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Original article

Complex strength performance in patients with haemophilia A Method development and testing B. Runkel; M. Kappelhoff; T. Hilberg Department of Sports Medicine, University of Wuppertal, Germany

Keywords

Schlüsselwörter

Haemophilia, strength, method development, testing

Hämophilie, komplexe Kraftleistungsfähigkeit, Messmethode, Testungen

Summary

Zusammenfassung

The aim of this study was to develop a complex strength measurement method and to apply this new method for the first time in patients with haemophilia (PwH). 20 PwH with severe haemophilia A and 20 controls were included into the study. All subjects completed ten measurements of maximum isometric strength. Furthermore, the 20 control subjects completed re-test-measurements to evaluate the method. As a result, the method showed a high reliability (ICC 0.764 to 0.934). Between the two groups significant reductions in PwH between –(19–35%) were detected, regarding the relative force of the M. triceps brachii (–19%; p = 0.008), M. biceps brachii (–19%; p = 0.031), M. latissimus dorsi (–17%; p = 0.019), M. biceps femoris right (–20%; p = 0.036) and M. quadriceps femoris (right: –29%; p = 0.004; left: –35%; p = 0.002). No differences were found for M. rectus abdominis and in the hand strength. Thus, there is no general deficit in the muscle strength in PwH. The most obvious deficits exist in the upper and lower extremities and in the back muscles. Conclusion: PwH should carry out complex muscle strength training and integrate it early into a comprehensive treatment concept.

Ziel dieser Studie war die Entwicklung einer komplexen Kraftmessmethode und diese bei Patienten mit Hämophilie (PmH) anzuwenden. Insgesamt wurden 20 PmH mit schwerer Hämophilie A und 20 Kontrollpersonen (K) in die Studie eingeschlossen. Alle absolvierten zehn isometrische Maximalkraftmessungen. Zusätzlich absolvierten die 20 K Re-Testmessungen zur Evaluierung der Messmethode. Im Ergebnis zeigte sich eine hochgradig reliable Messmethode (ICC 0,764–0,934). Beim Vergleich der Gruppen zeigte sich eine reduzierte Relativkraft in PmH zwischen –(19–35%): M. trizeps brachii (–19%; p = 0,008), M. bizeps brachii (–19%; p = 0,031), M. latissimus dorsi (–17%; p = 0,019), M. bizeps femoris rechts (–20%; p = 0,036), M. quadrizeps femoris (rechts: –29%; p = 0,004; links: –35%; p = 0,002). Der M. rectus abdominis sowie die Handkraft wiesen keine Differenzen zwischen PmH und K auf, was zeigt, dass kein generelles Kraftdefizit bei PmH vorliegt. Das deutlichste Defizit bestand bei den oberen und unteren Extremitäten, sowie der Rückenmuskulatur. Schlussfolgerung: Für die Praxis lässt sich ableiten, dass es von Bedeutung ist, die Muskelkraft der PmH komplex zu trainieren und dies in ein umfassendes Behandlungskonzept zu integrieren.

Correspondence to: Britta Runkel Department of Sports Medicine, University of Wuppertal, Pauluskirchstraße 7, 42285 Wuppertal Tel. 02 02/439 59 13, Fax 02 02/439 59 10 E-Mail: [email protected]

Komplexe Kraftleistungsfähigkeit bei Patienten mit Hämophilie A Methodenentwicklung und Testung Hämostaseologie 2015; 35 (Suppl 1): S12–S17 received: February 20, 2015 accepted in revised form: July 9, 2015

Haemophilia is an X-linked recessive disease, which is associated with damage in the affected structures. The frequency of occurrence of haemophilia for newborns is estimated 1 : 10 000 (1). The tendency of spontaneous bleeding episodes is characteristic for patients with haemophilia (PwH). Most bleedings occur in large synovial joints such as ankles, knees and elbows (1, 2). As a consequence, pathological articular changes with a reduced strength performance can be observed. Strength is an important factor regarding everyday activities of PwH. Good strength performance of the periarticular muscles stabilises and protects the joints. For this reason, muscle strength in PwH plays a major role in prevention (3, 4). Different studies on the relationship between haemophilia and sports show that exercise has positive effects on the progress of the disease and the quality of life of PwH (4, 5). Most studies of strength performance in PwH deal with the muscles of the quadriceps femoris and leg extension (3, 6–10) and have detected a significant lower muscular strength in this muscle group compared to non-haemophilic adults. Brunner et al. (7) tested the strength of the quadriceps femoris in different age groups and identified lower strength performance of PwH in contrast to controls (C) in all ages. Pietri et al. (11) found that young PwH with unilateral haemarthrosis in the knee had lower quadriceps strength and a neuromuscular disbalance in the affected side in comparison with the unaffected side. Falk et al. (8) detected lower strength in knee-extensor and flexor and elbow-extensor and flexor in 13 young PwH compared to controls. In addition, they concluded that strength performance in young PwH did not increase in relation to age in the same extent as in the control

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group. Along with the study by Brunner et al. (7) it becomes apparent that deficits of strength performance begin at the age of adolescence and progress into old age. However, complex strength measurement has not been investigated so far. Therefore, it is still open whether there is a general strength deficit or a deficit only in the upper and lower limb. There are proven methods of measurement like an isometric-measurement chair, a hand-held-dynamometer and an isokinetic measurement method. For PwH, isometric strength measurement is joint-friendly and the movement is easier to control in contrast to dynamic strength measurements (3).

In terms of practicability, isometricmeasurement chairs were too big and heavy as well as inflexible and immobile. Portable isometric force transducer in diagnostic have been described in several studies (12–16), however, but were never used in strength testing in PwH. Furthermore, these studies examined only muscles of the lower limb and have shown a high reliability of this measurement method regarding the lower limb (12, 13). Consequently, there is no method of identifying complex strength by PwH. The aim of this study in the first place was to develop a new measurement system which is able to identify the complex strength of PwH and which is safe, simple, mobile and reliable. Secondly, its purpose was the evaluation of complex isometric strength performance in PwH compared with control subjects by using this new method.

Patients, material, methods Subjects Anthropometric characteristics of PwH (n = 20) and healthy controls (C; n = 20) are shown (▶ Tab. 1). Controls were recruited in the area of Wuppertal. PwH with severe haemophilia A were acquired by the ‘Haemophilia-exercise Project’ (www.haemophilia-exercise.de) in Germany. The study was confirmed by the ethics committee vote from the University

of Wuppertal. Additionally, an information letter and a written informed consent were completed by all participants. Factor substitution before the measurement was not obligatory and was handled differently by PwH. Bleedings occurred neither during nor after testing.

Complex strength test In this context, complex means that the strength of several muscles were considered to generate a comprehensive picture of isometric strength performance. In order to determine the maximum voluntary complex strength performance, a mobile measurement (KD 9363 including DMS measuring amplifier GVS-2 from MEmeasuring systems GmbH, Hennigsdorf, Germany) with strain gage was used. Additionally, ropes, a treatment table, a leg-cuff, lashing straps, carabiner, a goniometer and a tapeline were needed. For the measurement of the maximal isometric strength performance (in Newton), the sensor was placed between two ropes, similar to a cable system. As an isometric system it protects the joints and simplifies the correct performance for PwH due to its non-dynamic measurement (3). With the complex mobile force gauge six muscle groups (M. triceps brachii, M. biceps brachii, M. latissimus dorsi, M. rectus abdominis, M. biceps femoris and M. quadriceps femoris) were measured (as example ▶ Fig. 1a–c). Before beginning they performed a standardised warm-up. Then three passes with a break of 45 seconds were completed in each position. Maximal strength was built up about four

to five seconds, kept for two seconds and then slowly released. The joint angle in each position was defined by different studies (17–22): • M. triceps brachii/ M. biceps brachii/ M. latissimus dorsi 90° elbowflexion, • M. rectus abdominis 60° anteversion, • M. biceps femoris 30° kneeflexion and • M. quadriceps femoris 75° kneeflexion. In order to get comparable results external motivation was prohibited. To classify subjective effort and pain, the rating of perceived exertion-scale (RPE-Scale) (23) and the numeric rating-scale (NRS) were used. The hand force (90° elbowflexion) was measured applying a Hand-Dynamometer (Saehan SH5001, AFH, Hameln, Germany).

Study design The testing period was from February to June 2013. Initially the test-retest-reliability of the mobile measurement method was verified. Therefore 20 healthy controls realised two measurement performances within one week. Retests were carried out at the same time as the first test. Additionally, 20 PwH were tested once with the same testing procedure. These results were compared to the first complex maximal measurement results of healthy controls.

Statistical analyses The statistical analyses were conducted using SPSS program version 20 (SPSS Inc., Chicago, IL, USA). For the Test-Retest-Reliability, the interclass correlation coefficient (ICC, 2k) was applied (24). The inter-

Tab. 1 Anthropometric data of PwH (with severe haemophilia A) and controls: p values calculated with T-Test for independent sample (PwH: n = 20; C: n = 20) subjects

controls

age (years) height (m) body mass index

(kg/m2)

p

mean (± SD)

min. – max.

mean (± SD)

min. – max.

38 (± 14)

21 – 66

45 (± 9.5)

25 – 67

1.82 (± 0.07)

weight (kg)

PwH

1.70 – 1.97

1.77 (± 0.08)

0.058

1.63 – 1.96

0.046*

83.8 (± 12.6)

66.0 – 107.0

83.3 (± 15.2)

62.8 – 133.5

0.911

25.3 (± 3.7)

20.4 – 33.0

26.4 (± 3.3)

20.8 – 34.8

0.327

*significant difference; SD: standard deviation; min. – max.: minimal and maximal values

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pretation of the ICC was done according to the classification of Bös et al. (25). Kolmogorov-Smirnov test was utilized to determine the distribution of data, followed by the T-Test. As the data were not normally distributed, the Mann-Whitney U test was used. Parametric data was described as mean (M) ± standard deviation (SD) and range (min to max). The global alpha level for all tests was set at p ≤ 0.05.

Results

a)

c)

Anthropometric data of the study population is displayed (▶ Tab. 1). Significant differences were identified concerning the body height of the two groups. Differences in age were observed although these were not significant. Concerning the self-reported level of activity per week no differences were found between the two groups (mean ± SD; p = 0.339): • PwH: 3.4 ± 2.9; • C: 4.3 ± 2.9.

b)

Fig. 1 Measurement position of a) M. triceps brachii b) M. biceps brachii c) M. quadriceps femoris

The results of the test-retest-reliability showed a high correlation (r > 0.70) in each measurement position (▶ Tab. 2). The highest value of ICC was determined in the quadriceps femoris left (r = 0.934; 95% CI [0.841–0.973]), the lowest ICC in the biceps brachii (r = 0.764; 95% CI [0.494–0.899]). The standard error of measurement (SEM) varied in the measurement positions between 17.8 and 42.7 Newton. By comparing the maximal strength values from test and retest N-values ranged from 0.7% to 7.6%. Comparison of the relative maximal strength between PwH and controls differed in the various measurement positions and are shown (▶ Tab. 3). Significant differences in the relative force (N/kg body weight) of the triceps brachii (p = 0.008), the biceps brachii (p = 0.031), the latissimus dorsi (p = 0.019), the biceps femoris right (p=0.036) and the quadriceps femoris (right: p=0.004 and left: p=0.002) were detected. The difference between the biceps femoris left was not significant (p = 0.059). The rectus abdominis (p = 0.953) and the hand muscle (right: p = 0.196 and left: p = 0.126) showed no differences between PwH and C.

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Tab. 2

Intraclass-correlation (ICC) of the measurement at the first and second test-day of controls (C: n = 20)

muscle group

day

M. triceps brachii M. biceps brachii M. latissimus dorsi M. rectus abdominis M. biceps femoris

right left

M. quadriceps femoris right left

mean ± SD [n]

min. – max. [n]

1

303.2 (± 50.3)

195.9 – 380.5

2

318.0 (± 64.5)

206.4 – 442.8

1

471.5 (± 91.4)

295.1 – 723.6

2

480.2 (± 84.2)

276.6 – 643.9

1

327.7 (± 74.8)

172.1 – 452.5

2

339.5 (± 74.0)

209.8 – 465.4

1

232.7 (± 50.4)

141.8 – 307.0

2

243.2 (± 50.0)

139.4 – 299.0

1

262.3 (± 68.3)

116.3 – 375.1

2

273.2 (± 57.2)

176.3 – 385.5

1

257.8 (± 70.7)

113.3 – 398.0

2

277.4 (± 62.6)

184.2 – 391.2

1

461.6 (± 125.3)

173.1 – 684.9

2

464.8 (± 130.6)

189.6 – 692.6

1

494.1 (± 107.2)

294.7 – 665.5

2

482.6 (± 108.7)

273.7 – 680.7

ICC

confidence interval

SEM [n]

difference [%]

lower

upper

0.872

0.706

0.947

20.7

4.7

0.764

0.494

0.899

42.7

1.8

0.879

0.720

0.950

25.9

3.5

0.839

0.639

0.933

20.1

4.3

0.920

0.809

0.967

17.8

4.0

0.889

0.741

0.955

22.3

7.1

0.910

0.788

0.964

38.4

0.7

0.934

0.841

0.973

27.8

2.4

SEM: standard error of measurement; SD: standard deviation; min.-max.: minimal and maximal values

The subjective perceived exertion (RPEscala) did not reveal any difference between PwH and controls (mean ±SD): • PwH: 13.09 (± 2.07); • C: 13.74 (± 2.75) points; on a scale of 6–21 points.

Pain was reported very low on a scale of 0–10 points (NRS scale) during the measurement (mean ±SD): • PwH: 1.11 (± 1.35); • C: 0.00 (0.00) points.

The differences between the two groups showed that the strength performance of control was greater in seven of ten measured muscle groups than in PwH. The most obvious deficit existed in the upper and lower limb and back muscles in PwH.

Tab. 3 Comparison of the relative maximal strength performance between PwH and controls; p-values calculated with T-Test for independent sample (PwH: n = 20; C: n = 20) muscle group

relative maximal strength [ N/kg] controls

p PwH

mean (± SD)

min. – max.

mean (± SD)

min. – max.

M. triceps brachii

3.68 (± 0.73)

2.24 – 4.73

2.98 (± 0.84)

1.45 – 4.37

0.008**

M. biceps brachii

5.69 (± 1.17)

4.04 – 8.51

4.62 (± 1.80)

2.46 – 7.74

0.031*

M. latissimus dorsi

3.96 (± 0.97)

2.36 – 5.97

3.30 (± 0.70)

2.46 – 5.00

0.019*

M. rectus abdominal M. biceps femoris M. quadriceps femoris hand muscle

2.80 (± 0.64)

1.95 – 4.04

2.82 (± 0.72)

1.50 – 4.10

0.953

right

3.18 (± 0.89)

1.59 – 4.62

2.53 (± 0.99)

1.18 – 4.60

0.036*

left

3.11 (± 0.85)

1.55 – 4.39

2.49 (± 1.16)

0.52 – 4.52

0.059

right

5.52 (± 1.36)

2.37 – 7.87

3.93 (± 1.86)

0.69 – 7.01

0.004**

left

5.94 (± 1.21)

4.04 – 8.07

3.88 (± 2.36)

0.51 – 8.90

0.002**

right

0.51 (± 0.10)

0.30 – 0.77

0.46 (± 0.13)

0.21 – 0.78

0.196

left

0.52 (± 0.10)

0.35 – 0.74

0.46 (± 0.16)

0.21 – 0.75

0.126

*significant; **highly significant; SD: standard deviation; min.–max.: minimal and maximal values

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As a result, strength differences increased with age. The differences between PwH and controls of the current study are lo7 cated in this range, too (▶ Fig. 2). Al35 % 19 % 29 % 6 though there were significant differences in 5 17 % 19 % body height of the two groups, it can be as4 20 % 20 % 1% 3 sumed that the height did not influence the 2 10 % 12 % accuracy of the measurement method, 1 0 which allows individual positions and joint-angles for each height. Strength performance in most measurement positions is higher in healthy controls than in PwH. The biggest differences in strength were identified in the quadriceps Fig. 2 Differences in strengh (in %) of patients with haemophilia (PwH) and control subjects T. T. Hilberg Hilberg femoris with 35% on the left side and 29% Sporttherapie und hämophile Arthropathie EPC unter Belastung on the right side (▶ Fig. 2). Further differences were found in the strength of the the measurement system used in our study biceps and triceps brachii, the biceps femoDiscussion is its mobility. It can be measured at any ris and the latissimus. This could be exThe new method of complex isometric cable system. However, it has to comply plained by the most affected joints of the strength testing showed high correlations with the precise measurement positions. hemarthrosis, i. e. knee, ankle and elbow. in the test-retest-reliability (r = 0.764 – Another benefit of this method is its cost- Therefore, it can be assumed that the 0.934) in all positions. These values can be efficiency. In total, the new complex strength of the muscles close to these joints compared with Flansbjer and Lexel (26) measurement testing-system is reliable, af- is weaker than the strength of the abwho measured the maximal strength with a fordable, flexible, mobile, safe and easy for domen. Biodex Multi-Joint System 3 Dynamometer a briefed therapist to handle. The results of the quadriceps femoris (ICC 0.98) and with Wessel et al. (27) who All PwH who participated in this study can be compared with the results of other applied an isokinetic dynamometer (ICC were acquired through the Haemophilia- studies (3, 4, 7, 10). Hilberg et al. (4) deter0.83–0.95). Therefore, the test-retest results exercise Project. Therefore, it should be mined that PwH had 32–38% lower isomeof the new mobile method are similar to critically considered that this study popu- tric strength in contrast to control subjects standardized methods used in previous lation might be more physically active when applying a knee flexion similar to the studies (26, 28–30). Furthermore, the small compared to other PwH. Nevertheless, current study. With a knee angle of about confidence interval (▶ Tab. 2) illustrates within this study no differences in the 90°, Gonzales et al. (10) showed strength the accuracy of the measurement method. weekly level of activity in both groups were difference of around 50% between PwH SEM values were between 17.8 and 42.7 identified. It should be noted, that the type and control subjects. However, data were Newton. In further studies, these values of training was not further differentiated evaluated for the non-dominant leg only. need to be considered for data interpre- and this could have influenced the study Out of these, the results of the current tation, but in relation to the respective ab- results. study by Brunner et al. (7) reach the highsolute values. Especially for the interpreThe anthropometric data display a dif- est consensus. It compared the strength of tation of longitudinal studies, the values of ference in mean age of PwH (45 years) and the quadriceps femoris between 106 PwH the SEM must be assessed as measuring er- controls (38 years), (▶ Tab. 1). It cannot be and 80 controls. The results showed differrors and not as an increase in strength. Dif- disputed that the variation of seven years ences of 29% on the left side and 28% on ferences in the maximal strength values could have an influence on the maximal the right side. Although a different (absolute) from test-retest were from 0.7% strength performance. In fact, there are no measurement method had been applied in up to 7.1%. These differences can be ex- significant differences between the age of our study and fewer subjects had been inplained by test adaptation or motivation in both groups (p = 0.058). Additionally, our vestigated, the results for the quadriceps fethe test days. Differences up to 5% are results of the percentage discrepancy of the moris are rather similar. Additionally, the suited for clinical trials (3). Only for the quadriceps femoris match with the results other muscle groups with significant differbiceps femoris deviations were 7.1% and, of Brunner et al. (7). In this study, the dif- ences were almost in the same percentage therefore, need to be verified. ference in the quadriceps femoris between range (17–20%) which Brunner et al. Furthermore, this method is particu- PwH and controls within the age of (2013) indicates for the age-group of 30–49 larly suitable due to its variable positions • 30–39 years was 20% (left) / 23% (right), for the quadriceps femoris (20–36%). and its adaptability to individual joint- • 40–49 years 36% (left) / 35% (right). Thereby, these percentage differences bestatus of PwH. PwH described the position tween PwH and controls were transferable as very pleasant. The major advantage of for the other muscle groups, which are Relative Max. Strength (N/kg)

(mean)  Control  PwH (mean)

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B. Runkel et al.: Complex strength performance

close to the issue joints. However, it cannot be concluded that the strength of PwH is weaker in general, because hand and abdominal strength of PwH and controls are approximately at the same level. Our data reveal for the first time that PwH have a lower strength performance in most muscle groups but not in general when compared to healthy controls. The loss of muscular strength and size is the most frequent result of chronic inactivity and unloading (31). Bleeding in the joints in PwH often implicate such phase of inactivity and discharge concomitant with pain. If no suitable rehabilitation is undertaken, a manifestation of muscle deficiency could be the consequence. This would lead to an increased sensitivity of the joint, which after a long process, would finally result in a limitation of the physical activity level. To avoid this, it is mandatory to train the complex muscle strength of PwH and integrate this as early as possible into a comprehensive treatment of PwH.

Conclusion With the revised test tool we have established a reliable system for mobile and complex strength measurement in patients with haemophilia. Strength deficits are not only located in the lower limb, but also in the upper limb and in the back. However, a general strength deficit cannot be proven.

Nevertheless, it is indispensable to train the muscle strength of PwH in complex means and to integrate this early into a comprehensive treatment of PwH. Additionally, further studies will be necessary to give specific recommendations for training and to assess their effectiveness in the long term. Acknowledgements

The authors thank Baxter Germany for supporting the Haemophilia in Motion Projekt (HIM). In addition they thank Dr. U. F. Wehmeier, H. Stephan, M. Stecher, J. Winter and E. Wangari for their scientific and linguistic input on the manuscript.

Conflict of interest

Prof. T. Hilberg has received funding for the research carried out in this work by Baxter.

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