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Scand J Med Sci Sports 2013: ••: ••–•• © 2013 John Wiley & Sons A/S.

doi: 10.1111/sms.12137 Published by John Wiley & Sons Ltd

Prospective analysis of intrinsic and extrinsic risk factors on the


development of Achilles tendon pain in runners
T. Hein1,2, P. Janssen1, U. Wagner-Fritz1, G. Haupt1, S. Grau1,2
1
Medical Clinic, Department of Sports Medicine, University of Tuebingen, Tuebingen, Germany, 2Department of Food and Nutrition,
and Sport Science, University of Gothenburg, Gothenburg, Sweden
Corresponding author: Tobias Hein, Medical Clinic, Department of Sports Medicine, University of Tuebingen, Hoppe-Seyler-Strasse 6,
72076 Tuebingen, Germany. Tel: 0049 7071 29 85143, Fax: 0049 7071 29 25028, E-mail: tobias.hein@med.uni-tuebingen.de
Accepted for publication 4 September 2013

There are currently no generally accepted, consistent jured state, AT runners already demonstrated decreased
results that clearly characterize factors causing Achilles knee flexor strength and abnormal lower leg kinematics
tendon pain (AT) in runners. Therefore, we carried out a (sagittal knee and ankle joint) compared with a matched
prospective study to evaluate the multifactorial influence control group. A relationship between years of running
of clinical, biomechanical (isometric strength measure- experience or previous overuse injuries and the develop-
ments and three-dimensional kinematics) and training- ment of new symptoms could not be established. The
related risk factors on the development of AT. Two interrelationship of biomechanical and training-specific
hundred sixty-nine uninjured runners were recruited and variables on the generation of AT is evident. A combina-
underwent an initial examination. One hundred forty- tion of alterations in lower leg kinematics and higher
two subjects completed their participation by submitting impacts caused by fast training sessions might lead to
training information on a weekly basis over a maximal excessive stress on the Achilles tendon during weight
period of 1 year. Forty-five subjects developed an overuse bearing and thus to AT in recreational runners.
injury, with 10 runners suffering from AT. In an unin-

Running has become increasingly popular over the last flexion leads to greater pronation, which again may
decades and by association, the amount of runners suf- cause a whipping action of the Achilles tendon, gener-
fering from overuse injuries has also risen. Epidemio- ating microtears in the tendon and finally causing AT.
logic studies show that 19–80% of all runners develop an Lower muscular strength or muscular imbalances are
overuse injury every year (Hreljac, 2005; van Gent et al., also cited in reviews as potential risk factors for AT
2007) whereby 5–34% generate Achilles tendon pain (Alfredson & Lorentzon, 2000; Paavola et al., 2002).
or Achilles tendinopathy (AT; Clement et al., 1984; This assumption is mostly based on data showing that
Haglund-Akerlind & Eriksson, 1993; Mahieu et al., strengthening calf muscles leads to a quicker rehabilita-
2006). Hence, the Achilles tendon is one of the most tion and earlier return to training. Abnormalities in
prevalent sites for overuse injuries for both recreational movement patterns have been a topic of discussions
and elite runners, leading to training reductions or rest. about risk factors for AT since the 1980s. The findings by
Determining potential risk factors for developing Smart et al. (1980) and Clement et al. (1984), who
overuse injuries, not only AT, in runners is of major defined increased pronation as a major risk factor for AT,
interest for biomechanical research and is the subject of are supported by more recent studies (McCrory et al.,
daily clinical routines. 1999; Donoghue et al., 2008; Ryan et al., 2010). Over
Numerous studies and reviews have been published the last decades, training or training errors have also
investigating intrinsic and extrinsic risk factors for devel- been considered to be potential risk factors for develop-
oping AT to understand the multifactorial mechanisms ing AT, e.g., excessive training distance, changes in
causing these symptoms. In particular, runners suffering training routines, increases in training intensity, faster
from AT have limitations in ankle joint motions and a training pace, running surface and terrain, and footwear
poor flexibility in the gastrocnemius/soleus complex to name a few (Clement et al., 1984; Kannus, 1997;
resulting from regular training (Clement et al., 1984; Murphy et al., 2003; van Gent et al., 2007).
Kvist, 1991; Haglund-Akerlind & Eriksson, 1993; The development of AT seems to be multifactorial,
Kaufman et al., 1999). According to Smart et al. (1980) with influences of clinical, biomechanical, and training-
and Clement et al. (1984), the unsuccessful compensa- specific variables. One main reason for the lack of
tion of decreased ankle flexibility by additional knee success in defining evidence-based risk factors is the

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Hein et al.
retrospective design the majority of the described studies (2) Increased pronation and, as a consequence to cou-
are based on. Clarifying cause and effect is not possible pling mechanisms, additional alterations in lower leg
using a retrospective study design and interpreting kinematics are found for AT runners in an uninjured state
obtained results is hardly possible (Almekinders & compared with healthy controls. (3) Excessive mileage
Temple, 1998). Low measurement accuracy based on and modifications in training programs favor the devel-
goniometers or two-dimensional high-speed video opment of AT.
systems in order to analyze rearfoot and ankle kinemat-
ics might be another reason. Further, the lack of a control
group (Smart et al., 1980; Clement et al., 1984) or the Material and methods
comparison of injured runners with a non-matched Subjects
control group (Ryan et al., 2010) do not allow distinct Healthy recreational runners were included in the prospective
causes for the development of AT to be identified. No study starting with an initial examination (IE), which comprised
standardized clinical examinations, biomechanical testing proce-
direct link between a distinct training parameter and the dures (isometric strength measurements, three-dimensional kine-
occurrence of AT can be found. Reasons for the diversity matics) and a questionnaire about training behavior and years of
of results are studies that include and compare different running experience. After the IE, every subject was urged to keep
populations of runners (novice, recreational or elite a weekly training diary over a period of 52 weeks with information
runners, military recruits, etc.) over various time periods about their individual training habits. In the event that a subject
incurred a running-related overuse injury, a second examination
using different approaches (supervised training program, including the same clinical and biomechanical testing procedures
non-influenced training), and inconsistent definitions of as in the IE with additional diagnostics was necessary. The fol-
injury (Hoeberigs, 1992; Rolf, 1995). lowing inclusion and exclusion criteria were defined: all runners
Consequently, prospective studies are essential to needed to be between the ages of 18 and 55, and had to have a
define possible intrinsic and extrinsic risk factors or a minimum weekly running volume of 20 km. If a runner suffered
from any running-related injury or had visited a physical therapist
combination of different factors for developing AT, and during the last 6 months before their participation or wore ortho-
to clarify the principle of cause and effect (Bovens et al., pedic insoles in their running shoes, participation in the study was
1989; Kader et al., 2002; Paavola et al., 2002; Murphy not possible. This study complies with the declaration of Helsinki,
et al., 2003; Ryan et al., 2010). Van Ginckel et al. (2009) and all subjects signed a written consent form approved by the
carried out one of three prospective studies on the gen- university ethics committee prior to IE.
Two hundred sixty-nine uninjured runners were recruited and
eration of AT and show a more laterally shifted force passed the IE. One hundred twenty-seven subjects (47%) had to be
distribution underneath the forefoot and a decreased excluded from the study because of missing feedback, other inju-
forward progression of the center of force for runners ries, and personal or timing reasons, which did not allow any
generating AT. Mahieu et al. (2006) name decreased further training. One hundred forty-two subjects (53%) completed
strength of the plantar flexors and a greater dorsiflexion their participation and handed in their training data on a regular
weekly basis. Ninety-seven of the included runners remained unin-
range of motion (ROM) as predictors of AT. In contrast, jured and serve as controls (CO); 45 subjects (32%) developed an
Kaufman et al. (1999) describe restricted ankle dorsi- overuse injury with 10 runners suffering from AT. A detailed list is
flexion and increased hindfoot inversion as potential risk shown in Table 1.
factors. Despite the prospective study design, the rel- Because literature shows a sex-related influence and an effect of
evance of these findings needs to be questioned, as these anthropometric differences on the biomechanical results (Krauss,
2006; Grau et al., 2008), the subjects of both groups were matched
studies carry out a supervised training program including according to gender, body mass index (BMI), height, weight, and
either novice runners (Van Ginckel et al., 2009) or mili- age. Consequently, two groups of 10 runners including eight men
tary recruits (Kaufman et al., 1999; Mahieu et al., 2006)
and therefore do not reflect the situation for experienced Table 1. Overview of all subjects who passed the initial examination
recreational runners.
There are currently no generally accepted and consis- Subjects Number Percentage
tent results that clearly characterize factors causing AT,
Passed initial examination 269 100
and a reduction of the incidence rate has not been Completed participation 142 53
achieved. Van Gent et al. (2007) state that future well- Dropouts 127 47
designed prospective studies, focusing on one distinct Completed participation 142 100
symptom, including clearly defined running populations Uninjured runners (controls) 97 68
and using a universal definition of running injury are Injured runners 45 32
required to achieve comparable results. Therefore, we Injured runners 45 100
carried out a prospective study including experienced Achilles tendon pain 10 22
Plantarfasciitis 7 16
recreational runners to evaluate the multifactorial influ- Patella tendinopathy 6 13
ence of clinical, biomechanical, and training-related risk Iliotibial band syndrome 3 7
factors on the development of AT. Based on previous Shin splints 3 7
findings, three research hypotheses are proposed: Hip overall 4 9
Knee unknown/other 7 16
(1) Runners who generate AT already show restricted Foot unknown/other 5 11
sagittal ankle joint mobility in an uninjured state.

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Risk factors for Achilles tendon pain
and two women each {CO: mean BMI 23 kg/m2 standard devia- for stabilization. Assessing AF, the upper body was in an upright
tion [ (SD) 2], mean height 177 cm (5), mean weight 72 kg (8), position (0°). For BE, the upper body was positioned at a 30°
mean age 40 years (7); AT: mean BMI 23 kg/m2 (3), mean height forward incline. Hip abduction and adduction was tested both
177 cm (4), mean weight 72 kg (8), mean age 45 years (5)} were bilaterally and unilaterally. Bilateral measurements were per-
included in the data analysis. formed in a seated position (bHAB, bHAD) with a hip abduction
angle of 30° (15° each leg). Unilateral measurements were con-
ducted in a standing position (uHAB, uHAD) with a hip abduction
Definition of overuse injury angle of 20° for uHAB and uHAD. The realization of a function-
A runner was classified as injured if medical attention was needed, ally relevant hip abduction angle of 15° as described by Johnson
more than 66% of all training sessions in 2 consecutive weeks or et al. (2004) was not possible because of device-specific limita-
more than 50% of all training sessions in 4 consecutive weeks tions. Therefore, a hip abduction angle of 20° was chosen, which
were accompanied by running-related pain and an overuse injury also enabled a comparison with the seated measurements. Knee
was diagnosed by the orthopedic surgeon. flexion and extension (KFL, KEX) was tested unilaterally in a
seated position with a knee flexion angle of 30° for KFL and 60°
for KEX (Knapik et al., 1983; Overend et al., 1992). Performing
Experimental procedures the seated measurements, all subjects were fixated with an addi-
Clinical examination tional seatbelt and not allowed to self-stabilize during the mea-
surement using their hands. In the standing position, the subject’s
All clinical examinations were carried out by an experienced pelvis was fixated by individually adjustable flanking pads to
orthopedic surgeon and sports physician including the measure- enable a stable upright position for the testing procedures. The
ment of active and passive ranges of motion for hip, knee, and unilateral hip strength measurements were accomplished using the
ankle joints according to the neutral-zero method (Ryf & Hip Machine (FREI SWISS AG, Thalwil, ZH, Switzerland),
Weymann, 1995). All measurements were performed in a supine whereas all other isometric strength measurements were per-
position and compared with standard values to determine whether formed using DAVID devices (David GmbH & CO KG, Neu-Ulm,
joint mobility was normal, limited, or excessive. The following Germany).
standards for active ROM measurements were defined according
to the neutral-zero method: hip flexion (with flexed knee): 130°– Three-dimensional kinematics. All subjects ran barefoot with
140°; hip extension (Thomas test): 10°–20°; hip abduction (knee a controlled speed of 12 km/h (SD 5%) on a 13 m ethylene-vinyl
extended): 50°–80°; hip adduction (knee extended): 20°–30°; hip acetate foam runway in the laboratory. Sufficient time was allowed
internal rotation (knee flexed): 30°–40°; hip external rotation for the subjects to get used to the laboratory, running surface and
(knee flexed): 40°–50°; knee flexion: 120°–150°; knee extension: speed, enabling an individual and natural running style. A
0°–10°; ankle dorsiflexion (knee flexed): 10°–20°; ankle minimum of 25 running trials were recorded for each subject using
plantarflexion (knee flexed): 40°–50° (Ryf & Weymann, 1995). a six-camera infrared system (ViconPeak, MCam, M1, Oxford,
Passive standards were 5°–10° larger than the corresponding UK) with a sampling frequency of 250 Hz. The applied marker set
active values. The quantification of angular values was neglected consisted of 34 spherical markers according to ISB recommenda-
as the reliability and comparability of ROM measurements is tions (Wu et al., 2002) marking pelvis (2xASIS, 2xPSIS) and both
considered to be more critical (Roaas & Andersson, 1982). There- lower extremities, each consisting of three segments: thigh
fore, the joint amplitudes were compared between both legs to (greater trochanter, lateral, and medial femoral epicondyle), shank
discriminate between normal and abnormal ROM (Boone & Azen, (lateral and medial tibia plateau, tibial tuberosity, tibial crest, and
1979; Roaas & Andersson, 1982; Ryf & Weymann, 1995). A lateral and medial malleolus), and foot (lateral, medial and poste-
difference of at least 10°–15° between sides was necessary for a rior calcaneus, metatarsals 1 and 5, and hallux). Three-
definite classification into limited or increased mobility. The inci- dimensional joint motions were quantified by calculating Cardan
dence of past operations and overuse injuries to the lower extremi- angles according to Söderkvist and Wedin (1993) with the distal
ties was also documented. segment rotating with respect to the proximal segment. Here, the
first rotation occurred around the sagittal axis (extension/flexion),
Biomechanical measurements followed by a rotation around the frontal axis (abduction/
adduction or eversion/inversion), and lastly by a rotation around
Isometric strength measurements. The isometric strength the transversal axis (internal/external rotation). Data analysis was
measurements were carried out for the upper body and lower restricted to the stance phase, which was detected according to
extremities according to a standardized testing protocol. This pro- Maiwald et al. (2009). Joint angle curves were time-normalized to
tocol is implemented in the daily clinical routine and has proved 100 data points. Mean angular displacements and discrete vari-
itself in practice over the last 15 years. During a short familiariza- ables were based on 10 valid trials and calculated for hip flexion/
tion period, all subjects were allowed to get used to the direction of extension (HFL, HEX), hip abduction/adduction (HAB, HAD),
movement by performing the dynamic task against an increasing knee flexion/extension (KFL, KEX), knee external/internal rota-
resistance. Following this, each subject had to perform two tion (KER, KIR), ankle dorsi/plantarflexion (ADF, APF) and
maximum isometric contractions at a standardized angle accord- rearfoot inversion/eversion (RFINV, RFEV).
ing to recent studies and its functional relevance (Murray et al., The discrete kinematic variables were:
1980; Johnson et al., 2004). All measurements were supervised by
an experienced physiotherapist who determined whether the task • Initial joint excursion [°] at touchdown for hip flexion (HFLinit),
was accomplished successfully by increasing the applied force hip abduction (HABinit), knee flexion (KFLinit), knee external
slowly to a maximum without explosive maximal contractions. rotation (KERinit), ankle dorsiflexion (ADFinit), and rearfoot
The maximal torque was documented. inversion (RFINVinit)
The maximal isometric strength was assessed for the upper • Maximal joint excursion [°] and its timing [% ROP = roll-over
body by measuring the maximal isometric torque of the straight process/stance phase] for hip flexion (HFLmax, t HFLmax),
abdominal muscles, called “abdominal flexion” (AF) and the hip adduction (HADmax, t HADmax), knee flexion (KFLmax,
straight back muscles, called “back extension” (BE). For both t KFLmax), knee internal rotation (KIRmax, t KIRmax), ankle dor-
measurements, subjects were fixated in a seated position with a siflexion (ADFmax, t ADFmax), and rearfoot eversion (RFEVmax,
knee flexion angle of 90° and were not allowed to use their hands t RFEVmax)

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Hein et al.
• Maximal joint excursion [°] for hip extension (HEXmax), hip or AT runner, so that clinical data were not presented. Six
abduction (HABmax), knee extension (KEXmax), knee external of ten CO runners suffered from an overuse injury to the
rotation (KERmax), ankle plantarflexion (APFmax), and rearfoot
inversion (RFINVmax)
lower extremity in the past; one runner underwent an
• ROMs [°] for hip flexion and extension (HFLROM, HEXROM), hip operation of the lower extremity. Two of ten AT runners
adduction and abduction (HADROM, HABROM), knee flexion and suffered from an overuse injury in the past; three under-
extension (KFLROM, KEXROM), knee internal and external rota- went an operation.
tion (KIRROM, KERROM), ankle dorsiflexion and plantarflexion
(ADFROM, APFROM), and rearfoot eversion and inversion
(RFEVROM, RFINVROM)
• Maximal motion velocity [°/s] for hip flexion and extension Biomechanical measurements
(HFLvelmax, HEXvelmax), hip adduction and abduction (HADvelmax, Isometric strength measurements
HABvelmax), knee flexion and extension (KFLvelmax, KEXvelmax),
internal and external knee rotation (KIRvelmax, KERvelmax), ankle As high correlations exist between unilateral and bilat-
dorsiflexion and plantarflexion (ADFvelmax, APFvelmax), and eral measurements of hip joint surrounding muscles, uni-
rearfoot eversion and inversion (RFEVvelmax, RFINVvelmax).
lateral measurements were excluded from the upcoming
analysis. Hence, data evaluation includes AF, BE,
Training-specific variables bHAB, bHAD, KFL and KEX. Results are displayed in
Individual training diaries were submitted on a weekly basis for a Table 2 and Fig. 1.
maximal period of 52 weeks and contained information about Runners who developed AT already showed decreased
running frequency, distance, duration, type of training session knee flexor strength compared with CO in an uninjured
(slow, medium, fast, interval, or competition), running terrain state even though 95% confidence intervals slightly
(hard, medium, or soft underground; even, medium or uneven overlap. No differences in maximal isometric strength
surface), occurrence of running-related pain and its location as
well as any additional exercising. were found for the upper body, hip joint surrounding
muscles, or knee extensors between AT and CO.

Statistical analysis
The analysis of clinical and biomechanical variables, except the Three dimensional kinematics
maximal strength measurements of bilateral hip abduction and
adduction, was conducted either for the injured leg of an injured
Please note that because of forefoot running, one
runner or for a randomly selected leg of a non-injured runner. subject had to be excluded from the kinematic analysis.
The randomization of legs was performed prior to the statistical Measurement errors forced the omission of another
analysis. subject for the evaluation of ankle and rearfoot motion.
Because of the low number of subjects and high amount of Therefore, the analysis of hip and knee kinematics
variables, the current study design is an explorative evaluation of
risk factors influencing the development of AT without any statis-
contains nine subjects per group. The analysis of ankle
tical tests. Instead, descriptive statistical methods, such as, means, and rearfoot motion is based on eight runners per
SDs, medians and 95% confidence intervals were included in data group.
analysis. Data is graphically presented by box plots with 25th and The presentation of hip joint and transversal knee joint
75th percentiles and whiskers extending to 1.5 interquartile range. kinematics was abandoned as there were no differences
Prior to the descriptive analysis, Pearson’s correlation coefficients
were computed to detect redundancies and to reduce the quantity
between CO and AT. Correlation coefficients greater
of variables for presentation. Variables were pooled for r > 0.6. than 0.6 were found for several discrete knee, ankle,
and rearfoot variables, so that 12 of 24 were included in
data analysis: Sagittal knee motion: KFLmax, t KFLmax,
Results KFLROM, KEXROM. Sagittal ankle motion: ADFmax, t
Clinical examination ADFmax, ADFROM, APFROM. Frontal rearfoot motion:
The clinical examination revealed no limited or exces- RFEVmax, RFINVmax, RFEVROM, RFINVROM. Kinematic
sive mobility of the hip, knee or ankle joints for any CO results are shown in Table 3 and Fig. 2.

Table 2. Isometric strength measurements of the control group (CO, n = 10) and runners generating Achilles tendon pain (AT, n = 10)

AF (Nm) BE (Nm) bHAB (Nm) bHAD (Nm) KFL (Nm) KEX (Nm)

CO AT CO AT CO AT CO AT CO AT CO AT

Mean (SD) 133 (33) 116 (29) 215 (84) 242 (75) 216 (41) 224 (32) 314 (66) 318 (79) 149 (22) 124 (26) 201 (54) 193 (50)
Median 124 113 207 233 215 220 304 289 149 119 207 186
Up 95% CI 153 134 267 288 241 244 355 367 163 140 234 224
Low 95% CI 113 98 163 196 191 204 273 269 135 108 168 162

Upper body including abdominal flexion (AF) and back extension (BE). Lower extremity including bilateral hip abduction (bHAB), bilateral hip adduction
(bHAD), unilateral knee flexion (KFL) and unilateral knee extension (KEX). Displayed are means (and standard deviations, SD), medians, and upper and
lower limits of the 95% confidence interval (CI).

4
Risk factors for Achilles tendon pain

450 CO
AT
400

350

300

Torques (Nm)
250

200

150

100

50

AF 0° BE 30° bHAB 30° bHAD 30° KFL 30° KEX 60°


(Nm) (Nm) (Nm) (Nm) (Nm) (Nm)

Fig. 1. Isometric strength measurements of the control group (CO, n = 10, white) and runners generating Achilles tendon pain (AT,
n = 10, gray): Upper body including abdominal flexion (AF) and back extension (BE). Lower extremity including bilateral hip
abduction (bHAB) and adduction (bHAD), unilateral knee flexion (KFL) and extension (KEX). Displayed are box plots with 25th and
75th percentiles, whiskers extending to 1.5 interquartile range as well as medians and outliers (marked by +).

50 CO

AT

40
Joint excursion (°)/stance phase (%)

30

20

10

–10

KFL t KFL KFL KEX ADF t ADF ADF APF RFEV RFINV RFEV RFINV
max max ROM ROM max max ROM ROM max max ROM ROM

Fig. 2. Three-dimensional kinematics of the control group (CO, white) and runners generating Achilles tendon pain (AT, gray): sagittal
knee motion (CO: n = 9, AT: n = 9), sagittal ankle motion (CO: n = 8, AT: n = 8) and frontal rearfoot motion (CO: n = 8, AT: n = 8).
Displayed are box plots with 25th and 75th percentiles, whiskers extending to 1.5 interquartile range as well as medians and outliers
(marked by +).
Note: Selected variables for sagittal knee motion: maximal knee flexion (KFLmax), its timing (t KFLmax), knee flexion range of motion
(KFLROM) and knee extension range of motion (KEXROM). Selected variables for sagittal ankle motion: maximal ankle dorsiflexion
(ADFmax), its timing (t ADFmax), ankle dorsiflexion range of motion (ADFROM) and ankle plantarflexion range of motion (APFROM).
Selected variables for frontal rearfoot motion: maximal rearfoot eversion (RFEVmax), maximal rearfoot inversion (RFINVmax), rearfoot
eversion range of motion (RFEVROM) and rearfoot inversion range of motion (RFINVROM).

Although variability in kinematic data is high, the joint angles, it can be concluded that AT also show a more
authors intend to highlight some kinematic aspects. AT extended knee joint, a lower dorsiflexed ankle joint and a
runners revealed a lower ADFmax and a greater RFEVmax more everted rearfoot at touchdown compared with CO.
compared with CO. For sagittal joint motion, runners No differences in ROMs, timing values and maximal
generating AT showed a reduced KFLmax in an uninjured velocities for ankle, rearfoot, and knee motions were
state. As maximal joint excursions correlate with initial found between the two groups of runners.

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Hein et al.
Training-specific variables

ankle motion: maximal ankle dorsiflexion (ADFmax), its timing (t ADFmax), ankle dorsiflexion range of motion (ADFROM) and ankle plantarflexion range of motion (APFROM). Selected variables for frontal rearfoot motion:
Note: Selected variables for sagittal knee motion: maximal knee flexion (KFLmax), its timing (t KFLmax), knee flexion range of motion (KFLROM) and knee extension range of motion (KEXROM). Selected variables for sagittal

maximal rearfoot eversion (RFEVmax), maximal rearfoot inversion (RFINVmax), rearfoot eversion range of motion (RFEVROM) and rearfoot inversion range of motion (RFINVROM). Sagittal knee motion (CO: n = 9, AT: n = 9),
sagittal ankle motion (CO: n = 8, AT: n = 8) and frontal rearfoot motion (CO: n = 8, AT: n = 8). Displayed are means (and standard deviations, SD), medians and upper and lower limits of the 95% confidence interval
8 (2) 8 (3) 8 (6) 9 (1)
RFINVmax (°) RFEVROM (°) RFINVROM (°)

AT

9
10
8
After a correlation analysis, the evaluation of training
data were reduced to the following variables: weekly

CO

8
12
4
running distance, additional weekly exercising, percent-
age distributions of slow, medium and fast training ses-
sions (including fast endurance runs, interval training

AT

8
10
6
sessions, and competitions), and the percentage distribu-
CO tions of hard, soft, even, and uneven running terrain.

8
9
7
4 (3)
AT

5
6
2
Group comparison
5 (5)
CO

3
9
1 Comparing the averaged training variables (see Table 4
−5 (3)

and Fig. 3), AT and CO documented comparable training


RFEVmax (°)

AT

−4
−3
−7

concepts with nearly equal amounts of weekly running


−3 (4)

distance, distributions of training sessions and chosen


CO

−3
−1
−5

running terrain. High variability in averaged training


35 (3)

data was found for both groups. Two AT runners


APFROM (°)

AT

35
37
33

recorded high amounts of additional exercising during


their participation in the study. Both groups of runners
37 (5)

had similar running experience of 10 years [CO: 10 years


CO

36
40
34

(SD 10); AT 10 years (8)].


13 (2) 11 (2)
t ADFmax (%ROP) ADFROM (°)

AT

11
13
9

Prospective training data


CO

13
14
12

The prospective analysis of ATs’ training data is dis-


43 (4)

played in Table 5 and Fig. 4. Here, two subjects were


Table 3. Three-dimensional kinematics of the control group (CO) and runners generating Achilles tendon pain (AT)

AT

43
45
41

excluded from data analysis as injury occurred in weeks


4 and 5 of their participation, respectively. Consequently,
45 (1)

the prospective analysis of training data was based on


CO

45
46
44

eight runners.
14 (5) 9 (3)

Subjects generating AT reported a slight shift from


AT

8
11
7
ADFmax (°)

slow to fast training sessions and an increase in addi-


tional exercising throughout the last 4 weeks prior to
CO

15
18
10

injury. Any modifications in weekly mileage and com-


25 (6)

parable percentage distributions of training sessions and


KEXROM (°)

AT

27
29
21

choice of running surface were documented. Again,


there was a high variability in all recorded training
25 (6)

variables.
CO

24
29
21
26 (4)
AT

26
29
23
t KFLmax (%ROP) KFLROM (°)

Discussion
26 (3)

Clinical examination
CO

26
28
24

Clinical examination of the subjects did not find any


abnormalities in the ranges of motion for hip, knee, or
34 (2)

ankle joints in all three planes of motion between the two


AT

34
36
32

groups of runners. These findings comply in part with


35 (3)

recent studies because hypo- or hypermobility of the hip


CO

35
37
33

and knee joints have never been associated with AT in


37 (7)

runners. In contrast, decreased ankle mobility is named


AT

36
41
33
KFLmax (°)

as potential risk factor for developing AT by several


41 (4)

studies (Kvist, 1991; Haglund-Akerlind & Eriksson,


CO

41
44
38

1993; Kaufman et al., 1999). This relationship cannot be


supported by the results of the current study.
Low 95% CI
Up 95% CI
Mean (SD)

There are three possible reasons for these contradict-


Median

ing results. First, goniometer-based quantitative mea-


(CI).

surements to assess joint mobility were not carried out in

6
Risk factors for Achilles tendon pain

100 1000
CO
AT
90 900
Kilometers (km)/percent (%)/minutes (min)

80 800

70 700

60 600

50 500

40 400

30 300

20 200

10 100

0 0

Distance TS slow TS medium TS fast UG hard UG soft UG uneven UG even Add. exercise
(km/week) (%) (%) (%) (%) (%) (%) (%) (min/week)

Fig. 3. Averaged training data of controls (CO, n = 10, white) and runners generating Achilles tendon pain (AT, n = 10, gray) over their
time of participation. Displayed are box plots with 25th and 75th percentiles, whiskers extending to 1.5 interquartile range as well as
medians and outliers (marked by +). Please note: TS = training session, UG = underground.

our study. However, subjective estimations were mini- review by van Gent et al. (2007). The authors speculate
mized by carrying out measurements with an experi- that a past overuse injury implies a learning effect
enced orthopedic surgeon and by dividing mobility into leading to a sensible and sophisticated training design to
three categories (restricted, normal, or increased) minimize the risk of generating an overuse injury. A
according to the neutral-zero method (Boone & Azen, possible influence of gender, age, or weight cannot be
1979; Roaas & Andersson, 1982; Ryf & Weymann, evaluated in the current study because AT runners were
1995). In addition, a bilateral comparison was conducted matched with healthy controls.
to enable a clinically useful and relevant approach to
judge restricted or increased joint mobility. The findings
of recent studies (Haglund-Akerlind & Eriksson, 1993; Biomechanical measurements
Kaufman et al., 1999; Mahieu et al., 2006) have to be
Isometric strength measurements
considered as over-interpreted because differences
between injured and uninjured runners are too small The authors consider the decreased knee flexor strength
according to the neutral-zero method. Second, most shown by runners developing AT to be of great impor-
studies are based on a retrospective approach, which tance. The high variability of data (see Fig. 1) is a con-
does not enable the clarification of cause–effect rela- sequence of the diversity of included subjects, as both
tionships. For example, reduced ankle dorsiflexion groups consisted of runners of both sexes with different
might either be the result of tight calf muscles weights and ages. A normalization of torque according to
(Haglund-Akerlind & Eriksson, 1993) or be the reason body weight is omitted as both groups were matched
for higher loads on the Achilles tendon (Cook et al., according to BMI and body weight prior to data evalu-
2002). Therefore, prospective approaches as carried out ation. A potential influence of weak knee flexor muscles
by Mahieu et al. (2006) and Kaufman et al. (1999) on developing AT will be discussed in combination with
appear to be the appropriate methods to determine poten- lower-leg kinematics in the next section.
tial risk factors, not only for clinical parameters. The There are currently no studies that implement isomet-
studies by Mahieu et al. (2006) and Kaufman et al. ric strength measurements of the upper body, hip, or
(1999), however, demonstrate a third limitation, as they knee joint surrounding muscle groups to investigate the
include military or naval recruits with no previous development of AT. Therefore, we have nothing to
running experience. As only experienced recreational compare our results with. In contrast, a connection
runners are included in the current study, a comparison between weak calf muscles and the generation of AT has
of results seems to be inappropriate. been demonstrated in several studies. Haglund-Akerlind
The findings of the current study do not demonstrate a and Eriksson (1993), as well as Mahieu et al.
connection between previous overuse injuries and the (2006), both measured the muscular strength of the
development of a new symptomatic as presented in a gastrocnemius/soleus complex or calf muscles using a

7
Hein et al.
dynamometer for isokinetic concentric and/or eccentric

228 (314)
add. exercise (min)
measurements. Although their study is based on a retro-

94
423
33
spective design, Haglund-Akerlind and Eriksson (1993)

AT
consider reduced eccentric torques of the gastrocnemius/

110 (77)
soleus complex as a possible reason for the development

113
158
62
of AT. Mahieu et al. (2006) found that decreased strength

CO
of the plantar flexors leads to the genesis of AT in a

59 (24)
cohort consisting of military recruits. Consequently,
UG even (%)
the authors admit that measuring the maximal strength
AT

48
74
44
of the gastrocnemius/soleus complex using isometric,

Displayed are means (and standard deviations, SD), medians and upper and lower limits of the 95% confidence interval (CI). Please note: TS, training session; UG, underground.
59 (19)
isokinetic concentric, or eccentric measurements would
CO

59
71
47
27 (26) have been a great benefit to their study.
UG uneven (%)

Three-dimensional kinematics
AT

20
43
11

Based on the presented kinematic data, a conclusive


29 (20)

statement about whether pronation influences the devel-


CO

31
42
16

opment of AT in runners as shown in previous studies


(McCrory et al., 1999; Donoghue et al., 2008; Ryan
15 (24)
Table 4. Averaged training data of controls (CO, n = 10) and runners generating Achilles tendon pain (AT, n = 10) over their time of participation

et al., 2010) is not possible. Sample sizes are too small


AT

3
30
0
UG soft (%)

and variability of data is too high. The assumption that


13 (12)

increased pronation results in a “whipping action” of the


Achilles tendon and finally leads to AT (Smart et al.,
CO

9
20
6

1980; Clement et al., 1984) still seems logical and needs


71 (24)

to be part of future studies.


In the current study, runners developing AT already
UG hard (%)

AT

76
86
56

revealed small alterations in the sagittal upper ankle joint


75 (17)

and in sagittal knee motion in a non-injured state com-


CO

77
85
65

pared with CO. These abnormalities occur especially


during the first half of the stance phase until the foot flat
16 (11)

phase (De Cock et al., 2005) is terminated. Despite the


AT

13
23
9

problems of sample size and data variability, the authors


TS fast (%)

intend to outline two possible mechanisms leading to


22 (13)

more tension on the Achilles tendon and finally to AT.


CO

26
30
14

First, decreased knee flexor strength might be a reason


for alterations in lower leg kinematics, since a more
43 (23)
TS medium (%)

extended knee joint is necessary to compensate insuffi-


AT

44
57
29

cient stabilization of the knee joint. The stabilization is


47 (15)

usually ensured by the knee flexor muscles, especially


when the joint flexes during the weight bearing stage. An
CO

48
56
38

increased extension of the knee, reaching its maximum


42 (21)

at about 35% stance phase, induces more tension on


the gastrocnemius/soleus complex. The higher stress is
AT

35
55
29
TS slow (%)

transferred directly to the Achilles tendon as it merges


30 (17)

into the Achilles tendon and inserts at the calcaneus.


CO

Because of the origin at the medial border of the tibia, a


29
41
19

more extended soleus muscle might lead to higher


Distance (km/week)

33 (15)

torsion on the Achilles tendon. To relieve this excessive


stress on the Achilles tendon, the runners tend to ease the
AT

28
42
24

distal tension by decreasing ankle dorsiflexion during the


weight-bearing stage of running. A second approach may
32 (20)

lead to the conclusion that weak knee flexor muscles


CO

29
44
20

might be a result of abnormal lower leg kinematics. In


detail, stress on the Achilles tendon is initiated by a
Low 95% CI
Up 95% CI
Mean (SD)

higher eversion of the rearfoot, which has been demon-


Median

strated in previous studies (McCrory et al., 1999;


Donoghue et al., 2008; Ryan et al., 2010) and can be

8
Risk factors for Achilles tendon pain

100 1000
Rest
L4w
90 900
Kilometers (km)/percent (%)/minutes (min)

80 800

70 700

60 600

50 500

40 400

30 300

20 200

10 100

0 0

Distance TS slow TS medium TS fast UG hard UG soft UG uneven UG even Add. exercise.
(km/week) (%) (%) (%) (%) (%) (%) (%) (min/week)

Fig. 4. Prospective training data of runners generating Achilles tendon pain (AT, n = 8). Comparison of training data between a period
of 4 weeks before the onset of Achilles tendon pain (last 4 weeks, L4w, gray) and the rest of their participation (rest, white). Displayed
are box plots with 25th and 75th percentiles, whiskers extending to 1.5 interquartile range as well as medians and outliers (marked by
+). Please note: TS, training session; UG, underground.

seen in part in our population of AT runners. Higher Training-specific variables


pronation causes a greater internal rotation of the tibia Group comparison
because of coupling mechanisms as shown by Tiberio
(1987) and Bellchamber and van den Bogert (2000), and A relationship between the individual running experi-
finally induces a tensed gastrocnemius/soleus complex. ence and the generation of AT cannot be established in
Increased gastrocnemius/soleus tension results in a more our population as both groups consisted of runners with
extended knee joint during running because of its inser- an average training age of 10 years. In contrast, recent
tion at the femoral epicondyles. Thus, the Achilles studies and reviews (Marti et al., 1988; Macera et al.,
tendon is exposed to excessive stress that the runners 1989; Walter et al., 1989; van Gent et al., 2007) describe
compensate with reduced dorsiflexion of the upper ankle less-experienced runners as more exposed to the danger
joint. As a consequence, the knee flexor group might not of developing an overuse injury than experienced
be innervated as usual for stabilizing the flexed knee runners.
joint and subsequently degrades. Based on the presented According to the results of the current study, training
results, the importance of multifactorial study concepts errors do not appear to influence the development of
for the future is apparent. Alterations in movement pat- AT, as averaged training data did not differ between
terns appear to influence the generation of overuse inju- CO and AT. Several studies use questionnaires to assess
ries so that analyses of lower extremity kinematics need individual training concepts leading to different results
to be part of future study designs. The authors are aware about training parameters causing AT (Clement et al.,
that overuse injuries usually occur running shod and 1984; Kvist, 1991; Haglund-Akerlind & Eriksson,
outdoors, and that data from barefoot running in a labo- 1993; McCrory et al., 1999). McCrory et al. (1999)
ratory setup is difficult to compare with data from shod show that runners suffering from AT ran a significantly
running outside the laboratory. Both conditions lead to higher training pace than controls and did not regularly
different running patterns and consequently to non- implement stretching habits in their training routines.
comparable results. On the one hand, shod running leads According to Clement et al. (1984), overtraining, in
to adaptation processes like a flatter touchdown of the general, is described as a major risk factor leading to
foot. On the other hand, marker placement on individual the development of AT, including increases in weekly
running shoes does not enable an appropriate measure- running distance, single running sessions, increases in
ment of rearfoot and ankle kinematics. Therefore, a com- intensity, running hilly profiles, returning from training
promise needs to be found and the authors decided to breaks or a combination of these factors. In 1993,
ensure equal conditions for every subject in the study Haglund-Akerlind & Eriksson described a longer
and to eliminate the influence of different shoe construc- weekly training distance as a major risk factor for
tions on lower leg kinematics. AT.

9
Hein et al.
The evaluation of averaged training data, either docu-

Comparison of training data between a period of 4 weeks before the onset of AT (last 4 weeks; L4w) and the rest of their participation (rest). Displayed are means (and standard deviations, SD), medians, and upper
153 (161)
Add. exercise (min)
mented on a weekly basis or assessed by questionnaires,

L4w

102
264
42
does not seem to be appropriate. One-year training
periods are often characterized by training breaks, reduc-

60 (64)
tions, and increases of training intensity so that a pro-

Rest

46
104
16
spective analysis of training is essential. As high
variability of averaged training data within both groups

27 (27)
was detected, the evaluation of individual training con-

L4w
cepts is indispensable. In the authors’ opinions, identi-
UG even (%)

17
47
7
fying training-related risk factors for a small group of
30 (33)
runners can only be accomplished by examining indi-
Rest

16
53
7
vidual data. For example, two subjects who develop AT
document excessive amounts of additional exercising
59 (25)
UG uneven (%)

during their time of participation, displayed as outliers in


L4w

58
78
40
Fig. 3. These subjects generated AT in week 4 and 5
during their participation. Hence, excessive additional
55 (28)

exercising has to be considered a potential risk factor for


Rest

48
74
36

generating AT. The necessity of increasing the study


sample in the future is obligatory to define injury-
15 (27)

specific training errors using cluster analyses or other


L4w

0
35
−5
UG soft (%)

statistical methods.
21 (30)
Rest

9
42
0

Prospective data
71 (24)

The current study is the first prospective study investi-


L4w

gating the development of AT in experienced recre-


UG hard (%)

67
89
53

ational runners without a supervised training program.


64 (28)

Despite the high variability in training data, the authors


Rest

66
83
45

consider modifications in training concepts as one major


and lower limits of the 95% confidence interval (CI). Please note: TS, training session; UG, underground.

risk factor contributing to the development of AT. Con-


19 (22)

clusive connections cannot be established, but changes


L4w

10
36
2

in individual training concepts and higher variability in


TS fast (%)

the percentage distributions during the last 4 weeks prior


11 (11)

to the onset of AT were observed. For example, a shift


Rest
Table 5. Prospective training data of runners generating Achilles tendon pain (AT, n = 8)

9
19
3

from slow endurance runs to fast training sessions and


competitions might lead to higher impacts on the struc-
45 (31)
TS medium (%)

tures of the musculoskeletal system and thus generate


L4w

36
68
22

AT. Further, additional exercising, such as soccer or


47 (22)

hiking, might also increase eccentric stress on the


Rest

tendon, and consequently, affect the development of AT.


51
62
32

Therefore, the prospective analysis of non-


36 (32)

manipulated training programs is a promising method to


L4w

determine training-related risk factors and should be part


25
60
12
TS slow (%)

of future studies. Supervised training programs that


42 (20)

increase exercise volume prior to injury do not lead to


Rest

individual training-related risk factors (Kaufman et al.,


39
56
28

1999; Mahieu et al., 2006; Van Ginckel et al., 2009).


Distance (km/week)

34 (26)
L4w

39
52
16

Summary
The current study clearly demonstrates the necessity for
35 (15)

further complex prospective studies of intrinsic and


Rest

37
45
25

extrinsic risk factors on the development of overuse inju-


ries in runners. It also reveals several difficulties in
Low 95% CI
Up 95% CI
Mean (SD)

carrying out such a prospective study. The subjective


Median

measurements of joint mobility and the absence of


isokinetic–eccentric maximal strength measurements

10
Risk factors for Achilles tendon pain
show that compromises in experimental procedures are bearing and finally to microtears in the tendon. The role of
necessary. The feasibility of the study in terms of carry- weak knee flexor muscles remains unclear, as they might
ing out diverse measurements using adequate techniques be a cause or effect of abnormal lower leg kinematics.
within a reasonable period of time is essential to recruit
and to include subjects in the study. Additional difficul- Perspective
ties such as high dropout rates of almost 50% complicate
the realization of prospective studies. Further, the occur- The increase of the study’s population will be the most
rence of other overuse injuries results in small sample important step over the next years to enlarge the sample
sizes and slow down the process of defining injury- size of controls and injured runners and to determine
specific risk factors. evidence-based and injury-specific risk factors. A com-
The authors are aware of the small sample size, com- parison of risk factors between the uninjured and injured
promises in experimental procedures and the missing state will also be essential to clarify the principle of cause
statistical tests, but believe that first insights in possible and effect, not only for AT. And finally, a decision will be
multifactorial mechanisms favoring the development of made about whether retrospective approaches might be
AT in recreational runners have been gained. With ref- sufficient for future studies to investigate possible inter-
erence to the initially proposed research hypotheses, actions of risk factors leading to injury.
Hypothesis 1 cannot be confirmed because no restric- The authors encourage other researchers not only to
tions in mobility of hip, knee, or ankle joint were mea- focus on one specific risk factor when carrying out future
sured. Hypothesis 2 can be partly confirmed. Runners studies, but to become aware of the interrelationship of
generating AT did not show excessive pronation in an intrinsic and extrinsic risk factors on the development of
uninjured state, but demonstrated altered lower leg kine- overuse injuries. Thus, the realization of complex study
matics, especially in the sagittal planes of motion of the designs is difficult, but might be the only way to reveal the
knee and ankle joints. Hypothesis 3 can either be con- interactions of risk factors contributing to injury and to
firmed or rejected. An increase in faster training sessions develop preventive measures against overuse symptomatic.
and resulting higher impacts on the musculoskeletal From a clinical point of view, it seems inevitable not
system seem to be a potential risk factor for AT, but an only to include frontal, but also a sagittal perspective to
individual evaluation of training concepts might lead to a examine hip, knee, and ankle joint motions in two-
better understanding of the relationship between training dimensional clinical gait analyses to determine potential
and injury. Further, additional exercising should also be risk factors and to prevent the generation of overuse
taken into account as possible reasons for the develop- injuries, in general. Furthermore, balanced knee joint-
ment of overuse injuries in recreational runners without surrounding muscles (flexor/extensor ratio) stabilizing
supervised training programs. the ankle joint to minimize internal rotation of the tibia
Finally, we feel there is a clear interrelationship during running is essential for preventing and treating AT
between clinical, biomechanical, and training-specific in runners.
variables and the development of AT. We speculate that a
combination of alterations in lower leg kinematics and Key words: overuse injury, achilles tendon pain,
higher impacts caused by fast training sessions lead to running, prospective, clinical data, 3D-kinematics, iso-
excessive stress on the Achilles tendon during weight metric strength measurement, training, multifactorial.

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