Central Journal of Veterinary Medicine and Research

Research Article *Corresponding author Shenja Loderstedt, Small Animal Clinic (WE20), FreieUniversität Berlin, Oertzenweg 19b, 14163 Berlin, Evaluation of the biceps tendon Germany, Tel: 49 30 838 62356 / 422; Email:

Submitted: 17 October 2014 in dogs Accepted: 13 December 2014 Felix Giebels1, Barbara Kohn1, Nadia Shihab2, Holger A Volk3 and Published: 15 December 2014 Shenja Loderstedt1* Copyright © 2014 Loderstedt et al. 1Small Animal Clinic (WE20), Department of Veterinary Medicine, Freie Universität Berlin, Germany OPEN ACCESS 2Southern Counties Veterinary Specialists, Unit 6 Forest Corner Farm, UK 3 Department of Clinical Science and Services, Royal Veterinary College, University of Keywords London, UK • Biceps • Dog; Interobserver-agreement Abstract The biceps tendon reflex (BTR) of thirty-two dogs with a median age of 5 (0.5- 15) years and a median weight of 17.5 (5.8-57) kg was assessed by two examiners. The examinations were videotaped and evaluated by 12 observers. The observers were divided in three groups depending on level of expertise (neurologists, veterinary surgeons and students). Each group evaluated the reflex-presence and reflex-briskness. Kappa-analysis and Intercorrelation-coefficient (ICC) were applied for analysis of interobserver-agreement. Logistic regression analysis was used to investigate the influence of sex, age, weight, fur length and examiner on the interobserver-agreement. The interobserver-agreement was highest for the neurologist-group and lowest for the student-group. Neither sex, weight, age, fur length or the person who did the exam influences the interobserver-agreement. The level of expertise is an influencing factor on interobserver-agreement of canine BTR evaluation. In healthy dogs the BTR can be reliable assessed by veterinary neurologists. The clinical significance is still unknown as the BTR was only assessed in healthy dogs.

ABBREVIATIONS ANOVA: Analysis of Variance; BTR: examination to determine the neuroanatomical localization of a CI (95%): ICC: lesion and therefore requires being comparable between different KC: Cohen´s Kappa; KF: Fleiss-Kappa;Biceps Tendon KW: Reflex; observers [10]. Different studies in human medicine aimed to Kappa; SE: 95% ConfidenceSEM: interval; Inter Correlation identify such influencing factors and objectify the reflex-activity Coefficient; Weighted by different standardization procedures of the examination and INTRODUCTION Standard Error; Standard Error of the Mean the evaluation of the reflex-activity [8,11-13]. The aims of this study were: (1) evaluation of interobserver- In veterinary literature, authors rarely report the biceps agreement of BTR assessment depending on the observer´s level tendon reflex (BTR) when describing the neurological of expertise and (2) detection of influencing factors for the BTR examination findings in dogs. The BTR has been described to response.MATERIALS AND METHODS be non-consistent and challenging to elicit [1-4]. In human medicine, on the other hand the BTR is thought to be reliable and is commonly used for the assessment of the integrity of the Thirty-two dogs of different breeds with a median age of 5 cervical segments C5-C6 and the brachial plexus and also for the (0.5-15) years and a median weight of 17.5 (5.8-57) kg were diagnosis and follow-up of cervical myelopathies [5,6]. In dogs, included. There were twenty female and twelve male dogs. Eleven the musculocutaneous nerve, the function of which is tested by (34.4%) dogs were mixed breed (Table 1). Including criteria this reflex, originates from the spinal-cord-segments C6-C8 and were a normal clinical, orthopedic and neurological examination innervates the canine biceps brachii muscle, a flexor of the elbow. and no history of neurological disorders. Examinations were The reflex response involves an elbow flexion and/ or movement performed by two of the authors (FG, SL) and videotaped under over the biceps brachii muscle [3]. standardised conditions: same room, fixed camera position, lateral recumbency of the dog, same reflex-hammer. Each dog In general, segmental can be influenced was examined by one or both examiners within one hour, each by a number of factors [4,7] and its evaluation is highly subjective examination took about 3 minutes. The owner was watching the [8,9]. It remains, however, an integral part of the neurological dog´s head during the examination. Dogs were anonymised by Cite this article: Giebels F, Kohn B, Shihab N, Volk HA, Loderstedt S (2014) Evaluation of the biceps tendon reflex in dogs. J etV Med Res 1(3): 1013. Loderstedt et al. (2014) Email: Central

Table 1: Age Weight Number OverviewSex of the examinedBreed dogs. by both examiners and nineteen by only one examiner, so that (years) (kg) altogether one hundred and three examination-sequences were fa observed.Data analysis 1 f Mixed 0,5 16 2 f Bavarian scenthound 2 19 For statistical data analysis SigmaPlot 11.1 (Systat Software 3 f Marshall Beagle 4 10 table of agreement Inc.) and SPSS Statistics 22.0 (IBM) were used. The results were 5 f 4 Mixed 3 8 tabulated in a ‘ ’ [15] depending on their level of f Mixed 2 16 agreement among each group. Interobserver-agreement between C W 6 f Dalmatian 6 26,5 the observers and between the groups was analysed using Kappa analysis. The Cohen´s Kappa (K )- and weighted Kappa (K )- 7 f Giant Schnauzer 2 18 values were calculated for each pair of observers, including 98 Mixed 96 17 thepoor pair of examiners,slight within eachfair group. According moderate to Landis’ m b Golden Retriever 39 and Koch (1977)substantial the strength of agreement wasnear designated perfect as to 10 m Mixed 12 18,5 perfect‘ ’ (Κ<0.0), ‘ ’ (0.0≤Κ≤0.2), ‘ ’ (0.21≤Κ≤0.4), ‘ f (0.41≤Κ≤0.6), ‘ ’ (0.61≤Κ≤0.8), and ‘ 11 m Mixed 7 30 C W F ’ (0.81≤Κ≤1.0). ANOVA was used to test significance of 12 f Mixed 2 27,5 the mean Κ , mean Κ - and Fleiss-Kappa (K )-values between f 13 Labrador 2,5 25,5 the three groups of observers. For every K-value standard error KF 14 f Mixed 1,25 10 (SE) and the 95% Confidence interval (CI 95%) were calculated. 15 f Mixed 8,5 23 does not take into account the grade of discrepancy between the observers, so the Intercorrelation Coefficient (ICC; two- 16 f Labradoodle 4,5 23 way random, absolute agreement definition) was additionally f 17 Belgian Malinois 7,5 24,7 calculated for the reflex-briskness for each group. The ICC of each 18 French bulldog 4,5 10,6 group was compared to each other using one-way ANOVA under 19 mf Greater swiss mountaindog 7 57 estimation of the standard error of the mean (SEM). The p-values were Holm-Šidak adjusted. Furthermore, data from reflex- 20 Mixed 6 11,8 presence evaluation were used for regression analysis. The dogs 21 m Labrador 1,5 28 were subdivided into groups depending on sex, weight, age, fur 22 m Australianshepherd 1 12 length and Pthe examining person (Table 2). The interobserver- 23 mf Australianshepherd 2,5 15 agreement was set as dependent variable, all others were RESULTS 24 Australiancattledog 5,5 20 covariates. <0.05 was considered significant. 25 m BostonTerrier 14 6,4 Analysis of reliability 26 mf Bernese mountaindog 6,75 40,5 a) Reflex-presence: C F 27 Dachshund 12,2 14,75 substantial Mean K (0.706)- and K (0.753)-value 28 m German Shorthairedpointer 2,5 40 C near perfect to perfect’ are significantly highest (‘ ’) for Group 1, where the (‘fair’) C F 29 m Wire-haired dachshund 12 7,35 highest K -value (0.852) is ‘ . Group 2 shows 30 mf YorkshireTerrier 4,5 5,8 the second highest mean K (0.401)- and K (0.380)-value (‘fair’) C f and Group 3 has the lowest interobserver-agreement in the 31 AustralianTerrier 11,25 10 and a KF C Abbreviations: a reflex-presence evaluation with a mean K -value of 0.313 32 Mixed 6 8,4 (‘substantial’) b -value of 0.304. The K -value for the pair of examiners f: female; m: male wasb) 0.658 Reflex-briskness: (Figure 1). randomised numbering. The examination footage was evaluated The number of Complete agreement- by 12 observers. Observers were divided into three groups of four evaluations was highest for Group 1 (65.1%; n=67) and lowest for depending on their level of expertise: veterinary neurologists Group 3 (24.3%; n=25). Group 2 shows most often a discrepancy (Group 1), veterinary surgeons without special affinity to of one point among the observers; Group 3 has the highest neurology and three to four years of work experience (Group number of two-point-discrepancy decisions. The total amount 2) and final year veterinary students (Group 3). Both examiners of non-agreement-decisions (sum of Partial (dis)agreement and were included in Group 1 and evaluated the anonymised video Complete disagreement-decisions) is 36/103 (35%) for Group 1; in the same manner. Each observer evaluated if the reflex was 66/103 (64.1%) for Group 2 and 79/103 (76.7%) for Group 3 present or absent (0=absent, 1=present) and scored the level (Figure 2). W F W ‘moderate’- of reflex briskness using a scoring-scale (0=absent; 1=reduced; Mean K (0.542)- and the K (0.331)-value are highest for F ‘fair’ 2=normal; 3=exaggerated; 4=clonus) [14]. One dog had an Group 1. For Group 1 and 2 the mean K is within the amputated right forelimb and two examination-videos had to level, whereas the K -value for both groups reach the -level. W is ‘fair’ be excluded due to poor quality resulting in sixty-one examined Group 3 shows the significant lowest interobserver-agreement thoracic limbs. Forty-two thoracic limbs of these were examined among the groups, where the mean K (0.286) and the J Vet Med Res 1(3): 1013 (2014) 2/7 Loderstedt et al. (2014) Email: Central

KF slight

W moderate’ ‘ ’ (0.17). No significance could be shown between Group reflexes in veterinary medicine [16-20]. De Lahunta and Glass W 1 and 2. The K -value for the pair of examiners was ‘ (2009) for veterinary and Litvan et al. (1996) for human (0.445), which is the lowest K -value within Group 1 (Figure 3). medicine stated that the patellar reflex has the highest reliability. De Lahunta and Glass (2009) stated their doubts regarding the ICC of Group 3 (0.321) is significant lower compared to Group reliability of tendon reflexes in the thoracic limbs. However, 1 and 2. Group 1 has the highest ICC (0.557). The difference this statement is based on personal experience rather than on comparedCorrelation to Group analysis 2 (0.483) is not significant (Figure 3). a systematic investigation of the interobserver-agreement. To the authors’ knowledge the present study is the first prospective analysis on interobserver-agreement of a tendon reflex in None of the parameters sex, age, weight, fur length or veterinary medicine. examiner show a significant influence on the interobserver- agreementDISCUSSION of the reflex-presence. In general, three factors can influence the interobserver- agreement: the examining person, the examined subject and the examination itself [21]. Perfect agreement‘moderate’ is highly unlikely Our data show that the interobserver-agreement of the in clinical studies [22] and many medical studies using Kappa BTR assessment in dogs increases with the observer’s level of analysis for reflex-evaluation score a interobserver- expertise, with experienced observers having a high level of agreement [10, 22-27]. Our data show that the canine BTR agreement. None of the examined parameters influenced the can be assessed reliably by experienced observers. However, interobserver-agreement in any of the three groups. comparing the results of different studies is critical since they differ in methodology, examiner`s expertise, task characteristics Several studies examined the reliability of different spinal or the applied scoring scale [25]. Besides the naturally occurring

Figure 1 A: C . B:KF ♦

Kappa analysis of reflex-presence. Mean K -value ( ) with its maximum and minimum value for each group. -value ( ) with the upper and lower bound of its CI(95%). Group 1=veterinary neurologists, Group 2= veterinary surgeons, Group 3 =veterinary students. (* =significant).

Figure 2 Complete agreement Partial (dis) agreement if one (1pt) (≥2pts) Complete disagreement if Table of agreement. Levels of agreement were: for equal scoring by all four observers, observer scored 1 point respectively atleast 2 points higher or lower than the other three observers and atleast two observers counted different. Group 1= veterinary neurologists, Group2= veterinary surgeons, Group3=veterinary students. Numbers above the columns represent the amount of each decision. J Vet Med Res 1(3): 1013 (2014) 3/7 Loderstedt et al. (2014) Email: Central

Figure 3 A: W . B: KF ♦ C:  Interobserver-agreement of the reflex-briskness. Mean K -value ( ) with its minimum and maximum value. - value ( ) with the upper and lower bound of its CI (95%). ICC ( ) with the upper and lower bound of it CI (95%). Group 1 = veterinary neurologists, Group 2 = veterinary surgeons, Group 3 = veterinary students.(*=significant). interobserver variability, other factors were described in both are included the lower the interobserver-agreement [12,22,24]. C human and veterinary medicine to have an influence on the This is in agreement with the results of the current study where W F reflex-activity such as intramuscular temperature, muscle tone, mean K -values are higher for each of the three groups compared positioning of the subject, patient´s age, body weight, and the to mean K -values. Additionally K -values are higher for the used armamentarium [7,28,29]. Increased muscle tone, fear dichotomous scoring of the reflex-presence than for the five- or anxiety [30,31] and a stress-induced hyperthermia of the point scoring-scale of reflex-briskness. patient [29] might influence the neurological examination of the O`Keeffe et al. (1994) stated that the performed technique veterinary patient. Several studies in human medicine attempted influences the reliability between observers. The examination to quantify the reflex response more objectively and in this technique differs slightly between both examiners in our study; way make it more reliable and comparable between observers however, the scoring did not show any significant difference [32,33]. Most of the studies that identified influencing factors of Table 2: the reflex-activity used electromyography (EMG) [7,15,20,31]. Subdivision of the dogs dependingon the covariates sex, weight, Due to the high vulnerability to confounding factors such as the age,Covariate furlength and the examining person.Total Percentage (%) activity of adjacent muscles [9,31,34] or the alertness [29] of the examined subject, EMG needs to be performed under general anesthesia in veterinary medicine [34] and thus is not performed Sex 39 37,9 routinely during the neurological exam. The aim of this study was male female to test the reliability of the BTR in a clinical setting to establish if 64 62,1 this test is useful for the routine neurological examination and therefore EMG studies were not performed. Weight 42 40,8 We standardized the examination procedure by using <15kg 15-30kg >30kg 46 44,7 standardized conditions for each subject, a scoring-scale and 15 14,6 video-analysis. Although video-analysis does not reflect clinical Age settings, several studies used it for interobserver-agreement calculation [8,27,35].Myotatic When reflex evaluating scales a videotape the setup is 38 36,9 the same for each observer and thus its results can be considered <3a 3-7a >7a 43 41,8 comparable. ‘ ’ [13] were developed as an 22 21,4 instrument to increase the comparability of reflex evaluation among different observers [32] and are routinely used in Furlength 38 36,9 veterinary and human medicine [11-14]. Manschot et al. longhairedshorthaired (1998) named three criterions for a scoring-scale to increase 65 63,1 interobserver-agreement:normal abnormal not too many categories, unambiguous formulated categories and the possibility to distinguish between ‘ ’ and ‘ ’. The higher the number of categories a ExaminerSL FG 47 45,6 scoring-scale has and the greater the number of observers that 56 54,4 J Vet Med Res 1(3): 1013 (2014) 4/7 Loderstedt et al. (2014) Email: Central

CONFLICT OF INTEREST between them and therefore can most likely be neglected [22]. Different authors showed that knowledge of the patient´s history None of the authors of this paper has a financial or personal improve significantly the reliability [10,26]. Except of the two relationship with other people or organisations that could examiners none of the observers was aware of the unremarkable inappropriatelyREFEERENCES influence or bias the content of the paper. clinical, orthopaedic and neurological examination and absence of any history of neurological disorders within the study C population. Nevertheless the agreement for the non-blinded pair 1. Braund KG, Sharp JH. Textbook of Small Animal Surgery. Slatter D, W of examiners was only medium for the reflex-presence (K =0.658) editor. 3rd ed. Philadelphia: Saunders. 2002. and lowest for the reflex-briskness (K =0.445) within Group 2. Oliver JE, Lorenz MD, Kornegay JN, editors. Handbook of Veterinary 1. 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Cite this article Giebels F, Kohn B, Shihab N, Volk HA, Loderstedt S (2014) Evaluation of the biceps tendon reflex in dogs. J Vet Med Res 1(3): 1013.

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