. These dfferences may be an ndcatve of dfferent control mechansms that men and women adopt to control ther walkng. They may also help the rehabltaton staff to recrut gender-specfc nterventons to prevent falls n older people. Acknowledgments Ths study was funded by Unversty of Socal Welfare and Rehabltaton Scences, Tehran. We are deeply thankful to Unversty of Socal Welfare and Rehabltaton Scences and Khuzestan Retrement Organzatons for ther sncere help and support. References 1. Callsaya ML, Blzzard L, Schmdt MD, Martn KL, McGnley JL, Sanders LM, et al. Gat, gat varablty and the rsk of multple ncdent falls n older people: a populaton-based study. Age and ageng. 2011;40(4): Barak Y, Wagenaar RC, Holt KG. Gat characterstcs of elderly people wth a hstory of falls: a dynamc approach. Physcal therapy. 2006;86(11): Auvnet E, Multon F, Meuner J. Lower lmb movement asymmetry measurement wth a depth camera. Conference proceedngs: Annual Internatonal Conference of the IEEE Engneerng n Medcne and Bology Socety IEEE Engneerng n Medcne and Bology Socety Conference. 2012: Beauchet O, Dubost V, Allal G, Gonther R, Hermann FR, Kressg RW. 'Faster countng whle walkng' as a predctor of falls n older adults. Age and ageng. 2007;36(4): Voermans NC, Snjders AH, Schoon Y, Bloem BR. Why old people fall (and how to stop them). Practcal neurology. 2007;7(3): Hollman JH, Kovash FM, Kubk JJ, Lnbo RA. Age-related dfferences n spatotemporal markers of gat stablty durng dual task walkng. Gat & posture. 2007;26(1): Stevens JA, Corso PS, Fnkelsten EA, Mller TR. The costs of fatal and non-fatal falls among older adults. Injury preventon: journal of the Internatonal Socety for Chld and Adolescent Injury Preventon. 2006;12(5): Stevens JA, Sogolow ED. Gender dfferences for non-fatal unntentonal fall related njures among older adults. Injury preventon: journal of the Internatonal Socety for Chld and Adolescent Injury Preventon. 2005;11(2): Cooper R, Hardy R, Ahe Sayer A, Ben-Shlomo Y, Brne K, Cooper C, et al. Age and gender dfferences n physcal capablty levels from md-lfe onwards: the harmonsaton and meta-analyss of data from eght UK cohort studes. PloS one. 2011;6(11):e Talbot LA, Musol RJ, Wtham EK, Metter EJ. Falls n young, mddle-aged and older communty dwellng adults: perceved cause, envronmental factors and njury. BMC publc health. 2005;5: Oberg T, Karszna A, Oberg K. Basc gat parameters: reference data for normal subjects, years of age. Journal of rehabltaton research and development. 1993;30(2): Chumanov ES, Wall-Scheffler C, Hederschet BC. Gender dfferences n walkng and runnng on level and nclned surfaces. Clncal bomechancs. 2008;23(10): Callsaya ML, Blzzard L, Schmdt MD, McGnley JL, Srkanth VK. Sex modfes the relatonshp between age and gat: a populaton-based study of older adults. The journals of gerontology Seres A, Bologcal scences and medcal scences. 2008;63(2): Barrett R, Noordegraaf MV, Morrson S. Gender dfferences n the varablty of lower extremty knematcs durng treadmll locomoton. Journal of motor behavor. 2008;40(1): Bohannon RW. Comfortable and maxmum walkng speed of adults aged years: reference values and determnants. Age and ageng. 1997;26(1): Hardy SE, Allore HG, Guo Z, Gll TM. Explanng the effect of gender on functonal transtons n older persons. Gerontology. 2008;54(2): Mann TM, Everhart JE, Patel KV, Schoeller DA, Cummngs S, Mackey DC, et al. Actvty energy expendture and moblty lmtaton n older adults: dfferental assocatons by sex. Amercan journal of epdemology. 2009;169(12): Kozaka R, Tsuzuku S, Yabe K, Ando F, Nno N, Shmokata H. Age-related changes n gat velocty and leg extenson power n mddle-aged and elderly people. Journal of epdemology / Japan Epdemologcal Assocaton. 2000;10(1 Suppl):S Steffen TM, Hacker TA, Mollnger L. Age- and genderrelated test performance n communty-dwellng elderly people: Sx-Mnute Walk Test, Berg Balance Scale, Tmed Up & Go Test, and gat speeds. Physcal therapy. 2002;82(2): Steffen TM, Mollnger LA. Age- and gender-related test performance n communty-dwellng adults. Journal of neurologc physcal therapy: JNPT. 2005;29(4): Feld-Fote EC, Tepavac D. Improved ntralmb coordnaton n people wth ncomplete spnal cord njury followng tranng wth body weght support and electrcal stmulaton. Physcal therapy. 2002;82(7): Byrne JE, Stergou N, Blanke D, Houser JJ, Kurz MJ, Hageman PA. Comparson of gat patterns between young and elderly women: an examnaton of coordnaton. Perceptual and motor sklls. 2002;94(1): Wang TM, Yen HC, Lu TW, Chen HL, Chang CF, Lu YH, et al. Blateral knee osteoarthrts does not affect nter-jont coordnaton n older adults wth gat devatons durng obstacle-crossng. Journal of bomechancs. 2009;42(14): Vol. 12, No. 21, September. 2014

6 24. Chu SL, Osterng L, Chou LS. Concusson nduces gat nter-jont coordnaton varablty under condtons of dvded attenton and obstacle crossng. Gat & posture. 2013;38(4): Chu SL, Lu TW, Chou LS. Altered nter-jont coordnaton durng walkng n patents wth total hp arthroplasty. Gat & posture. 2010;32(4): Chu SL, Chou LS. Varablty n nter-jont coordnaton durng walkng of elderly adults and ts assocaton wth clncal balance measures. Clncal bomechancs. 2013;28(4): Chu SL, Chou LS. Effect of walkng speed on nter-jont coordnaton dffers between young and elderly adults. Journal of bomechancs. 2012;45(2): Hutn E, Pradon D, Barber F, Graces JM, Bussel B, Roche N. Lower lmb coordnaton patterns n hemparetc gat: factors of knee flexon mparment. Clncal bomechancs. 2011;26(3): Haddad JM, van Emmerk RE, Wheat JS, Hamll J, Snapp- Chlds W. Relatve phase coordnaton analyss n the assessment of dynamc gat symmetry. Journal of appled bomechancs. 2010;26(1): Yen HC, Chen HL, Lu MW, Lu HC, Lu TW. Age effects on the nter-jont coordnaton durng obstacle-crossng. Journal of bomechancs. 2009;42(15): Sparrow WA, Begg RK, Parker S. Varablty n the footground clearance and step tmng of young and older men durng sngle-task and dual-task treadmll walkng. Gat & posture. 2008;28(4): Haddad JM, van Emmerk RE, Whttlesey SN, Hamll J. Adaptatons n nterlmb and ntralmb coordnaton to asymmetrcal loadng n human walkng. Gat & posture. 2006;23(4): Buzz UH, Stergou N, Kurz MJ, Hageman PA, Hedel J. Nonlnear dynamcs ndcates agng affects varablty durng gat. Clncal bomechancs. 2003;18(5): Regnaux JP, Roberston J, Smal DB, Danel O, Bussel B. Human treadmll walkng needs attenton. Journal of neuroengneerng and rehabltaton. 2006;3:19. Iranan Rehabltaton Journal 11

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