Validity, reliability and measurement error of quadriceps femoris muscle thickness obtained by ultrasound in healthy adults: a systematic review

Validade, confiabilidade e erro da medida da espessura muscular do quadríceps femoral obtida pela ultrassonografia em adultos saudáveis: uma revisão sistemática

Abstracts

Abstract

Due to its low cost and operational simplicity, ultrasound has been used to monitor muscle thickness in laboratory environments, rehabilitation clinics, and sports clubs. However, it is necessary to determine the measurement's quality to infer whether the possible changes observed are derived from the treatment or the measurement error. Therefore, we performed a systematic review to determine the validity, reliability, and measurement error of quadriceps femoris muscle thickness obtained by ultrasound in healthy adults. A search was conducted in the Pubmed, Scopus, and Web of Science databases until April 2022. The study selection process was carried out by two independent researchers, with the presence of a third researcher in case of disagreements. Twenty-six studies were eligible for the review, being 4 of validity, 4 of reliability only, and 18 of reliability and measurement error. The intraclass correlation coefficient ranged from 0.60 to 0.99 in validity studies and from 0.44 to 0.99 in reliability studies. The typical error of measurement ranged from 0.01 to 0.47 cm, and the coefficient of variation was from 0.5 to 17.9%. Four studies received “very good” classification in all the risk of bias analysis criteria. Therefore, it is concluded that the quadriceps femoris muscle thickness obtained by ultrasound was shown to be valid, reliable, and to have low measurement errors in healthy adults. The weighted average of the relative error was 6.5%, less than typical increases in resistance training studies. The raters' experience and methodological care for repeated measurements were necessary to observe low measurement errors.

Key words:
Atrophy; Hypertrophy; Magnetic resonance imaging; Reproducibility; Ultrasonography

Resumo

Devido ao baixo custo e simplicidade operacional, a ultrassonografia tem sido utilizada para monitorar a espessura muscular em ambientes laboratoriais, clínicas de reabilitação e clubes desportivos. Porém, é necessário determinar a qualidade da medida para inferir se as possíveis modificações observadas são decorrentes do tratamento ou do erro da medida. Portanto, realizamos uma revisão sistemática para determinar a validade, confiabilidade e erro da medida da espessura muscular do quadríceps femoral obtida pela ultrassonografia em adultos saudáveis. Foi realizada busca nas bases de dados Pubmed, Scopus e Web of Science até abril de 2022. O processo de seleção dos estudos foi realizado por dois pesquisadores independentes, com a presença de um terceiro pesquisador em caso de divergências. Vinte e seis estudos foram elegíveis para a revisão, sendo 4 de validade, 4 apenas de confiabilidade e 18 de confiabilidade e erro de medida. O coeficiente de correlação intraclasse variou de 0,60 a 0,99 em estudos de validade e 0,44 a 0,99 em estudos de confiabilidade. O erro típico da medida variou de 0,01 a 0,47 cm e o coeficiente de variação foi de 0,5 a 17,9%. Quatro estudos receberam classificação “muito bom” em todos os critérios na análise de risco de viés. Portanto, concluiu-se que a espessura muscular do quadríceps femoral obtida pela ultrassonografia se mostrou válida, confiável e com baixos erros de medida em adultos saudáveis. A média ponderada do erro relativo foi de 6,5%, menor do que os aumentos típicos em estudos de treinamento resistido. A experiência dos avaliadores e o cuidado metodológico com as medidas repetidas foram necessários para observar baixos erros de medida.

Palavras-chave:
Atrofia; Hipertrofia; Imagem por ressonância magnética; Reprodutibilidade dos testes; Ultrassom

INTRODUCTION

Muscle thickness (MT) obtained through ultrasound (US) has been used to monitor hypertrophy¹,² and muscle atrophy³,⁴ in the quadriceps femoris. The US uses waves with varying frequencies that penetrate the body while traveling through tissues with different acoustic impedances and reflecting echoes to the transducer, which are converted into electrical signals⁵. The angle and pressure of the transducer on the skin interfere with the measurement, as the incorrect positioning of the transducer can cause the reflected echoes not to be detected⁶,⁷.

For a quality image, there is a need for more outstanding care in positioning the transducer based on a more detailed methodological description⁸,⁹, allowing the records made with the US to be replicated when there is a need to perform repeated measurements¹⁰,¹¹. This need is essential in experimental studies when treatment is applied to the muscle tissue, such as resistance training, where small changes in MT are often observed¹²,¹³.

US is a commonly used to measure muscle architecture variables, such as quadriceps femoris MT¹⁴,¹⁵. Its operational simplicity, low cost compared to magnetic resonance imaging (MRI) or computed tomography (CT), and ease of image evaluation with free software make it attractive in research laboratory environments, rehabilitation clinics, and sports clubs. Therefore, it is necessary to verify valid and reliable ultrasound methods capable of monitoring quadriceps femoris MT in the literature. It is also necessary to verify the magnitude of the measurement error in order to be able to infer whether the possible changes observed experimentally are derived from the treatment itself instead of caused by measurement error.

The study aimed to determine the validity, reliability, and magnitude of measurement error of MT of the rectus femoris, vastus lateralis, vastus medialis, and vastus intermedius muscles obtained by the US in healthy adults.

METHODS

Protocol and registration

This systematic review followed the recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) Statement¹⁶. It was registered in the International Prospective Register of Systematic Reviews (PROSPERO) under the identification CRD42020205566.

Eligibility criteria

US studies that performed a validity test comparing the measurements of MT in cadavers or in vivo through MRI or CT could be included. Studies that tested the relative reliability or error of intra- or inter-rater measurement of MT for healthy adults aged 18 to 65 were also included. The muscles observed here were: rectus femoris, vastus lateralis, vastus medialis, and vastus intermedius. Studies in English and Portuguese were reviewed. Abstracts published in conference proceedings, dissertations, theses, inadequate measures or analyses, literature review studies, and research reports were excluded.

Search strategy

Searches were performed in Pubmed, Scopus, and Web of Science databases until April 2022. The following terms were combined: validity, reliability, measurement error, error of measurement, coefficient of variation, thickness, quadriceps femoris, rectus femoris, vastus lateralis, vastus medialis, and vastus intermedius. The terms were combined using the Boolean operators “AND” between descriptors and “OR” between tests and muscles. The search equation was adjusted to the specificity of each database. A manual search was also performed in references cited in published studies on similar topics.

Study selection

After removing the duplicates, there was the screening process, where the title and abstract of the studies were read by two researchers independently. In cases of conflicting screening, a discussion between the researchers was carried out to keep the article in the review. When disagreement occurred, a third researcher made the final decision. Subsequently, the same researchers read potentially eligible articles to select studies that met the eligibility criteria. Again, in cases of disagreement, a third researcher evaluated the studies and determined their permanence or exclusion from the review.

Risk of bias

Two researchers performed the risk of bias analysis independently. When there was disagreement, the researchers discussed the difference. A third researcher made the final decision when there was no consensus. The risk of bias in the validity, reliability, and measurement error studies was analyzed according to the Consensus-Based Standards for the Selection of Health Measurement Instruments (COSMIN)¹⁷. Seven criteria were evaluated, classifying them into five different discriminatory states.

Ratings were as follows: very good, when there was convincing evidence or arguments provided that the standard was met; adequate, when it is assumed, although not explicitly described, that the standard has been met; doubtful when it was unclear whether the standard was met; inadequate, when there was evidence that the standard was not met; information not available when there was no information to help in the judgment of the criterion.

Data extraction

One researcher extracted data from the studies that the second researcher later checked. The following data were extracted: n sample, gender and age of the participants, validity test (cadaver, magnetic resonance imaging, or computed tomography), type of reliability or measurement error (intra- or inter-rater), muscles (rectus femoris, vastus lateralis, vastus medialis or vastus intermedius) and statistical indices, such as intraclass correlation coefficient (ICC), typical error of measurement (TEM), standard error of measurement (SEM) and coefficient of variation (CV).

Weighted average of relative error

The statistical index's weighted average (WA) representing the relative error (TEM%, SEM%, or CV%) was performed, considering sample n, according to the equation below. The highest reported error value was considered when the result was presented through amplitude bands with the lowest and highest error value.

$$WA=\frac{\sum (\text{RE}\times n)}{\sum n}$$ (1)

Where:

WA = weighted average

Σ = sum

RE = relative error

n = number of subjects

RESULTS

Study selection

The search identified 375 records, 101 in the PubMed database, 114 in Scopus, and 160 in the Web of Science. Three records from other sources were added (studies detected from the reference of other studies). One hundred thirty-one duplicates were removed, and 247 records were selected for screening. After reading the title and abstract, 211 records were excluded, and 36 articles were selected for eligibility. Subsequently, the full text was read, and ten studies were excluded for different reasons. Six studies presented inadequate samples, two did not measure MT, one did not perform an adequate analysis, and one did not inform the type of comparison. The summary of the selection of studies is presented in Figure 1 in the form of a flowchart.

Figure 1
Study selection flowchart.

Studies characteristics

Of the 26 studies included, 4 were validity studies¹⁸-²¹, and 4 were reliability only²²-²⁵. Eighteen were of reliability and measurement error²⁶-⁴³. Four hundred ninety subjects were included, from which 311 men, 164 women, and 15 were not identified. Participants were primarily young adults, and the mean age ranged from 18 to 49. The characteristics of the included studies are summarized in Table 1.

Table 1
Overview of eligible studies.

Studies	N Gender	Age (years)	Study type	Comparison	Muscle	Statistical index
Arruda et al.26	25M	24±4	Reliability & measurement error	Intra- & inter-rater	VL	Intra: ICC = 0.991-0.998; TEM = 0.01-0.03 cm; CV = 0.5-1.8%
						Inter: ICC = 0.990-0.996; TEM = 0.02-0.03 cm; CV = 0.6-2.3%
Barotsis et al.22	8M & 5W	24±3	Reliability	Intra-rater	RF	ICC = 0.621-0.976
					VI	ICC = 0.411-0.938
Betz et al.18	7M & 9W	33±11	Validity & Reliability	MRI, intra- & inter-rater	VL	Validity: ICC = 0.835-0.895
		47±11				Intra: ICC = 0.928-0.961
						Inter: ICC = 0.936-0.965
Caresio et al.23	25M & 25W	31±11	Reliability	Inter-rater	RF	ICC = 0.98
					VL	ICC = 0.99
Carr et al.27	7M & 10W	24±3	Reliability & measurement error	Inter-rater	VL	ICC = 0.826-0.854; SEM = 0.19 cm; SEM% = 7.7-7.8%
		21±2
Chiaramonte et al.24	21M	26-38	Reliability	Intra- & inter-rater	VL	Intra: ICC = 0.92
						Inter: ICC = 0.97
Cleary et al.28	15 NI	18-35	Reliability & measurement error	Intra- & inter-rater	RF	Intra: SEM = 0.03-0.07 cm; SEM% = 1.2-2.8%
						Inter: ICC = 0.984; SEM = 0.06 cm
					VL	Intra: SEM = 0.04-0.08 cm; SEM% = 1.6-3.3%
						Inter: ICC = 0.993; SEM = 0.05 cm
Dudley-Javoroski et al.29	8M & 8W	26±5	Reliability & measurement error	Intra- & inter-rater	VL	Intra: ICC = 0.66-0.99; CV = 0.8-6.4%
						Inter: ICC = 0.742
Ema et al.30	7M & 7W	24±1	Reliability & measurement error	Intra-rater	RF	ICC = 0.981-0.984; CV = 2.3-2.4%
Franchi et al.31	9M	24±2	Reliability & measurement error	Intra-rater	VL	ICC = 0.99; SEM% = 1.7%
Gomes et al.32	7M & 8W	34±11	Reliability & measurement error	Intra-rater	RF	ICC = 0.929; CV = 4.6%
Hagoort et al.33	7M & 5W	23±4	Reliability & measurement error	Intra- & inter-rater	VL	Intra: ICC = 0.93-0.98; SEM = 0.05-0.11 cm
						Inter: ICC = 0.98; SEM = 0.10 cm
Ishida et al.34	14M	21±1	Reliability & measurement error	Intra- & inter-rater	RF	Intra: ICC = 0.99; SEM = 0.04 cm
						Inter: ICC = 0.96; SEM = 0.07 cm
Jacob et al.35	32M	18±1	Reliability & measurement error	Intra-rater	VL	ICC = 0.95; SEM = 0.04 cm
Lanferdini et al.36	11M & 11W	27±5	Reliability & measurement error	Intra- & inter-rater	RF	Intra: ICC = 0.848; SEM = 0.11 cm; CV = 14.8%
						Inter: ICC = 0.803; SEM = 0.15 cm; CV = 17.9%
					VL	Intra: ICC = 0.987; SEM = 0.04 cm; CV = 14.7%
						Inter: ICC = 0.882; SEM = 0.09 cm; CV = 13.1%
Lima and Oliveira37	4M & 10W	22±2	Reliability & measurement error	Intra-rater	VL	ICC = 0.95-0.99; TEM = 0.10-0.11 cm; CV = 3.1-3.8%
Mairet et al.38	10M & 9W	30±6	Reliability & measurement error	Intra-rater	VL	ICC = 0.65-0.75; SEM = 0.15-0.18; SEM% = 6.7-7.9%
Mechelli et al.19	10M & 10W	49±10	Validity	MRI	RF + VI	ICC = 0.99; SEM = 0.07 cm
Mechelli et al.39	12M & 12W	49±10	Reliability & measurement error	Intra- & inter-rater	RF + VI	Intra: ICC = 0.96; SEM = 0.13 cm
						Inter: ICC = 0.98; SEM = 0.10 cm
Nijholt et al.20	5M & 9W	33±NI	Validity & Reliability	MRI & intra-rater	RF	Validity: ICC = 0.60
						Reliability: ICC = 0.87
Oranchuck et al.40	26M	29±5	Reliability & measurement error	Intra-rater	RF	ICC = 0.93-0.95; TEM = 0.23-0.47 cm; CV = 2.7-4.1%
					VL	ICC = 0.94-0.98; TEM = 0.15-0.26 cm; CV = 2.4-3.8%
					VI	ICC = 0.88-0.98; TEM = 0.14-0.37 cm; CV = 2.8-9.3%
Ruas et al.41	10M	23±2	Reliability & measurement error	Intra-rater	RF	ICC = 0.97; SEM = 0.07 cm
					VL	ICC = 0.97; SEM = 0.10 cm
					VM	ICC = 0.97; SEM = 0.14 cm
					VI	ICC = 0.99; SEM = 0.07 cm
Santos and Armada-da-Silva42	10M & 10W	20±2	Reliability & measurement error	Intra-rater	RF	ICC = 0.88-0.99; SEM = 0.09-0.14 cm
					VL	ICC = 0.70-0.99; SEM = 0.09-0.15 cm
					VM	ICC = 0.80-0.98; SEM = 0.07-0.16 cm
					VI	ICC = 0.74-0.99; SEM = 0.13-0.19 cm
Soares et al.43	12M	24±6	Reliability & measurement error	Intra-rater	VL	ICC = 0.964; TEM = 0.07 cm; CV = 2.9%
Takahashi et al.25	12M	27±4	Reliability	Intra- & inter-rater	RF	Intra: ICC = 0.95
						Inter: ICC = 0.70
Worsley et al.21	12M	18-30	Validity & Reliability	MRI & intra-rater	VM	Validity: ICC = 0.84-0.94
						Reliability: ICC = 0.90-0.98

• Note. CV = coefficient of variation; ICC = intraclass correlation coefficient; M = men; MRI = magnetic resonance imaging; N = number of subjects; NI = not informed; RF = rectus femoris; SEM = standard error of measurement; TEM = typical error of measurement; VI = vastus intermedius; VL = vastus lateralis; VM = vastus medialis; W = women.

Risk of bias in studies

The risk of bias analysis performed using the COSMIN tool showed that four studies were classified as “very good” in the seven criteria²⁰,²¹,²⁶,³⁹ and two with at least one “inadequate” criterion²²,²⁷. Table 2 presents the classification of studies for each of the seven criteria.

Table 2
Analysis of the risk of bias by the COSMIN tool.

Studies	C1	C2	C3	C4	C5	C6	C7
Arruda et al.26	Very good	Very good	Very good	Very good	Very good	Very good	Very good
Barotsis et al.22	Inadequate	Very good	Adequate	Very good	Doubtful	Very good	Very good
Betz et al.18	Very good	Very good	Adequate	Adequate	Very good	Very good	Adequate
Caresio et al.23	Very good	Very good	Adequate	Very good	Very good	Very good	Very good
Carr et al.27	Very good	Very good	Adequate	Inadequate	Very good	Very good	Very good
Chiaramonte et al.24	Very good	Very good	Adequate	Adequate	Adequate	Very good	Adequate
Cleary et al.28	Very good	Very good	Adequate	Adequate	Very good	Very good	Very good
Dudley-Javoroski et al.29	Adequate	Doubtful	Adequate	Adequate	Adequate	Doubtful	Very good
Ema et al.30	Very good	Very good	Very good	Adequate	Adequate	Very good	Adequate
Franchi et al.31	Adequate	Doubtful	Adequate	Adequate	Doubtful	Very good	Very good
Gomes et al.32	Doubtful	Very good	Very good	Adequate	Very good	Very good	Adequate
Hagoort et al.33	Adequate	Very good	Adequate	Adequate	Very good	Very good	Very good
Ishida et al.34	Very good	Very good	Very good	Very good	Very good	Very good	Adequate
Jacob et al.35	Very good	Very good	Adequate	Adequate	Adequate	Very good	Very good
Lanferdini et al.36	Very good	Very good	Adequate	Adequate	Adequate	Very good	Adequate
Lima and Oliveira37	Very good	Very good	Very good	Doubtful	Doubtful	Very good	Adequate
Mairet et al.38	Adequate	Adequate	Adequate	Adequate	Adequate	Doubtful	Adequate
Mechelli et al.19	Very good	Very good	Very good	Very good	Very good	Very good	Very good
Mechelli et al.39	Very good	Very good	Adequate	Adequate	Doubtful	Very good	Adequate
Nijholt et al.20	Very good	Very good	Very good	Very good	Very good	Very good	Very good
Oranchuck et al.40	Very good	Very good	Very good	Adequate	Doubtful	Very good	Adequate
Ruas et al.41	Very good	Very good	Very good	Adequate	Adequate	Very good	Very good
Santos and Armada-da-Silva42	Very good	Very good	Adequate	Adequate	Doubtful	Very good	Very good
Soares et al.43	Very good	Very good	Adequate	Adequate	Adequate	Very good	Very good
Takahashi et al.25	Very good	Very good	Adequate	Very good	Very good	Very good	Very good
Worsley et al.21	Very good	Very good	Very good	Very good	Very good	Very good	Very good

• Note. C1 = volunteers were stable in time between repeated measurements; C2 = the time interval between repeated measurements was adequate; C3 = the conditions of repeated measures were similar; C4 = the collection was repeated without knowledge of the values of the previous measurement; C5 = the score values were determined without knowledge of the previous values; C6 = there was some other major flaw in the study design or statistical methods; C7 = the appropriate statistical index for the study was calculated.

Weighted average result

For the WA calculation, the 16 relative error values of the MT of different quadriceps femoris muscles obtained from 12 of the 26 included studies were considered. From the relative error, weighted by the sample n, the WA was 6.5%.

DISCUSSION

The studies included in the systematic review showed that US is valid and reliable for measuring quadriceps femoris MT in healthy adults and having a low absolute and relative measurement error, both intra- and inter-raters. However, for the measurement to be reproducible, the raters must pay attention to the description of the method they will use, including the definition of the measurement location⁸, anatomical landmarks²⁶, stability of the subject³⁵, positioning of the transducer³⁴, and experience in image analysis²⁸.

Four eligible validity studies compared MT obtained by the US versus MRI. Worsley et al.²¹ evaluated MT in three different portions of the vastus medialis and observed a high ICC ranging from 0.84 to 0.94. Nijholt et al.²⁰ observed a moderate ICC of 0.60 in the rectus femoris muscle. However, Mechelli et al.¹⁹ found an almost perfect correlation of 0.99 in the rectus femoris and vastus intermedius muscles. Finally, Betz et al.¹⁸ measured the proximal, medial, and distal portions of the vastus lateralis muscle and observed correlations ranging from 0.835 to 0.895. Other validity studies were not eligible as they were performed with a sample with some disease⁴⁴ or with measurements performed in muscle groups other than the quadriceps femoris⁴⁵-⁴⁷. All the studies mentioned concluded that the US measurement was valid for measuring MT.

Twenty-five studies included in the review performed relative reliability analysis. The lowest ICC value was 0.441²², and the highest was 0.99, observed in 9 studies²³,²⁶,²⁸,²⁹,³¹,³⁴,³⁷,⁴¹,⁴². The low reliability found in the study by Barotsis et al.²² may have occurred because the MT measurement was performed four times during 24 hours to observe the measurement's reproducibility throughout the day. Participants were instructed to maintain their usual routine in the intervals between collections, including the practice of physical activity, thus impairing stability between measurements.

Higher correlations were observed when the comparison was intra-rater, probably due to the reproducibility of the technique. However, some inter-rater reliability studies have found high correlations when comparing experienced raters against novice raters²⁷,²⁸,³⁶. They observed ICC values between 0.803 and 0.993 in rectus femoris and vastus lateralis MT. Cleary et al.²⁸ suggest that inexperienced and more experienced raters continue to practice their measurements on control images to maintain a high level of reliability before conducting an experimental study. Furthermore, Carr et al.²⁷ highlighted the need for a detailed method description so that different raters can replicate the technique in different environments and samples.

Although the ICC is a widely used statistical analysis to verify reliability, its results are affected by the heterogeneity of the sample. Thus, it must be accompanied by other analyzes to detect the measurement error, such as TEM or SEM⁴⁸,⁴⁹. The present review found that absolute errors ranged from 0.01 to 0.47 cm. Our laboratory experience indicates that the methodological care of the entire process, associated with the constant training of the raters, has decreased TEM. In the first study, our group presented an intra-rater TEM of 0.07 cm for vastus lateralis MT⁴³. In a recent study, intra- and inter-rater TEM decreased to 0.01 to 0.03 cm for the same variable²⁶.

In the exercise and sports sciences areas, it was recommended as a criterion that the error of the acceptable relative measure should be at most 10%⁴⁸. Except for one study eligible for this review, all had CV below 10%. Lanferdini et al.³⁶ observed CVs of 13.1 to 17.9%. The authors argued that the magnitude of the error was probably due to the raters' inexperience with the US measurement.

The WA analysis of the relative error found was 6.5%. This value is a less arbitrary and evidence-based way to define a reasonable cut-off point for the measurement error of quadriceps femoris MT in healthy adults. Previous studies show that it is possible to achieve this index when raters are trained to collect and analyze the measure²⁶,²⁸,²⁹,³¹,³²,³⁷,⁴³.

Based on the recent experience of our laboratory, it is suggested that the responsible raters carry out a reliability and measurement check before an experimental study, where the US will be used to detect changes in MT. In addition to the precise definition of the measurement site and the training of raters in carrying out the measurement itself, it is recommended the operational description of some procedures based on COSMIN¹⁷, such as: guiding volunteers not to perform physical activity for at least 24 hours before the collection of images, inform the interval between repeated measurements, describe in detail where the transducer will be positioned on the skin to obtain the image of the muscle, encode and shuffle the images in order to blind the raters of the images, experience in the analysis of MT by the software and perform the appropriate statistical analysis to the objectives.

CONCLUSIONS

The current systematic review concluded that the MT of the rectus femoris, vastus lateralis, vastus medialis, and vastus intermedius obtained by the US is a valid, reliable measurement and had low measurement errors in healthy adults. High correlation values were observed for both validity studies and reliability studies. In addition, a low magnitude of measurement errors was observed, with an average error of 6.5%. Experience and care are needed in the steps discussed here to observe low measurement errors.

• How to cite this articleSoares ALC, Carvalho RF, Mogami R, Meirelles CM, Gomes PSC. Validity, reliability and measurement error of quadriceps femoris muscle thickness obtained by ultrasound in healthy adults: a systematic review. Rev Bras Cineantropom Desempenho Hum 2023, 25:e93936. DOI: https://doi.org/10.1590/1980-0037.2023v25e93936

• Funding

  Soares ALC was supported with scholarship from Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Capes (protocol number: 88887.603070/2021-00). Gomes PSC was supported by PROCIÊNCIA grant from Universidade do Estado do Rio de Janeiro - UERJ.

• Ethical approval

  Does not apply to the current study.

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Publication Dates

• Publication in this collection
  15 Sept 2023
• Date of issue
  2023

History

• Received
  20 Apr 2023
• Accepted
  11 July 2023