1 MUSCLE ECHOGENICITY AND CHANGES RELATED TO AGE AND BODY MASS INDEX

3 Andrea Z Pereira, MD, PhD1,2; Clarissa Baia Uezima, RD1; Maria Teresa Zanella,
4 MD, PhD1; Rogério Ruscitto do Prado, MsC, PhD1; Maria Cristina Gonzalez, MD, PhD3;
5 Jolene Zheng, MD, PhD4; Steven B Heymsfield, MD4

6
1
7 Endocrinology Division, UNIFESP, S.Paulo, Brazil
2
8 Oncology and Hematology Department, Hospital Israelita Albert Einstein, S.Paulo,
9 Brazil
3
10 Post-graduation Program in Health and Behaviour, Catholic University of Pelotas,
11 Brazil
4
12 Pennington Biomedical Research Center, Louisiana State University System, Baton
13 Rouge, LA

14

15 Corresponding author:
16 Andrea Z Pereira
17 Hospital Israleita Albert Einstein
18 Av. Albert Einstein, 627/520
19 São Paulo (SP) - Brazil
20 CEP 05651-901

21 Tel.: (55 11) 3773-6590 and (55 11) 2151-3203

22 Fax: (55 11) 2151-3522
23 E-mail: andreap_pereira@hotmail.com

24

25 Key words: Ultrasound-Echogenicity-Muscle-Elderly-Obesity-Body Composition

26

27 Conflicts of interest: None of the authors have any financial disclosure statements and
28 conflicts of interest to declare

29

This is the author manuscript accepted for publication and has undergone full peer review but has not
been through the copyediting, typesetting, pagination and proofreading process, which may lead to
differences between this version and the Version of Record. Please cite this article as doi:
10.1902/jpen.2030.

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30 Financial support: none.

31

32 Clinical Relevance: Echogenicity, which is a practical, low-cost and specific method, can be
33 used in clinical practice to assess muscle functionality.

34

35 ABSTRACT

36

37 INTRODUCTION: Muscle fibers are lost and replaced by fat and fibrous tissue infiltration
38 during aging. This process decreases muscle quality and influences tissue appearance on
39 ultrasound images over time. Increased muscle “echogenicity” represents changes caused by
40 fat and fibrous tissue infiltration and can be quantified with recently developed software.
41 OBJECTIVE: To investigate skeletal muscle quality through echogenicity estimates
42 according to participant body mass index (BMI) and age. METHODS: This was a cross-
43 sectional study performed at the Pennington Biomedical Research Center, Baton Rouge,
44 Louisiana with 117 participants (57 men and 60 women), with mean age (X±SD) 38.9±17.0
45 years and BMI 28.6±6.2 kg/m². All participants were examined by ultrasound (GE
46 LOGIC®), using a 5.0 MHz linear transducer. Participants had muscle thickness measured by
47 ultrasound at 4 anatomic locations (biceps and triceps brachial, femoral quadriceps and calf
48 triceps). Echogenicity was analyzed with specific software (Pixel Health®) that evaluated
49 image gray scale. RESULTS: According to BMI, 41% of participants were obese. There was
50 a positive correlation between age and thigh muscle echogenicity (rp = 0.534; p <0.0001) and
51 a negative correlation between thigh muscle echogenicity and thickness (rp = -0.395; p
52 <0.0001). In addition, there was high muscle echogenicity in participants with overweight
53 and obesity age 50 years or older (p<0.05). CONCLUSION: Older age and higher BMI were
54 associated with stronger echogenicity signals and smaller muscle thickness. People with
55 overweight and obesity and/or people older than age 50 years have reduced muscle quality
56 with smaller muscle thickness as observed with ultrasound.

57

58 INTRODUCTION

59

60 By the age of 80 healthy people lose about 30-40% of their fat-free mass and have a
61 20% of decline in cross-sectional area of their skeletal muscles; acute or chronic diseases can
62 further increase this muscle loss.(1–3) Structural changes occur in skeletal muscles with some
63 disease states and during the aging process, when muscle fibers, mainly type IIs, are lost and
64 replaced by adipose and fibrous tissue infiltration.(2,4–7) The replacement of skeletal muscle

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65 fibers decreases muscle quality and increases density and thereby increases echogenicity on
66 ultrasound images.(7–10)

67 In medical practice, ultrasound has been used since the early 1950s.(5) Ultrasound is
68 based on echo reflections and represents a two-dimensional gray-scale image that ranges in
69 echogenicity between relatively light strongly reflected echoes and dark non-reflected echoes
70 that identify borders of the skin-subcutaneous fat, fat-muscle and muscle-bone
71 interfaces.(5,11)

72 Ultrasound evaluations have high spatial resolution, include real-time evaluation with
73 ability to compare to the contralateral site, and are non-invasive, portable, safe and an easy to
74 use imaging method.(11–14) However, interpretation of ultrasound images are more difficult
75 and subjective because of a lack of standardized procedures and measurements.(11)

76 Increased muscle density or echogenicity represents changes caused by adipose and

77 fibrous tissue infiltration and these effects can be analyzed by pixel gray-scale.(1,2,7,9,15–
78 17)

79 The objective of the present study was to investigate skeletal muscle quality through
80 echogenicity estimates and its association with body mass index (BMI), age, and body
81 composition.

82

83 MATERIALS AND METHODS

84

85 Study Design and Subjects

86

87 A cross-sectional study was performed in 117 healthy volunteer participants (57 men
88 and 60 women) from August 2013 to January 2014 at Pennington Biomedical Research
89 Center, Louisiana State University, Baton Rouge, USA. The sample was recruited through
90 advertisements in the local community and by word of mouth. Participants aged less than 18
91 years old and adults with chronic diseases were excluded from the study.

92 The study was exploratory with the aim of acquiring a sample >100 participants for
93 echogenicity evaluation across the full adult lifespan. The study was approved by the
94 institutional Ethics Committee and all the volunteers signed the written consent.

95

96 Anthropometric Measurements

97

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 98 In order to determine height (m), a stadiometer (with total height of 2.0 m and precision
99 of 1.0 mm) was used, duly posted on the wall, with the patient standing, barefoot, with their
100 heels together, with the back straight and arms outstretched at the sides of the body. The
101 measurement of weight (kg) was performed with a calibrated scale, with the participant
102 standing in the center of the scale base, barefoot and wearing light clothing. The magnitude
103 of height and weight were measured twice; a third measurement was acquired only when the
104 first two differed > 0.5 cm or > 0.5 kg, respectively. Results were averaged.
105 BMI was used to classify nutritional status of the adult participants as: < 16 kg/m2:
106 malnutrition grade III; 16 – 16,9 kg/m2: malnutrition grade II; 17 – 18,4 kg/m2: malnutrition
107 grade I; 18,5 – 24,9 kg/m2: normal; 25 – 29,9 kg/m2: overweight;30 – 34,9 kg/m2: obesity
108 grade I; 35 – 39,9 kg/m2: obesity grade II; ≥ 40 kg/m2: obesity grade III.(18,19)

109

110 Body Composition

111

112 All participants were evaluated with dual X-ray absorptiometry (DXA) (iDXA, GE,
113 USA) and bioelectrical impedance analysis (BIA) (MC980, Tanita Corp, Tokyo, Japan). Two
114 DXA scans were made on each participant. The coefficients of variation (CVs) for
115 appendicular lean mass and total lean mass were both <2%. Any DXA scans that had
116 artefacts rendering them unreadable were excluded from the statistical analysis. The first scan
117 was used for analysis unless it was excluded because of an artefact when the second scan was
118 used instead. The MC980 BIA system had an 8-electrode configuration that separately
119 captured each arm and leg along with trunk and right and left-body electrical properties.
120 Appendicular lean mass, total lean mass, and total skeletal muscle mass were derived by the
121 MC980 software.

122 Participants were classified as sarcopenic or non-sarcopenic by DXA criteria based on

123 appendicular lean mass/ht2, male <7.0 kg/m2 and female ≤ 5.0 kg/m2, and by BIA criteria
124 based on total muscle mass/ht2, male ≤ 8.5 kg/m2 and female ≤ 5.75 kg/m2. (20) Both DXA
125 and BIA criteria were used to screen participants for sarcopenia.

126

127 Ultrasound

128

129 All participants were examined by ultrasound (GE LOGIC®), using a 5.0 MHz linear
130 transducer. The quadriceps femoris and calf triceps, in the lower limb, and the biceps brachii
131 and brachialis muscles in the upper limb, were the sites chosen for evaluation. The biceps
132 brachii and brachialis muscles were measured in one thickness area only. A single reading
133 was taken at each site and read in duplicate by the expert ultrasound technician; results were
134 averaged unless the two readings differed at which point a third measurement was taken.

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135 The right side was evaluated by a single experienced physician examiner, who
136 obtained the mean of three ultrasound measurements performed in the same place in both the
137 longitudinal and transverse planes. The subject rested in the supine position prone and
138 relaxed, with arms and legs fully extended during the measurements. To standardize the
139 measurements, the probe was held perpendicular to the corresponding bone. Water-soluble
140 transmission gel provided acoustic contact without depression of the skin surface while the
141 probe was placed perpendicular to the tissue interface under the marked sites.

142 The ultrasound probe was placed at the position of maximum circumference. In the upper
143 limbs, the location of the muscle measurement was taken 15 cm from the humeral head, then
144 distally on the ventral and intermediate area of the biceps muscle. In the lower limbs, the
145 positions of muscle tissue measurements were performed 15 cm from the superior pole of the
146 patella on the quadriceps muscle in the ventral, mid-line of the thigh. Measurement of calf
147 triceps was taken in the position of maximum circumference in the mid-line.

148 Echogenicity was analyzed using a computer assisted gray-scale analysis (Pixel
149 Health®, Uezima, Brazil). A region of interest was selected in the transverse ultrasound
150 image in each muscle without any bone or surrounding fascia. The mean echo intensity of
151 this region was calculated. (Figure 1) The ultrasound images were analyzed for echogenicity
152 off-line and low-quality scans that were technically inadequate were excluded from further
153 evaluation. The software generated a single echogenicity value for each image.

154

155 Statistical Methods

156

157 Categorical variables were described by absolute and relative frequencies. The
158 quantitative variables were described using mean and standard deviation or median,
159 minimum and maximum according to the distribution of normality of the data evaluated by
160 the Kolmogorov-Smirnov test. We evaluated the correlations between quantitative variables
161 using Spearman’s test, Mann-Whitney`s and/or Kruskal-Wallis tests and Dunn’s test were
162 used for comparison between groups.

163 All analyses were carried out with SPSS (IBM Corp. Released 2016. IBM SPSS
164 Statistics for Windows, Version 24.0. Armonk, NY: IBM Corp.) and p-values less than 0.05
165 were considered statistically significant.

166

167 RESULTS

168

169 The sample included 117 participants, 51% of whom were female. The mean (±SD)
170 sample age was 38.9±17.0 years; 11% (13/117) were over the age of 65 years. BMI

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171 distribution detected 1.6% with malnutrition, 26.4% as normal, 38% as overweight, and 34%
172 were obese; the sample BMI was 28.6±6.2 kg/m2. None of the participants had sarcopenia
173 based on either DXA or BIA criteria.

174 Ultrasound measurements and echogenicity are presented in Table 1. Due to technical
175 issues not all the images had echogenicity evaluated and thus the sample described in the
176 following section have different participant numbers.

177 There was a significant difference in thigh muscle thickness in elderly (age >65 years)
178 and non-elderly participants (30±9 mm and 39±10 mm respectively, p=0.002). BMI was
179 similar between elderly and non-elderly participants.

180 Echogenicity was positively associated with age, being higher in elderly people. We
181 found a significant difference between elderly and non-elderly people in thigh echogenicity
182 (p<0.001; Table 2)

183 Related to BMI, using Dunn’s multiple comparisons, we found a significant thigh
184 echogenicity difference when we compared participants who were overweight/obese and
185 normal weight (p<0.05). This higher BMI group had higher thigh echogenicity. This
186 observation is also shown in Table 3 according to BMI group.

187 We found a positive correlation between thigh echogenicity and age (rs=0.5;
188 p<0.001), but thigh echogenicity had a negative correlation with total lean mass evaluated by
189 BIA and DXA (rs=-0.3, p<0.01; -0.25, p<0.01) and with thigh muscle thickness (mm) (rs=-
190 0.4; p<0.01). Calf and biceps echogenicity were not significantly correlated with any of these
191 measures.

192 The results of multiple linear regression and power calculations are presented Table
193 4. Thigh echogenicity lost power in relation to BMI. However, biceps and thigh echogenicity
194 remained significant in association with age.

195

196 DISCUSSION

197

198 A muscle from a healthy young person has low echogenicity with a dark appearance
199 on ultrasound images; on the other hand, muscle from an old or unhealthy person that has
200 adipose tissue and fibrous tissue infiltration has high echogenicity with a lighter appearance
201 on ultrasound images.(21) Several studies using ultrasound echogenicity and computed
202 tomography density to evaluate muscle at different ages detected more fat and fewer muscle
203 fibers in the elderly.(2,22–24) In our study, people who were elderly had higher echogenicity.
204 (1)

205 Additionally, thigh echogenicity correlated negatively to total lean mass evaluated by
206 BIA and DXA and with thigh muscle thickness evaluated by ultrasound that were higher in

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207 elderly participants. These results could be associated to low muscle fibers and high fat and
208 fibrosis infiltration, as shown in other studies.(2,7,9,15,16)

209 Participants who were overweight and obese in this study had higher thigh
210 echogenicity with no obvious clinical signs of sarcopenia. There are studies using computed
211 tomography to evaluate the muscle area and muscle quality of people who are obese and
212 sarcopenic and non-sarcopenic, nevertheless there are no studies using ultrasonography in
213 this group of patients.(25–27)

214 In our study, measurement of easily identified thigh muscles showed the least
215 variation for repeated measurements evaluating muscle and gray scale by ultrasound. Our
216 observation is in agreement with other reports that chose thigh to evaluate muscle,
217 sarcopenia, or muscle loss by ultrasound.(13,16,28–30) As well as in our clinical experience,
218 the ultrasound transversal plane is more practical and convenient to evaluate muscle
219 mass.(13)

220 The present study had several limitations, including ultrasound measurements by a
221 single examiner in a relatively small sample and inclusion of healthy adults across a wide age
222 range but none of whom had sarcopenia. Future studies need to address these limitations with
223 focus on patients with both malnutrition and sarcopenia.

224

225 CONCLUSION

226

227 Echogenicity is a practical and safe method for evaluating the amount and quality
228 (echogenicity) of skeletal muscle. The elderly, as compared to young adults, had more muscle
229 loss and fat infiltration leading to higher echogenicity in the current study, an observation that
230 reflects the well-known effects of senescence. Our findings suggest that ultrasound is a
231 promising nutritional assessment tool as the instruments are widely available and are often
232 operated by trained technicians in the clinical settings.

233

234 Statement of Authorship

235

236 Andrea Z Pereira, Steven Heymsfield and Maria Teresa Zanella equally contributed to
237 the conception and design of the research; Jolene Zheng and Clarissa B Uezima contributed
238 to the acquisition and analysis of the data; Andrea Z Pereira, Steven Heymsfield and Rogério
239 Ruscitto contributed to the interpretation of the data; Maria Cristina Gonzalez, Maria Teresa
240 Zanella, Andrea Z Pereira and Steven Heymsfield drafted the manuscript. All authors
241 critically revised the manuscript, agree to be fully accountable for ensuring the integrity and
242 accuracy of the work, and read and approved the final manuscript.

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243 In this study we had no financial support and no author had a conflict of interest.

244

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329

330 Table 1. Biceps, calf, and thigh muscle thickness (mm) and echogenicity (pixel count).

Area Echogenicity (pixels) Thickness (mm)

N Median Min Max N Median Min Max

Biceps 117 18,429 1,333 31,280 119 27 17 45

Calf 106 9,363 362 30,250 116 41 6 68

Thigh 105 19,426 4,028 31,045 117 38 19 62

331

332 Table 2: Biceps, calf, and thigh, muscle thickness (±SD).

Area N Mean

Biceps 119 28.0 ± 6.8

Thigh 117 38.0 ± 10.0

Calf 116 41.0 ± 14.0

333

334 Table 3: Echogenicity (pixels) in elderly (≥65 years-old) and non-elderly (<65 years-old)
335 participants.
336
Echogenicity Elderly Median Minimum Maximum N p*

(pixel) (yes or no) (pixels)

Biceps No 17,896 1333 31,280 104 0.006

Yes 24,997 13,905 30,061 13

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 Calf No 8,849 362 26,325 94 0.026

Yes 12,827 4,864 30,250 12

Thigh No 19,140 4,028 30,319 94 <0.001

Yes 26,590 22,109 31,045 11

*
Mann-Whitney's test

337

338

339 Table 4. Multiple linear regression results.

Hypothesis
Echogenicity Std. Power
Factors Coefficient Test df p
(pixels) Error observed
(Wald)
Intercept 20,702 3284 39.7 1 <0.001
Gender
Biceps (female) -670 1331 0.25 1 0.078 0.615
Age (yrs) 172 41 18 1 0.985 <0.001
2
BMI (kg/m ) -297 112 7 1 0.737 0.008
Intercept 12,254 2,487 24 1 <0.001
Gender
Thigh (female) -4,129 885 22 1 0.995 <0.001
Age (yrs) 194 27 52 1 >0.999 <0.001
BMI (kg/m2) 74.6 88 0.7 1 0.131 0.394
BMI, body mass index; df, degrees of freedom.
340

341 Figure1: Echogenicity(A) and ultrasound thickness measurements(B) of triceps in transverse

342 plane

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343

344

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