Kinetische und elektromyographische Bewegungsanalyse beim Hund mit reversibel induzierter Hinterhandlahmheit
INAUGURAL – DISSERTATION
zur Erlangung des Grades einer Doktorin der Veterinärmedizin - Doctor medicinae veterinariae -
(Dr. med. vet.)
vorgelegt von Stefanie Fischer
Höxter
2. PD Dr. Nadja Schilling
Institut für Spezielle Zoologie und Evolutionsbiologie, Jena
1. Gutachter: Prof. Dr. Ingo Nolte
2. Gutachter: Prof. Dr. Peter Stadler
Tag der mündlichen Prüfung: 27.05.2013
Diese Arbeit wurde im Rahmen des Graduiertenkolleg Biomedizintechnik des SFB 599 (finanziert durch die Deutsche Forschungsgemeinschaft), der
Meiner Familie
• The Veterinary Journal
Compensatory load redistribution in walking and trotting dogs with hind limb lameness
Stefanie Fischer, Alexandra Anders, Ingo Nolte, Nadja Schilling DOI: 10.1016/j.tvjl.2013.04.09
Der zweite Teil dieser Arbeit ist bei folgender Zeitschrift eingereicht:
• PloS One
Adaptations in muscle activity to induced hindlimb lameness in trotting dogs
Stefanie Fischer, Ingo Nolte, Nadja Schilling
• SFB599 Kolloquium 2012
Electromyographical and computerized gait analyses in dogs with and without hindlimb lameness
• 21. Jahrestagung der Fachgruppe “Innere Medizin und Klinische Labordiagnostik” der DVG
Muskelfunktionsdiagnostik beim trabenden Hund mit Hinterhandlahmheit
Inhaltsverzeichnis
1. Einleitung und Literaturüberblick ... 11
2. Material und Methoden ... 17
2.1. Hunde ... 17
2.2. Datenaufzeichnung ... 17
2.2.1. Kinetische Messungen ... 18
2.2.2. Elektromyographische Messungen ... 18
2.3. Datenanalyse ... 18
3. Studie I ... 19
3.1. Abstract ... 20
3.2. Introduction ... 21
3.3. Materials and Methods ... 23
3.3.1. Animals ... 23
3.3.2. Study design ... 23
3.3.3. Data collection and analysis ... 24
3.3.4. Statistical analyses ... 25
3.4. Results ... 25
3.4.1. Load distribution ... 25
3.4.2. Symmetry indices ... 26
3.4.3. Relative stance duration ... 26
3.5. Discussion ... 26
3.6. Conclusion ... 30
3.7. Acknowledgements ... 30
3.8. References ... 30
3.9. Tables and Figures ... 36
4. Studie II ... 43
4.1. Abstract ... 44
4.2. Introduction ... 45
4.3. Materials and Methods ... 47
4.3.1. Ethics statement ... 47
4.3.2. Animals and experimental design ... 47
4.3.3. Data collection ... 48
4.3.4. Data analysis ... 49
4.3.5. Statistical analyses ... 50
4.4. Results ... 50
4.4.1. M. triceps brachii (N=7) ... 50
4.4.2. M. vastus lateralis (N=7) ... 51
4.4.3. M. longissimus dorsi (N=5) ... 51
4.5. Discussion ... 52
4.5.1. M. tricpes brachii ... 52
4.5.2. M. vastus lateralis ... 53
4.5.3. M. longissimus dorsi ... 55
4.6. Concluding remarks ... 57
4.7. Acknowledgements ... 58
4.8. References ... 58
4.9. Tables and Figures ... 66
5. Diskussion ... 71
6. Zusammenfassung ... 78
7. Summary ... 81
8. Literaturverzeichnis ... 83
9. Danksagung ... 103
Abkürzungsverzeichnis
In dieser Arbeit wurden folgende Kurzformen verwendet:
CoM Körpermasseschwerpunkt EMG Elektromyographie
Fc Kontralaterale Vordergliedmaße Fi Ipsilaterale Vordergliedmaße Fx Mediolaterale Bodenreaktionskraft Fy Kraniokaudale Bodenreaktionskraft Fz Vertikale Bodenreaktionskraft GRF Bodenreaktionskräfte
Hc Kontralaterale Hintergliedmaße Hi Ipsilaterale Hintergliedmaße HD Hüftgelenksdysplasie
IFz Vertikaler Impuls L3 3. Lendenwirbel L4 4. Lendenwirbel
MFz Mittlere vertikale Bodenreaktionskraft
OA Osteoarthrose
OEMG Oberflächen-Elektromyographie
PFz Maximale vertikale Bodenreaktionskraft Post op Nach der Operation
SD Standardabweichung
1. Einleitung und Literaturüberblick
Lahmheit ist durch eine Funktionseinschränkung einer Gliedmaße gekennzeichnet, die zu Veränderungen des Bewegungsablaufes bei der Fortbewegung führt. Um abzuschätzen, welche Kurz- und Langzeitfolgen für den Bewegungsapparat des Hundes damit verbunden sein können, muss man zuerst verstehen, wie die Funktionseinschränkung kompensiert wird. Da diese Kompensationsmechanismen beim Hund noch nicht ausreichend verstanden sind, wie im Folgenden ausgeführt wird, die Kenntnis der veränderten Gangparameter jedoch die Grundlage für weiterführende medizinische Maßnahmen und neue therapeutische Ansätze darstellt, ist es notwendig, weitere Untersuchungen durchzuführen.
Die Bewegungen des Hundes und damit auch deren Veränderungen aufgrund einer Lahmheit werden mittels folgender etablierter Gangparameter bzw. Techniken beschrieben:
Als sogenannte metrische Gangparameter werden die zeitlich-räumlichen Charakteristika der Bodenkontakte aller Gliedmaßen anhand von Länge und Dauer des Schrittzyklus sowie seiner Subphasen —Stand- und Schwingphase— und der relativen Abfolge der Fußungen zueinander beschrieben. Eine bewährte Darstellungsform der zeitlichen Parameter sind beispielsweise die Fußfallmuster nach Hildebrand (HILDEBRAND 1966; Abb.1).
Abb. 1: Fußfallmuster eines gesunden Hundes in Schritt und Trab (Mittelwert ± Standardabweichung).
Ein Schrittzyklus beschreibt die Zeit vom Auffußen bis zum Wiederauffußen derselben Gliedmaße; Die schwarzen Balken zeigen die mittlere Zeit (±SD), die sich die Gliedmaße innerhalb eines Schrittzyklus in der Standphase befindet. Hc: kontralaterale Hintergliedmaße, Fc: kontralaterale Vordergliedmaße, Fi: ipsilaterale Vordergliedmaße, Hi: ipsilaterale Hintergliedmaße (aus Studie I, Abb. 1).
Das Teilgebiet der Kinematik beschreibt die zeitlich-räumlichen Beziehungen der Körperabschnitte zueinander bzw. zum Raum. Anhand von kinematischen Daten lassen sich die Bewegungen der einzelnen Segmente, sowie unterschiedliche Winkelparameter der zu untersuchenden Gliedmaßen erfassen (DECAMP et al.
1993; ALLEN et al. 1994; RAGETLY et al. 2010). Hiermit kann z. B. gezeigt werden, ob es beim lahmenden Hund in bestimmten Gelenken zu einer vermehrten oder verminderten Extension bzw. Flexion kommt, was wiederum Auswirkungen auf das gesamte Gangbild des Hundes haben kann.
Kinetische Gangparameter stellen einen weiteren Teilbereich dar. Die während der Lokomotion vom Hund auf den Boden ausgeübten Kräfte werden als Bodenreaktionskräfte erfasst. Zur besseren Veranschaulichung werden sie in ihre drei orthogonalen Vektoren zerlegt: vertikal (Fz), kraniokaudal (Fy) und mediolateral (Fx) (BUDSBERG 1987; MCLAUGHLIN 2001). Die Bodenreaktionskräfte geben Aufschluss über die Richtung und Höhe der externen Kräfte, die während der Standphase auf die Gliedmaße einwirken. Hierbei wird insbesondere die vertikale Kraft Fz zur quantitativen Beurteilung einer Lahmheit und zur Evaluierung der Gewichtsumverteilung zwischen den Gliedmaßen herangezogen.
Einen zusätzlichen Analysebereich liefert die Elektromyographie (EMG). Obwohl kinesiologisches EMG zu den Standardmethoden der Bewegungsanalyse in der Humanmedizin gehört, wird es in der Veterinärmedizin noch so gut wie nicht verwendet. Als der „Motor“ von Bewegungen ist die Muskulatur aber von besonderem Interesse und daher in die Funktionsanalyse des Bewegungsapparates einzubeziehen. Die EMG gibt Auskunft über das Aktivitätsmuster der Muskeln während unterschiedlicher Bewegungen. Das Rekrutierungsmuster ausgesuchter Muskeln kann beispielsweise nicht-invasiv mittels oberflächen- elektromyographischer Aufzeichnungen (OEMG) beurteilt werden.
Von den genannten Möglichkeiten der Bewegungsbeurteilung konzentrieren sich die Untersuchungen der vorliegenden Arbeit auf die Veränderungen der zeitlich- räumlichen Charakteristika der Bodenkontakte, der vertikalen Bodenreaktionskräfte (Fz) aller Gliedmaßen und des Aktivierungsmusters ausgewählter Muskeln beim lahmenden Hund im Vergleich zum physiologischen Gangbild. In der vorliegenden
Arbeit wird der Fokus speziell auf die Gangveränderungen bedingt durch eine Hinterhandlahmheit gelegt, da mehr als die Hälfte der muskuloskelettalen Probleme beim Hund durch Gelenkserkrankungen der Hintergliedmaße verursacht werden (v.a.
Hüfte und Knie; JOHNSON et al. 1994). Bezogen auf diese drei Analysebereiche — Metrik, Kinetik, EMG— lässt sich der aktuelle Kenntnisstand für Hunde mit Hinterhandlahmheit folgendermaßen zusammenfassen:
Veränderungen von zeitlich-räumlichen Gangparametern wurden bisher entweder in Bezug auf die Schrittlänge (z. B. DECAMP et al. 1996; RAGETLY et al. 2010;
SANCHEZ-BUSTINDUY et al. 2010), die Schrittdauer (z. B. RAGETLY et al. 2010) oder die Schrittfrequenz (z. B. BENNETT et al. 1996; DECAMP et al. 1996) untersucht. Eine Abnahme der Schrittlänge im betroffenen Bein (DECAMP et al.
1996; SANCHEZ-BUSTINDUY et al. 2010), sowie eine Abnahme der Schrittdauer der geschädigten im Vergleich mit der klinisch gesunden Gliedmaße (RAGETLY et al. 2010) wurde bei Hunden mit kranialem Kreuzbandriss festgestellt. Bei Hunden mit Hüftgelenksdysplasie (HD) kam es im Vergleich mit der Kontrollgruppe in der stärker erkrankten Gliedmaße zu einer Zunahme der Schrittlänge (BENNETT et al. 1996).
Eine Differenzierung von Stand- und Schwingphase wurde bisher nur vereinzelt vorgenommen (z. B. VILENSKY et al. 1994; BENNETT et al. 1996; RAGETLY et al.
2010; DE MEDEIROS et al. 2011; BÖDDEKER et al. 2012). Hier zeigten alle Hunde mit kranialem Kreuzbandriss eine verkürzte Standphasendauer der betroffenen Gliedmaße (VILENSKY et al. 1994; RAGETLY et al. 2010; DE MEDEIROS et al.
2011; BÖDDEKER et al. 2012). Hunde mit HD zeigten im Vergleich mit der Kontrollgruppe weder eine Zu- oder Abnahme in der Standphasendauer noch der Schrittfrequenz (BENNETT et al. 1996). Komplette Fußfallmuster, die sowohl Veränderungen der Stand- und der Schwingphase als auch zeitliche Beziehungen zwischen allen Extremitäten und die Abfolge der Fußungen bei einer Hinterhandlahmheit aufzeigen, gibt es bisher nicht.
Bisherige kinetische Studien haben in Bezug auf die veränderte Belastungssituation bei Hunden mit Hinterhandlahmheit entweder nur die betroffene Hintergliedmaße untersucht (z. B. CROSS et al. 1997; HOELZLER et al. 2004; CONZEMIUS et al.
2005; EVANS et al. 2005; MADORE et al. 2007; PUNKE et al. 2007) oder beide
Hintergliedmaßen verglichen (z. B. BUDSBERG et al. 1988; VOSS et al. 2008;
RAGETLY et al. 2010; BÖDDEKER et al. 2012; SEIBERT et al. 2012). Bei den genannten Studien wurde die jeweils betroffene Gliedmaße weniger belastet (Fz vermindert), wohingegen die kontralaterale Hintergliedmaße, sofern untersucht, vermehrt belastet wurde (Fz erhöht). Ob es bei einer Hinterhandlahmheit auch zu einer Gewichtsumverteilung auf die Vordergliedmaßen kommt, ist aufgrund der widersprüchlichen Befundlage ungeklärt (z. B. ja: DUPUIS et al. 1994; nein: RUMPH et al. 1993; RUMPH et al. 1995; JEVENS et al. 1996; KATIC et al. 2009).
Zahlreiche EMG-Studien haben in der Vergangenheit die Aktivitätsmuster einer Reihe von Gliedmaßen- und Rückenmuskeln beim gesunden trabenden Hund beschrieben (NOMURA et al. 1966; TOKURIKI 1973; GOSLOW et al. 1981;RITTER et al. 2001; CARRIER et al. 2006; CARRIER et al. 2008; SCHILLING et al. 2009;
SCHILLING u. CARRIER 2009; SCHILLING u. CARRIER 2010; DEBAN et al. 2012), aber nur wenige Studien haben die Veränderungen der Muskelrekrutierung in Adaptation an eine Lahmheit untersucht (HERZOG et al. 2003; ZANEB et al. 2009;
BOCKSTAHLER et al. 2012a). OEMG bietet im Gegensatz zum intramuskulären EMG eine weniger invasive Methode, welche in der Humanmedizin routinemäßig angewendet wird (SUTHERLAND 2001). In der Veterinärmedizin gibt es nur vereinzelt OEMG-Studien, die die Muskelrekrutierung von gesunden (LAUER et al.
2009; BOCKSTAHLER et al. 2009) und lahmen Hunden (BOCKSTAHLER et al.
2012a) untersucht haben. In der zuletzt genannten Arbeit wurden die Rekrutierungsmuster des M. vastus lateralis, des M. biceps femoris und des M.
glutaeus medius von gesunden und an Hüftgelenksarthrose (OA) erkrankten Hunden verglichen. Bei den Hunden mit OA zeigte sich in allen drei Hinterbeinmuskeln während der frühen Schwingphase eine verminderte Aktivität und während der frühen Standphase im M. vastus lateralis und im M. glutaeus medius eine höhere Aktivität. Kommt es bei einer Hinterhandlahmheit auch zu einer Gewichtsumverteilung nach kranial, ist zu erwarten, dass die Muskulatur der Vorderextremitäten ebenfalls Veränderungen im Rekrutierungsmuster aufzeigt.
Darüber hinaus hat keine der bisher vorliegenden OEMG-Studien den Rücken in die Untersuchung mit einbezogen. Daher bleibt die Rolle der Rückenmuskulatur bei der
Kompensation einer Hinterhandlahmheit offen. Zusammenfassend lässt sich feststellen, dass es beim lahmen Hund keine Studien gibt, welche die Aktivierungsmuster der ausgewählten Muskeln aller vier Gliedmaßen sowie des Rückens simultan untersucht haben.
Ziel der vorliegenden Arbeit ist es, einen Beitrag zum Verständnis der Lahmheitskompensation des Hundes zu leisten. Hierfür sollen im Hinblick auf eine Hinterhandlahmheit die Veränderungen in ausgewählten metrischen, kinetischen und elektromyographischen Parametern untersucht werden. Folgende Fragen stehen in dieser Arbeit im Vordergrund: 1) Sind bei einem Hund mit Hinterhandlahmheit zeitliche Verschiebungen im Schrittzyklus aller vier Gliedmaßen festzustellen?
Hierfür werden Fußfallmuster erstellt, welche die Veränderungen der zeitlichen Gangparameter von Stemm- und Vorschwingphase sowie die Folge der Bodenkontakte darstellen. 2) Wird zur Entlastung der betroffenen Gliedmaße das Gewicht ausschließlich zur kontralateralen Extremität verlagert oder sind alle vier Gliedmaßen in ihrer vertikalen Kraft verändert? Zur Beantwortung dieser Frage werden maximale und mittlere Kraft sowie der Impuls von Fz von allen vier Gliedmaßen synchron analysiert. 3) Inwiefern ändern sich die Aktivierungsmuster ausgewählter Bein- und Rückenmuskeln? Hierzu sollen erstmalig die Veränderungen der Rekrutierungsmuster vom M. triceps brachii, M. vastus lateralis und M.
longissimus dorsi in Bezug auf zeitliche Verläufe und die Amplitudenhöhe untersucht werden. Die Ergebnisse dieser Arbeit können durch ein besseres Verständnis der Kompensationsmechanismen des Hundes neue Ansätze für Therapien und Rehabilitationsmaßnahmen (z. B. Physiotherapie) liefern.
Alle Gangparameter sind von der Geschwindigkeit bzw. der Gangart abhängig.
Beispielsweise steigt die maximale vertikale Kraft mit zunehmender Geschwindigkeit an (z. B. BUDSBERG 1987; RIGGS et al. 1993; MCLAUGHLIN u. ROUSH 1994;
DECAMP 1997; RENBERG et al. 1999; BERTRAM et al. 2000; MCLAUGHLIN 2001;
EVANS et al. 2003; MÖLSA et al. 2010; VOSS et al. 2010). Da eventuell Lahmheiten visuell nur im Trab, aber nicht im Schritt auszumachen sind (QUINN et al. 2007;
VOSS et al. 2007), ist anzunehmen, dass sich die jeweiligen Kompensationsmechanismen zwischen den Gangarten unterscheiden. Aus diesem
Grund werden die beiden symmetrischen Gangarten, die auch bei der klinischen Lahmheitsevaluation herangezogen werden —Schritt und Trab— bei der Untersuchung der oben genannten Fragen berücksichtigt.
Die Veränderungen im Bewegungsablauf beim lahmenden im Vergleich zum nichtlahmenden Hund wurden mit Hilfe der computergestützten Ganganalyse unter Verwendung eines instrumentierten Laufbandes dokumentiert, das die gleichzeitige Erfassung der metrischen, kinetischen und elektromyographischen Daten erlaubt.
Um einen direkten Vergleich der physiologischen und pathologischen Werte bei ein und demselben Individuum zu ermöglichen und somit die Variabilität in den Ergebnissen aufgrund von Grad und Ursache der Lahmheit oder auch Alter, Körpergröße und Körperbau zu reduzieren, wurde hier das Modell der induzierten Lahmheit herangezogen, und es wurden ausschließlich Hunde einer Rasse —dem Beagle— eingesetzt. Den Hunden wurde dafür eine mittelgradige, reversible, distale Hinterhandlahmheit mit Hilfe einer „Stein im Schuh“-Methode induziert. Dies ermöglicht die genaue Bestimmung des Lahmheitsgrades und legt eine genaue Lokalisation für die Ursache der Lahmheit fest, welche sich bei allen untersuchten Probanden leicht reproduzieren ließ.
Die Ergebnisse dieser Arbeit werden in zwei getrennten Studien präsentiert, um eine angemessene Einordnung der einzelnen Befunde in die vorhandene Datenlage und eine eingehendere Diskussion dieser zu erlauben. Dabei werden in der ersten Studie die in dieser Arbeit erhobenen kinetischen und metrischen Daten mit den Ergebnissen bereits publizierter Arbeiten verglichen, welche Hunde mit klinischen und induzierten Lahmheiten ganganalytisch untersucht haben. Es wird diskutiert inwiefern die Ergebnisse auf den klinisch lahmen Hund übertragen werden können und welche Auswirkungen Lahmheiten generell auf die Belastung der übrigen Gliedmaßen haben. Die zweite Studie konzentriert sich auf die Veränderungen in den Aktivierungsmustern der ausgewählten Bein- und Rückenmuskeln, die mit einer Lahmheit einhergehen. Hierzu werden die erstmalig mittels OEMG erhobenen Aktivierungsmuster des M. triceps brachii und des M. longissimus dorsi zuerst mit vorhandenen Befunden intramuskulärer Ableitungen verglichen, um das methodische Vorgehen für diese beiden Muskeln zu verifizieren. Anschließend werden die
Unterschiede im Rekrutierungsmuster aller untersuchten Muskeln zwischen gesunden und lahmenden Hunden diskutiert und in die aktuelle Befundlage eingeordnet.
2. Material und Methoden
2.1. Hunde
Insgesamt wurden in dieser Studie neun klinisch gesunde Beagle mit einem Alter von 4 ± 1 Jahren (Mittelwert ± Standardabweichung) untersucht. Das mittlere Körpergewicht der zwei weiblichen und sieben männlichen Hunde betrug 15,1 ± 1,1 kg. Alle Hunde gehörten zur Beagle-Population der Klinik für Kleintiere der Stiftung Tierärztliche Hochschule Hannover. Die Hunde wurden allgemein und orthopädisch untersucht, um eine Lahmheit bzw. eine eventuell vorliegende Erkrankung am Bewegungsapparat auszuschließen. Zu Beginn der Studie wurden die Beagle an das Laufen auf dem Laufband gewöhnt und die Datenaufzeichnung startete, sobald sich die Hunde gleichmäßig und entspannt auf dem Laufband bewegten. Zur reversiblen Lahmheitsinduktion wurde eine mit Watte gepolsterte Styroporkugel (Durchmesser von 9,5 oder 16 mm) zwischen Haupt- und die Vorderballen positioniert und mittels Mullbinde und Klebeband für die Dauer der Untersuchung unter der Pfote der rechten Hintergliedmaße fixiert (s. Abb.1 in Abdelhadi et al. 2012). Alle Untersuchungen wurden in Übereinstimmung mit dem Deutschen Tierschutzgesetz durchgeführt und durch das Niedersächsische Landesamt für Verbraucherschutz und Lebensmittelsicherheit (LAVES) geprüft und genehmigt (Nr. 12/0717).
2.2. Datenaufzeichnung
Die simultane Aufzeichnung der metrischen, kinetischen und elektromyographischen Daten erfolgte im Schritt (0,9 m/s) und im Trab (1,4 m/s) jeweils zuerst ohne und dann mit induzierter Hinterhandlahmheit auf einem instrumentierten Laufband.
2.2.1. Kinetische Messungen
Die Aufzeichnung der kinetischen Daten erfolgte durch vier in das Laufband integrierte Kraftmessplatten (Model 4060-08, Bertec Corporation, Columbus, Ohio, USA). Es wurden die Bodenreaktionskräfte (Aufzeichnungsrate 1000 Hz) in vertikaler (Fz), kraniokaudaler (Fy) und mediolateraler (Fx) Richtung für jede Gliedmaße separat aufgezeichnet. Die vertikale Bodenreaktionskraft wurde zur objektiven Bestimmung des induzierten Lahmheitsgrades herangezogen.
2.2.2. Elektromyographische Messungen
Oberflächenelektromyographische Ableitungen wurden vom M. triceps brachii an beiden Vordergliedmaßen, vom M. vastus lateralis an beiden Hintergliedmaßen und vom M. longissimus dorsi auf Höhe L3/L4 beidseits unter der Verwendung von selbstklebenden Oberflächen-Gelelektroden (H93SG; Arbo; Tyco Healthcare, Deutschland) durchgeführt. Hierfür wurde das Hautareal über dem zu untersuchenden Muskel rasiert, gereinigt und entfettet, bevor die Elektroden an den mittels skelettaler Landmarken definierten Stellen angebracht wurden (Abb. 1 in Studie II). Die Ableitfläche der Elektroden betrug 1,6 cm im Durchmesser und der Elektrodenabstand war 2,5 cm. Die Oberflächenelektroden wurden immer von dem gleichen Untersucher an der vorher definierten Lokalisation angebracht, um die Variabilität der Platzierung zwischen den Hunden so gering wie möglich zu halten.
2.3. Datenanalyse
Die Auswertung der kinetischen und elektromyographischen Daten wurde anhand von 10 aufeinanderfolgenden Schrittzyklen pro Hund und Gangart durchgeführt. Die in Vicon Nexus (Vicon Motion Systems Ltd, Oxford, UK) aufgezeichneten vertikalen Bodenreaktionskräfte und elektromyographischen Daten wurden zuerst zeitnormiert und dann in Microsoft Excel (Excel, Microsoft Corp, Redmond, Wash, USA) für die weitere Bearbeitung exportiert. Das weitere Vorgehen bei der Datenaufbereitung und die jeweilige statistische Auswertung sind detailliert in Fischer et al. subm. (Studie I und II) beschrieben.
3. Studie I
Die folgende Studie wurde am 08.10.2012 bei The Veterinary Journal eingereicht.
Akzeptiert am 12.04.2013.
Compensatory load redistribution in walking and trotting dogs with hind limb lameness
S. Fischer a, A. Anders a, I. Nolte a, N. Schilling b*
a University of Veterinary Medicine Hannover, Foundation, Small Animal Clinic, Hannover, Germany
b Friedrich-Schiller-University, Institute of Systematic Zoology and Evolutionary Biology, Jena, Germany
* Corresponding author
3.1. Abstract
This study evaluated adaptations in vertical force and temporal gait parameters to hind limb lameness in walking and trotting dogs. Eight clinically normal adult Beagles were allowed to ambulate on an instrumented treadmill at their preferred speed while the ground reaction forces were recorded for all limbs before and after a moderate, reversible, hind limb lameness was induced. At both gaits, vertical force was decreased in the ipsilateral and increased in the contralateral hind limb. While peak force increased in the ipsilateral forelimb, no changes were observed for mean force and impulse when the dogs walked or trotted. In the contralateral forelimb, the peak force was unchanged, but the mean force significantly increased during walking and trotting; vertical impulse increased only during walking. Relative stance duration increased in the ipsilateral hind limb when the dogs trotted. In the contralateral fore and hind limbs, relative stance duration increased during walking and trotting, but decreased in the ipsilateral forelimb during walking. Analysis of load redistribution and temporal gait changes during hind limb lameness showed that compensatory mechanisms were similar regardless of gait. The centre of mass consistently shifted to the contralateral body side and cranio-caudally to the side opposite the affected limb. These biomechanical changes indicate substantial short- and long-term effects of hind limb lameness on the musculoskeletal system.
Keywords: Canine, Gait analysis; Hind limb lameness; Force plate
3.2. Introduction
More than half of the musculoskeletal problems in dogs are caused by joint diseases affecting the hind limb (i.e. hip and knee; Johnson et al., 1994) and are commonly associated with alterations in the gait (i.e. lameness) due to the animal’s effort to unload the affected limb. The biomechanical consequences of orthopaedic diseases, such as hip dysplasia and cranial cruciate ligament rupture, have been evaluated by investigating the load bearing characteristics of either the affected hind limb only (Gordon et al., 2003; Hoelzler et al., 2004; Conzemius et al., 2005; Evans et al., 2005; Madore et al., 2007) or both hind limbs (Budsberg et al., 1988; Voss et al., 2008; Ragetly et al., 2010; Böddeker et al., 2012; Seibert et al., 2012). Fewer studies have evaluated the effects of hind limb lameness on the forelimbs (Rumph et al., 1993, 1995; Dupuis et al., 1994; Jevens et al., 1996; Katic et al., 2009).
Nevertheless, unloading one limb causes biomechanical adaptations in all remaining limbs and results in an irregular gait pattern and a compensatory redistribution of limb loading.
During the standard orthopaedic examination, dogs are usually ambulated at different speeds and gaits to diagnose lameness. Since locomotor forces increase with speed and depend on gait (Riggs et al., 1993; McLaughlin and Roush, 1994; Renberg et al., 1999; Evans et al., 2003; Voss et al., 2010), not only may lameness be more apparent during trotting compared to walking (Quinn et al., 2007; Voss et al., 2007), but the compensatory mechanism used by the animal may differ. Additionally, the fundamental biomechanical differences between walking and trotting (i.e. legs behaving like inverted pendula vs. ‘pogo sticks’; Cavagna et al., 1977) may result in differences in the locomotor adaptations to lameness. Previous studies have evaluated induced hind limb lameness in trotting dogs (O’Connor et al., 1989; Rumph et al., 1993, 1995; Dupuis et al., 1994) or clinical lameness in walking dogs (Budsberg et al., 1988; Katic et al., 2009; Böddeker et al., 2012). It is uncertain if dogs show the same locomotor adaptations to hind limb lameness when walking and trotting.
In dogs, as in most quadrupedal mammals, fore and hind limbs play different functional roles during locomotion (Gray, 1968). The forelimbs exert a net-braking force, while the hind limbs exert a net-propulsive force during steady state locomotion (Budsberg et al., 1987; Riggs et al., 1993; Bertram et al., 1997; Lee et al.,1999).
Forelimbs function as compliant struts (Carrier et al., 2008), whereas hind limbs function as levers (Schilling et al., 2009). Regardless of gait, the forelimbs bear a greater proportion of the dog’s bodyweight (BW) in comparison with the hind limbs (Budsberg et al., 1987; Rumph et al., 1994; Bertram et al., 2000; Bockstahler et al., 2007; Voss et al., 2010). Therefore, when the function of a limb is partially lost, the dog’s mechanism to cope with this loss has been expected to differ depending on whether a fore or a hind limb is affected (Roy, 1971; Leach et al., 1977). To gain a better understanding of the compensatory load-shifting mechanisms in lame dogs, we induced a moderate, reversible, load-bearing hind limb lameness in Beagles while they were walking and trotting on an instrumented treadmill, and evaluated the changes in the ground reaction force (GRF) and temporal gait parameters. Force plate analysis was used because it is an accurate and objective way of evaluating limb function and provides a reproducible measurement of the load bearing characteristics of the limbs. Inducing hind limb lameness allowed for a direct comparison of the gait parameters between sound and lame dogs and the precise determination of the degree and cause of lameness.
The aims of this study were: (1) to determine changes occurring in the vertical GRF, i.e. peak vertical forces (PFz), mean vertical forces (MFz) and vertical impulse (IFz), as well as the temporal gait parameters (i.e. footfall pattern, relative stance duration) in all four limbs; (2) to determine whether the observed locomotor adaptations differed between the gaits; and (3) to determine whether the compensatory mechanisms in response to hind limb lameness differed from the ones used to cope with forelimb lameness. To address the latter, we compared our results with the ones from a previous study (Abdelhadi et al., 2013), which used the same experimental design and therefore allowed for a direct comparison of load redistribution strategies.
3.3. Materials and Methods 3.3.1. Animals
Eight Beagles aged 4 ± 1 years (mean ± standard deviation, SD) were used in this study. The sample size sufficient for this study was determined using Win Episcope 2.0 with a level of confidence of 95%, a power of 80% and the outcome measures PFz, MFz and IFz (Thrusfield et al., 2001). The BW (mean ± SD) of the two females and six males was 15.2 ± 1.1 kg. All dogs belonged to the Beagle population of the Small Animal Clinic of the University of Veterinary Medicine, Hannover, Germany.
Inclusion criteria were absence of lameness (see results) and orthopaedic abnormalities in the previous clinical examination. Before data collection, the dogs were habituated to ambulating on the treadmill. Data collection started as soon as the dogs were walking and trotting smoothly and comfortably. All experiments were carried out in accordance with the German Animal Welfare guidelines of the State of Lower Saxony (approval number 12/0717).
3.3.2. Study design
To allow for comparison of the compensatory load redistribution mechanisms in forelimb vs. hind limb lameness, the same experimental protocol as in Abdelhadi et al. (2013) was used in the current study, but lameness was induced in the right hind limb (i.e. ipsilateral hind limb, Hi). Before inducing lameness, each Beagle walked (0.9 m/s) and trotted (1.4 m/s) on a horizontal treadmill. Despite the short temporal overlap in ground contacts between the forelimbs at the faster gait (duty factor, D >
0.5; i.e. running walk according to Hildebrand (1966); Fig. 1), from a mechanical point of view, this gait represented a trot (i.e. using spring-mass mechanics; Cavagna et al., 1977) and will subsequently be referred to as trot. The selected speeds were determined during the habituation sessions, as were the preferred speeds for the dogs at the respective gait. At these speeds, the dogs ambulated smoothly and comfortably matched the treadmill speed, which allowed us to record single limb forces (see below).
After recording the control trials, a moderate and reversible hind limb lameness was induced using a small sphere, which was coated with cotton gauze and taped under
the paw with adhesive tape and bandages. The size of the sphere (9.5 or 16.0 mm in diameter) depended on the degree of lameness it induced in a given dog. The degree of lameness was evaluated based on the GRF data. To be able to compare our data with previous results (Abdelhadi et al., 2013), we aimed at an unloading of
~30–40% with regard to PFz (in %BW) compared with the sound condition.
3.3.3. Data collection and analysis
Data collection and analysis are described in detail in Abdelhadi et al. (2013). A treadmill with four separate belts and force plates underneath each belt (Model 4060- 08, Bertec) was used to record single limb GRF (sampling rate 1000 Hz). Data were recorded and evaluated to ensure a sufficient number of valid steps using Vicon Nexus (Vicon). Control data comprising at least 5–10 trials, each lasting up to 30 s and covering between 48 and 65 strides, were recorded for each dog while walking and trotting comfortably at the selected speed. After a break of approximately 15 min, lameness was induced and the data collection repeated. To evaluate kinetic changes, 10 valid consecutive strides were selected for each dog, gait and condition.
Mean ± SD for PFz, MFz and IFz were calculated for all four limbs. Additionally, relative stance duration (i.e. duration of stance phase as percentage of total stride duration = D), as well as symmetry indices for the vertical forces of the fore and hind limbs, were determined. After manual identification of the footfall events in Vicon Nexus using the GRF, the force data were time normalised to 100% of the stance duration of the respective limb and transferred to Microsoft Excel for further analysis.
The vertical force parameters were then normalised to the dog’s BW using the following equation:
GRFs (%BW) = Fz * 100/(BM *9.81).
These BW-normalised data were used to compare the load-bearing characteristics among the four limbs before and after lameness was induced (Steiss et al., 1982):
% BW bearing = Fz of the limb/total Fz of all limbs*100.
Symmetry in the vertical force and temporal variables was quantified using the following equation (Herzog et al., 1989):
(3) SI = 100*(Xi – Xc)/(0.5*(Xi + Xc)).
In this equation, X represents the mean value of PFz, MFz or IFz of the ipsilateral (i) and the contralateral (c) limbs from the 10 steps. Footfall patterns and D were evaluated to test for significant differences in the temporal gait parameters due to lameness. A stride cycle begins with the contact of the affected limb (ipsilateral hind limb, Hi) and ends with its subsequent touch-down. Therefore, one locomotor cycle comprises one complete stance and one complete swing phase of the reference limb.
3.3.4. Statistical analyses
Data were tested for normal distribution using the Kolmogorov–Smirnov test. The significance of the differences in PFz, MFz and IFz between the sound and lame conditions was determined using one-way analysis of variance (ANOVA) for repeated measures, followed by a post hoc Tukey test. Paired t tests were used to compare relative stance durations between sound and lame conditions. P values <0.05 were considered to be significant. All statistical tests were performed in GraphPad Prism (version 4).
3.4. Results
3.4.1. Load distribution
No significant differences in GRF (i.e. PFz, MFz and IFz) between the two forelimbs and between the two hind limbs were observed during walking and during trotting before lameness was induced (Table 1). Compared to the sound condition, all parameters decreased significantly in the ipsilateral hind limb when lameness was induced. During walking, these changes were primarily due to a decrease of the first
peak in the m-shaped force curve (Fig. 2). In the contralateral hind limb, PFz, MFz and IFz increased significantly at both gaits. Additionally, PFz increased significantly during walking and trotting in the ipsilateral forelimb, while no significant changes were observed in MFz and IFz. While PFz remained unchanged, MFz significantly increased during both walking and trotting in the contralateral forelimb. In this limb, IFz increased during walking, but not during trotting (Fig. 3).
3.4.2. Symmetry indices
For the sound condition, no asymmetry was detected between the right and left forelimb, or between the right and left hind limb, either during trotting or during walking (Table 2). After lameness was induced, asymmetry significantly increased in all GRF parameters of the hind limbs during walking and trotting. Symmetry indices for PFz and IFz for the forelimbs indicated significant changes for walking but not for trotting.
3.4.3. Relative stance duration
In the lame condition, relative stance duration significantly increased in the ipsilateral hind limb while the dogs were trotting; thereby lift-off was significantly delayed (Table 3; Fig. 1). Relative stance duration was significantly increased in the contralateral forelimb and hind limb during walking and trotting compared to the sound condition.
This increased stance duration was associated with a significant later lift-off of the contralateral forelimb during walking and of the contralateral hind limb during trotting.
Relative stance duration significantly decreased in the ipsilateral forelimb during walking.
3.5. Discussion
Prior to the induction of lameness, we observed no significant differences in GRF values (PFz, MFz and IFz) between the two forelimbs and the two hind limbs in walking and trotting dogs. Correspondingly, the calculated symmetry indices were in the normal range (<6%, Budsberg et al., 1993; <3.2%, Fanchon and Grandjean,
2007), which indicated symmetrical load distribution between the two forelimbs and the two hind limbs. The values of this study compared well with previous observations in dogs (Budsberg et al., 1993; Fanchon and Grandjean, 2007; Voss et al., 2008). Each forelimb bore about 30% and each hind limb about 20% of the dog’s BW. Comparison with previous results (Budsberg et al., 1987; Jevens et al., 1993;
Rumph et al., 1994; Bertram et al., 2000; Bockstahler et al., 2007) confirmed that the Beagles in the current study were sound and affirmed that the data collected before hind limb lameness was induced were valid as a control.
In most published studies in which hind limb lameness was induced in dogs, the vertical GRF parameters (PFz, MFz and IFz) were significantly lower in the affected limb (Fig. 3) and IFz and PFz were increased in the contralateral hind limb (O’Connor et al., 1989; Rumph et al., 1993, 1995; Dupuis et al., 1994; Jevens et al., 1996), the exceptions to these studies being Budsberg (2001) and Ballagas et al. (2004).
However, adaptations in the vertical GRF parameters in forelimbs varied among studies (Fig. 3). Similar to the observations in induced lameness, most clinical studies observed a decrease in GRF values in the affected hind limb and an increase in these values in the contralateral hind limb, while the results for the forelimbs varied again among the studies (Fig. 3). Taken together, comparison of the results from this study with clinical studies shows that the load redistribution pattern observed in walking dogs which were lame due to stifle disease was most comparable with the results from this study.
A confounding factor when comparing different studies is that one or more parameters critical to the recorded gait parameters may vary. For example, speed, gait or breeds have been shown to affect GRF characteristics (Riggs et al., 1993;
McLaughlin and Roush, 1994; Renberg et al., 1999; Evans et al., 2003; Mölsa et al., 2010; Voss et al., 2010, 2011). Furthermore, differences in data collection (e.g. force plates in a walkway vs. instrumented treadmill) or the degree and cause of lameness (e.g. location within the limb or induced vs. clinical lameness) may have an impact on the compensatory load shifting. For example, unloading of the affected limb in dogs with induced stifle joint lameness due to transaction of the craniate cruciate ligament or synovitis (33–81% reduction in PFz; O’Connor et al., 1989; Rumph et al., 1993,
1995; Dupuis et al., 1994; Jevens et al., 1996; Budsberg, 2001; Ballagas et al., 2004) generally produced a greater effect than in dogs with clinical stifle or hip joint lameness (2–18%; Budsberg et al., 1988; Hofmann, 2002; Katic et al., 2009;
Böddeker et al., 2012). This may partially explain why the locomotor adaptations to hind limb lameness observed in this study, inducing a 34 ± 9% reduction in PFz, compared better with the more severe lameness studied previously (Dupuis et al., 1994).
To limit variability in the results introduced by differences among patient populations and the experimental setting, and to allow for the direct comparison between the sound and the lame condition in the same individual, lameness was induced in this study instead of enrolling patients. Furthermore, the induced lameness model controlled for the cause and degree of lameness. Therefore, in contrast to clinical patients, which may only show lameness during faster gaits when greater locomotor forces act and thus the level of discomfort and pain increases, the degree of unloading was the same during walking and trotting in this study, forcing the animal to redistribute loading for both gaits.
Despite profound mechanical differences between the two gaits studied, such as the inverted pendulum vs. the spring-mass behaviour of the legs and thus differences in the trajectory of the centre of mass (CoM) of the body (Dickinson et al., 2000), the load redistribution was comparable in this study. In both gaits, the BW was shifted to the contralateral side and cranially. Only one difference was observed; IFz increased in the contralateral forelimb during walking, but did not significantly change during trotting (Fig. 3). Similarly, in dogs with induced forelimb lameness, load redistribution was comparable between walking and trotting (except PFz in the contralateral forelimb; Abdelhadi et al., 2013). Therefore, all other factors being equal (e.g. cause and degree of unloading, breed), dogs which walk and trot at their preferred speeds appear to redistribute the loading of the limbs in a similar way.
Furthermore, during both walking and trotting, relative stance duration increased in both limbs contralateral to the affected limb. However, gait-dependent differences were observed in the stance adaptations of the ipsilateral limbs; relative stance duration decreased in the forelimb during walking and increased in the hind limb
during trotting. The shorter contact time, associated with a larger peak force, most likely acted as a compensatory mechanism so that the mean force and impulse in the ipsilateral forelimb could be maintained. The longer contact times of both hind limbs during trotting resulted in a reduction of the shared swing phase of the hind limbs.
During walking, the significant increase in the relative stance duration of the contralateral forelimb was first and foremost due to a later lift-off. Since this later lift- off is associated with a greater limb retroversion (S. Fischer unpublished observations), the paw of the contralateral forelimb would be placed closer to the CoM, which may facilitate the unloading of the affected hind limb (Roy, 1971).
Compared to the sound condition, relative stance duration of the affected hind limb decreased significantly during walking, but not during trotting.
In dogs, the cranio–caudal body mass distribution has been shown to vary slightly among breeds, but the forelimbs consistently bear a greater percentage of BW than the hind limbs. In the Beagles, as in other mesomorphic breeds, the forelimbs bear
~60% and the hind limbs ~40% of the BW (Rumph et al., 1994; Bertram et al., 2000;
Katic et al., 2009; Abdelhadi et al., 2013). Due to this difference in loading, the dog’s mechanism to cope with fore vs. hind limb lameness was expected to differ (O’Connor et al., 1989; Rumph et al., 1993, 1995; Dupuis et al., 1994; Jevens et al., 1996; Katic et al., 2009). However, the comparison of the changes in the vertical GRF values and the temporal gait parameters shows some striking similarities.
Since the same experimental design, cause and degree of lameness were used, the results of the present study are comparable with those of Abdelhadi et al. (2013); in both studies, there were reductions in PFz at walk (35 ± 9% vs. 34 ± 4%, respectively) and trot (33 ± 9% vs. 34 ± 12%), respectively. While the ipsilateral hind limb showed no change when forelimb lameness was induced, PFz increased in the ipsilateral forelimb in hind limb lameness. However, this increase was combined with a decreased stance duration, which resulted in unchanged MFz and IFz, similar to the results for the ipsilateral hind limb in forelimb lameness (Abdelhadi et al., 2013).
Thus, changes in load redistribution and temporal gait variables were very similar and appeared not to be dependent on whether a forelimb or a hind limb was affected.
These observations suggest that: (1) ground contact times decreased in the limb
ipsilateral to the affected limb and increased in the contralateral limbs; and (2) the CoM was shifted to the contralateral body side and to the rear in forelimb lameness and to the front in hind limb lameness.
3.6. Conclusion
The lameness model used in this study controlled several parameters, which probably introduce variability in the results and permitted precise determination of the degree and cause of lameness. When all variables are comparable, dogs ambulating at their preferred speeds redistribute the load among the limbs and adapted their temporal gait parameters regardless of the gait and whether a forelimb or a hind limb is affected. Dogs unloaded the affected limb and shifted the CoM to the contralateral side and cranio- caudally to the side opposite to the affected limb.
3.7. Acknowledgements
The authors wish to thank J. Abdelhadi, A. Fuchs, V. Galindo-Zamora and D.
Helmsmüller for discussions and their assistance in the data collection and analyses.
This study was supported via a scholarship to SF by Modul Graduiertenkolleg Biomedizintechnik des SFB 599 funded by the German Research Foundation (DFG) (to IN), Hannoversche Gesellschaft zur Förderung der Kleintiermedizin e.V. (HGFK), and the Center of Interdisciplinary Prevention of Diseases related to Professional Activities (KIP) funded by the Berufsgenossenschaft Nahrungsmittel und Gastgewerbe, Erfurt and the Friedrich-Schiller-University Jena (to NS).
3.8. References
Abdelhadi, J., Wefstaedt, P., Galindo-Zamora, V., Anders, A., Nolte, I., Schilling, N., 2013. Load redistribution in walking and trotting Beagles with induced forelimb lameness. American Journal of Veterinary Research 74, 34-39.
Ballagas, A.J., Montgomery, R.D., Henderson, R.A., Gillette, R.L., 2004. Pre- and postoperative force plate analysis of dogs with experimentally transected cranial
cruciate ligaments treated using tibial plateau leveling osteotomy. Veterinary Surgery 33, 187-190.
Bertram, J.E.A., Lee, D.V., Case, H.N., Todhunter, R.J., 2000. Comparison of the trotting gaits of Labrador Retrievers and Greyhounds. American Journal of Veterinary Research 61, 832-838.
Bertram, J.E.A., Lee, D.V., Todhunter, R.J., Foels, W.S., Williams, A.J., Lust, G., 1997. Multiple force platform analysis of the canine trot: a new approach to assessing basic characteristics of locomotion. Veterinary and Comparative Orthopaedics and Traumatology 10, 160-169.
Bockstahler, B.A., Skalicky, M., Peham, C., Müller, M., Lorinson, D., 2007. Reliability of ground reaction forces measured on a treadmill system in healthy dogs. The Veterinary Journal 173, 373-378.
Böddeker, J., Drüen, S., Meyer-Lindberg, A., Fehr, M., Nolte, I., Wefstaedt, P., 2012.
Computer-assisted gait analysis of the dog: Comparison of two surgical techniques for the ruptured cranial cruciate ligament. Veterinary and Comparative Orthopaedics and Traumatology 25, 11-21.
Budsberg, S., 2001. Long-term temporal evaluation of ground reaction forces during development of experimentally induced osteoarthritis in dogs. American Journal of Veterinary Research 62, 1207-1211.
Budsberg, S., Verstraete, M.C., Soutas-Little, R.W., Flo, G.L., Probst, A., 1988. Force plate analyses before and after stabilization of canine stifles for cruciate injuries.
American Journal of Veterinary Research 49, 1522-1524.
Budsberg, S.C., Jevens, D.J., Brown, J., Foutz, T.L., DeCamp, C.E., Reece, L., 1993. Evaluation of limb symmetry indices, using ground reaction forces in healthy dogs. American Journal of Veterinary Research 54, 1569-1574.
Budsberg, S.C., Verstraete, M.C., Soutas-Little, R.W., 1987. Force plate analysis of the walking gait in healthy dogs. American Journal of Veterinary Research 48, 915-918.
Carrier, D.R., Deban, S.M., Fischbein, T., 2008. Locomotor function of forelimb protractor and retractor muscles of dogs: Evidence of strut-like behavior at the shoulder. Journal of Experimental Biology 211, 150-162.
Cavagna, G.A., Heglund, N.C., Taylor, C.R., 1977. Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure. American Journal of Physiology 233, R243-R261.
Conzemius, M.G., Evans, R.B., Besancon, M.F., Gordon, W.J., Horstman, C.L., Hoefle, W.D., Nieves, M.A., Wagner, S.D., 2005. Effect of surgical technique on limb function after surgery for rupture of the cranial cruciate ligament in dogs.
Journal of the American Veterinary Association 226, 232-236.
Dickinson, M.H., Farley, C.T., Full, R.J., Koehl, M.A.R., Kram, R., Lehmann, S., 2000.
How animals move: an integrative view. Science 288, 100-106.
Dupuis, J., Harari, J., Papageorges, M., Gallina, A.M., Ratzlaff, M., 1994. Evaluation of fibular head transposition for repair of experimental cranial cruciate ligament injury in dogs. Veterinary Surgery 23, 1-12.
Evans, R., Gordon, W., Conzemius, M., 2003. Effect of velocity on ground reaction forces in dogs with lameness attributable to tearing of the cranial cruciate ligament. American Journal of Veterinary Research 64, 1479-1481.
Evans, R.B., Horstman, C., Conzemius, M., 2005. Accuracy and optimization of force platform gait analysis in Labradors with cranial cruciate disease evaluated at a walking gait. Veterinary Surgery 34, 445-449.
Fanchon, L., Grandjean, D., 2007. Accuracy of asymmetry indices of ground reaction forces for diagnosis of hindlimb lameness in dogs. American Journal of
Veterinary Research 68, 1089-1094.
Gordon, W.J., Conzemius, M.G., Riedesel, E., Besancon, M.F., Evans, R., Wilke, V., Ritter, M.J., 2003. The relationship between limb function and radiographic osteoarthrosis in dogs with stifle osteoarthrosis. Veterinary Surgery 32, 451-545.
Gray, J., 1968. Animal locomotion. Norton, New York, 1-479.
Herzog, W., Nigg, B.M., Read, L.J., Olsson, E., 1989. Asymmetries in ground reaction force patterns in normal human gait. Medicine and Science in Sports and Excercise 21, 110-114.
Hildebrand, M., 1966. Analysis of the symmetrical gaits of tetrapods. Folia Biotheoretica 6, 9-22.
Hoelzler, M.G., Millis, D.L., Francis, D.A., Weigel, J.P., 2004. Results of arthroscopic versus open arthrotomy for surgical management of cranial cruciate ligament deficiency in dogs. Veterinary Surgery 33, 146-153.
Hofmann, D., 2002. Ganganalytisches Profil verschiedener Gelenkerkrankungen beim Hund. Dissertation Tierärztliche Fakultät, Ludwig-Maximilians-Universität München, 1-127.
Jevens, D.J., DeCamp, C.E., Hauptman, J., Braden, T.D., Richter, M., Robinson, R., 1996. Use of force-plate analysis of gait to compare two surgical techniques for treatment of cranial cruciate ligament rupture in dogs. American Journal of Veterinary Research 57, 389-393.
Jevens, D.J., Hauptman, J.G., DeCamp, C.E., Budsberg, S.C., Soutas-Little, R.W., 1993. Contributions to variance in force-plate analysis of gait in dogs. American Journal of Veterinary Research 54, 612-615.
Johnson, J.A., Austin, C., Breuer, G.J., 1994. Incidence of canine appendicular musculoskeletal disorders in 16 veterinary teaching hospitals from 1980 through 1989. Veterinary and Comparative Orthopaedics and Traumatology 7, 56-69.
Katic, N., Bockstahler, B.A., Müller, M., Peham, C., 2009. Fourier analysis of vertical ground reaction forces in dogs with unilateral hindlimb lameness caused by degenerative disease of the hip joint and in dogs without lameness. American Journal of Veterinary Research 70, 118-126.
Leach, D., Sumner-Smith, G., Dagg, A.I., 1977. Diagnosis of lameness in dogs: A preliminary study. Canadian Veterinay Journal 18, 58-63.
Lee, D.V., Bertram, J.E., Todhunter, R.J., 1999. Acceleration and balance in trotting dogs. Journal of Experimental Biology 202, 3565-3573.
Madore, E., Huneault, L., Moreau, M., Dupuis, J., 2007. Comparison of trot kinetics between dogs with stifle or hip arthrosis. Veterinary and Comparative
Orthopaedics and Traumatology 20, 102-107.
McLaughlin, R.M.J., Roush, J.K., 1994. Effects of subject stance time and velocity on ground reaction forces in clinically normal greyhounds at the trot. American Journal of Veterinary Research 55, 1666-1671.
Mölsa, S.H., Hielm-Björkman, A.K., Laitinen-Vapaavouri, O.M., 2010. Force platform analysis in clinically healthy Rottweilers: comparison with Labrador Retrievers.
Veterinary Surgery 39, 701-707.
O'Connor, B.L., Visco, D.M., Heck, D.A., 1989. Gait alterations in dogs after
transection of the anterior cruciate ligament. Arthritis and Rheumatism 32, 1142- 1147.
Quinn, M.M., Keuler, N.S., Lu, Y., Faria, M.L.E., Muir, P., Markel, M.D., 2007.
Evaluation of agreement between numerical rating scales, visual analogue scoring scales, and force plate gait analysis in dogs. Veterinary Surgery 36, 360- 367.
Ragetly, C.A., Griffon, D.J., Mostafa, A.A., Thomas, J.E., Hsiao-Wecksler, E.T., 2010.
Inverse dynamics analysis of the pelvic limbs in Labrador retrievers with and without cranial cruciate ligament disease. Veterinary Surgery 39, 513-522.
Renberg, W.C., Johnston, S.A., Ye, K., Budsberg, S.C., 1999. Comparison of stance time and velocity as control variables in force plate analysis of dogs. American Journal of Veterinary Research 60, 814-819.
Riggs, C.M., DeCamp, C.E., Soutas-Little, R.W., Braden, T.D., Richter, M.A., 1993.
Effects of subject velocity on force plate-measured ground reaction forces in healthy Greyhounds at the trot. American Journal of Veterinary Research 54, 1523-1526.
Roy, W.E., 1971. Examination of the canine locomotor system. Veterinary Clinics of North America: Small animal practice 1, 53-70.
Rumph, P.F., Kincaid, S.A., Baird, D.K., Kammermann, J.R., Visco, D.M., Goetze, L.F., 1993. Vertical ground reaction force distribution during experimentally induced acute synovitis in dogs. American Journal of Veterinary Research 54, 365-369.
Rumph, P.F., Kincaid, S.A., Baird, D.K., Kammermann, J.R., West, M.S., 1995.
Redistribution of vertical ground reaction force in dogs with experimentally induced chronic hindlimb lameness. Veterinary Surgery 24, 384-389.
Rumph, P.F., Lander, J.E., Kincaid, S.A., Baird, D.K., Kammermann, J.R., Visco, D.M., 1994. Ground reaction force profiles from force platform gait analyses of
clinically normal mesomorphic dogs at the trot. American Journal of Veterinary Research 55, 756-761.
Schilling, N., Fischbein, T., Yang, E.P., Carrier, D.R., 2009. Function of extrinsic hindlimb muscles in trotting dogs. Journal of Experimental Biology 212, 1036- 1052.
Seibert, R., Marcellin-Little, D., Roe, S.C., DePuy, V., Lascelles, B.D., 2012.
Comparison of body weight distribution, peak vertical force, and vertical impulse as measures of hip joint pain and efficiacy of total hip replacement. Veterinary Surgery 41, 443-447.
Steiss, J.E., Yuill, G.T., White, N.A., Bowen, J.M., 1982. Modifications of a force plate system for equine gait analysis. American Journal of Veterinary Research 43, 538-540.
Thrusfield, M., Ortega, C., de Blas, I., Noordhuizen, J.P., Frankena, K., 2001. Win Episcope 2.0: improved epidemiological software for veterinary medicine.
Veterinary Record 148, 567-572.
Voss, K., Damur, D.M., Guerrero, T., Haessig, M., Montavon, P.M., 2008. Force plate gait analysis to assess limb function after tibial tuberosity advancement in dogs with cranial cruciate ligament disease. Veterinary and Comparative Orthopaedics and Traumatology 21, 243-249.
Voss, K., Galeandro, L., Wiestner, T., Heassig, M., Montavon, P.M., 2010.
Relationships of body weight, body size, subject velocity, and vertical ground reaction forces in trotting dog. Veterinary Surgery 39, 863-869.
Voss, K., Imhof, J., Kaestner, S., Montavon, P.M., 2007. Force plate gait analysis at the walk and trot in dogs with low-grade hindlimb lameness. Veterinary and Comparative Orthopaedics and Traumatology 20, 299-304.
Voss, K., Wiestner, T., Galeandro, L., Hässig, M., Montavon, P.M., 2011. Effect of dog breed and body conformation on vertical ground reaction forces, impulses, and stance times. Veterinary and Comparative Orthopaedics and Traumatology 24, 106-112.
3.9. Tables and Figures
Tab. 1. Load distribution indicated by peak vertical forces (PFz), mean vertical forces (MFz), and vertical impulse (IFz) in % bodyweight (BW) for the sound condition and when lameness was induced in the right hind limb (ipsilateral hind limb, Hi).
Significant at * P<0.05, ** P<0.01, *** P<0.001; n.s.=not significant.
sound lame sound lame
Fc Fi
Walk PFz 29.2±0.8 30.9±1.2 n.s. 29.3±0.8 32.0±0.7 ***
MFz 30.5±0.7 32.6±1.0 * 29.8±1.0 30.9±0.8 n.s.
IFz 31.3±1.0 33.6±1.3 * 30.6±1.1 30.4±1.1 n.s.
Trot PFz 29.6±1.2 31.0±1.5 n.s. 29.8±1.1 31.9±1.1 *
MFz 29.0±1.1 31.1±1.6 * 28.5±1.2 30.2±1.4 n.s.
IFz 31.4±1.5 33.2±2.0 n.s. 31.1±1.2 31.2±1.6 n.s.
Hc Hi
Walk PFz 20.8±0.9 23.6±1.3 *** 20.7±0.7 13.5±1.8 ***
MFz 19.8±0.9 22.2±1.5 ** 19.9±0.8 14.4±2.1 ***
IFz 18.9±1.2 22.3±1.5 *** 19.2±0.7 13.7±2.1 ***
Trot PFz 20.4±1.0 23.6±0.8 *** 20.3±1.8 13.5±1.6 ***
MFz 21.3±1.1 24.5±1.0 *** 21.3±1.3 14.2±1.7 ***
IFz 18.9±1.2 22.5±1.6 *** 18.6±1.5 13.1±1.9 ***
Tab. 2. Symmetry indices for the sound condition and when lameness was induced in the right hind limb (i.e., ipsilateral hind limb). Perfect symmetry is given at SI=0.
Negative values indicate that the respective parameter was greater for the contralateral than the ipsilateral limb; positive values indicate the opposite. Significant at * P<0.05, ** P<0.01, *** P<0.001; n.s.=not significant.
Forelimb Hindlimb
sound lame sound lame
Walk PFz 0.3±1.6 3.6±2.6 ** -0.5±1.7 -54.8±14.9 ***
MFz -2.5±2.8 -5.3±3.1 n.s. 0.8±4.0 -42.7±19.3 ***
IFz -2.2±3.7 -10.2±5.1 * 1.9±5.5 -47.9±19.3 ***
Trot PFz 0.8±1.6 3.1±7.1 n.s. -0.7±1.6 -55.1±13.2 ***
MFz -1.8±2.3 -3.1±8.2 n.s. 0.0±3.9 -53.6±13.0 ***
IFz -1.1±2.3 -6.2±9.0 n.s. -1.9±3.9 -53.7±16.6 ***
Tab. 3. Relative stance duration (D) in sound dogs and when lameness was induced in the right hind limb (ipsilateral hind limb, Hi). Significant at * P<0.05, ** P<0.01, ***
P<0.001; n.s.=not significant.
sound lame sound lame
Fc Fi
Walk 64.0±1.0 65.7±1.4 * 64.1±1.5 62.2±2.0 **
Trot 53.6±2.7 55.8±1.9 ** 54.0±2.4 54.2±2.4 n.s.
Hc Hi
Walk 59.2±1.6 64.8±2.5 *** 60.2±1.5 59.3±3.7 n.s.
Trot 44.0±4.4 48.6±4.9 ** 43.9±4.4 48.2±4.0 **
Fig. 1. Stride cycle with mean ± standard deviation (SD) stance duration for footfall patterns of all eight Beagles during walking (A) and trotting (B) for the sound (control) condition (black bars) and after lameness was induced (grey bars) in the right hindlimb (ipsilateral hindlimb, Hi). Stance duration was the interval between touch- down to lift-off of a paw. *Touch-down of the paw of a limb after induced lameness was shifted significantly during walking (Fc P < 0.05) and at trotting (Hc P < 0.05; Hi P
< 0.01), in comparison with results for that same limb in the sound condition. Stride cycle was the interval between touch-down to next touch-down of the same limb.
Fc = contralateral forelimb. Fi = ipsilateral forelimb Hc = contralateral hind limb. Hi = ipsilateral hind limb (i.e., affected limb, bold).
Fig. 2. Vertical ground reaction forces of all eight Beagles during walking (A) and trotting (B) for the sound (control) condition (black) and after lameness was induced (grey) in the right hind limb (ipsilateral hind limb, Hi). Plotted are the mean values as well as the standard deviations (SDs) as error bars. Stance duration was the interval between touch-down to lift-off of the respective limb.
Fc = contralateral forelimb. Fi = ipsilateral forelimb Hc = contralateral hind limb. Hi = ipsilateral hind limb (i.e., affected limb, bold).
Fig. 3. Summary of the results of this study and previous studies illustrating the changes in the GRF parameters due to induced (A) and clinical (B) hind limb lameness. Triangles pointing upwards indicate a significant increase in the respective parameter and limb. Triangles pointing downwards indicate a significant decrease of the parameter. Horizontal bars represent no change. Solid symbols illustrate the observations for the walk, open symbols for the trot.
Fc = contralateral forelimb. Fi = ipsilateral forelimb Hc = contralateral hindl imb. Hi = ipsilateral hind limb (i.e., affected limb, bold). PFz = peak vertical force. MFz = mean vertical force. IFz = vertical impulse.
4. Studie II
Die folgende Studie wurde am 04.02.2013 bei PloS One eingereicht.
Manuskript Nummer: PONE-S-13-06194
Adaptations in muscle activity to induced hindlimb lameness in trotting dogs
S. Fischer a, I. Nolte a, N. Schilling b*
a University of Veterinary Medicine Hannover, Foundation, Small Animal Clinic, Hannover, Germany
b Friedrich-Schiller-University, Institute of Systematic Zoology and Evolutionary Biology, Jena, Germany
*Corresponding author
Short title: Muscle activity adaptations to hindlimb lameness
4.1. Abstract
Muscle tissue has a great intrinsic adaptability to changing functional demands.
Triggering more gradual responses such as tissue growth, the immediate responses to altered loading conditions involve changes in the activity patterns. Because a loss of limb function is associated with marked deviations in the gait pattern, understanding the muscular responses in laming animals will provide further insight into their compensatory mechanisms as well as help to improve treatment options to prevent musculoskeletal sequelae in chronic patients. Therefore, this study evaluated the changes in muscle activity in adaptation to a moderate, load-bearing hindlimb lameness in two leg and one back muscle using surface electromyography (SEMG).
In eight sound adult dogs that trotted on an instrumented treadmill, bilateral, bipolar recordings of the m. triceps brachii, the m. vastus lateralis and the m. longissimus dorsi were obtained before and after lameness was induced. Consistent with the unchanged vertical forces as well as temporal parameters, neither the timing nor the excitement changed significantly in the m. triceps brachii. In the ipsilateral m. vastus lateralis, peak activity and integrated SEMG area were decreased, while they were significantly increased in the contralateral limb. In both sides, the duration of the muscle activity was significantly longer due to a delayed offset. These observations are in accordance with previously described kinetic and kinematic changes as well as changes in muscle mass. Alterations in the activation patterns of the m. longissimus dorsi concerned primarily the unilateral activity and is discussed regarding known alterations in truncal and limb motions. The results of this study using a transient hindlimb lameness model indicate that SEMG is a valuable diagnostic tool to detect muscular adaptations to altered functional demands. Hence, it should be further established in basic and clinical veterinary medicine in order to improve therapeutic and rehabilitative management of orthopedic patients.
Keywords: gait analysis, canine, electromyography, Canis
4.2. Introduction
Muscle is one of the most plastic tissues in the animal body. Its great phenotypic plasticity allows it to adapt to various tasks and respond to changing functional demands throughout life (reviewed in [1]). While immediate responses to altered functional requirements involve for example changes in muscle recruitment and activation patterns, more gradual adaptations include quantitative and qualitative changes in gene expression as well as tissue growth and remodeling [2,3]. When diseased or injured, however, an animal must immediately respond to the new situation to ensure survival and this is first and foremost accomplished by adaptations in muscular recruitment.
To cope with the loss of limb function, animals have evolved compensatory strategies, and the resulting lameness is marked by deviations of the animal’s gait from the physiological pattern. Locomotor adaptations to lameness include changes in kinetics and kinematics as well as muscle activity. While the changes in the ground reaction forces (GRF) (e.g., hindlimb lameness in dogs [4-9]) or the motion patterns (e.g., [10-17]) are comparatively well established, adaptations in muscle activity have only been studied marginally. Nonetheless, the consistently observed redistribution of body weight and the dynamic shift of the position of the center of body mass (CoM) alters the loading of the limbs and the trunk and must be met and are accomplished by changes in muscle function. Because such changes in muscle function trigger more gradual tissue responses [3] and muscles are the primary determinant of joint loading, stimulating skeletal remodeling or joint degeneration [18], understanding the adaptations in muscle activity to altered functional demands will provide insight into their short- and long-term effects on the musculoskeletal system.
One mean to evaluate muscle function is to record the electrical signal associated with the activation of the muscle fibers (i.e., electromyography, EMG). Besides its widespread use in basic physiological and biomechanical studies, EMG is a standard tool in medical research, sport sciences and rehabilitation in humans with nowadays hundreds of publications a year [19]. Compared to that, EMG seems still in the fledging stages in veterinary medicine [20]. EMG has been used in numerous studies to document the activity of a series of limb and back muscles in sound dogs for
