Acessibilidade / Reportar erro

ASSOCIATION BETWEEN BODY COMPOSITION AND FAT INFILTRATION IN THE LUMBAR MULTIFIDUS IN YOUNG ADULTS

ASSOCIAÇÃO ENTRE A COMPOSIÇÃO CORPORAL E A INFILTRAÇÃO DE GORDURA NOS MULTÍFIDOS LOMBARES EM ADULTOS JOVENS

ASOCIACIÓN ENTRE LA COMPOSICIÓN CORPORAL Y LA INFILTRACIÓN DE GRASA EN LOS MULTÍFIDOS LUMBARES EN ADULTOS JÓVENES

ABSTRACT

Introduction:

The increase in body fat is a natural and progressive process with aging, allowing fat infiltration in ectopic sites, such as skeletal muscle, which disrupts its function.

Objective:

To evaluate the association between body composition, fat infiltration into the low back multifidus muscles, and history of low back pain.

Methods:

This is a transversal and qualitative study that included young adult subjects of both sexes, and excluded individuals with neurological and musculoskeletal disorders and pregnant women. Fat infiltration into the multifidus and cross section area by magnetic resonance imaging; body composition by Dual-energy X-ray absorptiometry (DXA), and physical activity level determined by the International Physical Activity Questionnaire (IPAQ) were evaluated. The sample was divided by sex and. Pearson and Spearman's correlation and stepwise linear regression were performed. For this study, a p<0.05, a level of significance of 5% and confidence interval of 95% were adopted.

Results:

Thirty-two individuals were evaluated (59.37% women; 40.63% men). There was a correlation between fat percentage and total cross-sectional area (CSAtotal) (r=0.525; p=0.021), in women, and with lean abdominal mass (r= −0.648; p=0.017) and Body Mass Index (BMI) (r= −0.644; p=0.018) in men. There was also an association, in women, between fat percentage and cross section area (R2=0.275; p=0.021; CI=0.364 − 3.925) and, in men, with lean abdominal mass (R2=0.420; p=0.017; CI: −9.981- [-1.235]).

Conclusion:

There was correlation between fat percentage in the multifidus and CSA in women, and lean abdominal mass and BMI in men. There was also an association between fat percentage and cross section area in women, and lean abdominal mass in men. However, there was no evidence of any correlation between pain and low back dysfunction. Level of evidence I; Diagnostic studies - Investigating a diagnostic test.

Keywords:
Body composition; Adipose tissue; Paraspinal muscles; Magnetic resonance imaging

RESUMO

Introdução:

O aumento da gordura corporal é um processo natural e progressivo com a idade, propiciando a infiltração de gordura em locais ectópicos, como por exemplo, na musculatura esquelética, o que prejudica sua função.

Objetivo:

Avaliar a associação entre a composição corporal e a infiltração de gordura nos músculos multífidos lombares e o histórico de dores lombares.

Métodos:

Estudo transversal e quantitativo em que foram incluídos adultos jovens de ambos os sexos e excluídos indivíduos com distúrbios neurológicos, musculoesqueléticos e grávidas. Avaliou-se a infiltração de gordura nos multífidos e a área de secção transversa por meio de ressonância magnética; a composição corporal por meio de Absorciometria com raios-X de Dupla Energia (DXA) e o nível de atividade física através do Questionário Internacional de Atividade Física (IPAQ). A amostra foi dividida por sexo e feita sua respectiva caracterização, correlação de Pearson e Spearman e regressão linear stepwise. Foi adotado o valor de p<0,05, nível de significância de 5% e intervalo de confiança de 95%.

Resultados:

Foram avaliados 32 indivíduos (59,37% mulheres; 40,63% homens). Houve correlação entre o percentual de gordura e a área de secção transversa total (ASTtotal) (r=0,525; p=0,021), nas mulheres, e com a massa magra abdominal (r= −0,648; p=0,017) e Índice de Massa Corporal (IMC) (r= −0,644; p=0,018) nos homens. E associação, nas mulheres, entre o percentual de gordura e a área de secção transversa (R2=0,275; p=0,021; IC=0,364 − 3,925) e, nos homens, com a massa magra abdominal (R2=0,420; p=0,017; IC: −9,981- [-1,235]).

Conclusão:

Encontrou-se correlação entre o percentual de gordura nos multífidos e a AST, nas mulheres, e com a massa magra abdominal e IMC para os homens, além da associação entre o percentual de gordura e a área de secção transversa, para as mulheres, e com a massa magra abdominal para os homens. Entretanto, não foi evidenciada nenhuma correlação com dor e disfunções na coluna lombar. Nível de evidência I; Estudos diagnósticos - Investigação de um exame para diagnóstico.

Descritores:
Composição corporal; Tecido adiposo; Músculos paraespinais; Ressonância magnética

RESUMEN

Introducción:

El aumento de la grasa corporal es un proceso natural y progresivo con la edad, propiciando la infiltración de grasa en lugares ectópicos, como, por ejemplo, en la musculatura esquelética, lo que perjudica su función.

Objetivo:

Evaluar la asociación entre la composición corporal y la infiltración de grasa en los músculos multífidos lumbares y el historial de dolores lumbares.

Métodos:

Estudio transversal y cuantitativo en el que fueron incluidos adultos jóvenes de ambos sexos, y excluidos individuos con disturbios neurológicos, musculoesqueléticos y gestantes. Se evaluó la infiltración de grasa en los multífidos y el área de sección transversa por medio de resonancia magnética; la composición corporal por medio de Absorciometría con rayos X de Doble Energía (DXA) y el nivel de actividad física a través del Cuestionario Internacional de Actividad Física (IPAQ). La muestra fue dividida por sexo y fue hecha su respectiva caracterización, correlación de Pearson y Spearman y regresión lineal stepwise. Fue adoptado el valor de p <0,05, nivel de significancia de 5% e intervalo de confianza de 95%.

Resultados:

Se evaluaron 32 individuos (59,37% mujeres, 40,63% hombres). Hubo correlación entre el porcentaje de grasa y el área de sección transversa (ASTtotal) (r = 0,525, p = 0,021), en las mujeres, y con la masa magra abdominal (r = −0,648, p = 0,017) e Índice de Masa Corporal (IMC) (r = −0,644, p = 0,018) en los hombres, y asociación, en las mujeres, entre el porcentaje de grasa y el área de sección transversa (R2 = 0,275; p = 0,021; IC = 0,364 − 3,925) y, en los hombres, con la masa magra abdominal (R2 = 0,420; p = 0,017; IC: −9,981- [-1,235]).

Conclusión:

Se encontró correlación entre el porcentaje de grasa en los multífidos y la AST, en las mujeres, y masa magra abdominal e IMC para los hombres, además de la asociación entre el porcentaje de grasa y el área de sección transversa, para las mujeres, y con la masa magra abdominal para los hombres. Entretanto, no fue evidenciada ninguna correlación con dolor y disfunciones en la columna lumbar. Nivel de evidencia I; Estudios diagnósticos – Investigación de un examen para diagnóstico.

Descriptores:
Composición corporal; Tejido adiposo; Músculos paraespinales; Resonancia magnética

INTRODUCTION

The fat deposition in interleaved adipocyte among the muscular fiber feature the fat infiltration, the intramuscular adipose tissue (TAI)11. Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90(6):1579-85.,22. Hadar H, Gadoth N, Heifetz M. Fatty replacement of lower paraspinal muscles: normal and neuromuscular disorders. AJR Am J Roentgenol. 1983;141(5):895-8.. Among the factor that can lead to TAI, may be: female, because they have a physiological higher percentage of fat; age, because the misfunction of lipidic metabolism; and the body composition, because the excess of free floating fat 11. Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90(6):1579-85.,33. Zamboni M, Rossi AP, Fantin F, et al. Predictors of ectopic fat in humans. Curr Obes Rep. 2014;3(4):404-13.66. Vidt ME, Santago AC, Tuohy CJ, Poehling GG, Freehill MT, Kraft RA, et al. Assessments of fatty infiltration and muscle atrophy from a single magnetic resonance image slice are not predictive of 3-dimensional measurements. Arthroscopy. 2016;32(1):128-39..

The TAI results in decrease of strength production and muscular mass, consequently, function decrease11. Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90(6):1579-85.,33. Zamboni M, Rossi AP, Fantin F, et al. Predictors of ectopic fat in humans. Curr Obes Rep. 2014;3(4):404-13., as relation of a transverse section area decrease, although there are controversial researches these alterations are commonly reported in this musculature11. Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90(6):1579-85.,33. Zamboni M, Rossi AP, Fantin F, et al. Predictors of ectopic fat in humans. Curr Obes Rep. 2014;3(4):404-13.,77. Wan Q, Lin C, Li X, Zeng W, Ma C. MRI assessment of paraspinal muscles in patients with acute and chronic unilateral low back pain. Br J Radiol. 2015;88(1053):20140546.,88. Fortin M, Macedo LG. Multifidus and paraspinal muscle group cross-sectional areas of patients with low back pain and control patients: a systematic review with a focus on blinding. Phys Ther. 2013;93(7):873-88.. At lumbar spine musculature, the lumber multifidus (LM) shows higher predisposition for infiltration and like one of the main stabilization muscle of lumber spine it may result in lumbar pain22. Hadar H, Gadoth N, Heifetz M. Fatty replacement of lower paraspinal muscles: normal and neuromuscular disorders. AJR Am J Roentgenol. 1983;141(5):895-8.,99. de Siqueira GR, da Silva GAP. Alterações posturais da coluna e instabilidade lombar no indivíduo obeso. Fisioter Mov. 2011 jul/set;24(3):557-66..

The studies focus in female elderly, rare among adult population. In this sense, this study aims to evaluate the association between fat infiltration percentage in lumbar muscles, the body composition and history of pain and lumbar spine misfunction in young adults of both sexes.

METHODS

Study type and Sample

Transversal and quantitative study, developed at Recife/PE-Brazil, from September of 2016 to march of 2017, attached to Universidade Federal de Pernambuco (UFPE) and with the approval of this university Committee of Etic and Research (Advice Number: 1.479.824). The participation of the study was ensured by reading and signing an Informed Consent (IC)

There was included subjects young adults from both genders, with and without lumbar pain and excluded the subjects with neurological, musculoskeletal (fractures, abnormalities, trauma history or spine surgery), pregnant, body with metal pieces and claustrophobic history. The sample was composed by 32 volunteers stratified by gender.

Observational Desing:

The evaluation was performed over two days and all of them made over the first day, except the fat infiltration evaluation, performed at the same week of the first gathering.

Fat infiltration and Multifidus CSA: through magnetic resonance (Signa HDxt 1.5T - GE Healthcare, Wisconsin, United States), in axial T1, with cutting thickness of 5mm (Figure 1).

Figure 1
Axial T1-weighted image shows the lumbar multifidus in L5. The dashed line delimits the multifidus lumbar muscle, the arrows point to the fat infiltration.

It was standardized for analysis the images that correspond with the superior edge of L5 and observed with software ImageJ 1.50i (National Institute of Health, USA). It was measured a. the total cross-sectional area (CSAtotal), that comprehends the muscle and the fat inlfiltration; b. the fat-free cross-sectional area (CSAfatfree), with the muscular mass; c. the fat cross-sectional area (CSAfat), muscle fat infiltration area. Them, it was quantified the multifidus fat percentage (Multifidus fat percentage = CSAfat/CSAtotal x 100) by Color Threshold77. Wan Q, Lin C, Li X, Zeng W, Ma C. MRI assessment of paraspinal muscles in patients with acute and chronic unilateral low back pain. Br J Radiol. 2015;88(1053):20140546. method.

Body Composition. It was evaluated the percentage of body and abdominal fat, lean body and abdominal mass and free-fat mass through Double Energy Radiologic Absormetry (DXA) - Lunar Prodigy Primo (GE Medical Systems Lunar, Wisconsin, United States).

Physical activity level. It was used the International Physics Activity Questionnaire (IPAQ), short way, self-applied and referring to the last week1010. Matsudo S, Araújo T, Matsudo V, Andrade D, Andrade E, Oliveira LC, et al. Questionário Internacional de Atividade Física (IPAQ): estudo de validade e reprodutibilidade no Brasil. Rev Bras Ativ Fis Saude. 2001;6(2):5-18.. To determine the weekly energy expenditure, it was attributed the value of Metabolic Equivalent Estimate (MET) for each activity (Walk: 3,3 MET; moderate: 4 MET; vigorous: 8 MET) and multiplied by the frequency and duration in minutes1111. IPAQ Research Committee. Guidelines for data processing and analysis of the International Physical Activity Questionnaire (IPAQ) – short and long forms; 2005. Disponível em: <https://docs.google.com/viewer?a=v&pid=sites&srcid=ZGVmYXVsdGRvbWFpbnx0aGVpcGFxfGd4OjE0NDgxMDk3NDU1YWRlZTM>. Acesso em: 09 de jul. de 2015.]
https://docs.google.com/viewer?a=v&pid=s...
. For the weekly caloric expenditure the MET weekly value was multiplied by the weight and divided by 60 min1111. IPAQ Research Committee. Guidelines for data processing and analysis of the International Physical Activity Questionnaire (IPAQ) – short and long forms; 2005. Disponível em: <https://docs.google.com/viewer?a=v&pid=sites&srcid=ZGVmYXVsdGRvbWFpbnx0aGVpcGFxfGd4OjE0NDgxMDk3NDU1YWRlZTM>. Acesso em: 09 de jul. de 2015.]
https://docs.google.com/viewer?a=v&pid=s...
.

History of lumbar pain. It was investigated the occurrence of lumbar pain in the last three months and applied the Oswestry Functional Index (IFO) to evaluate the pain and the intensity by the time of gathering1212. Masselli MR, Fregonesi CEPT, de Faria CRS, Bezerra MIS, Junges D, Nishioka TH. índice funcional de Owestry após cirugia para descompressão de raízes nervosas. Fisioter Mov. 2007;20:115-22..

Statistical Analysis

It was performed the Shapiro-Wilk test to verify the normality of variables. Then, to compare the averages between male and female was used the Independent Samples t-Test for the normal variables and Mann-Whitney for the outside normality, beside the exactly test of Fisher for categoric variables.

It was applied the Pearson Correlation, to normal variables and Spearman, to variables outside normality. The results of correlation were classifieds as weak (<0.4), moderate (0.4 − 0.7) and strong (>0.7)1313. Franzblau AN. A primer of statistics for non-statisticians. New York: Harcourt, Brace & World. 1958.. Then, it was applied the stepwise multiple linear regression between multifidus fat percentage and the predicted variables. The collected data were tabulated and processed by the software Statistical Package for the Social Sciences (SPSS), 22.0 version. It was adopted the p-value < 0.05 for all analysis.

RESULTS

The research was made with 32 volunteers of which 59,37% women (n=19), 40,63% men, with characterization between groups for anthropometric measures, body composition, multifidus CSA and physical activity level presented in Table 1.

Table 1
Baseline participant characteristics related to anthropometric measurements, body composition, multifid CSA and physical activity.

Regarding lumbar pain, 65,6% (n=21) of the volunteers reported any episode in last three months, more frequently between women (71.43%; n=15), comparing to men (28.57%; n=6). However, at the gathering time, only 37.5% (n=12) reported lumbar pain with higher occurrence in women (75%; n=9) comparing to men (25%; n=3) and pain intensity average of 1,2 (±0.389) and 1, for women and men, respectively. 25% (n=8) of the volunteers showed musculoskeletal disfunction of the lumbar spine, more frequently in men (75%; n=6) comparing to women (25%; n=2).

For statistical analysis of correlation and association there was chosen the left multifidus. Regarding multifidus fat percentage there was noticed a positive moderate correlation (r=0.525; p=0.021) with CSAtotal of the multifidus for women. A negative moderate correlation between the quantity of lean abdominal mass (r= −0.648; p=0.017) and the body mass index (BMI) (r= −0.644; p=0.018) (Table 2).

Table 2
Correlation between the multifidus fat percentage and anthropometric measurements, body composition, multifidus CSA and physical activity.

For men, the regression linear pattern correlated 42% of the data, with F test (F=7.967), used to check the model suitability, showed p-value of 0.017 and standard combings of 1.489 to 2.114 (Table 3).

Table 3
Regression between the multifidus fat percentage and the abdominal lean mass in males.

For women, the regression linear pattern correlated 27.5% of data variability, with test F (F=6.456), showing p-value of 0.021 and standard combings of −1.428 to 2.484 (Table 4).

Table 4
Regression between the multifidus fat percentage and the multifidus cross-sectional area in females.

DISCUSSION

There was noticed a moderate correlation and positive association between multifidus fat percentage and CSA in women and negative moderate correlation among BMI and lean abdominal mass in men. However, was not found correlation between pain and disfunction in lumbar spine.

Men got higher averages of anthropometric measures and higher values related to lean mass both body and abdominal and free-fat body mass as observed by another studies1414. Marcus RL, Addison O, Dibble LE, Foreman KB, Morrell G, Lastayo P. Intramuscular adipose tissue, sarcopenia, and mobility function in older individuals. J Aging Res. 2012;2012:629637.1717. Larsson I, Lissner L, Samuelson G, Fors H, Lantz H, Naslund I, et al. Body composition through adult life: swedish reference data on body composition. Eur J Clin Nutr. 2015;69(7):837-42.. As well as muscle CSA was higher too1818. Laskey MA. Dual-energy X-ray absorptiometry and body composition. Nutrition. 1996;12:45-51.,1919. Crawford RJ, Filli L, Elliott JM, Nanz D, Fischer MA, Marcon M, et al. Age- and level-dependence of fatty infiltration in lumbar paravertebral muscles of healthy volunteers. Am J Neuroradiol. 2016;37(4):742-8.. In women, the percentage of superior body fat match the expected physiological result for this population2020. Addison O, Marcus RL, Lastayo PC, Ryan AS. Intermuscular fat: a review of the consequences and causes. Int J Endocrinol. 2014;2014:309570.,2121. Fosbøl MØ, Zerahn B. Contemporary methods of body composition measurement. Clin Physiol Funct Imaging. 2015;35(2):81-97. and showed in the National Health and Nutrition Examination Survey (NHANES) study with evaluation of body composition using DXA1919. Crawford RJ, Filli L, Elliott JM, Nanz D, Fischer MA, Marcon M, et al. Age- and level-dependence of fatty infiltration in lumbar paravertebral muscles of healthy volunteers. Am J Neuroradiol. 2016;37(4):742-8.,2222. Hodges PW, James G, Blomster L, Hall L, Schmid A, Shu C, et al. Multifidus muscle changes after back injury are characterized by structural remodeling of muscle, adipose and connective tissue, but not muscle atrophy: molecular and morphological evidence. Spine (Phila Pa 1976) . 2015;40(14):1057-71.. Like the fat percentage in multifidus that also follow the total body distribution in women33. Zamboni M, Rossi AP, Fantin F, et al. Predictors of ectopic fat in humans. Curr Obes Rep. 2014;3(4):404-13.,1515. Santos DA, Dawson JA, Matias CN, Rocha PM, Allison DB. Reference values for body composition and anthropometric measurements in athletes. PLoS One. 2014;9(5): e97846..

In men, the fat percentage in lumbar multifidus negatively correlated with lean abdominal mass as showed by another studies1414. Marcus RL, Addison O, Dibble LE, Foreman KB, Morrell G, Lastayo P. Intramuscular adipose tissue, sarcopenia, and mobility function in older individuals. J Aging Res. 2012;2012:629637.,2222. Hodges PW, James G, Blomster L, Hall L, Schmid A, Shu C, et al. Multifidus muscle changes after back injury are characterized by structural remodeling of muscle, adipose and connective tissue, but not muscle atrophy: molecular and morphological evidence. Spine (Phila Pa 1976) . 2015;40(14):1057-71.2424. Addison O, Drummond MJ, Lastayo PC, Dibble LE, Wende AR, McClain DA, et al. Intramuscular fat and inflammation differ in older adults: The impact of frailty and inactivity. J Nutr Health Aging. 2014;18(5):532-8., therefore we estimate the lean circumscribed mass to the lumbar multifidus practice higher influence over the fat percentage than the fat related measures and we should evaluate it to investigate fat infiltration.

Although the lumbar multifidus fat (ML) has presented correlation with BMI in different thigh muscles2424. Addison O, Drummond MJ, Lastayo PC, Dibble LE, Wende AR, McClain DA, et al. Intramuscular fat and inflammation differ in older adults: The impact of frailty and inactivity. J Nutr Health Aging. 2014;18(5):532-8.,2525. Dahlqvist JR, Vissing CR, Hedermann G, Thomsen C, Vissing J. Fat replacement of paraspinal muscles with aging in healthy adults. Med Sci Sports Exerc. 2017;49(3):595-601. and none correlation for paravertebral muscles2525. Dahlqvist JR, Vissing CR, Hedermann G, Thomsen C, Vissing J. Fat replacement of paraspinal muscles with aging in healthy adults. Med Sci Sports Exerc. 2017;49(3):595-601., in LM we found negative and moderate correlation. As the measure of BMI includes lean mass, we presume it influences the relation between these too variables.

In women there was correlation and association between fat multifidus percentage and CSAtotal, estimating this relation with the multifidus area is due the higher space available for intramuscular fat deposition. These findings diverge from a study made in elderly that showed decrease of CSAtotal2626. Kelly TL, Wilson KE, Heymsfield SB. Dual energy X-Ray absorptiometry body composition reference values from NHANES. PLoS One. 2009;4(9):e7038.,2727. Rahemi H, Nigam N, Wakeling JM. The effect of intramuscular fat on skeletal muscle mechanics: implications for the elderly and obese. J R Soc Interface. 2015;12(109):20150365., however, this decrease can be due an natural reduction of muscular mass in elderly55. Moore CD, Craven BC, Thabane L, Laing AC, Frank-Wilson AW, Kontulainen SA, et al. Lower-extremity muscle atrophy and fat infiltration after chronic spinal cord injury. J Musculoskelet Neuronal Interact. 2015;15(1):32-41..

The limitations of this study refer to the absence of investigation of others factors as protein supplementation and vitamin D concentration, directly attached to adipocyte deposition and muscle function evaluation.

CONCLUSION

It was evidente association between LM fat percentage and CSA in women, suggesting that CSA may increase due the fat infiltration present in LM. In men the LM fat percentage was inversely associated with lean mass, leading to consider it as main factor in young adults fat infiltration presence.

It is suggested that investigations may be performed to make the findings more accessible like adipometer and bioimpedance and ultrasound, even golden pattern, magnetic resonance and DXA are high cost gadgets.

REFERENCES

  • 1
    Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90(6):1579-85.
  • 2
    Hadar H, Gadoth N, Heifetz M. Fatty replacement of lower paraspinal muscles: normal and neuromuscular disorders. AJR Am J Roentgenol. 1983;141(5):895-8.
  • 3
    Zamboni M, Rossi AP, Fantin F, et al. Predictors of ectopic fat in humans. Curr Obes Rep. 2014;3(4):404-13.
  • 4
    Fortin M, Videman T, Gibbons LE, Battié MC. Paraspinal muscle morphology and composition: a 15-yr longitudinal magnetic resonance imaging study. Med Sci Sport Exerc. 2014;46(5):893-901.
  • 5
    Moore CD, Craven BC, Thabane L, Laing AC, Frank-Wilson AW, Kontulainen SA, et al. Lower-extremity muscle atrophy and fat infiltration after chronic spinal cord injury. J Musculoskelet Neuronal Interact. 2015;15(1):32-41.
  • 6
    Vidt ME, Santago AC, Tuohy CJ, Poehling GG, Freehill MT, Kraft RA, et al. Assessments of fatty infiltration and muscle atrophy from a single magnetic resonance image slice are not predictive of 3-dimensional measurements. Arthroscopy. 2016;32(1):128-39.
  • 7
    Wan Q, Lin C, Li X, Zeng W, Ma C. MRI assessment of paraspinal muscles in patients with acute and chronic unilateral low back pain. Br J Radiol. 2015;88(1053):20140546.
  • 8
    Fortin M, Macedo LG. Multifidus and paraspinal muscle group cross-sectional areas of patients with low back pain and control patients: a systematic review with a focus on blinding. Phys Ther. 2013;93(7):873-88.
  • 9
    de Siqueira GR, da Silva GAP. Alterações posturais da coluna e instabilidade lombar no indivíduo obeso. Fisioter Mov. 2011 jul/set;24(3):557-66.
  • 10
    Matsudo S, Araújo T, Matsudo V, Andrade D, Andrade E, Oliveira LC, et al. Questionário Internacional de Atividade Física (IPAQ): estudo de validade e reprodutibilidade no Brasil. Rev Bras Ativ Fis Saude. 2001;6(2):5-18.
  • 11
    IPAQ Research Committee. Guidelines for data processing and analysis of the International Physical Activity Questionnaire (IPAQ) – short and long forms; 2005. Disponível em: <https://docs.google.com/viewer?a=v&pid=sites&srcid=ZGVmYXVsdGRvbWFpbnx0aGVpcGFxfGd4OjE0NDgxMDk3NDU1YWRlZTM>. Acesso em: 09 de jul. de 2015.]
    » https://docs.google.com/viewer?a=v&pid=sites&srcid=ZGVmYXVsdGRvbWFpbnx0aGVpcGFxfGd4OjE0NDgxMDk3NDU1YWRlZTM
  • 12
    Masselli MR, Fregonesi CEPT, de Faria CRS, Bezerra MIS, Junges D, Nishioka TH. índice funcional de Owestry após cirugia para descompressão de raízes nervosas. Fisioter Mov. 2007;20:115-22.
  • 13
    Franzblau AN. A primer of statistics for non-statisticians. New York: Harcourt, Brace & World. 1958.
  • 14
    Marcus RL, Addison O, Dibble LE, Foreman KB, Morrell G, Lastayo P. Intramuscular adipose tissue, sarcopenia, and mobility function in older individuals. J Aging Res. 2012;2012:629637.
  • 15
    Santos DA, Dawson JA, Matias CN, Rocha PM, Allison DB. Reference values for body composition and anthropometric measurements in athletes. PLoS One. 2014;9(5): e97846.
  • 16
    Powers C, Fan B, Borrud LG, Looker AC, Shepherd JA. Long-term precision of dual-energy X-ray absorptiometry body composition measurements and association with their covariates. J Clin Densitom. 2015;18(1):76-85.
  • 17
    Larsson I, Lissner L, Samuelson G, Fors H, Lantz H, Naslund I, et al. Body composition through adult life: swedish reference data on body composition. Eur J Clin Nutr. 2015;69(7):837-42.
  • 18
    Laskey MA. Dual-energy X-ray absorptiometry and body composition. Nutrition. 1996;12:45-51.
  • 19
    Crawford RJ, Filli L, Elliott JM, Nanz D, Fischer MA, Marcon M, et al. Age- and level-dependence of fatty infiltration in lumbar paravertebral muscles of healthy volunteers. Am J Neuroradiol. 2016;37(4):742-8.
  • 20
    Addison O, Marcus RL, Lastayo PC, Ryan AS. Intermuscular fat: a review of the consequences and causes. Int J Endocrinol. 2014;2014:309570.
  • 21
    Fosbøl MØ, Zerahn B. Contemporary methods of body composition measurement. Clin Physiol Funct Imaging. 2015;35(2):81-97.
  • 22
    Hodges PW, James G, Blomster L, Hall L, Schmid A, Shu C, et al. Multifidus muscle changes after back injury are characterized by structural remodeling of muscle, adipose and connective tissue, but not muscle atrophy: molecular and morphological evidence. Spine (Phila Pa 1976) . 2015;40(14):1057-71.
  • 23
    Mannion AF, Kaser L, Weber E, Rhyner A, Dvorak J, Muntener M, et al. Influence of age and duration of symptoms on fibre type distribution and size of the back muscles in chronic low back pain patients. Eur Spine J. 2000;9(4):273-81.
  • 24
    Addison O, Drummond MJ, Lastayo PC, Dibble LE, Wende AR, McClain DA, et al. Intramuscular fat and inflammation differ in older adults: The impact of frailty and inactivity. J Nutr Health Aging. 2014;18(5):532-8.
  • 25
    Dahlqvist JR, Vissing CR, Hedermann G, Thomsen C, Vissing J. Fat replacement of paraspinal muscles with aging in healthy adults. Med Sci Sports Exerc. 2017;49(3):595-601.
  • 26
    Kelly TL, Wilson KE, Heymsfield SB. Dual energy X-Ray absorptiometry body composition reference values from NHANES. PLoS One. 2009;4(9):e7038.
  • 27
    Rahemi H, Nigam N, Wakeling JM. The effect of intramuscular fat on skeletal muscle mechanics: implications for the elderly and obese. J R Soc Interface. 2015;12(109):20150365.

Publication Dates

  • Publication in this collection
    13 Jan 2020
  • Date of issue
    Jan-Feb 2020

History

  • Received
    05 Oct 2017
  • Accepted
    22 May 2019
Sociedade Brasileira de Medicina do Exercício e do Esporte Av. Brigadeiro Luís Antônio, 278, 6º and., 01318-901 São Paulo SP, Tel.: +55 11 3106-7544, Fax: +55 11 3106-8611 - São Paulo - SP - Brazil
E-mail: atharbme@uol.com.br