Diversity of parameters in the muscle strength evaluation of Brazilian school children and adolescents: a systematic review

- Muscle strength (MS) is considered important indicative of global health regardless of age or clinical condition. The aim of this study was to summarize evidence from research carried out in Brazil that investigated MS in school children and adolescents, showing the objectives, tests, protocols and quantitative of youngsters who met the health criteria for MS. Systematic review conducted in the PubMed, Web of Science, Scopus, Sportdiscus, LILACS and Scielo databases, with complementary searches in reference lists. In all articles, the risk of bias was analyzed. Of the 15,609 articles initially identified, 27 were included, comprising data from 29,604 children and adolescents. The 27 studies included presented moderate (37%) and low risk of bias (63%). Three out of four studies investigating MS in children and adolescents were carried out in southern and southeastern Brazil (77.7%). It was found that 65.9% of boys and 58.2% of girls had adequate levels of MS for health, with results varying from 14.8% to 66.0% in girls and from 20.4% to 76.9% in boys. Several MS measurement protocols were identified; however, horizontal jump was the most used test to evaluate MS (59.2%). MS is a physical valence searched in children and adolescents and a variety of protocols are used. In addition, it is necessary to propose MS cutoff points based on health criteria for the accurate estimation of this physical valence in children and adolescents in Brazil.


INTRODUCTION
Muscle strength (MS) is one of the most important physical valences, since it is an indispensable element in the accomplishment of any type of movement, from the most simple to the most complex, being fundamental to the performance of daily activities, either recreational, domestic or physical performance, considered important indicative of global health regardless of age or clinical condition 1 .In the pediatric population, MS is essential for the improvement of motor skills 2 , and the development of this physical valence is directly related to maturational progression, with higher values for boys compared to girls in all age groups 3 .
Studies with children and adolescents have shown a relationship between MS levels and health prognoses 4,5 .Research conducted with male adolescents in Sweden has found that higher MS levels in adolescence were directly associated with lower risk of premature death from cardiovascular disease in adulthood 4 .Another study conducted with 669 Colombian schoolchildren found that low MS levels were directly associated with higher blood pressure (diastolic and systolic) values, higher HOMA index, and elevated triglyceride and C-reactive protein concentrations 5 .
The evaluation/use of MS is necessary because this physical valence is basic to all the others, is a way to prevent specific damages, is necessary to good appearance, and is one of the elements of physical fitness related to health and performance 1 .However, since there are several types of strength (isometric, isotonic and isokinetic), there are several ways of measuring them 1 .This variety of protocols results in difficulty in comparing results between studies and there is need to compile what has been researched on this topic 6 .
Although several studies conducted in Brazil have investigated the relationship between MS in children and adolescents and related aspects [7][8][9] , information regarding the objectives addressed, quality of identified results, regional distribution of researches, tests used, classification adopted for the classification of MS levels and discussion of results were not compiled in systematic reviews or official documents intended for sports, health and physical education professionals, so that they can direct professional actions.In this sense, the systematic gathering of information is justified by objectively presenting results of research investigating MS in children and adolescents in Brazil.
The aim of this study was to verify, through a systematic review, the diversity of parameters for MS evaluation in the fulfillment of health criteria of school children and adolescents in Brazil.

Search strategy
The systematic review was performed from December 2017 to January 2018 in the following databases: 1) Medical Literature Analysis and Retrieval System Online (MEDLINE), through PubMed; 2) Web of Knowledge (WEB of Science); 3) Scopus; 4) Sportdiscus, through the EBSCOhost platform; 5) Latin American and Caribbean Literature in Health Sciences (LILACS); 6) Scientific Electronic Library Online (Scielo).
The investigation of possible articles in databases was carried out using the advanced search tool (searches carried out using "keywords") available in databases based on the construction of blocks of descriptors made by the author.Descriptors were inserted in Portuguese, English and Spanish.The first block (outcome) was composed of MS terms: "muscle strength"; "muscular fitness"; "musculoskeletal fitness"; "resistance training"; "weight training"; "muscle endurance"; "muscle power"; "lower limb strength"; "upper limb strength"; "isometric strength"; "dynamic force"; "force resistance"; "isotonic contraction"; "isometric contraction".The second block was composed of terms related to the target population (children and adolescents): "young adult"; adolescents; young; adolescence; youth; adolescent; children; child; "Pre-school children."The Boolean "OR" operator was used to add in the advanced search at least one word from each block and the "AND" operator to relate the blocks of "keywords" to each other.Further information in relation to the search of studies and descriptors used can be verified in Appendix A.
The risk of bias/methodological quality assessment of studies was independently performed by three reviewers/authors (TRL, PCM, MSM).The instrument used to assess risk of bias/methodological quality was the National Heart, Lung and Blood Institute (NHLBI) 10 questionnaire for cohort and cross-sectional studies covering 14 criteria to determine the risk of bias/methodological quality of studies.This instrument evaluates the internal validity of studies and includes questions that help in the identification of possible risk of selection bias, information bias, measurement bias and confounders 10 .For each criterion evaluated, scores from 0 "no" and 1 "yes" were assigned, and at the end of the study classification, a total score was assigned to each study based on the number of positive responses to the questionnaire in relation to the total number of questions.Questionnaire questions that could not be answered by the available information and/or which were not applicable to the assessed study and/or aspects that had not been reported were excluded from the calculation to determine the final methodological quality score/risk of bias 10 .
According to the subjective evaluation of the reviewers / authors, studies were classified as having good methodological quality/low risk of bias (final score ≥ 0.70), moderate methodological quality/moderate risk of bias (final score ≥ 0.50), low methodological quality / high risk of bias (final score <0.50) 11 .Three reviewers/authors (TRL, PCM, MSM) applied the methodological quality/risk of bias assessment tool for all studies that met the inclusion criteria.The reviewers/authors' non-agreement regarding the evaluation of a particular study was resolved through a consensus meeting.
The EndNote® X7 bibliographic manager software was used to create specific libraries, which allowed the identification and exclusion of duplicate studies, division and organization of results of each database.

Eligibility criteria
Articles were included according to the following criteria: original articles published in journals (review studies, theses, dissertations, abstracts of scientific meetings were excluded); to have measured MS and described in the body of the article, the test/method used to evaluate MS levels, among them: handgrip strength (HGS, isometric force), tests with isokinetic dynamometer (isokinetic force), horizontal jump (HJ, muscle power/ explosive strength), vertical jump (VJ, muscle power/explosive strength), maximum repetition test (1MR) or medicine ball throw (TMB, muscle power / explosive strength); with a population of Brazilian children and adolescents aged 0-19 years (and/or mean age included in this interval), without specific clinical conditions, without diagnosis of any disease, nonathletes and of both sexes.
Articles that evaluated MS by means of localized muscle strength tests, such as the repetition tests of trunk flexion (abdominal exercises), repetition tests of elbow flexion (support), repetition tests of lumbar resistance and pull-up in the bar were not include in this review.

Article selection process
The article selection process was performed by two independent reviewers (TRL and MSM).Firstly, articles applying the inclusion criteria by reading titles and abstracts were excluded.Then, the full texts of the selected articles were read in full to determine which studies that met the inclusion criteria would be selected.In case of doubts among researchers regarding the inclusion of articles, a third researcher was consulted (DASS).After selecting the articles that would be included in the review, the studies described in the references of these selected articles were read with the objective of identifying some possible study not identified in the systematic search in databases.

RESULTS
The systematic search for articles that investigated MS in Brazilian children and adolescents identified 15,609 studies.After evaluating the total of studies by title and abstract, 95 articles had texts analyzed in full.When considering losses (n = 68), a total of 33 studies were excluded because the test used did not investigate MS as defined for the present study: [repetition test of trunk flexion (n = 28)], repetition test of elbow flexion "support" (n = 06), pull-up in bar (n = 04), lumbar resistance (n = 02), evaluation of the combination of resistance tests and MS simultaneously (n = 01)].The other losses were related to the age group of participants (n = 02), to the study topic (n = 21), to the special groups evaluated (n = 04), the nationality of the investigated population (n = 06), and duplicate studies (n = 02).Twenty-seven original articles were included for this review (Figure 1).

DISCUSSION
In the present review, 27 studies that investigated MS in children and adolescents were identified, and a large number of these studies were published after 2010 [7][8][9]17,[19][20][21][22][23][24][25][27][28][29][30][31]33,35,36 , demonstrating that the subject has current research in the Brazilian scenario. Although the body of evdence regarding the cardiovascular and metabolic health benefits attributed to MS are unambiguous 4,5 , it is speculated that the contemporary consolidation of recommendations for MS improvement in children and adolescents 1 could justify the recent research relating MS in studies with children and adolescents.
Regarding the methodological quality of the studies included in the review, low or moderate risk of bias was identified, and no evidence from studies with a high risk of bias/low methodological quality was identified.This shows that studies in Brazil on this subject are well delineated and yield reliable results.Although MS research was the main objective of a small part of articles included in the review 9 , the high methodological rigor adopted by the studies gives a greater probability that the results regarding MS have not been biased, conferring valid interpretations and applications.
Approximately three out of four MS-related studies in children and adolescents in Brazil were conducted in the Southeastern and Southern regions of the country (77.7%).In contrast, studies from the northerner region of Brazil were not identified.The strong expansion in the number of Physical Education courses in Brazil observed in the decade of 2000 38 , coupled with the demand for the qualification of higher education teachers, has exerted a strong pressure on the demand for graduate students.However, this scenario is not established in an equitable way in the country, … continue which may have converged to the discrepancy in the number of productions in relation to MS according to the Brazilian regions 38 .In Brazil, 54.0% of stricto sensu graduate programs in Physical Education are concentrated in the Southeastern, 24.3% in the Southern, 10.8% in the Northeastern, 8.2% in the Midwestern and 2.7% in the Northern regions 38 .
The findings of the present review indicated a high number of tests used to measure MS.This is because there is a lack of consensus regarding the MS nomenclature and the tests used to evaluate it 2 .Metabolic, physiological and muscular demands involved, or the motor action necessary to perform the measurement/test are among the limiting factors for the elaboration of a "reference" method to evaluate MS levels 2 .1MR and repetition tests for certain percentages of 1MR (Ex: 50% of 1MR or 70% of 1MR) have been used as a "benchmark" for determination of performance-related aspects; however, the HGS test with the use of manual dynamometer is another method used to investigate MS, considered valid and indicative of general MS 2 .In addition, HJ and VJ tests (muscle strength/explosive strength) were identified as good indicators of lower limb strength and general MS 2 .This variety of MS evaluation tests shows how difficult it is to compile all this information and compare the findings.
Several criteria for classification of MS values were identified in the studies included in this review.Although higher MS levels are directly associated with general health indicators in children and adolescents 4,5 , the results obtained in tests are difficult to interpret, given the lack of "reference" cutoffs to detect adequate or inadequate MS levels 2 .The criteria proposed by the Canadian Society of Exercise Physiology (CSEP) and those suggested by the Brazilian Sports Project (PROESP-BR) are among those used in studies for this classification, both elaborated with the proposition of indicating health zones and even performance 6,37 .Among the limitations of the classification of results through these criteria are the bases used to propose cutoffs based on normative standards (results presented in percentiles), which reflect the result of a subject in relation to the others, which do not excludes the possibility that this individual is positioned at a high percentile within that reference population and that the chances of presenting health problems or risk factors are higher or lower 39 .The proposal of criteria-based cutoff points is related to the achievement or not of specific values that guarantee less possibilities of developing a certain health problem, regardless of the result that this value has reached within a normative distribution, which increases the validity of the interpretation of results 39 .In this sense, Brazil should propose cutoff points based on health criteria for MS in order to have a more accurate overview of these inferences.
In the present study, the percentage of children and adolescents classified as having adequate MS levels according to some physical test battery ranged from 14.8% to 66.0% in girls and from 20.4% to 76.9 % in boys.The great diversity of protocols and cutoffs used to measure and classify the MS results makes it difficult to compare results between surveys.Stud-ies performed in southern Brazil 8,9 were those that presented the lowest percentage of individuals classified as having adequate MS; however, the cutoff points used to classify the MS values adopted in these studies were established based on the population of Canadian children and adolescents, different from the characteristics of the Brazilian population, which may have contributed to the difference between percentages.
When considering the results of studies conducted in Brazil, 65.9% of boys and 58.2% of girls had adequate MS levels for health.In the population-based study of adolescents (15 to 19 years) in Canada, whose cutoff points for MS score classification were based on percentiles, 41% of boys and 52% of girls had adequate MS levels 40 .Other studies 4,5 did not use specific cutoff points to classify MS values, but only to distribute the values obtained in MS tests into tertiles or quartiles.The monitoring of MS levels of the Brazilian pediatric population should be permanent as a health monitoring measure.Some limitations of the results of this systematic review should be mentioned.Since the aim of the review was to identify studies that investigated MS in children and adolescents in Brazil, it should be recognized that the reviewed studies were heterogeneous in relation to the main objective, sample size, tests and instruments used to evaluate MS, making the comparison among results difficult 9 .Another limitation is that this review did not focus on localized muscle strength tests routinely used in physical test batteries for children and adolescents 6,37 .In addition, the limited number of researches whose main objective was to investigate the relationship of MS in children and adolescents is also a limitation.However, positive aspects of this review should be emphasized, such as the coverage of MS themes identified in research conducted in Brazil.The evaluation of the methodological quality of the included studies and the high number of databases used in MS investigation studies in children and adolescents in Brazil are strengths of this review.

CONCLUSION
The diversity of goals identified in MS-related studies in children and adolescents in Brazil demonstrates the importance of this physical valence in the health / performance context.However, there is need for a greater number of studies in Brazil, since information from some Brazilian regions regarding MS in children and adolescents is unknown.Moreover, although studies conducted in Brazil have identified low proportion of children and adolescents with adequate MS levels, the high number of cutoff points and tests used to classify / measure MS makes the comparison of results difficult, where greater number of surveys using tests and similar cutoff points to evaluate and classify FM are required.In addition, although the reduced proportion of children and adolescents in Brazil with adequate MS levels is similar to that identified in literature, the need for interventions aimed at increasing MS in the pediatric population is reinforced.

Figure 1 .
Figure 1.Results of data searches and criteria used in the selection of studies that sought to investigate MS correlates in children and adolescents in Brazil.

Table 1 :
Descriptive characteristics of included studies.To identify the influence of low birth weight on PF.
14idence from cross-sectional studies (n = 22) Schneider el al.,14Porto Alegre, RS 57 students (7-15 years) 49.1To compare isometric and isokinetic MS in boys and girls.To compare LLS and ULS among obese and non-obese adolescents and to verify the association of MS with anthropometric variables and body composition.To estimate the prevalence of high adiposity and its association with musculoskeletal fitness, by economic level, in male children and adolescents.Freitas et al., 35 Montes Claros, MG 2,040 girls (8-15.9years) NA To identify the relationship between biological maturation, body morphology and physical performance.Matsudo et al., 20 Ilhabela, SP 233 school children (10-17 years old) 54.9To examine the association between FPM and PF in children and adolescents of different stages of sexual maturation.De Farias et al., 21 Jacarezinho, PR 21 students (12-16 years) 57.1 Correlating MS with anthropometric indicators, maturational stage, neuromotor tests in adolescents.W: Womem; Mean; ±: standard deviation; ND: not described; MA: Mato Grosso; FD: Federal District; MG: Minas Gerais; CE: Ceará; RJ: Rio de Janeiro; PR: Paraná, SP: São Paulo; RS: Rio Grande do Sul; SC: Santa Catarina; SE: Sergipe; MS: muscle strength; HGS: Handgrip strength; 1MR: maximum repetition; BC: body composition; PA: physical activity; PF: physical fitness; NA: not applicable; ULS: upper limb strength; LLS: lower limb strength; PROESP-BR: Project Sports Brazil -Brazil;

Table 2 .
Bias risk assessment of included studies.
ND. Can not be determined; NR.Not reported; NA.Not applicable; 0. No; 1. Yes; ≥ 0.70: low risk of bias; ≥ 0.50: moderate risk of bias;< 0.50 high risk of bias; * to determine the total score, the following equation was considered: (total of positive answers / total of questions considered for that study).

Table 4 .
30aracteristics of studies that classified muscle strength in categories based on test batteries that have health criteria.†samplesizeavailableforthehorizontal jump test; ‡ sample size available for the Medicine-ball throw test; § the categories excellent, very good, good and regular were considered as suitable; ll for studies that presented more than one test to measure muscle strength (Luguetti et al.,16; Brandão et al.,29; Mello et al.,30was considered the information for the total calculation of the test that presented more subjects classified as adequate in relation to muscular strength (e.g., Medicine-ball throw test); ¶ for the calculation of the percentage of subjects with adequate muscle strength the following equation was considered: (number of subjects classified as having adequate muscle strength / number of subjects from all studies considered)*100; HJ: horizontal jump; TMB: medicine-ball throw test; HGS: handgrip strength; SP: São Paulo state; SC: Santa Catarina state; MT: Mato Grosso state.