PubMed Central (PMC)

Abstract

Objective

To review the efficacy of exercise interventions on sport-related concussion (SRC) incidence, as well as on linear and rotational head accelerations, and isometric neck strength and to assess reporting completeness of exercise interventions using the Consensus on Exercise Reporting Template (CERT).

Design

Systematic review and meta-analysis, according to the Prisma in Exercise, Rehabilitation, Sport medicine and SporTs science guidelines.

Data sources

Six databases (MEDLINE, Embase, CINAHL, Scopus, Web of Science CC and SPORTDiscus) were searched up to 26 June 2023.

Eligibility criteria for selecting studies

Randomised controlled trials (RCTs), cluster RCTs or quasi-experimental studies, evaluating exercise interventions on SRC incidence, linear and rotational head accelerations, and/or isometric neck strength in male and/or female athletes of any age, and/or in a healthy general population.

Results

A total of 26 articles were included. A large effect size was observed for resistance training (RT) on isometric neck strength (standardised mean difference (SMD) 0.85; 95% CI 0.57 to 1.13; high-quality evidence). Non-significant effect sizes were observed for neuromuscular warm-up programmes on SRC incidence (risk ratio 0.69; 95% CI 0.39 to 1.23; low-quality evidence), or for RT on linear head acceleration (SMD −0.43; 95% CI −1.26 to 0.40; very low-quality evidence) or rotational head acceleration (SMD 0.08; 95% CI −0.61 to 0.77; low-quality evidence). No studies assessed the impact of RT on SRC incidence. CERT scores ranged from 4 to 16 (out of 19) with median score of 11.5 (IQR 9–13).

Conclusion

RT increases isometric neck strength, but the effect on SRC incidence is unknown. More adequately powered and rigorous trials are needed to evaluate the effect of exercise interventions on SRC incidence, and on linear and rotational head accelerations. Future studies should follow CERT guidelines, as the included interventions were generally not reported in sufficient detail for accurate replication.

PROSPERO registration number

CRD42023435033.

Keywords: Exercise, Sports, Brain Concussion, Neck, Preventive Medicine


WHAT IS ALREADY KNOWN ON THIS TOPIC

  • Given the reported rise in the incidence of sport-related concussion (SRC), it is important to explore primary prevention strategies.

  • Potential primary prevention strategies include policy and rule changes, individual protective equipment and exercise interventions. Research on the efficacy of exercise interventions in the prevention of SRC is scarce.

  • Higher values for linear and rotational head accelerations and lower values for isometric neck muscle strength may be potential indicators of SRC risk.

WHAT THIS STUDY ADDS

  • This systematic review and meta-analysis on the efficacy of exercise interventions demonstrates that there is no significant effect size observed following neuromuscular warm-up programs on SRC incidence.

  • A large effect size is observed following resistance training (RT) on isometric neck strength, whereas non-significant effect sizes are observed for RT on linear and rotational head accelerations.

  • Dynamic and multimodal resistance programmes are more efficacious in increasing isometric neck strength than static resistance programmes, with higher effect sizes for males than females and adults than adolescents.

  • No study evaluated the efficacy of neck RT on SRC incidence.

  • Exercise interventions are generally not reported in sufficient detail, which can hinder accurate replication.

Introduction

Sport-related concussion (SRC) is defined as ‘a traumatic brain injury caused by a direct blow to the head, neck or body resulting in an impulsive force being transmitted to the brain that occurs in sports and exercise-related activities’.1 When the head is impacted, the skull rapidly accelerates while the brain’s movement is delayed due to its own inertia.2 This delay can lead to strain and pressure gradients within the brain tissue, which can result in injury if the tolerable limits are exceeded.2 SRC can result in a range of symptoms and signs, such as headache, nausea, confusion and sleep disturbance. These symptoms can appear immediately or develop over time, and while they usually resolve within days, some cases may take longer to recover.3 Approximately, 10%–25% of participants may experience prolonged symptoms beyond the 4-week recovery period.4 5 Given the reported rise in the incidence of SRC in recent years,6,8 and its potential for severe short-term and long-term health consequences, there is a growing focus on exploring the effects of primary prevention strategies.1

A recent systematic review on prevention strategies and modifiable risk factors for SRC and head impacts demonstrated that prevention strategies such as policy/rule changes (eg, limiting contact practice in American football) and individual protective equipment (eg, mouthguards in ice hockey) reduced the rate of SRC.9 The review also suggested that future research should focus on exercise components targeting SRC prevention.9 Since neck muscle strength has been proposed as a potentially modifiable factor in SRC prevention,10 alongside policy/rule changes and individual protective equipment, neck muscle training could become another effective SRC prevention strategy.11

It is hypothesised that targeted training to strengthen the neck musculature may improve the initial resistance of the head to external forces.11 This, in turn, could reduce the postimpact kinematic response of the head and lower the risk of SRC.11 Although there is no definitive evidence confirming a direct association between neck muscle strength and SRC incidence,9 several studies have suggested that individuals with lower isometric neck muscle strength experience greater head acceleration following head impacts.12,17 Furthermore, some studies have reported that such individuals may be at a greater risk of sustaining SRC.18,20 Research has also suggested that youth and females exhibit increased head accelerations following head impacts,1221,23 likely due to their significantly lower mean isometric neck muscle strength when compared with adults12 and males.12 14 20 In the interests of reducing the risk of SRC, it has been recommended that future research investigates the inclusion of neck strength components within already existing injury prevention programmes.9 Therefore, by evaluating the efficacy of different neck exercise modalities on isometric neck muscle strength, valuable insights could be gained into the implementation of appropriate neck strength components in such injury prevention programmes.

It is believed that linear and rotational head accelerations accurately reflect the inertial response of the brain24 and that both types of head accelerations contribute to concussive injury, however, with two distinctly different injury mechanisms.25 Linear acceleration can cause a transient increase in intracranial pressure while rotational head acceleration can lead to shear strain due to relative motion.25 It is important to recognise that the severity and outcome of concussive injuries are often determined by the combined impact of both types of head accelerations. This highlights the complex interrelationship between linear and rotational forces in head trauma.2 26

For these reasons, further exploration of exercise interventions and their efficacy on kinematic parameters (linear and rotational head accelerations), and a potential intrinsic modifiable factor (isometric neck muscle strength) is warranted. Therefore, the primary aim of this study was to systematically review the efficacy of exercise interventions on SRC incidence, as well as on kinematic parameters (linear and rotational head accelerations), and a potentially modifiable factor related to the prevention of SRC (isometric neck strength). The secondary aim was to assess reporting completeness of the exercise interventions using the Consensus on Exercise Reporting Template (CERT).

Methods

Guidelines and review process

The review was preregistered in PROSPERO (CRD42023435033) and conducted in accordance with the guidelines for implementing Prisma in Exercise, Rehabilitation, Sport medicine and SporTs science.27 A completed Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist is available in online supplemental file 1.

Two authors (BI and KJ) independently evaluated articles for inclusion, performed data extraction and carried out the risk of bias, reporting completeness and certainty of evidence assessments. All disagreements were resolved by a consensus discussion between the two authors and remaining authors (AC and EA) if consensus could not be reached.

Information sources and search strategy

The literature search strategy was developed with the assistance of two experienced librarians. The search was performed between 24 June 2023 and 26 June 2023 in the following databases: MEDLINE, Embase, CINAHL, Scopus, Web of Science CC and SPORTDiscus (details available in online supplemental file 2). No language or year restrictions were applied. A citation search was performed in the reference lists of included articles, and the systematic and narrative reviews identified in the literature search.

Selection process and eligibility criteria

All identified articles were imported into the systematic review software Covidence28 for duplicate removal, selection process and data extraction.

The inclusion criteria were (1) full-text, original, peer-reviewed randomised controlled trials (RCTs), cluster RCTs, crossover-RCTs and quasi-experimental studies; (2) articles including: (a) male and/or female athletes of any age, on all competitive levels and/or healthy general population; (b) exercise interventions of any modality and delivery method; (c) control groups that received interventions which did not include cervical exercises, and/or received no intervention and (d) outcome measures of SRC incidence and/or primary kinematic parameters (linear and rotational head accelerations) and/or a potential modifiable factor related to the prevention of SRC (isometric neck muscle strength).

The exclusion criteria were (1) publications in languages other than English; (2) abstract-only publications, review articles, cohort studies, case–control studies, cross-sectional studies and/or case reports; (3) articles including (a) athletes and/or general population with symptomatic acute or chronic neck or head injuries at the time of enrolment and (b) cognitive training, protective equipment and/or policy/rule changes aimed at outcomes related to prevention of SRC.

Data collection process

Data extraction included (1) general study information; (2) number and characteristics of study participants; (3) description of the intervention arm; (4) description of the control arm and (5) change from baseline values of measured outcomes (details available in online supplemental file 3).

Any missing data were sought out from the authors via email. The participants were classified as either athletes or healthy individuals from the general population based on their enrolment status in the respective studies. Those enrolled in a sport-related capacity at any competitive level (eg, elite, amateur and recreational) were classified as athletes. Conversely, individuals enrolled in non-athletic capacities (eg, military personnel, university students) were categorised as part of the healthy general population. If articles did not provide SD of change from baseline, these values were estimated using the formula: SDchange=√SD2baseline+SD2final–(2r×SDbaseline× SDfinal) as per guidelines in the Cochrane Handbook for Systematic Reviews of Interventions.29 If values of isometric neck strength were presented separately for multiple directions of movement (eg, flexion, extension and lateral flexion), a composite score was calculated (sum of change from baseline values for all reported directions divided by the number of reported directions). Composite scores were presented alongside mean SDs which were calculated using the formula: SDmean=√(s12+s22+…+sk2)/k (sk–SD for kth group; k–total number of groups). If articles with two or more intervention arms met the inclusion criteria, the change from baseline values for the intervention arm that was most applicable in real-world sport settings and/or the intervention group that best matched the control group were extracted. The first author (BI) categorised resistance training (RT) into various modalities (eg, dynamic, static and multimodal resistance programmes) based on neck muscle action.30 Adolescent participants were defined as younger than 19 years old while adult participants were 19 years and older. This age threshold was chosen based on standard organisational practices within the sports included in this review, that is, American football, soccer and rugby. In these sports, the under-19 age group typically represents the last youth category before athletes’ transition to senior competition.

Risk of bias assessment

The risk of bias assessment was performed using the Cochrane Risk-of-Bias tool for randomised trials (RoB 2)31 for every outcome across all articles in five domains: (1) bias arising from the randomisation process; (2) bias due to deviations from intended interventions; (3) bias due to missing outcome data; (4) bias in measurement of the outcome and (5) bias in the selection of the reported result. Based on the assessed bias in these domains, an overall risk-of-bias judgement was made for each outcome as follows: overall ‘low risk’ (all domains were at ‘low risk’); overall ‘some concern’ (no more than two ‘some concern’ domains and no ‘high-risk’ domains); overall ‘high risk’ (three or more ‘some concern’ domains or one or more ‘high-risk’ domains).

Effect measures and synthesis methods

Meta-analyses and subgroup analyses were performed by using the Cochrane Review Manager Web (RevMan Web, V.4.26.0).32 Meta-analysis was performed for all outcomes, where more than one article measured the same outcome. To explore the sources of heterogeneity and variations in the exercise efficacy, subgroup analyses were performed on outcomes for which an adequate number of articles was identified. Subgroups were based on (1) Exercise intervention modality—dynamic, static and multimodal resistance programmes; (2) Age—adolescent and adult participants and (3) Sex—male and female participants.

Dichotomous outcomes were analysed with a random effect Mantel-Haenszel method, presenting risk ratio (RR) alongside 95% CIs. Continuous outcomes were analysed with a random effect inverse-variance method, presenting standardised mean difference (SMD) alongside 95% CIs. SMD effect size was interpreted as small (SMD=0.2), medium (SMD=0.5) and large (SMD=0.8).33 Random effect models were used, as moderate to substantial heterogeneity was expected due to differences in characteristics of the included articles.

I2 statistics were used to assess the heterogeneity among articles. I2 statistics were interpreted using rough thresholds reported in the Cochrane Handbook for Systematic Reviews of Interventions: 0%–40% (might not be important); 30%–60% (may represent moderate heterogeneity); 50%–90% (may represent substantial heterogeneity) and 75%–100% (considerable heterogeneity).34 For subgroups in which statistical heterogeneity was detected, post hoc meta-regression was performed in order to relate specific study-level variables to the statistical heterogeneity. Meta-regression was performed using Stata (V.18, 2023).35

Sensitivity analyses were conducted by excluding articles with (1) healthy general population (2) cluster randomised and quasi-experimental designs and (3) overall ‘high risk’ of bias.

Reporting bias and certainty assessments

For outcomes with 10 or more included articles in the meta-analysis, potential reporting bias was assessed both visually with the examination of funnel plots and statistically using Egger’s test. Certainty of evidence was assessed by using the GRADEprofiler Guideline Development Tool software36 and by following the guidelines in the GRADE Handbook.37 The starting quality of evidence was rated as ‘high’ and could be downgraded one or two levels for each of the following domains: (1) risk of bias; (2) imprecision; (3) inconsistency; (4) indirectness and (5) publication bias.

Reporting completeness of the exercise interventions

The CERT38 was used to assess reporting completeness of the exercise interventions. CERT consists of 16 items over 7 sections: what (materials), who (provider), how (delivery), where (location), when, how much (dosage), tailoring (what, how) and how well (planned, actual). Each item was scored individually as a ‘0’ (not/inadequately described) or ‘1’ (adequately described). The resulting score ranges from 0 to 19, with a higher score indicating a more detailed description.

Equity, diversity and inclusion statement

The author group is composed of one male and three female researchers and represents a combination of junior (one author), mid-career (one author) and senior (two authors) researchers from two academic institutions in Sweden. This systematic review included athletes and a healthy general population from any nationality, sex, gender, age and competitive level. Analyses included considerations of age, sex and gender. However, due to the absence of gender-specific data in the articles, analyses based on gender were not possible.

Results

Study selection

The systematic search yielded a total of 15 931 articles. Of these, 40 full-text articles were screened according to the inclusion/exclusion criteria, and 14 were further excluded (reasons for exclusion available in online supplemental file 4). In addition, seven articles were identified through the citation search of included articles, systematic and narrative reviews, of which all seven were excluded as they failed to fulfil inclusion criteria (online supplemental file 4). Finally, 26 articles39,64 met all inclusion criteria and were included in the review (figure 1).

Figure 1. Study identification and selection PRISMA flow diagram. PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses.

Figure 1

Study characteristics

Detailed study characteristics are available in online supplemental file 5. 20 articles39,4446 47 49 50 52 included athletes in various sports while 6 articles45 48 51 56 57 59 included healthy general population. Sample sizes across articles ranged from 10 to 2452 (median n=32), and the median age was 20 years (range 10.8–38.6 years). In total, 96% of the participants were males and 4% were females.

10 articles evaluated the efficacy of dynamic resistance programmes.4547 51 53 57,61 63 All 10 evaluated the efficacy on isometric neck strength while 2 also evaluated the efficacy on linear and rotational head accelerations.47 63 Six articles evaluated the efficacy of multimodal resistance programmes on isometric neck strength.39 44 48 54 56 64 Five articles evaluated the efficacy of static resistance programmes.40 43 46 49 55 All five evaluated the efficacy on isometric neck strength while one also evaluated the efficacy on linear head acceleration.55 Three articles evaluated the efficacy of neuromuscular warm-up programmes (balance, resistance, plyometric and sport-specific landing and cutting exercises) on SRC incidence.41 42 50 All neuromuscular warm-up programmes included specific neck exercises. One article evaluated the efficacy of a multimodal resistance and mobility programme on isometric neck strength.52 Additionally, one article evaluated a dynamic resistance and skill programme on isometric neck strength, and linear and rotational head accelerations.62 No studies assessed the impact of RT on SRC incidence. Furthermore, no articles assessed the efficacy of exercise interventions on concussion incidence, or linear and rotational head accelerations in the healthy general population, specifically. The median duration of the exercise interventions was 8 weeks (range 4–42 weeks), and the median number of training sessions per week was 3 (range 1–5 sessions). Intervention details are available in online supplemental file 6.

Risk of bias

13 articles (50%) had high risk of bias, 12 articles (46%) had some concern and 1 article (4%) had overall low risk of bias. Inadequate randomisation process was the main source of bias in 27% of the articles, inadequate measurement of the outcome in 12% and deviations from the intended intervention in 4% of the articles (table 1).

Table 1. Risk of bias assessment (RoB 2 tool).

Author and publication year Domain 1: Randomisation process Domain 2: Deviations from intended interventions Domain 3: Missing outcome data Domain 4: Measurement of the outcome Domain 5: Selection of the reported results Overall risk-of-bias
Attwood et al40, 2022 graphic file with name bjsports-58-23-i001.jpg graphic file with name bjsports-58-23-i002.jpg graphic file with name bjsports-58-23-i003.jpg graphic file with name bjsports-58-23-i004.jpg graphic file with name bjsports-58-23-i005.jpg graphic file with name bjsports-58-23-i006.jpg
Attwood et al41, 2018 graphic file with name bjsports-58-23-i007.jpg graphic file with name bjsports-58-23-i008.jpg graphic file with name bjsports-58-23-i009.jpg graphic file with name bjsports-58-23-i010.jpg graphic file with name bjsports-58-23-i011.jpg graphic file with name bjsports-58-23-i012.jpg
Barden et al42, 2022 graphic file with name bjsports-58-23-i013.jpg graphic file with name bjsports-58-23-i014.jpg graphic file with name bjsports-58-23-i015.jpg graphic file with name bjsports-58-23-i016.jpg graphic file with name bjsports-58-23-i017.jpg graphic file with name bjsports-58-23-i018.jpg
Barrett et al43, 2015 graphic file with name bjsports-58-23-i019.jpg graphic file with name bjsports-58-23-i020.jpg graphic file with name bjsports-58-23-i021.jpg graphic file with name bjsports-58-23-i022.jpg graphic file with name bjsports-58-23-i023.jpg graphic file with name bjsports-58-23-i024.jpg
Becker et al44, 2019 graphic file with name bjsports-58-23-i025.jpg graphic file with name bjsports-58-23-i026.jpg graphic file with name bjsports-58-23-i027.jpg graphic file with name bjsports-58-23-i028.jpg graphic file with name bjsports-58-23-i029.jpg graphic file with name bjsports-58-23-i030.jpg
Burnett et al45, 2005 graphic file with name bjsports-58-23-i031.jpg graphic file with name bjsports-58-23-i032.jpg graphic file with name bjsports-58-23-i033.jpg graphic file with name bjsports-58-23-i034.jpg graphic file with name bjsports-58-23-i035.jpg graphic file with name bjsports-58-23-i036.jpg
Deng et al46, 2022 graphic file with name bjsports-58-23-i037.jpg graphic file with name bjsports-58-23-i038.jpg graphic file with name bjsports-58-23-i039.jpg graphic file with name bjsports-58-23-i040.jpg graphic file with name bjsports-58-23-i041.jpg graphic file with name bjsports-58-23-i042.jpg
Eckner et al12, 2018 graphic file with name bjsports-58-23-i043.jpg graphic file with name bjsports-58-23-i044.jpg graphic file with name bjsports-58-23-i045.jpg graphic file with name bjsports-58-23-i046.jpg graphic file with name bjsports-58-23-i047.jpg graphic file with name bjsports-58-23-i048.jpg
Fiebert et al48, 2004 graphic file with name bjsports-58-23-i049.jpg graphic file with name bjsports-58-23-i050.jpg graphic file with name bjsports-58-23-i051.jpg graphic file with name bjsports-58-23-i052.jpg graphic file with name bjsports-58-23-i053.jpg graphic file with name bjsports-58-23-i054.jpg
Geary et al49, 2014 graphic file with name bjsports-58-23-i055.jpg graphic file with name bjsports-58-23-i056.jpg graphic file with name bjsports-58-23-i057.jpg graphic file with name bjsports-58-23-i058.jpg graphic file with name bjsports-58-23-i059.jpg graphic file with name bjsports-58-23-i060.jpg
Hamlin et al39, 2020 graphic file with name bjsports-58-23-i061.jpg graphic file with name bjsports-58-23-i062.jpg graphic file with name bjsports-58-23-i063.jpg graphic file with name bjsports-58-23-i064.jpg graphic file with name bjsports-58-23-i065.jpg graphic file with name bjsports-58-23-i066.jpg
Hislop et al50,2017 graphic file with name bjsports-58-23-i067.jpg graphic file with name bjsports-58-23-i068.jpg graphic file with name bjsports-58-23-i069.jpg graphic file with name bjsports-58-23-i070.jpg graphic file with name bjsports-58-23-i071.jpg graphic file with name bjsports-58-23-i072.jpg
Leggett et al51, 1991 graphic file with name bjsports-58-23-i073.jpg graphic file with name bjsports-58-23-i074.jpg graphic file with name bjsports-58-23-i075.jpg graphic file with name bjsports-58-23-i076.jpg graphic file with name bjsports-58-23-i077.jpg graphic file with name bjsports-58-23-i078.jpg
Maconi et al52, 2016 graphic file with name bjsports-58-23-i079.jpg graphic file with name bjsports-58-23-i080.jpg graphic file with name bjsports-58-23-i081.jpg graphic file with name bjsports-58-23-i082.jpg graphic file with name bjsports-58-23-i083.jpg graphic file with name bjsports-58-23-i084.jpg
Mansell et al53, 2005 graphic file with name bjsports-58-23-i085.jpg graphic file with name bjsports-58-23-i086.jpg graphic file with name bjsports-58-23-i087.jpg graphic file with name bjsports-58-23-i088.jpg graphic file with name bjsports-58-23-i089.jpg graphic file with name bjsports-58-23-i090.jpg
Müller et al54, 2021 graphic file with name bjsports-58-23-i091.jpg graphic file with name bjsports-58-23-i092.jpg graphic file with name bjsports-58-23-i093.jpg graphic file with name bjsports-58-23-i094.jpg graphic file with name bjsports-58-23-i095.jpg graphic file with name bjsports-58-23-i096.jpg
Peek et al55, 2022 graphic file with name bjsports-58-23-i097.jpg graphic file with name bjsports-58-23-i098.jpg graphic file with name bjsports-58-23-i099.jpg graphic file with name bjsports-58-23-i100.jpg graphic file with name bjsports-58-23-i101.jpg graphic file with name bjsports-58-23-i102.jpg
Pollock et al56, 1993 graphic file with name bjsports-58-23-i103.jpg graphic file with name bjsports-58-23-i104.jpg graphic file with name bjsports-58-23-i105.jpg graphic file with name bjsports-58-23-i106.jpg graphic file with name bjsports-58-23-i107.jpg graphic file with name bjsports-58-23-i108.jpg
Salmon et al57, 2013 graphic file with name bjsports-58-23-i109.jpg graphic file with name bjsports-58-23-i110.jpg graphic file with name bjsports-58-23-i111.jpg graphic file with name bjsports-58-23-i112.jpg graphic file with name bjsports-58-23-i113.jpg graphic file with name bjsports-58-23-i114.jpg
Stump et al58, 1993 graphic file with name bjsports-58-23-i115.jpg graphic file with name bjsports-58-23-i116.jpg graphic file with name bjsports-58-23-i117.jpg graphic file with name bjsports-58-23-i118.jpg graphic file with name bjsports-58-23-i119.jpg graphic file with name bjsports-58-23-i120.jpg
Taylor et al59, 2006 graphic file with name bjsports-58-23-i121.jpg graphic file with name bjsports-58-23-i122.jpg graphic file with name bjsports-58-23-i123.jpg graphic file with name bjsports-58-23-i124.jpg graphic file with name bjsports-58-23-i125.jpg graphic file with name bjsports-58-23-i126.jpg
Tsuyama et al60, 2006 graphic file with name bjsports-58-23-i127.jpg graphic file with name bjsports-58-23-i128.jpg graphic file with name bjsports-58-23-i129.jpg graphic file with name bjsports-58-23-i130.jpg graphic file with name bjsports-58-23-i131.jpg graphic file with name bjsports-58-23-i132.jpg
Versteegh et al61, 2020 graphic file with name bjsports-58-23-i133.jpg graphic file with name bjsports-58-23-i134.jpg graphic file with name bjsports-58-23-i135.jpg graphic file with name bjsports-58-23-i136.jpg graphic file with name bjsports-58-23-i137.jpg graphic file with name bjsports-58-23-i138.jpg
Wahlquist et al62, 2022 graphic file with name bjsports-58-23-i139.jpg graphic file with name bjsports-58-23-i140.jpg graphic file with name bjsports-58-23-i141.jpg graphic file with name bjsports-58-23-i142.jpg graphic file with name bjsports-58-23-i143.jpg graphic file with name bjsports-58-23-i144.jpg
Waring et al63, 2022 graphic file with name bjsports-58-23-i145.jpg graphic file with name bjsports-58-23-i146.jpg graphic file with name bjsports-58-23-i147.jpg graphic file with name bjsports-58-23-i148.jpg graphic file with name bjsports-58-23-i149.jpg graphic file with name bjsports-58-23-i150.jpg
Wilson et al64, 2021 graphic file with name bjsports-58-23-i151.jpg graphic file with name bjsports-58-23-i152.jpg graphic file with name bjsports-58-23-i153.jpg graphic file with name bjsports-58-23-i154.jpg graphic file with name bjsports-58-23-i155.jpg graphic file with name bjsports-58-23-i156.jpg

RoB 2 criteria: +=indicates a low risk of bias; ?= Indicates that there are some concerns; –=indicates a high risk of bias.There were no differences in risk of bias between outcomes within trials.

RoB 2Risk-of-Bias tool

Synthesis of results

Three articles did not provide baseline or follow-up data to be included in the meta-analyses.51 52 60 Meta-analyses of between 2 and 20 articles (n=37–4466) were performed separately for the four outcomes. A non-significant effect size was observed for neuromuscular warm-up programmes on SRC incidence (RR 0.69; 95% CI 0.39 to 1.23; I2 69%; low-quality evidence), and for RT on linear head acceleration (SMD −0.43; 95% CI −1.26 to 0.40; I2 63%; very low-quality evidence) or rotational head acceleration (SMD 0.08; 95% CI −0.61 to 0.77; I2 0%; low-quality evidence) (online supplemental file 7, figures 1–3). A large effect size was observed for RT on isometric neck strength (SMD 0.85; 95% CI 0.57 to 1.13; I2 62%; high-quality evidence) (figure 2, table 2).

Figure 2. Forest plot of the efficacy of resistance training on isometric neck strength.

Figure 2

Table 2. GRADE summary of findings.

Outcomes No of participants(articles) Risk of bias Inconsistency Indirectness Imprecision Publication bias Summary of findings Certainty
Pooled effect 95% CI
SRC incidence 4466(3 articles) X X X RR 0.69 0.39 to 1.23 ⊕⊕◯◯Low*
Linear head acceleration 89(3 articles) X X SMD −0.43 −1.26 to 0.40 ⊕◯◯◯Very low§
Rotational head acceleration 37(2 articles) X X X SMD 0.08 −0.61 to 0.77 ⊕⊕◯◯Low**††
Isometric neck strength 638(20 articles) X X X X X SMD 0.85 0.57 to 1.13 ⊕⊕⊕⊕High

GRADE criteria: X=no serious limitations; –=serious limitation.

Bolded values represent the observed effect sizes of exercise interventions on the outcome measures.

*

Downgraded one level for inconsistency due to substantial unexplained heterogeneity (I2=69%).

Downgraded one level for imprecision due to wide CIs which crossed both large benefits, and no benefits (95% CI 0.39 to 1.23).

Downgraded one level for risk of bias in included articles.

§

Downgraded one level for inconsistency due to substantial unexplained heterogeneity (I2=63%).

Downgraded one level for imprecision due to wide confidence intervals which crossed both large benefits and no benefits (95% CI –1.26 to 0.40).

**

Downgraded one level for risk of bias in included articles.

††

Downgraded one level for imprecision due to wide confidence intervals which crossed both moderate benefits, and no benefits (95% CI –0.61 to 0.77).

GRADEGrading of Recommendations Assessment, Development and EvaluationRRrisk ratioSMDstandardised mean differenceSRCsport-related concussion

The three articles which were not included in the meta-analyses reported statistically significant increases in isometric neck strength, following the exercise interventions.51 52 60 Two articles reported a significant increase in isometric neck extension strength in six out of eight51 and four out of eight tested angles,60 respectively. One article reported a significant increase in isometric neck flexion, extension and rotation strength.52

Subgroup and meta-regression analyses

Subgroup analyses were performed for isometric neck strength, while meta-regression was performed for seven subgroups where statistical heterogeneity was detected.

Exercise modality

Large effect sizes were observed for dynamic and multimodal resistance programmes on isometric neck strength (SMD 0.86; 95% CI 0.46 to 1.26; I2 34% and SMD 1.13; 95% CI 0.64 to 1.62; I2 66%, respectively). In contrast, a medium effect size was observed for static resistance programmes (SMD 0.74; 95% CI 0.32 to 1.16; I2 44%) (online supplemental file 7, figure 4).

Heterogeneity in the dynamic resistance group was reduced from 34% to 12% when the number of sessions per week was used as a covariate, however, without statistically significant regression coefficient (slope 0.26; 95% CI −0.02 to 0.55) (online supplemental file 8, figure 1). Heterogeneity in the multimodal (I2 66%) and static (I2 44%) resistance groups could not be explained by any participant or intervention characteristics factors as covariates.

Age

A large effect size was observed for RT on isometric neck strength in adult participants (≥19 years) (SMD 1.19; 95% CI 0.53 to 1.84; I2 68%), whereas, a medium effect size was observed in adolescent participants (<19 years) (SMD 0.73; 95% CI 0.31 to 1.16; I2 66%) (online supplemental file 7, figure 5).

Heterogeneity in adolescent participants was reduced from 66% to 45% when age was used as a covariate, with statistically significant regression coefficient (slope 0.20; 95% CI 0.05 to 0.36). Heterogeneity in adult participants (I2 68%) could not be explained by any participant or intervention characteristics factors as covariates (online supplemental file 8, figure 2).

Sex

A large effect size was observed for RT on isometric neck strength in male participants (SMD 0.89; 95% CI 0.59 to 1.19; I2 43%), whereas, a medium effect size was observed in female participants (SMD 0.65; 95% CI 0.06 to 1.24; I2 63%) (online supplemental file 7, figure 6).

Heterogeneity in male (I2 43%) and female (I2 63%) groups could not be explained by any participant or intervention characteristics factors as covariates.

Sensitivity analyses

The pooled effect estimates remained similar for all sensitivity analyses performed (online supplemental file 9).

Reporting biases

Visual and statistical assessments were performed for isometric neck strength, where no evidence of potential publication bias was found (Egger’s test: p=0.16) (online supplemental file 10).

Reporting completeness of the exercise interventions

The final CERT scores ranged from 4 to 16 with a median of 11.5 (IQR 9–13). All 26 articles reported on ‘generic or tailored’ (item 14a) while no articles reported on ‘motivation strategies’ (item 6). ‘Rules for exercise progression’ (items 7a) and ‘starting levels’ (item 15), which are important for the accurate replication and implementation of exercise interventions, were reported in 13 (50%) and 10 (38%) articles, respectively (table 3).

Table 3. Reporting completeness of the exercise interventions (CERT) assessment.

What (exercise equipment) 2. Who (qualifications) How (individual or group) How (supervision) How (adherence measuring and reporting) How (motivation strategies) 7 a. How (progression rules) 7b. How (programme progression) How (exercises) How (home component) How (non-exercise component) How (adverse events) Where (setting) When, how much (exercise description) 14a. Tailoring (generic or tailored) 14b. Tailoring (description of tailoring) Tailoring (starting level) 16a. How well (adherence assessment) 16b. How well (delivery as planned) Total score
Attwood et al402022 1 1 1 1 1 0 1 1 1 0 1 1 1 1 1 1 0 0 1 15
Attwood et al412018 0 1 1 1 1 0 0 1 0 1 0 0 1 0 1 1 0 0 1 10
Barden et al422022 0 1 1 1 1 0 0 1 0 1 0 0 1 0 1 1 0 1 1 11
Barrett et al432015 1 1 0 1 0 0 1 1 1 0 1 1 0 1 1 1 1 0 0 12
Becker et al442019 1 0 0 0 0 0 0 1 1 0 1 0 0 1 1 1 0 0 1 8
Burnett et al452005 1 0 0 1 0 0 1 1 1 0 1 0 0 1 1 1 0 0 0 9
Deng et al462022 1 0 1 0 1 0 1 1 1 0 1 1 1 1 1 1 0 1 1 14
Eckner et al122018 1 1 0 1 0 0 1 1 1 1 0 1 0 1 1 1 0 0 1 12
Fiebert et al482004 1 0 1 1 0 0 1 1 1 1 0 0 0 1 1 1 0 1 1 12
Geary et al492014 1 1 1 1 0 0 0 0 1 1 0 0 1 1 1 0 0 0 0 9
Hamlin et al392020 1 1 1 1 0 0 1 1 1 0 1 0 1 1 1 1 1 0 0 13
Hislop et al502017 0 1 1 1 1 0 0 1 0 1 0 0 1 0 1 1 0 1 1 11
Leggett et al511991 1 0 0 0 0 0 0 1 1 1 0 0 1 1 1 1 1 0 0 9
Maconi et al522016 1 0 0 1 1 0 1 1 1 0 0 0 1 1 1 1 1 1 1 13
Mansell et al532005 1 1 1 1 1 0 1 1 0 1 0 0 0 1 1 1 1 0 1 13
Müller et al542021 1 0 1 0 1 0 0 0 1 1 0 1 1 1 1 1 0 1 1 12
Peek et al552022 1 0 1 1 0 0 0 0 1 0 1 0 1 1 1 1 0 0 0 9
Pollock et al561993 0 0 0 1 0 0 1 1 0 0 0 0 0 1 1 1 1 0 0 7
Salmon et al572013 1 1 0 1 1 0 1 1 1 1 1 0 1 1 1 1 1 1 1 16
Stump et al581993 1 0 0 0 0 0 0 0 1 0 0 0 1 0 1 0 0 0 0 4
Taylor et al592006 1 1 0 1 1 0 1 1 0 0 1 0 1 1 1 1 1 0 1 13
Tsuyama et al602006 0 0 0 0 0 0 1 1 0 0 1 0 0 1 1 1 1 0 0 7
Versteegh et al6,1
2020
1 1 1 1 1 0 0 1 0 1 0 1 1 1 1 1 1 1 1 15
Wahlquist et al62
2022
1 0 1 1 0 0 0 1 0 0 0 0 1 1 1 1 0 0 0 8
Waring et al632022 1 1 0 1 0 0 0 1 1 1 0 0 1 1 1 1 0 0 0 10
Wilson et al642021 1 0 1 1 1 0 0 1 1 1 0 1 1 1 1 1 0 1 1 14
Total score 21 13 14 20 12 0 13 22 17 13 10 7 18 22 26 24 10 9 15

CERT criteria: 1=adequately described; 0=not/inadequately described.

CERTConsensus on Exercise Reporting Template

Discussion

This systematic review and meta-analysis included 26 articles that evaluated the efficacy of exercise interventions of different modalities on outcomes related to SRC. Non-significant effect sizes were observed for neuromuscular warm-up programmes on SRC incidence, and for RT on linear and rotational head accelerations, with certainty of evidence ranging from very low to low. A large effect size was observed for RT on isometric neck strength, with 20 articles providing high certainty of evidence. The results of the CERT assessment suggest that exercise interventions were generally not reported in sufficient detail to allow accurate replication in future studies.

SRC incidence

The result of the meta-analysis indicated that neuromuscular warm-up programmes did not have a significant effect on SRC incidence. There could be several reasons for this. Although similar in study population (male rugby athletes) and intervention content (neuromuscular warm-up exercises), the included articles varied considerably in intervention duration (14 weeks vs 42 weeks), and definition of SRC injury (>24 hours vs >8 days). This likely contributed to the substantial statistical heterogeneity (I2 69%) and differences in effect sizes (mean RR range: 0.36–1.11). Another possible explanation for the observed lack of efficacy could be due to the dose–response relationship. While one article reported a 60% reduction in SRC incidence in the intervention group when compared with the control group,41 another article reported a similar reduction in SRC incidence (59%), but only when analyses included teams that implemented the programme at least three times a week.50 The authors of both articles reasoned that the observed reduction in SRC incidence was due to the inclusion of neck strengthening exercises within the neuromuscular warm-up programmes at all stages of the intervention period.41 50 As the association between greater neck muscle strength and reduced SRC incidence is not definitively established, it is difficult to evaluate whether neck muscle exercises alone could produce such results. It is possible that the inclusion of neck muscle exercises within multimodal injury prevention programmes could yield more beneficial results in reducing SRC than isolated neck muscle exercises alone; however, this remains to be investigated in future studies.

Linear and rotational head accelerations

The results of the meta-analyses indicated that RT did not have a significant effect on linear and rotational head accelerations. Limited data for linear head acceleration (n=3 articles; 89 participants) and rotational head acceleration (n=2 articles; 37 participants) contributed to the overall uncertainty, making it difficult to draw robust conclusions about the efficacy of exercise interventions on these outcomes. In addition, only one article provided a sample size calculation while the remaining articles were likely underpowered. Therefore, future research endeavours should examine these outcomes in greater detail.

Isometric neck strength

As all included articles on isometric neck strength implemented exercise interventions in the form of RT, the effect sizes observed in this review further reinforce the well-established benefits of RT on muscle strength.65 The change in muscle strength occurs due to a number of neuromuscular adaptations induced by RT.65 Neurologically, RT leads to the recruitment of an increased number and firing rate of motor units,66 heightened reflex potentiation67 and improved synchronisation,68 whereas muscular adaptations involve an increase in a cross-sectional area of the muscle65 and selective hypertrophy of fast-twitch fibres.69 70 Although the articles included in this review implemented RT with large differences in exercise prescriptions (eg, exercise modality, frequency, duration, intensity), meta-analysis showed an overall large effect size for RT on isometric neck strength. When separated by the exercise modality, all three modalities were efficacious in increasing isometric neck strength, with large effect sizes following dynamic and multimodal resistance programmes, and a medium effect size following static resistance programmes. This indicates that training-induced adaptations, and subsequent neck strength gains, can be achieved with a variety of RT prescriptions.

While RT was efficacious in increasing isometric neck strength in both males and females, the articles in this analysis predominantly included male participants, and the comparatively lower effect size observed in females may be attributed to the evident disparity in the representation of participants. Given the well-established benefits of RT on overall muscle strength in females,71,73 there is a compelling need to enhance the involvement of this demographic in research aimed at exploring outcomes related to prevention of SRC. This would contribute to greater equality in participant representation and result in a more accurate estimation of the effect sizes in the measured outcomes.

Similarly, the comparatively lower effect size for RT in adolescent participants when compared with adults cannot be definitively attributed to differences in physiological adaptations to RT between these two age groups. It is likely that the observed discrepancy is due to significant variations in RT prescriptions across all articles included in the analysis. Therefore, future research should align RT protocols with current recommendations on RT prescriptions74,76 in order to maximise strength gains in neck musculature.

It is important to note that as the definitive association between greater neck muscle strength and reduced SRC risk remains uncertain, the efficacy of RT on isometric neck strength observed in this review does not inherently imply a reduced risk of SRC. To substantiate such a claim in the future, trials directly investigating the efficacy of neck strength interventions on SRC incidence are warranted.

Reporting completeness of the exercise interventions

Generally, exercise interventions were not reported in sufficient detail. No articles described ‘motivational strategies’ (item 6). Motivation is an important factor for exercise adherence in athletes,77 78 therefore, the lack of information on motivational strategies could limit the efficacy of otherwise well-designed exercise interventions. Another commonly under-reported aspect was ‘starting level’ (item 15), which was lacking in 62% of articles. Since athletes have varying fitness levels, and abilities, accurately estimating the starting level can prevent situations where the initial exercise stimulus is too challenging for some, and not challenging enough for others. Also, only 50% of articles adequately described ‘rules for exercise progression’ (item 7a), which is essential for stimulating continuous neuromuscular adaptations.79 Thus, the reporting of important aspects of exercise interventions is consistently insufficient, therefore, future research should aim to improve reporting completeness in order to promote study replication and facilitate further implementation.

Strengths and limitations of this review

To our knowledge, this systematic review is the first to evaluate the efficacy of exercise interventions not only on SRC incidence but also on other outcomes potentially related to SRC. Throughout the review process, the authors diligently adhered to established guidelines to enhance transparency and the overall credibility of the systematic review.

This review has some limitations to acknowledge. First, the combination of neck strength directions into a single composite score allowed for a comprehensive evaluation of overall neck strength and facilitated the interpretation of the data. Moreover, as some articles measured isometric neck strength in non-traditional directions (eg, anterolateral neck flexion, posterolateral extension) by calculating composite scores, these values were also included in the analyses. Nevertheless, this approach may have obscured asymmetries in strength between different directions, potentially overlooking findings related to muscle balance and function. Furthermore, the composite score may have reduced the sensitivity to changes in specific areas of neck strength over time or in response to interventions.

Second, moderate to substantial heterogeneity was observed in the majority of meta-analyses and subgroup analyses. In some subgroups, the observed heterogeneity could not be explained by any participant or intervention characteristics included as covariates, and may be related to other relevant study-level characteristics not available for extraction. Moreover, as the post hoc meta-regression was conducted with a limited number of articles, generalisability and robustness of the results should be interpreted with caution.

Third, the RoB2 tool was originally developed for RCTs, therefore, its applicability in quasi-experimental studies may be limited. Since, in this review, the RoB2 tool was employed to evaluate the methodological quality of all included articles, irrespective of study design, this could result in high-quality articles being downgraded due to criteria that are not tailored to their design. Fourth, this review only included articles published in English, which may have introduced language bias due to the exclusion of any non-English articles relevant to the topic.

Implications for future research

Several key areas were identified in this review that warrant attention for future research. More adequately powered and rigorous trials are needed, particularly for investigating the efficacy of exercise interventions on SRC incidence, and linear and rotational head accelerations. Given that less than 5% of participants were females, future studies should make greater efforts to ensure equality in participant representation. Since articles included in this review predominantly included athletes from rugby, soccer and American football, future research should broaden its scope beyond these sports to encompass other sports where SRC frequently occurs (eg, ice hockey, handball). Future exercise interventions should align with evidence-based exercise prescription recommendations (eg, exercise modality, duration, frequency and load), but still maintain a sufficient level of simplicity to facilitate adherence and easy implementation in real-world sport settings. Finally, it is essential that researchers improve reporting completeness of exercise interventions in order to advance the understanding of exercise interventions, promote study replication and facilitate further implementation.

Conclusion

This systematic review and meta-analysis demonstrated non-significant effects for neuromuscular warm-up programmes on SRC incidence, and for RT on linear and rotational head accelerations. Large effect size was observed following RT on isometric neck strength. Dynamic and multimodal resistance programmes seem to be more efficacious in increasing isometric neck strength than static resistance programmes, with higher effect sizes for males than females and adults than adolescents. It is important to note that the observed efficacy of RT on isometric neck strength does not necessarily translate to a reduced SRC risk. Therefore, more adequately powered and rigorous trials are needed to determine the efficacy of exercise interventions on SRC incidence, as well as on linear and rotational head accelerations. Researchers need to include more females, different sports with high risk of SRC and follow exercise prescription recommendations, as well as improve exercise reporting to allow for replication of research and implementation in real-world sport settings.

supplementary material

online supplemental file 1

online supplemental file 2

online supplemental file 3

online supplemental file 4

online supplemental file 5

online supplemental file 6

online supplemental file 7

online supplemental file 8

online supplemental file 9

online supplemental file 10

No funding bodies were active in study design, data collection, analysis or preparation of the manuscript.

Footnotes

Funding: This study is funded by the Swedish Research Council for Sport Science (Project number: P2023-0048 and P2024-0018) and the Kock’s Foundation.

Provenance and peer review: Not commissioned; externally peer reviewed.

Patient consent for publication: Not applicable.

Data availability free text: Not applicable.

Contributor Information

Branimir Ivanic, Email: branimir.ivanic@med.lu.se.

Anna Cronström, Email: anna.cronstrom@med.lu.se.

Kajsa Johansson, Email: kajsa.johansson@liu.se.

Eva Ageberg, Email: eva.ageberg@med.lu.se.

Data availability statement

All data relevant to the study are included in the article or uploaded as online supplemental information.

References

  • 1.Patricios JS, Schneider KJ, Dvorak J, et al. Consensus statement on concussion in sport: the 6th International Conference on Concussion in Sport-Amsterdam, October 2022. Br J Sports Med. 2023;57:695–711. doi: 10.1136/bjsports-2023-106898. [DOI] [PubMed] [Google Scholar]
  • 2.Rowson S, Bland ML, Campolettano ET, et al. Biomechanical Perspectives on Concussion in Sport. Sports Med Arthrosc Rev . 2016;24:100–7. doi: 10.1097/JSA.0000000000000121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Leddy JJ, Haider MN, Noble JM, et al. Clinical Assessment of Concussion and Persistent Post-Concussive Symptoms for Neurologists. Curr Neurol Neurosci Rep. 2021;21:70. doi: 10.1007/s11910-021-01159-2. [DOI] [PubMed] [Google Scholar]
  • 4.Makdissi M, Cantu RC, Johnston KM, et al. The difficult concussion patient: what is the best approach to investigation and management of persistent (>10 days) postconcussive symptoms? Br J Sports Med. 2013;47:308–13. doi: 10.1136/bjsports-2013-092255. [DOI] [PubMed] [Google Scholar]
  • 5.McAllister TW, Broglio SP, Katz BP, et al. Characteristics and Outcomes of Athletes With Slow Recovery From Sports-Related Concussion: A CARE Consortium Study. Neurology (ECronicon) 2023;100:e1510–9. doi: 10.1212/WNL.0000000000206853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Amoo-Achampong K, Rosas S, Schmoke N, et al. Trends in sports-related concussion diagnoses in the USA: a population-based analysis using a private-payor database. Phys Sportsmed. 2017;45:239–44. doi: 10.1080/00913847.2017.1327304. [DOI] [PubMed] [Google Scholar]
  • 7.Finch CF, Clapperton AJ, McCrory P. Increasing incidence of hospitalisation for sport-related concussion in Victoria, Australia. Med J Aust. 2013;198:427–30. doi: 10.5694/mja12.11217. [DOI] [PubMed] [Google Scholar]
  • 8.Rosenthal JA, Foraker RE, Collins CL, et al. National High School Athlete Concussion Rates From 2005-2006 to 2011-2012. Am J Sports Med. 2014;42:1710–5. doi: 10.1177/0363546514530091. [DOI] [PubMed] [Google Scholar]
  • 9.Eliason PH, Galarneau J-M, Kolstad AT, et al. Prevention strategies and modifiable risk factors for sport-related concussions and head impacts: a systematic review and meta-analysis. Br J Sports Med. 2023;57:749–61. doi: 10.1136/bjsports-2022-106656. [DOI] [PubMed] [Google Scholar]
  • 10.Streifer M, Brown AM, Porfido T, et al. The Potential Role of the Cervical Spine in Sports-Related Concussion: Clinical Perspectives and Considerations for Risk Reduction. J Orthop Sports Phys Ther. 2019;49:202–8. doi: 10.2519/jospt.2019.8582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Michael Storr IG. Neck Muscle Strength Training in the Risk Management of Concussion in Contact Sports: Critical Appraisal of Application to Practice. J Athl Enhancement. 2015;4 doi: 10.4172/2324-9080.1000195. [DOI] [Google Scholar]
  • 12.Eckner JT, Oh YK, Joshi MS, et al. Effect of neck muscle strength and anticipatory cervical muscle activation on the kinematic response of the head to impulsive loads. Am J Sports Med. 2014;42:566–76. doi: 10.1177/0363546513517869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Jin X, Feng Z, Mika V, et al. The Role of Neck Muscle Activities on the Risk of Mild Traumatic Brain Injury in American Football. J Biomech Eng. 2017;139 doi: 10.1115/1.4037399. [DOI] [PubMed] [Google Scholar]
  • 14.Bretzin AC, Mansell JL, Tierney RT, et al. Sex Differences in Anthropometrics and Heading Kinematics Among Division I Soccer Athletes. Sports Health. 2017;9:168–73. doi: 10.1177/1941738116678615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Caccese JB, Buckley TA, Tierney RT, et al. Head and neck size and neck strength predict linear and rotational acceleration during purposeful soccer heading. Sports Biomech. 2018;17:462–76. doi: 10.1080/14763141.2017.1360385. [DOI] [PubMed] [Google Scholar]
  • 16.Peek K, Elliott JM, Orr R. Higher neck strength is associated with lower head acceleration during purposeful heading in soccer: a systematic review. J Sci Med Sport. 2020;23:453–62. doi: 10.1016/j.jsams.2019.11.004. [DOI] [PubMed] [Google Scholar]
  • 17.Gutierrez GM, Conte C, Lightbourne K. The relationship between impact force, neck strength, and neurocognitive performance in soccer heading in adolescent females. Pediatr Exerc Sci. 2014;26:33–40. doi: 10.1123/pes.2013-0102. [DOI] [PubMed] [Google Scholar]
  • 18.Collins CL, Fletcher EN, Fields SK, et al. Neck strength: a protective factor reducing risk for concussion in high school sports. J Prim Prev. 2014;35:309–19. doi: 10.1007/s10935-014-0355-2. [DOI] [PubMed] [Google Scholar]
  • 19.Farley T, Barry E, Sylvester R, et al. Poor isometric neck extension strength as a risk factor for concussion in male professional Rugby Union players. Br J Sports Med. 2022;56:616–21. doi: 10.1136/bjsports-2021-104414. [DOI] [PubMed] [Google Scholar]
  • 20.Nutt S, McKay MJ, Gillies L, et al. Neck strength and concussion prevalence in football and rugby athletes. J Sci Med Sport. 2022;25:632–8. doi: 10.1016/j.jsams.2022.04.001. [DOI] [PubMed] [Google Scholar]
  • 21.Tierney RT, Higgins M, Caswell SV, et al. Sex differences in head acceleration during heading while wearing soccer headgear. J Athl Train. 2008;43:578–84. doi: 10.4085/1062-6050-43.6.578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Tierney RT, Sitler MR, Swanik CB, et al. Gender differences in head-neck segment dynamic stabilization during head acceleration. Med Sci Sports Exerc. 2005;37:272–9. doi: 10.1249/01.mss.0000152734.47516.aa. [DOI] [PubMed] [Google Scholar]
  • 23.Caccese JB, Buckley TA, Tierney RT, et al. Sex and age differences in head acceleration during purposeful soccer heading. Res Sports Med. 2018;26:64–74. doi: 10.1080/15438627.2017.1393756. [DOI] [PubMed] [Google Scholar]
  • 24.Rowson S, Duma SM, Beckwith JG, et al. Rotational head kinematics in football impacts: an injury risk function for concussion. Ann Biomed Eng. 2012;40:1–13. doi: 10.1007/s10439-011-0392-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.King AI, Yang KH, Zhang L, et al. IRCOBI Conference; 2003. Is head injury caused by linear or angular acceleration? pp. 1–12. [Google Scholar]
  • 26.Rowson S, Brolinson G, Goforth M, et al. Linear and angular head acceleration measurements in collegiate football. J Biomech Eng. 2009;131:061016. doi: 10.1115/1.3130454. [DOI] [PubMed] [Google Scholar]
  • 27.Ardern CL, Büttner F, Andrade R, et al. Implementing the 27 PRISMA 2020 Statement items for systematic reviews in the sport and exercise medicine, musculoskeletal rehabilitation and sports science fields: the PERSiST (implementing Prisma in Exercise, Rehabilitation, Sport medicine and SporTs science) guidance. Br J Sports Med. 2022;56:175–95. doi: 10.1136/bjsports-2021-103987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Veritas Health Innovation . Melbourne, Australia: Veritas Health Innovation; 2023. Covidence systematic review software.www.covidence.org Available. [Google Scholar]
  • 29.Higgins JPT, Li T, Deeks JJ. In: Cochrane handbook for systematic reviews of interventions. Higgins JPT, Thomas J, Chandler J, et al., editors. Chichester (UK): John Wiley & Sons; 2019. Chapter 6: choosing effect measures and computing estimates of effect; pp. 143–76. [Google Scholar]
  • 30.Rivera-Brown AM, Frontera WR. Principles of exercise physiology: responses to acute exercise and long-term adaptations to training. PM R. 2012;4:797–804. doi: 10.1016/j.pmrj.2012.10.007. [DOI] [PubMed] [Google Scholar]
  • 31.Sterne JAC, Savović J, Page MJ, et al. RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ. 2019;366:l4898. doi: 10.1136/bmj.l4898. [DOI] [PubMed] [Google Scholar]
  • 32.The Cochrane Collaboration . The Cochrane Collaboration; 2023. Review manager web(revman web) ver. 4.26.0.www.revman.cochrane.org Available. [Google Scholar]
  • 33.Cohen J. Statistical power analysis for the behavioral sciences. 2nd. Hillsdale, NJ: Erlbaum; 1988. edn. [Google Scholar]
  • 34.Deeks JJ, Higgins JPT, Altman DG. In: Cochrane handbook for systematic reviews of interventions. Higgins JPT, Thomas J, Chandler J, et al., editors. Chichester (UK): John Wiley & Sons; 2019. Chapter 10: analyzing data and undertaking meta-analyses; pp. 241–84. [Google Scholar]
  • 35.StataCorp LLC . College station, TX: StataCorp LLC; 2023. Stata statistical software, ver. 18.https://www.stata.com Available. [Google Scholar]
  • 36.McMaster University and Evidence Prime; 2024. GRADEpro GDT: gradepro guideline development tool software.www.gradepro.org Available. [Google Scholar]
  • 37.Schünemann H, Brożek J, Guyatt G, et al.GRADE handbook for grading quality of evidence and strength of recommendations .The GRADE Working Group; 2013 [Google Scholar]
  • 38.Slade SC, Dionne CE, Underwood M, et al. Consensus on Exercise Reporting Template (CERT): Explanation and Elaboration Statement. Br J Sports Med. 2016;50:1428–37. doi: 10.1136/bjsports-2016-096651. [DOI] [PubMed] [Google Scholar]
  • 39.Hamlin MJ, Deuchrass R, Elliot CE. Effect of a 6-week exercise intervention for improved neck muscle strength in amateur male rugby union players. J S E S. 2020;4:33–9. doi: 10.36905/jses.2020.01.05. [DOI] [Google Scholar]
  • 40.Attwood MJ, Hudd L-JW, Roberts SP, et al. Eight Weeks of Self-Resisted Neck Strength Training Improves Neck Strength in Age-Grade Rugby Union Players: A Pilot Randomized Controlled Trial. Sports Health. 2022;14:500–7. doi: 10.1177/19417381211044736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Attwood MJ, Roberts SP, Trewartha G, et al. Efficacy of a movement control injury prevention programme in adult men’s community rugby union: a cluster randomised controlled trial. Br J Sports Med. 2018;52:368–74. doi: 10.1136/bjsports-2017-098005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Barden C, Hancock MV, Stokes KA, et al. Effectiveness of the Activate injury prevention exercise programme to prevent injury in schoolboy rugby union. Br J Sports Med. 2022;56:812–7. doi: 10.1136/bjsports-2021-105170. [DOI] [PubMed] [Google Scholar]
  • 43.Barrett MD, McLoughlin TF, Gallagher KR, et al. Effectiveness of a tailored neck training program on neck strength, movement, and fatigue in under-19 male rugby players: a randomized controlled pilot study. Open Access J Sports Med. 2015;6:137–47. doi: 10.2147/OAJSM.S74622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Becker S, Berger J, Backfisch M, et al. Effects of a 6-Week Strength Training of the Neck Flexors and Extensors on the Head Acceleration during Headers in Soccer. J Sports Sci Med. 2019;18:729–37. [PMC free article] [PubMed] [Google Scholar]
  • 45.Burnett AF, Naumann FL, Price RS, et al. A comparison of training methods to increase neck muscle strength. Work. 2005;25:205–10. [PubMed] [Google Scholar]
  • 46.Deng CL, Pearce AJ, Mentiplay BF, et al. An isometric neck strengthening program does not improve neck strength in elite women’s football-code athletes: a randomised controlled trial. J Sci Med Sport. 2022;25:327–33. doi: 10.1016/j.jsams.2021.10.009. [DOI] [PubMed] [Google Scholar]
  • 47.Eckner JT, Goshtasbi A, Curtis K, et al. Feasibility and Effect of Cervical Resistance Training on Head Kinematics in Youth Athletes: A Pilot Study. Am J Phys Med Rehabil. 2018;97:292–7. doi: 10.1097/PHM.0000000000000843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Fiebert IM, Roach KE, Cho P, et al. The effects of antigravity unsupervised home cervical muscle strengthening protocol on cervical strength in healthy young adults. BMR. 2004;17:41–9. doi: 10.3233/BMR-2004-17202. [DOI] [Google Scholar]
  • 49.Geary K, Green BS, Delahunt E. Effects of neck strength training on isometric neck strength in rugby union players. Clin J Sport Med. 2014;24:502–8. doi: 10.1097/JSM.0000000000000071. [DOI] [PubMed] [Google Scholar]
  • 50.Hislop MD, Stokes KA, Williams S, et al. Reducing musculoskeletal injury and concussion risk in schoolboy rugby players with a pre-activity movement control exercise programme: a cluster randomised controlled trial. Br J Sports Med. 2017;51:1140–6. doi: 10.1136/bjsports-2016-097434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Leggett SH, Graves JE, Pollock ML, et al. Quantitative assessment and training of isometric cervical extension strength. Am J Sports Med. 1991;19:653–9. doi: 10.1177/036354659101900618. [DOI] [PubMed] [Google Scholar]
  • 52.Maconi F, Venturelli M, Limonta E, et al. Effects of a 12-week neck muscles training on muscle function and perceived level of muscle soreness in amateur rugby players. Sport Sci Health. 2016;12:443–52. doi: 10.1007/s11332-016-0314-9. [DOI] [Google Scholar]
  • 53.Mansell J, Tierney RT, Sitler MR, et al. Resistance training and head-neck segment dynamic stabilization in male and female collegiate soccer players. J Athl Train. 2005;40:310–9. [PMC free article] [PubMed] [Google Scholar]
  • 54.Müller C, Zentgraf K. Neck and Trunk Strength Training to Mitigate Head Acceleration in Youth Soccer Players. J Strength Cond Res. 2021;35:S81–9. doi: 10.1519/JSC.0000000000003822. [DOI] [PubMed] [Google Scholar]
  • 55.Peek K, Andersen J, McKay MJ, et al. The Effect of the FIFA 11 + with Added Neck Exercises on Maximal Isometric Neck Strength and Peak Head Impact Magnitude During Heading: A Pilot Study. Sports Med. 2022;52:655–68. doi: 10.1007/s40279-021-01564-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Pollock ML, Graves JE, Bamman MM, et al. Frequency and volume of resistance training: effect on cervical extension strength. Arch Phys Med Rehabil. 1993;74:1080–6. doi: 10.1016/0003-9993(93)90065-i. [DOI] [PubMed] [Google Scholar]
  • 57.Salmon DM, Harrison MF, Sharpe D, et al. Exercise therapy for improved neck muscle function in helicopter aircrew. Aviat Space Environ Med. 2013;84:1046–54. doi: 10.3357/asem.3593.2013. [DOI] [PubMed] [Google Scholar]
  • 58.Stump J, Rash G, Semon J, et al. A comparison of two modes of cervical exercise in adolescent male athletes. J Manipul Physiol Ther. 1993;16:155–60. [PubMed] [Google Scholar]
  • 59.Taylor MK, Hodgdon JA, Griswold L, et al. Cervical resistance training: effects on isometric and dynamic strength. Aviat Space Environ Med. 2006;77:1131–5. [PubMed] [Google Scholar]
  • 60.Tsuyama K, Yamamoto Y, Nakazato K, et al. The effect of neck muscle training on the isometric cervical extension strength and cross-sectional area of the neck extensor muscles -combined training for neck extensor muscles using a cervical extension machine. Jpn J Phys Fitness Sports Med. 2006;55:S1–6. doi: 10.7600/jspfsm.55.S1. [DOI] [Google Scholar]
  • 61.Versteegh TH, Dickey JP, Emery CA, et al. Evaluating the Effects of a Novel Neuromuscular Neck Training Device on Multiplanar Static and Dynamic Neck Strength: A Pilot Study. J Strength Cond Res. 2020;34:708–16. doi: 10.1519/JSC.0000000000003091. [DOI] [PubMed] [Google Scholar]
  • 62.Wahlquist VE, Glutting JJ, Kaminski TW. Examining the influence of the Get aHEAD Safely in Soccer™ program on head impact kinematics and neck strength in female youth soccer players. Res Sports Med. 2024;32:17–27. doi: 10.1080/15438627.2022.2079982. [DOI] [PubMed] [Google Scholar]
  • 63.Waring KM, Smith ER, Austin GP, et al. Exploring the Effects of a Neck Strengthening Program on Purposeful Soccer Heading Biomechanics and Neurocognition. Int J Sports Phys Ther. 2022;17:1043–52. doi: 10.26603/001c.38327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Wilson JC, Levek C, Daoud AK, et al. Web-Based Exercise Program Increases Cervical Strength in Adolescent Athletes. J Strength Cond Res. 2021;35:1149–55. doi: 10.1519/JSC.0000000000002907. [DOI] [PubMed] [Google Scholar]
  • 65.Bandy WD, Lovelace-Chandler V, McKitrick-Bandy B. Adaptation of skeletal muscle to resistance training. J Orthop Sports Phys Ther. 1990;12:248–55. doi: 10.2519/jospt.1990.12.6.248. [DOI] [PubMed] [Google Scholar]
  • 66.Häkkinen K, Komi PV, Alén M. Effect of explosive type strength training on isometric force- and relaxation-time, electromyographic and muscle fibre characteristics of leg extensor muscles. Acta Physiol Scand. 1985;125:587–600. doi: 10.1111/j.1748-1716.1985.tb07759.x. [DOI] [PubMed] [Google Scholar]
  • 67.Sale DG, MacDougall JD, Upton AR, et al. Effect of strength training upon motoneuron excitability in man. Med Sci Sports Exerc. 1983;15:57–62. [PubMed] [Google Scholar]
  • 68.Milner-Brown HS, Stein RB, Lee RG. Synchronization of human motor units: possible roles of exercise and supraspinal reflexes. Electroencephalogr Clin Neurophysiol. 1975;38:245–54. doi: 10.1016/0013-4694(75)90245-x. [DOI] [PubMed] [Google Scholar]
  • 69.Häkkinen K, Alén M, Komi PV. Changes in isometric force- and relaxation-time, electromyographic and muscle fibre characteristics of human skeletal muscle during strength training and detraining. Acta Physiol Scand. 1985;125:573–85. doi: 10.1111/j.1748-1716.1985.tb07760.x. [DOI] [PubMed] [Google Scholar]
  • 70.Thorstensson A, Hultén B, von Döbeln W, et al. Effect of strength training on enzyme activities and fibre characteristics in human skeletal muscle. Acta Physiol Scand. 1976;96:392–8. doi: 10.1111/j.1748-1716.1976.tb10207.x. [DOI] [PubMed] [Google Scholar]
  • 71.Zouita A, Darragi M, Bousselmi M, et al. The Effects of Resistance Training on Muscular Fitness, Muscle Morphology, and Body Composition in Elite Female Athletes: A Systematic Review. Sports Med. 2023;53:1709–35. doi: 10.1007/s40279-023-01859-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Moran J, Sandercock G, Ramirez-Campillo R, et al. A Meta-Analysis of Resistance Training in Female Youth: Its Effect on Muscular Strength, and Shortcomings in the Literature. Sports Med. 2018;48:1661–71. doi: 10.1007/s40279-018-0914-4. [DOI] [PubMed] [Google Scholar]
  • 73.Hagstrom AD, Marshall PW, Halaki M, et al. The Effect of Resistance Training in Women on Dynamic Strength and Muscular Hypertrophy: A Systematic Review with Meta-analysis. Sports Med. 2020;50:1075–93. doi: 10.1007/s40279-019-01247-x. [DOI] [PubMed] [Google Scholar]
  • 74.Caswell SV, York M, Ambegaonkar JP, et al. Neck Strengthening Recommendations for Concussion Risk Reduction in Youth Sport. Int J Athl Ther Train. 2014;19:22–7. doi: 10.1123/ijatt.2014-0043. [DOI] [Google Scholar]
  • 75.Currier BS, Mcleod JC, Banfield L, et al. Resistance training prescription for muscle strength and hypertrophy in healthy adults: a systematic review and Bayesian network meta-analysis. Br J Sports Med. 2023;57:1211–20. doi: 10.1136/bjsports-2023-106807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Peterson MD, Rhea MR, Alvar BA. Maximizing strength development in athletes: a meta-analysis to determine the dose-response relationship. J Strength Cond Res. 2004;18:377–82. doi: 10.1519/R-12842.1. [DOI] [PubMed] [Google Scholar]
  • 77.Way A, Jones MV, Slater MJ. Exploring training adherence in elite school-age athletes. Qual Res Sport Exerc Health. 2012;4:154–71. doi: 10.1080/2159676X.2011.653496. [DOI] [Google Scholar]
  • 78.Almagro BJ, Sáenz-López P, Fierro-Suero S, et al. Intrinsic Motivation and Adherence in Athletes. Int J Environ Res Public Health. 2020;17 doi: 10.3390/ijerph17249441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Kraemer WJ, Adams K, Cafarelli E, et al. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc. 2002;34:364–80. doi: 10.1097/00005768-200202000-00027. [DOI] [PubMed] [Google Scholar]

Associated Data

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Supplementary Materials

online supplemental file 1

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Data Availability Statement

All data relevant to the study are included in the article or uploaded as online supplemental information.

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