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Manual therapy in the treatment of ankle hemophilic arthropathy. A

randomized pilot study

Article in Physiotherapy Theory and Practice · March 2014

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Haemophilia (2014), 20, e71–e78
ORIGINAL ARTICLE Musculoskeletal
Effectiveness of two modalities of physiotherapy in
the treatment of haemophilic arthropathy of the ankle:
a randomized pilot study

E Z - C O N E S A † and J . - A . L OP
R . C U E S T A - B A R R I U S O , * A . G OM
*Degree of Physiotherapy, Faculty of Health Sciences, Catholic University, San Antonio; †Research Group in Physiotherapy
and Health Promotion, Regional Campus of International Excellence ‘Campus Mare Nostrum’, University of Murcia; and
‡Department of Basic Phychology and Methodology, University of Murcia, Murcia, Spain
Summary. Although different techniques of physio-
therapy have been described for the treatment of
haemophilic arthropathy (HA) of ankle, hardly any
studies have been applied manual therapy or
educational physiotherapy and home exercises. The
aim of this study was to assess the effectiveness of
manual therapy and educational physiotherapy in the
treatment of HA of the ankle. Thirty-one patients
with HA of the ankle with a mean age of 35.29 (SD:
12.877) years randomized to manual therapy group
(n = 11), educational group (n = 10) and a control
group (n = 10). The two physiotherapy programmes
were one with manual therapy articular traction,
passive stretching of the gastrocnemius muscles, and
exercises for muscle strength and proprioception (MT
Introduction
Haemophilia is characterized by joint bleeding, which
after repetitive bleeding causes degenerative injuries in
the joints (haemophilic arthropathy) and disability in
these patients. Although nowadays the prophylactic
administration of factor concentrates is the gold stan-
dard for the management of the patients with haemo-
philia (PwH), the patients without access to clotting
factors develop injuries at an early age [1].
The ankle is the joint in which haemophilic
arthropathy (HA) is most prevalent in the second dec-
ade of life, so there is the high tendency to suffer
haemarthrosis in childhood [2].
Correspondence: Ruben Cuesta-Barriuso, PhD, PT, Degree of
Physiotherapy, Faculty of Health Sciences, Catholic University
San Antonio, Jer
onimos Campus s/n. 30107-Guadalupe, Murcia,
Spain.
Tef.: +34 968 278 806; fax: +34 968 278 820;
e-mail: ruben.cuestab@gmail.com
Accepted after revision 19 October 2013
© 2013 John Wiley & Sons Ltd
DOI: 10.1111/hae.12320

EZ-PINA‡
group) and the other with educational sessions and
home exercises (E group). The study lasted for
12 weeks. The treatment with manual therapy
improved the gastrocnemius muscle circumference,
and the pain of ankle (P < 0.05). Six months later,
MT group still enjoyed improvement. In the
educational group there were improvements, but not
significant, in the measured variables. No patient had
ankle haemarthrosis during the study. The treatment
with manual therapy improved the circumference of
gastrocnemius and lessened pain in the patients with
haemophilic arthropathy of the ankle.
Keywords: ankle, haemophilia, joint disease, physiotherapy
modalities
Progressive deterioration of the ankle is shown by
damage to the tibiotalar and subtalar joints, widening
of the distal tibia, hindfoot valgus and cause flat foot
due to flattening of the talar dome. These biomechani-
cal changes are linked to significant disruption to the
ankle’s mobility as the HA progresses [3].
The disability associated with these degenerative
lesions has a significant medical impact on PwH, and
therefore an evaluation of ankle arthropathy usually
involves physical and radiological assessments and
measuring joint pain [4].
In the advanced stages of deterioration of the ankle
joint, the treatment of choice is surgery by arthrodesis,
which is effective for pain relief, but one that removes
all mobility in the ankle [5].
There are few clinical studies in the literature that
analyse the role of physiotherapy in the treatment of
joint contractures. In terms of manual therapy, only
Heijnen et al. [6] used articular traction for the treat-
ment of HA.
Kurz et al. [4] described impaired coordination of
the muscles surrounding an ankle with HA, indicating
e71
e72 R. CUESTA-BARRIUSO et al.
the suitability of specific exercises for improving
muscle function.
Even though pain is one of the main symptoms of
HA, there are no evidence-based therapeutic guidelines
or guides for pain management [7]. Some studies, like
Santavirta et al. [8] have shown the positive effect of
physiotherapy and patient education in improving the
perception of pain in patients with HA, even when
advanced.
The aim of this study was to assess the effectiveness
of two physiotherapy treatments: one using articular
traction techniques, passive stretching of the gastroc-
nemius muscles, and exercises to increase muscle
strength and proprioception; and another consisting of
educational sessions and home exercises to improve
the range of motion (ROM), muscle strength and
the perception of pain in PwH who have ankle
arthropathy.
Materials and methods
A randomized clinical study was performed with two
treatment groups: one received articular traction, pas-
sive stretching of the gastrocnemius muscles and
exercises for muscle strength and proprioception
(group TM); another group received educational ses-
sions and home exercises (group E); and a control
group (group C). A person external to the study allo-
cated the subjects to each of the groups, using opa-
que envelopes.
Patients had to meet the following inclusion criteria:
be aged over 18, diagnosed with haemophilia A or B
and have HA in one or both ankles. Reasons for
exclusion from the study were medical diagnoses other
than those specified (e.g. von Willebrand disease) and
the presence of antibodies (inhibitors) to factor VIII or
IX (FVIII or FIX). Any patients who suffered ankle
haemarthrosis during the treatment would be excluded
from the study. During the study, the patients contin-
ued with same pharmacological treatment regime of
FVIII/FIX concentrates previously prescribed by their
haematologist (prophylactic or on demand). The Uni-
versity of Murcia’s Ethics Committee approved this
study (register number 43/2011) and all the patients
signed informed consent documents in accordance
with the Helsinki 1975 standards as revised in 2008.
Patients of the Virgen de la Arrixaca University
Hospital in Murcia participated in the study. Of the
PwH at this hospital, 35 had haemophilic ankle
arthropathy and 32 met the inclusion criteria, 31 of
them being randomized to each of the three groups to
be studied. Of the 31 patients included in the study,
six showed arthropathy in one of the two ankles,
while in 25 patients the ankle lesions were bilateral,
all the ankles with HA scored over five points on the
Pettersson scale [9] [range 0–13]. Figure 1 shows the
flow diagram of the study.
Haemophilia (2014), 20, e71--e78
Treatment was carried out for 12 weeks; assess-
ments were made pre- and post treatment, and
6 months after it ended. Group TM’s treatment con-
sisted of two 1 h sessions per week; and group E’s
treatment consisted of six 90 min sessions, once a
fortnight, with daily home exercises. No treatment
was given to the control group (group C). After allo-
cation to the groups, the composition of the groups
was as follows: group TM = 11 patients; group
E = 10 patients; group C = 10 patients. The contents
of the treatments are listed in Table 1.
Two experts in congenital bleeding disorders (a
physiotherapist and a rehabilitation physician),
blinded with regard to the conditions of the study and
the allocation of the subjects to each group, assessed
the following dependent variables:
1. Range of motion (ROM): the dorsal and plantar
ankle flexion was measured using a universal goni-
ometer. The anatomical references used were those
identified by Querol [10], using the zero reference
method for the mobile arm of the goniometer, as
described by Norkin et al. [11].
2. Gastrocnemius muscle circumference: a tape mea-
sure was used to measure at the midpoint of the
gastrocnemius muscle belly [10].
3. Muscular strength of the gastrocnemius muscles:
measured by the rupture test for PwH [12] (using
a scale from 0 to 5 points, where 0 indicates nor-
mal force and 5 is absence of any muscle contrac-
tion). This measurement was used instead of the
normalized 0–5 scale, so that the muscle balance
of the scores would be consistent with the radio-
logical joint deterioration score, as noted by Quer-
ol [10].
4. Pain perception: using the visual analogue scale,
EVA, this consists of a gradation from 0 to 10
points (from no pain, to the maximum pain imag-
inable).
5. Radiological assessment of joint deterioration: the
Pettersson scale [9] was used; it consists of 13 lev-
els, where 0 indicates a normal joint and 13 the
maximum level of joint deterioration.
For the physical measurements, a pilot was run to
determine the interrater reliability. The physiotherapist
who performed the assessments in the study, and
another expert physiotherapist, took part in this
pilot study of 10 subjects with no degenerative joint dis-
ease. The subjects’ ankle ROM and gastrocnemius mus-
cle strength and circumference were measured.
A daily record filled out by the patients was used to
evaluate how the patients in group E completed the
home exercises. This record was collected every
2 weeks, when the patient received the educational
treatment session.
Before the randomization of the subjects to different
groups, two patients who met the criteria for inclusion
© 2013 John Wiley & Sons Ltd
 TREATMENT OF HAEMOPHILIC ARTHROPATHY OF THE ANKLE e73

Patients with congenital

coagulopathiess in Region
of Murcia (n = 96)

Patients with ankle

arthropathy (n = 37 patients;
64 ankles)

Patients excluded:
- Patients under 18
years (n = 1)
- Patients with
inhibitor (n = 2)
- Patients with von
Willebrand disease
(n = 2)

Patients who met

the inclusion criteria
(n = 32 patients; 58
ankles)

Patients who declined to

participate in the study:
- By incompatibility of work
schedules (n = 1)

Patients included in
the study (n = 31
patients; 56 ankles)

Patients who dropped out the

study:
-By personal reasons (n = 1;
group C)
-By work reasons (n = 1; group
E)

Patients who
completed the
study (n = 29
patients; 52
ankles)
Fig. 1. Flow chart of the study.

in the study had decided not to participate in it. The
reasons given were lack of time due to work and the
distance between the treatment centre and home.
The average age of the 31 people who participated
in the study was 35.29 years (SD: 12.877), and the
average weight was 82.868 kg (SD: 10.945). Of the
patients, 26 had haemophilia A (83.9%) the most fre-
quent phenotype was severe haemophilia (61.3%) and
17 of the 31 patients were in prophylactic treatment
(54.8%).
The 31 patients had a total of 56 ankle joints that
had been diagnosed with HA. The radiological joint
deterioration of these ankles, as measured by the Pet-
tersson scale, was 9.95 points (SD: 3.071). In the year
prior to the treatment, the average incidence of bleed-
ing in the 56 ankles treated was 0.80 haemarthrosis
(SD: 0.672).
An analysis of variance (ANOVA) was performed
on the dependent variables between the three groups
in the study, to make sure that they were equal at the

© 2013 John Wiley & Sons Ltd Haemophilia (2014), 20, e71--e78
e74 R. CUESTA-BARRIUSO et al.

Table 1. Characteristics of the training programme in manual therapy and educational groups.

Group Intervention Characteristics

MT 5 min: thermotherapy shallow to 50 cm away from the ankle With a bulb of 250 W
15 min: joint traction, Grade I–II. Fixation of distal tibia and fibula Maintaining traction 15 s, with 20 s between each joint traction
with cinch and manual fixation of proximal talus. Patient in supine
position and the traction is carried out in the submaximal ranges of
dorsal and plantar flexion
10 min: passive muscle stretching of gastrocnemius (within the limits In submaximal ranges with 20 s between each stretch
of mobility), through compression muscle, passive muscle stretching
and relaxation of muscle
10 min: isometric and resisted exercises, in submaximal ranges, of 20 s of contraction, with 10 s of rest between each repetition
dorsal and plantar flexion
10 min: proprioception exercises with unipodal support, with and 30 s per repetition, with 10 s of rest between each repetition
without visual support, and posterior destabilization
10 min: local cryotherapy with ice pack We used a protective cloth between the skin and the icepack

Session Intervention Characteristics of the home exercises

E 1 Theory: introduction to haemophilia: clinic and treatment. Anatomy and bio 20 repetitions of 20 s each, with 10 s breaks between
mechanics of ankle repetitions. Twice a day
Theory: exercises for the maintenance and improvement of ROM, in favour
of gravity
Practice: exercises in favour of gravity
Resolution of questions and group discussion
2 Theory: anatomy of ankle musculature. Function of muscles and haematomas 20 repetitions with 20 s of contraction, with 10 s of
treatment rest between each repetition. Twice a day
Theory: exercise for maintaining and improving strength
Practice: isometric and isotonic exercises of ankle
Resolution of questions and group discussion
3 Theory: haemarthrosis, synovitis and arthropathy: clinical manifestations and 20 repetitions of 20 s each, with 10 s breaks between
treatment repetitions. Twice a day
Theory: treatment of pain and mobility
Practice: active exercises for mobility and pain management
Resolution of questions and group discussion
4 Theory: proprioception: definition and importance in haemophilia 20 repetitions with 30 s per repetition, with 10 s of
Theory: proprioception exercises rest between each repetition. Twice a day
Practice: ankle proprioception exercises
Resolution of questions and group discussion
5 Theory: physical activity and sport: risks and benefits Cycling (30 min in plain and with the tall seat) or
Theory: recommended sports in haemophilia swimming (10 sets of 100 m with a minute of rest
Practice: swimming and cycling technique between each set). Twice a week
Resolution of questions and group discussion
6 Theory review
Review of practical exercises and resolution of questions and group
discussion
MT, manual therapy group; E, educational group; ROM, range of motion.

beginning of the study. It was noted that, at the begin-
ning of the study, there were differences between the
groups in terms of the degree of radiological joint
deterioration, the extent of dorsal and plantar flexion
and the perception of ankle pain. For the other vari-
ables measured in the initial evaluation, no intergroup
differences were found. When the Kruskal–Wallis test
was applied to confirm the results obtained with the
ANOVA, it also found that there were differences in
radiological deterioration, dorsal and plantar flexion
and the perception of ankle pain.
Table 2 shows the descriptive characteristics of the
subjects that took part in the study, and by group and
the results of the intergroup analyses.
One patient in group E dropped out of the study in
the 7 week of treatment because it was impossible to
follow the exercise programme due to the hours he/
she worked, and another subject, in the control group,
did not attend the post treatment evaluation due to a
lack of interest in the study.
Evaluator reliability for the physical variables was
high (P < 0.01), with significant interrater correlations
for dorsal ankle flexion (intraclass = 0.893), plantar
ankle flexion (intraclass = 0.893), gastrocnemius mus-
cle strength (intraclass = 0.800) and gastrocnemius
muscle circumference (intraclass = 1.000).
Statistical analysis
This was conducted using the SPSS version 19.0 statis-
tical package for Windows (IBM Company, Armonk,
NY, USA). Descriptive statistics were obtained for the
variables (sample mean values and standard deviations
pre- and post treatment, and for the follow-up). The
interrater reliability was evaluated by calculating the
intraclass correlation.

Haemophilia (2014), 20, e71--e78 © 2013 John Wiley & Sons Ltd
 TREATMENT OF HAEMOPHILIC ARTHROPATHY OF THE ANKLE e75

Table 2. Subjects’ physical characteristics at the beginning of the study.

Manual therapy group Educational group Control group All subjects in the study

Variables n Mean SD n Mean SD n Mean SD n Mean SD Sig. K

Age of patient (years) 11 35.36 13.063 10 33.4 14.871 10 37.1 11.59 31 35.29 12.877 823 750
Weight of patient (kg) 11 85.12 8.194 10 80.0 16.147 10 83.19 6.99 31 82.868 10.945 583 173
Number of ankle 20 0.75 0.639 19 0.89 0.658 17 0.76 0.752 56 0.80 0.672 772 746
haemarthrosis, in previous year
Radiological joint deterioration 20 11.2 2.285 19 10.74 2.491 17 7.59 3.261 56 9.95 3.071 00 005
(Pettersson score; 0–13)
Strength of gastrocnemius (0–5) 20 0.125 0.222 19 0.158 0.374 17 0.00 0.00 56 0.098 0.259 162 117
Circumference of gastrocnemius (cm) 20 34.52 2.338 19 33.87 4.688 17 36.32 3.911 56 34.84 3.817 141 148
Dorsal flexion of ankle (degrees) 20 8.55 6.589 19 3.58 3.791 17 10.12 4.512 56 7.34 5.782 001 001
Plantar flexi

on of ankle (degrees) 20 38.35 8.356 19 32.0 14.514 17 41.82 8.791 56 37.25 11.488 03 024
Ankle pain (VAS score: 0–10) 20 2.95 2.389 19 0.842 1.424 17 0.618 1.111 56 1.527 2.037 00 000

n % n % n % n %
Type Haemophilia A 8 72.7 9 90 9 90 26 83.9
Haemophilia B 3 27.3 1 10 1 10 5 16.1
Severity severe 9 81.8 7 70 3 30 19 61.3
Moderate 2 18.2 3 30 7 70 12 38.7
Treatment 8 72.7 7 70 2 20 17 54.9
prophylaxis
On demand 3 27.3 3 30 8 80 14 45.1
n, Number of subjects (or ankles); SD, standard deviation; Sig., signification; K, non-parametric Kruskal–Wallis test.

An ANOVA test was performed to analyse the simi-
larity between the study groups, a function of the
independent variables. In addition, the non-parametric
Kruskal–Wallis test was used to analyse the equality
of the groups.
The Pearson correlation coefficient was used to
carry out a parametric analysis of pretreatment corre-
lations between the dependent variables, the age of
the patients and the radiological joint deterioration.
A comparison of the mean values, pre posttreatment
and posttreatment-follow-up, was performed for each of
the groups, by using the student t-test for paired data.
Similarly, a comparison was made using the non-para-
metric Wilcoxon test. Cohen’s formula [13] was used to
calculate the effect size from the results in the different
groups, taking into account the grading indicated by the
author (0.20, 0.50 and 0.80). The level determined for
the confidence interval estimate was 95%.
Results
An intention-to-treat analysis was used to analyse the
results, including all the 56 ankles with HA of the 31
subjects who began the study.
The results of the evaluations of pain, range of
motion and gastrocnemius muscle strength and cir-
cumference, before and immediately after the treat-
ment and then 6 months later, were calculated for the
ankles treated in both treatment groups (20 ankles in
group TM and 19 in group E) and for those in the
control group (17).
At the end of the treatment, for group TM,
improvement was found (P < 0.05) in gastrocnemius
muscle circumference and in the perception of ankle
pain, with marginally significant improvement in the
strength of the gastrocnemius muscles (P = 0.083). In
group E, there was an improvement in gastrocnemius
muscle circumference. In the control group, no differ-
ences were observed after the treatment period.
Six months after the treatment ended, patients in
group TM had maintained the improvement in ankle
pain and gastrocnemius muscle strength and circum-
ference. A marginally significant increase was also
observed in dorsal ankle flexion (P = 0.083). Group
E maintained the improvement in gastrocnemius mus-
cle circumference. As in the posttreatment evaluation,
no differences were found in the measurements made
on subjects in group C. Table 3 shows the means,
standard deviations and results of the three evalua-
tions of the dependent physical variables, by treat-
ment group.
During the treatment, none of the patients in the
experimental groups had ankle bleeding episodes.
During the follow-up period one patient (group E)
reported haemarthrosis of the ankle, which, after a
physical examination, was ruled out, as there was no
mobility limitation, swelling, heat, or pain at rest. The
painful ankle episode disappeared within a few hours
without any need to establish appropriate pharmaco-
logical treatment.
Discussion
Range of motion
Recurrent haemarthrosis of the ankle results in articu-
lar changes that cause a reduction in joint mobility.
The normative values of dorsal and plantar ankle flex-
ion for male patients between the ages of 20 and 44,
are 13º and 55º respectively [14].

© 2013 John Wiley & Sons Ltd Haemophilia (2014), 20, e71--e78
e76 R. CUESTA-BARRIUSO et al.

Table 3. Isometric muscular strength, Circumference of gastrocnemius, dorsal and plantar flexion and pain of ankle in the three groups after and follow-up
training.

Post treatment Follow-up

Group Variable Mean SD Sig. ES Mean SD Sig. ES

MT Strength (0–5) 0.05 0.153 0.08 0.33 0.00 0.00 0.16 0.32
Circumference (cm) 34.95 2.59 0.00* 0.18 34.9 2.782 0.73 0.02
Dorsal flexion (degrees) 8.05 6.278 0.68 0.07 9.50 7.229 0.08 0.23
Plantar flexion (degrees) 40.45 10.211 0.38 0.25 42.75 7.383 0.30 0.22
Ankle pain (0–10) 1.10 1.818 0.00* 0.77 1.075 1.549 0.93 0.01
E Strength (0–5) 0.053 0.157 0.10 0.28 0.00 0.00 0.16 0.33
Circumference (cm) 34.284 4.961 0.07 0.08 34.021 4.538 0.28 0.05
Dorsal flexion (degrees) 4.89 4.701 0.10 0.34 5.21 6.206 0.57 0.06
Plantar flexion (degrees) 34.84 11.403 0.10 0.19 34.58 11.017 0.86 0.02
Ankle pain (0–10) 0.447 0.831 0.10 0.27 0.237 0.694 0.13 0.25
† †
C Strength (0–5) 0.00 0.00 0.00 0.00 0.00 0.00
Circumference (cm) 36.447 3.576 0.53 0.03 36.501 3.797 0.66 0.01
Dorsal flexion (degrees) 9.88 4.567 0.74 0.05 9.82 5.57 0.93 0.01
Plantar flexion (degrees) 44.18 6.617 0.12 0.26 39.53 7.417 0.05** 0.70
Anklepain (0–10) 0.441 0.682 0.16 0.15 0.353 0.701 0.08 0.12
MT, manual therapy group; E, educational group; C, control group; SD, standard deviation; Sig., signification; ES, effect size.
*P < 0.05, differences before and after training.
**P < 0.05 differences after and follow-up training.
†
No can be calculated the signification and the correlation because the standard error of the difference is 0.

At the beginning of the study, the average dorsal
and plantar ankle flexion over all the subjects in the
sample was 7.34º (SD: 5.782) and 37.25º (SD:
11.488), respectively, which is far below the norma-
tive range of motion. This significant limitation in
joint mobility shows the advanced deterioration due
to haemophilic ankle arthropathy in the patients who
participated in the study.
After treatment with joint traction, passive stretch-
ing of the gastrocnemius muscles, and exercises for
muscle strength and proprioception, patients in group
TM showed no statistically significant improvement in
ankle ROM. After the follow-up period, an improve-
ment in dorsal ankle flexion was observed in this
group, as well as an increase in plantar ankle flexion,
although the latter was not significant. In the Heijnen
et al. study [6], in which joint traction treatment was
carried out, a slight decrease in ankle ROM was
observed after a 5-year follow-up period.
In patients in group E, who received educational ses-
sions and performed exercises at home to improve
ROM, including active gastrocnemius muscle stretching
and exercises to improve gastrocnemius muscle strength
and ankle proprioception, improvement was observed in
joint ROM, although this was not statistically signifi-
cant. In another study in which PwH and other congeni-
tal bleeding disorders were given individualized exercises
for strength, mobility and flexibility, carried out by
Mulvany et al. [15], improvement was observed in ankle
ROM, from 2.6º dorsal flexion and 39.7º plantar flex-
ion, to 1.2º and 47°, respectively, after the treatment.
Muscle strength and circumference
The aim of rehabilitation is early restoration of ROM
and periarticular muscle strength after acute joint
bleeds [1]. Once degenerative arthropathy is estab-
lished, one of the major symptoms is muscular atro-
phy [16], As a result, muscles need to be strengthened,
as appropriate muscle condition can protect joints
from progressive degeneration [17].
After the treatment, patients in group TM had
improved gastrocnemius muscle strength and circum-
ference. Similarly, patients in group E showed an
improvement in gastrocnemius muscle circumference.
After treating 33 patients with congenital bleeding dis-
orders with individualized strengthening exercises,
Mulvany et al. [15] observed an increase in the
strength of their leg muscles, but not in the circumfer-
ence. In this study, the circumference of the gastrocne-
mius muscles increased significantly for both
experimental groups. With regard to the increase in
gastrocnemius muscle strength, the improvement
observed in group TM as a result of isometric and
counter-resistance exercises, coincides with the results
of Mulvany et al. [15].
Perception of pain
It has been described in the literature [18] how pain
is one of the symptoms that most seriously affects
PwH and degenerative arthropathy, and as this pain
is secondary to joint deterioration, it is not related to
the patient’s age [19]. After treatment, there was an
improvement in perceived ankle pain in both experi-
mental groups, this being significant in the group TM
patients, probably as a result of the treatment and
the higher level of perceived pain at the start of the
study. This improvement was maintained after the fol-
low-up period. Our results are consistent with findings
provided by Heijnen et al. [6] after joint traction
treatment. Other authors [20,21] have also described

Haemophilia (2014), 20, e71--e78 © 2013 John Wiley & Sons Ltd
 TREATMENT OF HAEMOPHILIC ARTHROPATHY OF THE ANKLE e77

improvements in the perception of pain after a treat-
ment with home exercises for muscle strength and
proprioception.
Safety of the treatments used
During the treatment, no patient in any of the groups in
the study developed ankle haemarthrosis. During the
follow-up period, only one patient reported a haemor-
rhagic episode, which was ruled out after physical
examination confirmed a diagnosis of synovitis, and it
improved a few hours later, without any need to admin-
ister FVIII concentrates. The absence of ankle bleeds
during joint traction cannot be checked against other
studies, because to date this treatment has not been
applied in PwH, except by Heijnen et al. [6]. That study
reported a decrease in the frequency of bleeding 5 years
after joint traction had some studies in which exercises
for leg muscle strength and proprioception were per-
formed have described haemarthrosis in some patients
during the treatment [20]. Other authors have reported
the absence of joint bleeds in PwH, [21] or a decrease in
frequency [22] after a treatment with exercises for
strength and proprioception, which coincides with the
results obtained in this study for both treatments, thus
confirming the safety of these treatments.
The improvement in both groups in this study
should be highlighted, even though the improvements
are not significant in both the experimental groups,
nor for all the variables measured. This improvement
suggests that both these physiotherapy treatments are
suitable for HA of the ankle.
researcher and the physiotherapist who performed
assessments for this study, to maximize the reliability of
the measurements. To the same end, the assessments
were carried out using measurement practices which
are standard in clinical practice (goniometric measure-
ment, muscle balance test and measurement of muscle
circumference), following the guidelines set out by
Querol [10] for examining haemophilic arthropathy.
Future studies with a larger sample and using more
reliable outcome measurements should confirm the
results obtained in this study.
Conclusions
Manual therapy treatment using ankle joint traction,
passive stretching and isometric, proprioceptive and
active counter-resistance exercises, improves gastroc-
nemius muscle circumference and the perception of
ankle pain. Six months after the treatment, the
improvements in the patients treated with manual
therapy were maintained.
Treatment with educational sessions and home exer-
cises improves pain and range of motion in patients
with HA of the ankle.
Given the absence of ankle bleeds during the treat-
ment, physiotherapy treatment of HA of the ankle can
be carried out following the methods used in this
study. Future studies with a larger sample and using
more reliable outcome measurements should confirm
the results obtained in this study.
Acknowledgements

Limitations of the study
A limitation of this study is the fact that more reliable
tests were not used for measuring the results (e.g. Food-
Function-Index or CoP measurement), due to the lack
of specific questionnaires for haemophilia which have
been properly validated for Spanish, and due to the lack
of financial resources for this study. To minimize this
limitation, a pilot was run involving the principal
The authors are especially grateful to Manuel Moreno, MD of the Hospi-
tal of Murcia, for his monitoring of the PwH; Torres-Ortu~ no, PhD and
L
opez-Cabarcos,MD for their help in evaluating the sample.
Disclosures
The authors stated that they had no interests which might be perceived as
posing a conflict or bias.

References
1 Rodriguez-Merchan EC, Jimenez-Yuste V,
Aznar JA et al. Joint protection in haemo-
philia. Haemophilia 2011; 17(Suppl. 2): 1–
23.
2 Gamble JG, Bellah J, Rinsky LA, Glader
B. Arthropathy of the ankle in hemo-
philia. J Bone Joint Surg Am 1991; 73:
1008–15.
3 Pasta G, Forsyth A, Merchan CR et al.
Orthopaedic management of haemophilia
arthropathy of the ankle. Haemophilia
2008; 14(Suppl. 3): 170–6.
4 Kurz E, Anders C, Herbsleb M, Puta C,
Czepa D, Hilberg T. Ankle muscle activa-
tion in people with haemophilia. Haemo-
philia 2012; 18: 948–54.
5 Van Meegeren ME, Van Veghel K, De
Kleijn P et al. Joint distraction results in
clinical and structural improvement of
haemophilic ankle arthropathy: a series of
three cases. Haemophilia 2012; 18: 810–7.
6 Heijnen L, de Kleijn P. Physiotherapy for
the treatment of articular contractures in
haemophilia. Haemophilia 1999; 5(Suppl.
1): 16–9.
7 Holstein K, Klamroth R, Richards M,
Carvalho M, Perez-Garrido R, Gringeri A.
Pain management in patients with haemo-
philia: a European survey. Haemophilia
2012; 18: 743–52.
8 Santavirta N, Solovieva S, Helkama O, Le-
hto S, Konttinen YT, Santavirta S. Muscu-
loskeletal pain and functional ability in
haemophilia A and B. Physiotherapy and
rehabilitation in haemophilia patients.
Rheumatol Int 2001; 21: 15–9.
9 Pettersson H, Ahlberg A, Nilsson IM. A
radiologic classification of hemophilic
arthropathy. Clin Orthop Relat Res 1980;
149: 153–9.
10 Querol F. Exploraci
on cl
ınica de la artro-
pat
ıa hemof
ılica. Valencia: Palmero edi-
ciones, 2008.
11 Norkin C, White J. Goniometr
ıa. Evalua-
ci

on de la movilidad articular. Madrid:
Marban, 2006.

© 2013 John Wiley & Sons Ltd Haemophilia (2014), 20, e71--e78
 e78 R. CUESTA-BARRIUSO et al.
12 Daniels L, Worthingham C. Pruebas fun-
cionales musculares. T
ecnicas manuales de
exploraci
on. M
exico: Nueva Editorial
Interamericana, 1973.
13 Cohen J. Statistical Power Analysis for the
Behavioral Sciences. Hillsdale, NJ: Law-
rence Erlbaum, 1988.
14 Soucie JM, Wang C, Forsyth A et al. Range
of motion measurements: reference values
and a database for comparison studies.
Haemophilia 2011; 17: 500–7.
15 Mulvany R, Zucker-Levin AR, Jeng M
et al. Effects of a 6-week, individualized,
supervised exercise program for people
with bleeding disorders and hemophilic
arthritis. Phys Ther 2010; 90: 509–26.
Haemophilia (2014), 20, e71--e78
View publication stats
16 Molho P, Verrier P, Stieltjes N et al. A ret-
rospective study on chemical and radioac-
tive synovectomy in severe haemophilia
patients with recurrent haemarthrosis. Hae-
mophilia 1999; 5: 115–23.
17 Harris S, Boggio LN. Exercise may
decrease further destruction in the adult
haemophilic joint. Haemophilia 2006; 12:
237–40.
18 van GF, van Meeteren NL, Heijnen L, van
den Berg HM, Helders PJ. The use of a dis-
ability model in haemophilia research. Hae-
mophilia 2005; 11: 472–80.
19 Choiniere M, Melzack R. Acute and
chronic pain in hemophilia. Pain 1987; 31:
317–31.
20 Gurcay E, Eksioglu E, Ezer U, Cakir B,
Cakci A. A prospective series of musculo-
skeletal system rehabilitation of arthropath-
ic joints in young male hemophilic patients.
Rheumatol Int 2008; 28: 541–5.
21 Hill K, Fearn M, Williams S et al. Effec-
tiveness of a balance training home
exercise programme for adults with
haemophilia: a pilot study. Haemophilia
2010; 16: 162–9.
22 Tiktinsky R, Falk B, Heim M, Martinovitz
U. The effect of resistance training on the
frequency of bleeding in haemophilia
patients: a pilot study. Haemophilia 2002;
8: 22–7.
© 2013 John Wiley & Sons Ltd