Introduction

Muscle damage (DM) can occur in muscular structures—membranes, Z-line, sarcolemma, T-tubules, and myofibrils—as a consequence of the imposition of a mechanical overload [1]. In the literature, the onset of muscle damage associated with an inflammatory process after exercise is well documented [2, 3]. In addition, it is known that, among strength exercises, there is a higher incidence of exercise-induced muscle damage (EIMD) after exercises involving eccentric contraction [4, 5]. Many indirect markers have been used to evaluate muscle damage, but delayed onset muscle soreness (DOMS) and strength are the most remarkable ones.

Currently, cryotherapy modalities are widely used in the treatment of subjective (DOMS) and objective (strength) recovery characteristics [6, 7]. The cooling of the tissue is believed to produce a decrease in blood flow, tissue temperature, and metabolism, leading to a limitation of edema formation and a reduction of cells death by secondary hypoxia, protecting the muscle cells [8]. Cryotherapy can be applied in a variety of ways such as cold-water immersion (CWI) [9], whole-body cryotherapy (WBC) [7], partial-body cryotherapy (PBC) [10] and local cryotherapy [11]. There is a growing body of evidence elucidating the positive effects of CWI [12], WBC [13] and PBC [14]. However, those cooling strategies are more applicable in sports context [15] and have limited insertion in clinical practice. Local cryotherapy, on the other hand, might be a more practical and affordable option in a clinical environment, which justifies the need to investigate its potential effects. Furthermore, little is known about the optimal dosage of local cryotherapy. Periods of application between 15 and 20 min are often prescribed, but whether this time is appropriate and sufficient to generate benefits remains unknown.

Although local cryotherapy is more compatible with clinical practice, there is no consensus in scientific research regarding its effectiveness. Review studies that have analyzed the effects of cryotherapy on the symptoms related to EIMD emphasize WBC [6] and CWI [7, 16, 17]. To this date, no review studies have specifically examined the influence of local cryotherapy on subjective and objective markers of EIMD, and it remains uncertain whether local cryotherapy has any potential to accelerate recovery from symptoms of EIMD. Therefore, the aim of the present systematic review and meta-analysis is to verify the effects of local cryotherapy on the treatment of DOMS and muscle weakness related to EIMD. We hypothesized that local cryotherapy would help decrease DOMS and attenuate loss of strength following EIMD.

Methods

The current study utilized PRISMA (Preferred Reporting Items for Systematic Review and Meta-analyses) guidelines for Systematic Reviews and Meta-analysis [18]. The PRISMA is a checklist containing the 27 items that must be included in a systematic review.

Data sources and searches

We searched the following electronic databases (from inception to March 2018): MEDLINE (accessed by PubMed), Physiotherapy Evidence Database (PEDro), The Cochrane Central Register of Controlled Trials (Cochrane CENTRAL), and Centro Latino-Americano e do Caribe de Informação em Ciências da Saúde (LILACS). In addition, we searched the references of published studies. The search was performed for the last time in April 2018. The search comprised the following terms: “Cryotherapy”, “muscle damage”, “delayed onset muscle soreness”, “exercise induced muscle damage” combined with a high sensitivity combination of words used in the search for randomized clinical trials [19]. We included publications in English. For the combination of the keywords, we utilized the Boolean terms AND, and OR. The complete search strategy used for the MEDLINE database is shown in Table 1.

Table 1 Search strategy utilized for MEDLINE

Eligibility criteria

We included randomized clinical trials (RCT) and controlled clinical trials (CCT). Studies that applied a muscle damage protocol, performed cryotherapy as a therapy in comparison with a control group, and evaluated DOMS and/or strength were included. The following exclusion criteria were used: (1) samples comprised of people with any disease/dysfunction, (2) samples of people under 18 or over 40 years old; (3) non-application of local cryotherapy; (4) non assessment of some of the outcomes of interest; (5) cross-over designs.

Studies selection and data extraction

Two investigators independently evaluated titles and abstracts of all articles identified by the search strategy. All abstracts that did not provide sufficient information regarding the inclusion and exclusion criteria were selected for full-text evaluation. In the second phase, the same reviewers independently evaluated the full-text articles and made their selection in accordance with the eligibility criteria. Disagreements between reviewers were solved by consensus or through a third person review. Using standardized forms, the same two reviewers independently conducted data extraction with regard to the methodological characteristics of the studies, number of participants, age, groups, interventions, outcomes and results. Disagreements were also solved by consensus. DOMS and strength were the outcomes extracted. To improve the clarity of the information provided, the term “strength” is going to be used to refer the muscle ability to produce force.

Quality assessment

The methodological quality of the studies was evaluated using a scale developed by the PEDro database. Based on the Delphi concept, its overall score reliability is sufficient for use in systematic reviews of physical therapy RCTs [20]. The scale contains 11 items and for each criteria defined in the scale, a point (1) is attributed to the presence of quality indicators of the presented evidence, and zero point (0) is attributed to the absence of these indicators. Each satisfied item (except the first) contributes one point to the final score, which is obtained by summing all positive responses. In the present systematic review, the cutoff point of six (6) points was adopted to define the methodological quality of the studies. Thus, the articles were classified as high methodological quality when six or more criteria were positive and of low methodological quality when their score was less than five points.

Data synthesis and analysis

Pooled-effect estimates were obtained by post-intervention values [21]. Calculations were performed using a random-effects method. P value ≤ 0.05 and confidence interval of 95% (95% CI) were considered statistically significant. Statistical heterogeneity of the treatment effects among studies was assessed using Cochran’s Q test and the inconsistency I2 test, in which values above 25% and 50% were considered indicative of moderate and high heterogeneity, respectively [22]. The effect size (ES) between intervention and control groups was calculated using the Cohen’s d formula: ES = (Mgroup1 − Mgroup2)/SDpooled, where Mgroup1 is the mean of the post-values of the intervention group, Mgroup2 is the mean of the post-values of the control group, and SDpooled is the pooled standard deviation of the intervention and control groups measurements. All analyses were conducted using Review Manager version 5.3. We explored heterogeneity between studies by re-running the meta-analyses removing one paper at a time to check whether some individual study explained heterogeneity. The main outcome used in the meta-analysis was DOMS and strength.

Results

Identification of the studies

The search strategy yielded 221 articles, among which 19 studies were considered as potentially relevant and retrieved for detailed analysis. Seven of these studies met the eligibility criteria and were included in the systematic review (n = 222), but only 6 studies had suitable data for the meta-analysis (n = 182). Figure 1 shows the flow diagram of the studies included in this review and Table 2 summarizes the characteristics of these studies.

Fig. 1
figure 1

Flowchart of the studies included in the review

Table 2 Characteristics of the included studies

Risk of bias

Regarding the methodological quality of the studies evaluated through the PEDro scale, all included studies were considered of high quality, with scores varying from six to nine points. The mean scores of all studies were 7.28 points. The complete score of each of the studies is described in Table 3. From the analysis of the PEDro scale, it was found that statistical comparisons between groups were reported in all included studies for at least one outcome (criterion 10). In addition, all studies clearly defined criteria 2, 4, 8 and 11, respectively: random assignment of subjects to groups; similarity between groups regarding the most important prognostic indicators; measures of at least one primary endpoint in more than 85% sample; and presence of measures of variability and precision in at least one key result. It is not possible to blind either participants or therapists during local therapy. Therefore, the criteria 5 (blindness of participants) and 6 (blindly of the therapists) were not met by any study. Item 7 (blindness of the evaluators) were filled by four studies.

Table 3 Evaluation of the methodological quality (PEDro Scale)

Description of the studies

From the seven studies selected, six evaluated the effect of cryotherapy on EIMD using application of crushed ice at the site of interest [11, 23,24,25,26,27], and one using a cooling apparatus [28]. The groups for comparison included: control, TENS (transcutaneous electrical nerve stimulation) placebo, TENS, TENS associated with ice, photobiomodulation therapy.

The studies showed a great divergence regarding the protocols of muscle damage induction (series, repetitions, rest time between sets, load, type of contraction and muscle group). Regarding the muscle groups analyzed, three studies induced muscle damage on elbow flexors [24, 25, 27], one in knee flexors [11], two in knee extensors [26, 28], and one on ankle plantar flexors [23].

As for the intervention protocols, six studies applied cryotherapy in the injured area for 20 min [11, 24,25,26,27,28] and one study [23] calculated the time of the intervention according to the amount of subcutaneous tissue of the subject, ranging from 15 to 60 min. The duration of interventions ranged from immediately after protocol of muscle damage induction up to 96 h after, with a frequency of cryotherapy application ranging from 1 to 3 times per day.

Effects of interventions

Delayed onset muscle soreness

All included studies in the present review evaluated DOMS and used the visual analog pain scale (EVA) to evaluate it. However, only five studies provided suitable data for meta-analysis. The analysis showed that cryotherapy is not effective to improve DOMS at any of the time points evaluated (− 0.11; 95% CI − 0.8 to 0.57; I2: 79%; Fig. 2).

Fig. 2
figure 2

Analysis of the effects of local cryotherapy on delayed onset muscle soreness compared to a control/placebo group

Muscle strength

Six studies evaluated muscle strength. Four did so through the maximal voluntary isometric contraction (MVIC) of the muscle group of interest [11, 25,26,27]; one evaluated the peak of concentric and eccentric peak torque [24], and one evaluated peak power output [28]. However, only two studies had sufficiently homogeneous data for the meta-analysis. The analysis showed that cryotherapy is not effective to accelerate strength recovery at any of the time points evaluated (− 0.59; 95% CI − 2.89 to 1.71; I2: 0%; Fig. 3).

Fig. 3
figure 3

Analysis of the effects of local cryotherapy on strength compared to a control/placebo group

Discussion

The aim of this systematic review of the literature was to determine the efficacy of local cryotherapy for the treatment of subjective (DOMS) and objective (strength) symptoms associated with EIMD. After a complete analysis of the included articles, seven studies were included in the present review. DOMS and strength were chosen as outcome measures, because they are the variables most commonly investigated. Contrary to our hypothesis, it can be suggested that local cryotherapy is not effective in accelerating recovery of either DOMS or strength.

It is known that the decrease in tissue temperature reduces the oxygen demand, cellular metabolic activity and attenuates the release of vasodilators, reducing the microcirculatory overload by the decrease in circulating blood volume [8]. This, in turn, attenuates the hydrostatic pressure in the endothelial cell, decreasing the formation of edema. Furthermore, the decrease in blood flow causes a reduction in the formation of hematomas and muscle spasm associated with possible pain relief [29]. In addition, there is a decrease in nerve transmission caused by tissue cooling, which would reduce the release of acetylcholine and possibly stimulate inhibitory surface cells to increase the pain threshold [30].

Currently, there are three main common cryotherapy modalities used in sport: cold-water immersion (CWI), whole-body cryotherapy (WBC), partial-body cryotherapy (PBC). During CWI, the water is maintained at temperatures ranging from 5 to 13 °C for 10–24 min [6, 31]. WBC and PBC are more extreme forms of cryotherapy, in the first one the individuals enter two or three closed chambers, where they are exposed to extremely cold air up to 4 min, in temperatures ranging from − 10 to − 130 °C [32, 33], while the latter involves vaporized liquid nitrogen, generating temperatures from − 110 °C down to − 195 °C [10, 34] for 1–3 min. Even though there is a growing body of investigations analyzing the effects of the aforementioned cryotherapy modalities to reduce symptoms of EIMD, there is no consensus in the literature regarding the efficacy of such strategies [12, 13, 35, 36]. Furthermore, they are hardly applicable in a clinical environment, which is the main advantage of local cryotherapy.

Many theories have tried to explain the origin of DOMS [37]. However, whether the initiating stimulus is chemical, thermal, mechanical or a combination of more than one factor remains uncertain [38]. The most accepted theory hypothesize that DOMS is related to the inflammatory response and muscle damage caused by strenuous exercise [37]. Therefore, strategies capable of decreasing inflammatory response might contribute to attenuate symptoms of DOMS. Nevertheless, according to the results found in the present review, local cryotherapy does not seem to provide any benefit to improving symptoms of DOMS. There is a possibility that local cryotherapy does not provide the same physiological benefits seen in other cooling modalities (e.g., CWI and WBC) such as muscle oxygen saturation, cutaneous vascular conductance, and mean arterial pressure [39,40,41]. Perhaps, the cooling generated by local cryotherapy is just not sufficient to produce significant responses within the tissue. However, it is worth pointing out in this context that the two studies that found advantages of local cryotherapy over control/sham groups for attenuating symptoms of DOMS used more frequent applications (three times per day) [11] and chose the duration of application according to the amount of subcutaneous tissue [23]. Hence, it is plausible to assume that a single bout of local cryotherapy for a standard period of time (15–20 min) might not be sufficient to generate positive effects on DOMS. It is worth highlighting that even though DOMS is an important variable during muscle recovery it tends to significantly decrease as the activity begins [37]. Force production, on the other hand, seems to be the most remarkable variable to be recovered following strenuous exercises, considering that most sports depend on it.

The diminished ability to produce strength following EIMD is one of the most used and most reproducible objective markers of muscle damage in humans [42, 43]. The reason why muscles are unable to produce maximal force after EIMD remains unclear. However, it is known that contracting skeletal muscles have increased production of reactive oxygen species (ROS) [44], and the increased production of ROS leads to oxidative stress, which might impair force production [45]. The present review demonstrated that local cryotherapy does not seem to be effective to accelerate strength recovery following EIMD. There is no consensus in the literature regarding the effects of cold therapy strategies to accelerate strength recovery following EIMD [9, 35, 36], different methods of application and protocols make it hard to reach a definitive answer. However, it is been suggested that an increase in peripheral catecholamine concentration following CWI might generate an auto-oxidative process, which would perpetuate muscle fatigue [46] and impair force production. This premise was confirmed by a recent investigation that found that CWI seems to delay muscle recovery following EIMD [36]. Furthermore, there is a significant body of evidence suggesting that CWI might impair muscle adaptation during strength training [47,48,49]. Therefore, the use of cold therapy post-exercise has become questionable, considering that most athletes perform some sort of strength training in their routine. We are unable to state that the rules for CWI and other modalities of cold therapies apply for local cryotherapy. Therefore, the mechanisms underpinning the failure of local cryotherapy to accelerate strength recovery following EIMD remain unclear. Nonetheless, the data found in the present review allow us to suggest that local cryotherapy does not seem to be a worthwhile strategy to be used to accelerate strength recovery following EIMD.

To the best of the authors’ knowledge, this is the first review to systematically analyze the influence of local cryotherapy on DOMS and strength. The current review presents relevant methodological strengths such as the analysis of two of the most important variables of EIMD (DOMS and strength). Moreover, a strategy for a sensitive and comprehensive search to assure the location of all studies in this field was held. Another important quality of the present review is the high methodological quality of the included studies; this makes the information provided more reliable. However, the heterogeneity among the included studies prevented more robust meta-analyses, especially for strength, and this should be pointed out as a relevant limitation.

Conclusion

In conclusion, the present review showed that local cryotherapy does not seem to be effective to accelerate recovery from symptoms of EIMD. Even though, local cryotherapy is suitable for clinical practice, the evidence proving its efficacy is limited. It is possible that local cryotherapy might contribute to decrease DOMS if applied more frequently. However, cryotherapy might not be a worthwhile strategy, given the potential harm that it may cause on muscle strength. Considering the current evidence, we discourage physical therapists and conditioning coaches to use local cryotherapy in an attempt to attenuate symptoms of EIMD.