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Conditioned Pain Modulation in Elite Athletes: A Systematic Review and Meta-Analysis
Conditioned Pain Modulation in Elite Athletes: A Systematic Review and Meta-Analysis
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Systematic review
Jessica McDougall*, Catherine R. Jutzeler, Alex Scott, Peter R.E. Crocker and John L.K. Kramer
one could anticipate that elite athletes develop or are databases until December 12, 2019 were searched using
predisposed to greater CPM, a factor that facilitates with- the following databases: Cochrane Central Register of
standing high demands of training and competition. On Controlled Trials, SPORTDiscus, PsycINFO, CINAHL, Web
the other hand, athletes regularly experience acute, as of Science, and PubMed. Librarians at the University of
well as chronic pain in the course of competition (e.g. British Columbia assisted in the development of search
injuries persisting for more than 3 months) [13], which strategies. The complete search strategy was modified
may then drive reduced CPM over time. Additionally, other to fit the appropriate mesh terms and keywords for each
factors previously found to influence CPM in other popu- database, with an example search shown in Table 1 for
lations, such as age and sex [8], pain modality [14], or use PsychINFO. All titles and abstracts were assessed against
of differing CPM protocols [15] could be contributing to inclusion criteria, and in cases when the abstract did not
this paradox. give full information as to the application of criteria, full-
To provide clarity and inform future studies on the text versions of the articles were retrieved. Reference lists
impact of elite athletics on CPM, we performed a system- of relevant articles were also scanned for further studies to
atic review and meta-analysis/regression. Our goal was to expand the data set. The review was registered with PROS-
provide an overall estimate of CPM from published studies PERO (#CRD42018112925).
involving elite athletes and to address study level factors
(e.g. type of athlete, sample characteristics) associated
with outcome (i.e. the degree to which CPM in elite athletes 2.3 Study selection and data extraction
was different compared to controls). A secondary outcome
was to evaluate the quality of the studies investigating JM reviewed the studies to determine eligibility for inclu-
CPM in elite athletes to date, given that there has not been sion, with JK confirming inclusion. Data were extracted
a thorough investigation of variability in CPM protocols in into a Microsoft Excel© spreadsheet, with the template
this population. To this end, we developed novel evalua- adapted from the Cochrane Collaboration [17] to match
tion criteria based on available CPM guidelines [16]. this review’s goals. For all studies the study design,
number and characteristics of participants, population,
intervention and/or purpose, study procedure/time-
2.4 R
isk of bias assessment control groups baseline pain scores and conditioning step
pain scores (during or following the conditioning pain
Risk of bias was assessed using multiple measures. First, stimulus). If a study reported CPM values for different
the Downs and Black tool [18] was used to assess quality. sport type elite athlete groups (e.g. a study that looked at
The Downs and Black tool, which was designed to assess triathletes and weightlifters separately) the groups were
non-randomized controlled trials, consists of 27 one-point entered into the meta-analysis separately. This was done
questions. To simplify interpretation, scores ≥24 were to investigate potential differences in CPM scores based
considered methodologically to be of excellent quality; on sport type. Hedge’s G and 95% CI were the measures
20–23 were considered to be good quality; 15–19 were con- chosen to examine effect sizes (R function: esc_mean_sd).
sidered to be fair quality; and scores of ≤14 were consid- When means and standard deviations were only pre-
ered to be of poor quality [19]. In addition, a CPM Quality sented in graphical formats, values were extracted using
Assessment Tool was created based on recommendations an online graph digitizer (WebPlotDigitizer; https://apps.
from the current guidelines for CPM studies (Table 2) [16]. automeris.io/wpd/). When a confidence interval, stand-
The guidelines were examined, and each recommendation ard error, or interquartile range was presented it was
was turned into a question used in risk of bias and quality transformed into standard deviation. To calculate an
assessment. Three additional questions were added fol- overall effect size, a random effects model was used as we
lowing discussion with experts in CPM testing. When expected heterogeneous study populations (R function:
reviewing the articles in the meta-analysis, each question rma). Effect sizes from studies that compared elite athletes
was answered with either “yes” or “no”, with “yes” equal- to a control sample were entered into the overall measure.
ing one point, and “no” equaling zero points. This assess- We produced Forest plots to visualize the results from the
ment scored each article from 0 to 12, with 12 indicating random-effect models (R function: forest). Heterogeneity
that all recommendations were followed. Finally, a risk of was assessed using Q, τ2 and I2. Funnel plots were used
bias assessment criteria of CPM-specific studies was used to assess publication bias (R function: funnel). We used
[8]. This risk of bias assessment results in a score from 0 to the Egger test to examine asymmetry of the funnel plot for
8, with 0 indicating low risk of bias and 8 indicating high publication bias (R function: regtest) [21].
risk of bias. A subgroup analysis was planned to examine the
effects of sport type on CPM. Effect size estimates were
determined with the studies divided into sport subtypes,
2.5 Statistical analysis namely endurance sports and “other” sports. When a
study included multiple sport types the data from each
All statistical analyses were performed in R version 3.5.1 subgroup was entered separately into the data analysis.
[20]. Effect sizes for each study were calculated using This does violate assumptions of data independence;
means and standard deviations of the elite athlete and however, given that we expected a low number of studies
Table 2: Conditioned pain modulation quality assessment checklist, based on recommendations by Yarnitsky et al. [16].
1. Did the study use either (a) 2 different test stimuli with the same conditioned stimuli, or (b) 2 full CPM protocols?a Yes/no
2. Did the study use the recommended pain stimuli?a Yes/no
a. Either mechanical or heat pain as test stimuli
b. 1-min cold water bath as conditioned stimuli
3. Was the test stimulus delivered at a pain rating of 40/100 or higher?a Yes/no
4. Was the conditioned stimulus delivered at a pain rating of 20/100 or higher?a Yes/no
5. Was the test stimulus given at an ascending or fixed protocol?a Yes/no
6. Was test stimulus delivered twice?a Yes/no
7. Was a sequential (as opposed to concurrent/parallel) protocol used?a Yes/no
8. Was one upper and one lower limb used as the testing sites?a Yes/no
9. Results presentation: was pain inhibition presented as a negative value, and pain facilitation presented as a positive value?a Yes/no
10. Did study include a control condition to ensure CPM validity? Yes/no
11. Did the study include a familiarization process? Yes/no
12. Was an adequate sample size used/was the sample size justified through a power analysis? Yes/no
Total/12
to have multiple elite athlete groups, impact on the Quantitative descriptors of athletic performance varied
outcome is expected to be minimal. Analyses were per- widely. Variables included hours trained per week [2, 3,
formed using the rma function in R-Studio. 5–7], training sessions per week [2, 5–7], years or months
Exploratory meta-regression was also planned to spent training [3, 5, 7], VO2max [7, 23], BMI and other anthro-
examine potential confounders of CPM. Factors were pometric measures [7, 23], number of competitions per year
drawn from previous CPM reviews in non-athletic popula- [3], distance ran in a race [4], and other cardiorespiratory
tions and included age of study participants, proportion and energy expenditure measures [7, 23]. The test stimuli
of males in study samples [8], type of pain modalities used used was either heat [2, 3, 5, 7] or pressure [4, 6, 23]. Three
for both test and conditioning stimulus [14], and sample studies used pain threshold as their test stimuli intensity [4,
sizes. Additionally, the impact of a quantitative measure of 6, 23], two used a pain intensity of 7/10 on a visual analog
“elite” athleticism on CPM was examined using the most scale (VAS) [2, 5], one used 5/10 on a VAS [3], and one used
commonly reported quantitative measure of athleticism. 50/100 on a numerical rating scale (NRS) [7]. Conditioning
Assessing quantitative measures of performance has been stimuli included cold water baths [2, 4–7, 23] and heat [3].
recommended to measure and compare elite athletes of Three studies applied a sequential protocol [6, 7, 23].
different sport types [22]. This analysis is termed “explora- Three studies scored “fair” and four scored “poor” on
tory” as we expect a small number of studies to report on the Downs & Black scale. On the CPM Quality Assessment
all these characteristics. Analyses were performed using Tool, scores ranged from 2 to 7 out of 12, and on the CPM Risk
the rma function in R-Studio. of Bias Scale scores ranged from 3 to 5 out of 8. On the CPM
Quality Assessment Tool, only one study reported using
a second full CPM protocol [23], and no studies reported
3 Results using more than one type of test stimulus. One study [23]
used an upper and lower limb for test sites and five studies
reported that the pain rating of the conditioning stimulus
3.1 Search strategy exceeded the recommended 2/10 NRS rating [16]. On the
CPM Risk of Bias Scale, most studies showed poor partici-
A total of 1,816 studies were originally identified. Six pant and researcher blinding, only one study reporting that
hundred and forty-eight duplicates were removed, resulting the experimenter was blinded to results of the test [4].
in 1,168 articles screened (i.e. review of titles and abstracts).
One thousand and one hundred and twenty-nine studies
were excluded due to ineligibility, with the reasons for 3.3 Study outcomes
exclusion shown in Fig. 1. The most common reason for
exclusion was that the study did not examine CPM. Seven Three studies showed that elite athletes had significantly
articles were identified for inclusion in our review. higher CPM than controls [2, 4, 6], and one study found
control groups had higher CPM than elite athletes [7]. One
study found no difference in CPM between elite athletes
3.2 D
escription of studies and participants and controls [23]. One study examined elite strength and
endurance athletes separately and found endurance ath-
Table 3 provides a summary of information for each study. letes had greater CPM than controls, but strength athletes
Eligible studies ranged from 25 to 56 participants. Study CPM did not differ from controls [5]. One study did not
types included six non-randomized controlled trials [2, have a control group [3]. No study reported on the propor-
4–7, 23] and one case-control study [3]. tion of participants who demonstrated pain modulation in
Elite athlete types included triathletes, long dis- response to the CPM protocol.
tance runners, endurance athletes, and groups of mixed-
sport athletes. Average ages ranged from 20.8 ± 1.2 [23] to
42.1 ± 6.9 [4]. Four studies included male and female par- 3.4 Meta-analysis
ticipants [2, 4, 5, 23], and three studies included only male
participants [3, 6, 7]; no studies included only female par- Data from six of the seven studies were pooled for the
ticipants. Six of the seven studies included a control group meta-analysis. The Geva et al. [3] study was excluded as
[2, 4–7, 23], five of which were amateur or recreational ath- it did not include a control group. The overall effect size
letes [2, 5–7, 23] and one of which was a non-active control favored higher CPM in elite athletes but was not signifi-
group [4]. cant (Hedges g = 0.37 [CI95 −0.03−0.76]; p = 0.07, Fig. 2).
Articles identified from electronic databases 0 Articles identified from other sources
– PubMed – 695
– SportDiscus – 143 – Reference lists of articles identified
– CINAHL – 222 through electronic databases were
reviewed
– Web of Science – 618
– PsycINFO – 138
Fig. 1: Flow diagram of the study selection process. CPM = conditioned pain modulation.
Heterogeneity was high, with I2 = 95.27%, Q = 182.78 an elite endurance athlete group and a strength athlete
(p < 0.0001), τ2 = 0.52. The funnel plot is shown in Fig. 3, group [5]; this study was entered into the meta-analysis
and demonstrated symmetry (p = 0.55). as two separate entries sharing the same control group.
Flood et al. [6] examined a mixed group of elite endurance
and non-endurance athletes; this study was placed into
3.5 Subgroup analysis the “other” category as it was not possible to separate the
data according to sport type.
The data was separated into endurance [2, 4, 5, 7, 23] The pooled effect sizes favored both groups of elite
and other [5, 6] elite athletes. One study examined both athletes (Fig. 2), but in neither case was significant
Study Sport type Athlete criteria Control Hours Hours Age N Sex Protocol TS CS CPM score (SD)a Hedges G Outcome D&B CPM Bias
group trained trained (% male) type (95% CI) measure rating quality score (/8)
per week per week score (/12)
(athletes) (controls)
Tesarz Endurance Competed in regional Amateur 9.6 (3.5) <0.5 A: 27.8 (4.1) A: 25 A: 100% Seq Heat CW bath A: 3.1 0 (8.7) −0.60 [− 0.76, −0.44] PR Fair 6 4
et al. [7] mixed (triathlon, sport clubs. Trained athletes C: 28.0 (4.5) C: 26 C: 100% C: 9.60 (12.2)
cycling, 3 h/week for ≥3 years
running)
Geva and Triathlon Competed in ≥2 Amateur 13.18 (4.2) 2.4 (1.9) A: 39.6 (12.0) A: 19 A: 62.5% Con Heat CW bath A: 3.04 (2.28) 0.66 [0.42, 0.90] PR Poor 4 3
Defrin [2] national triathlon or athletes C: 36.5 (11.0) C: 17 C: 41.2% C: 1.50 (2.28)
Ironman triathlons
per year, trained
≥3 years
Flood Mixed Competed in top tier Amateur 14.8 (5.0) 2.1 (1.1) A: 24.4 (5.3) A: 15 A: 100% Seq Pressure CW bath A: 1.19 (1.12) 0.80 [0.53, 1.07] PTh Poor 5 4
et al. [6] (endurance, of local competition. athletes C: 23.4 (3.8) C: 15 C: 100% C: 0.30 (1.04)
football, Trained ≥10 h/week
weightlifting,
martial arts)
6 McDougall et al.: Conditioned pain modulation in elite athletes
Geva Triathlon Competed in ≥5 N/A 16.4 (9.8) 2.4 (1.9) A: 35.9 (10.0)a A: 25 A: 100% Con Heat Heat A: 3.15 (1.7) PR Fair 6 5
et al. [3] triathlons or Ironman
triathlons per year.
Trained ≥7 h/week
Agnew Runners (long Participants in 25, 50, Unknown N/A N/A A: 40.4 (8.3) A: 45 A: 51% Con Pressure CW bath A: 535.76 (149.15) 0.87 [0.65, 1.09] PTh Poor 2 5
et al. [4] distance) and 100 mile races C: 23.4 (4.7) C: 11 C: 54.5% C: 405.75 (143.15)
Assa Mixed (triathlon, Competed in Amateur E: 15.2 (7.7) 2.5 (1.9) E: 32.8 (9) E: 19 A: 61% Con Heat CW bath E: 2.70 (2.00) E: 0.62 [0.38, 0.86] PR Fair 5 3
et al. [5] weightlifting, ≥5 national or athletes S: 10.4 (3.1) S: 36.5 (11) S: 17 C: 41% S: 1.10 (2.50) S: 0.18 [−0.06, 0.42]
powerlifting, international C: 36.5 (11.0) C: 17 C: 1.49 (1.90)
hammer, competitions per year
shotput throw)
Peterson Runners Collegiate track team Amateur N/A N/A A: 20.8 (1.2) A: 13 A: 84% Seq Pressure CW bath A: 87.4 (229.09) 0.07 [−0.22, 0.36] PTh Poor 7 5
et al. [23] (≤1,500 m runners, ≥1,500 m athletes C: 22.8 (2.0) C: 13 C: 84% C: 106.8 (331.85)
distance) distances
a
Positive values represent pain inhibition. This goes against the recommendations of Yarnitsky et al. [16], however this was chosen in order to have positive effect sizes indicate greater CPM in
athletes.
A = athlete group; C = control group; TS = test stimulus; CS = conditioned stimulus; CPM = conditioned pain modulation; seq = sequential; con = concurrent; CW = cold water; PR = pain rating;
PTh = pain threshold; D&B = Downs & Black; E = endurance athletes; S = strength athletes; CI = confidence interval.
Endurance athletes
Tesarz et al. [7] 25 27.8 (4.1) 26 28.0 (4.5) −0.60 [−0.76, −0.44]
Peterson et al. [23] 13 20.8 (1.2) 13 22.8 (2.0) 0.07 [−0.22, 0.36]
Geva & Defrin [2] 19 39.6 (12.1) 17 36.5 (11.1) 0.66 [0.42, 0.90]
Assa et al. [5] 19 32.8 (9.0) 17 36.5 (11.0) 0.62 [0.38, 0.86]
Agnew et al. [4] 45 40.4 (8.3) 11 23.4 (4.7) 0.87 [0.65, 1.09]
Other athletes
Assa et al. [5] 17 28.3 (8.0) 17 36.5 (11.0) 0.18 [−0.06, 0.42]
Flood et al. [6] 15 24.4 (5.3) 15 23.4 (3.8) 0.80 [0.53, 1.07]
−1 0 0.5 1 1.5
Mean difference
Fig. 2: Forest plot of Hedge’s G for comparisons of elite athlete and control group conditioned pain modulation (CPM) scores, divided into
elite endurance athlete studies and studies that examined other types of elite athletes.
(Hedges g = 0.31 [CI95 −0.24−0.86] p = 0.27 for endur- measure in our meta-regression – hours trained per week
ance athlete group and Hedges g = 0.47 [CI95 −0.13−1.08] – alongside the planned factors (age of study participants,
p = 0.13 for the “other” athlete group). Heterogeneity in proportion of males, pain modalities of test and condi-
the elite endurance athlete studies was considerable, with tioning stimulus, and sample sizes). Two studies did not
I2 = 71.30%, Q = 15.28 (p < 0.01), τ2 = 0.36. The “other” elite report hours trained per week [4, 23] and were therefore
athlete group studies were more homogenous (I2 = 32.36%, not included in the meta-regression.
Q = 1.48, p = 0.22, τ2 = 0.06). According to our meta-regression, only hours spent
training on a weekly basis was positively related to CPM,
such that longer number of training hours per week
3.6 Meta-regression was associated with greater CPM (F1 = 10.58, p < 0.001,
R2 = 98.60%, Fig. 4). None of the other variables con-
To reduce potential collinearity, we opted to only assess sidered in our planned meta-regression analysis were
the most frequently reported quantitative performance significant.
Sport type
Endurance
Other 4.1 Summary
0.194
our meta-analysis revealed no overall significant differ-
ences. The quality of reporting in the majority of studies
was “poor” according to established reporting guidelines.
Meta-regression analysis revealed one study level factor
associated with CPM outcome – hours of training. Well-
0.29 designed studies with greater quantitative descriptions
of elite athlete inclusion criteria are warranted to better
understand the impact of elite athleticism on CPM.
0.387
Strength
0.0
Sport type
that found no significant difference between controls and
Endurance elite athletes [5, 23]. Also, there were studies that did not
Other report the pain intensity of the conditioning stimulus [2,
−0.5 Sample size 4, 5, 23], did not use upper and lower limb test sites [2–7],
Tesarz et al. [7] 10
20
and applied a test stimulus intensity that was less painful
40 than the recommended 4/10 on an NRS [4, 6, 23]. Painful
−1.0 stimuli are needed in order to generate CPM [16, 24], and
10 12 14 reporting these components is necessary to determine if
Hours trained per week CPM was, in fact, the phenomenon being investigated.
There was also very little consideration of potential con-
Fig. 4: Relationship between elite athlete’s training hours per week
and effect size. Size of bubble reflects sample size. Two studies founding factors. For example, only four studies clarified
did not report training hours per week and were excluded from the as to whether elite athletes were excluded based on signs/
analysis. symptoms of chronic pain. In light of high prevalence of
chronic pain in elite athletes [13] and effects of chronic Longitudinal exercise intervention studies suggest that
pain on CPM [8], this may have contributed to consider- pain tolerance and thresholds can be increased through
able heterogeneity. exercise [26–28], however, it is not yet clear if the same
applies to CPM.
4.3 M
eta-analysis and meta-regression
results 4.4 Limitations
Overall, we observed no effect of elite athleticism on CPM. An obvious limitation of our systematic review is that only
While this was primarily driven by the inclusion of one 7 studies were identified applying CPM in athletic popu-
study reporting significantly less CPM in elite athletes lations, examining 195 athletes. Our meta-analysis was
compared to controls [7], two others reported no differ- performed on an even smaller sample of studies (N = 6),
ence between the two groups [5, 23]. In the study reporting after one article was excluded because it lacked a control
lower CPM in elite athletes, the findings were proposed group. In comparison, pain tolerance and threshold have
as a function of continuously activating pain modulation been examined in 15 published studies including 560
networks (e.g. diffuse noxious inhibitory control), which athletes [1]. Our aim to examine the effects of sport type
rendered elite athletes less capable of responding to on CPM were hampered by the sparse number of studies
noxious conditioning [7]. In essence, CPM is already fully examining non-endurance sport athletes. Additionally,
engaged as a function of their participation in athletics it was a major challenge to objectively quantify elite ath-
and attempts to active the network using laboratory tests letic participation. Across studies, only hours spent train-
was insufficient. A similar mechanism has been proposed ing per week was consistently reported, which ultimately
to explain decreased CPM in patients with chronic pain, in limited the scope of our meta-regression.
whom pain modulation networks are purportedly already
fully engaged in the response to signs and symptoms
of chronic pain [8]. In contrast, studies have suggested
greater CPM is fundamental to manage repeated bouts of 5 Conclusions
acute pain experienced in the course of athletic competi-
tion [3]. The results of our meta-analysis indicate that the availa-
Our meta-regression analysis indicated one factor ble evidence does not yet support the notion that athletes
that may explain, in part, the divergence in study results have a greater CPM capacity compared to healthy controls.
and lack of overall effect: the number of hours trained per However, training duration may explain variability in
week. Average time spent training varied from less than 10 study findings. To improve our understanding of CPM in
[7] to more than 16 h per week [3], and was strongly related athletes, future studies should consider, or control for, the
to effect size at the study level. This is consistent with amount of training their athlete groups undertake each
individual subject level observations from three studies, week, as well as follow published CPM testing recommen-
which generally supported the notion that CPM is train- dations [16], and consider more rigorous methodological
ing duration dependent [2, 5, 6]. In principle, this suggests design (e.g. blinding examiner to participant’s athletic
that the effect of training on CPM are dose-dependent, status, report quantitative measures of performance).
or conversely, that having greater CPM allows athletes
to train longer. Contrasting these observations, a recent Authors’ statement
study in swimmers did not detect a relationship between Research funding: This research did not receive any spe-
CPM and training duration [25]. One possible explanation cific grant from funding agencies in the public, commer-
for the discrepancy between this study and our findings cial, or not-for-profit sectors. Dr. Kramer is supported by a
(and the reason for the study’s exclusion from our sys- NSERC Discovery Grant.
tematic review) is that the average age of the swimmers Conflict of interest: We declare that we have no conflicting
was ~15 years – younger than any study we reviewed and interests for this review.
potentially before CPM is modulated in relation to train- Informed consent: Not applicable.
ing, assuming CPM is plastic and changes over time. Ethical approval: Not applicable.
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