Obesity Surgery (2023) 33:1211–1217 https://doi.org/10.1007/s11695-023-06510-9 ORIGINAL CONTRIBUTIONS Usefulness of Ultrasound in Assessing the Impact of Bariatric Surgery on Body Composition: a Pilot Study A. Simó‑Servat1,2 · M. Ibarra1 · M. Libran1 · C. Quirós1 · N. Puértolas3 · N. Alonso1 · V. Perea1 · R. Simó4 · MJ. Barahona1 Received: 14 December 2022 / Revised: 8 February 2023 / Accepted: 15 February 2023 / Published online: 27 February 2023 © The Author(s) 2023 Abstract Background Bariatric surgery (BS) has a significant impact on body composition. The purpose of the study is to evaluate the usefulness of musculoskeletal ultrasound (MUS) to bioelectrical impedance (BIA) in the follow-up of patients undergoing BS in terms of body composition and quality of life (QoL). Methods This is a prospective pilot study including 32 subjects (75% female, mean age: 49.15 ± 1.9 years) who underwent BS. Fat mass (FM), lean mass (LM), and skeletal muscle index (SMI) were calculated by BIA. MUS measured subcutaneous fat (SF) and thigh muscle thickness (TMT) of the quadriceps. QoL was assessed by the Moorehead-Ardelt questionnaire. All these measurements were performed 1 month prior to BS and at 12-month follow-up. Results The mean BMI decreased by 6.63 ± 1.25 kg/m2 (p=0.001). We observed significant reductions in FM (p=0.001) and SF (p=0.007) and in LM (p=0.001) but not in SMI and TMT. We found a correlation between the FM and SF (pre-surgical, r=0.42, p=0.01; post-surgical, r=0.52, p=0.003) and between SMI and TMT (pre-surgical, r=0.35, p=0.04; post-surgical, r=0.38, p=0.03). QoL test showed significant improvement (p=0.001). In addition, a correlation between the QoL questionnaire and TMT post-surgery (r=0.91, p=0.019) was observed. However, we did not find any statistically significant correlation between QoL assessment and SMI or LM. Conclusions Our results suggest that MUS can be complementary to BIA for the evaluation and the follow-up of body composition after BS. TMT of quadriceps can provide relevant information about regional sarcopenia and has a significant correlation with QoL. Keywords Musculoskeletal ultrasound · Bariatric surgery · Sarcopenic obesity Introduction Bariatric surgery (BS) can achieve sustained significant weight loss providing major health benefits by reducing fat Key Points • Musculoskeletal ultrasound (MUS) can be complementary mass (FM) as it is an important determinant of co-morbidity to bioelectrical impedance (BIA) for the evaluation of body [1, 2]. However, after BS, a decrease in muscle mass also composition and regional sarcopenia in patients with obesity pre- occurs. This loss of muscle mass has been associated with and post-bariatric surgery (BS). lower psychological health and quality of life (QoL) and • MUS has a good correlation with BIA for subcutaneous fat (SF) and thigh muscle thickness (TMT) of quadriceps, pre- and post- higher prevalence of type 2 diabetes, hypertension, and all- BS. cause mortality [3, 4]. Accordingly, preservation of muscle • There is a correlation between QoL questionnaire and TMT mass during weight loss after BS is clinically relevant [5]. post-BS, but not between QoL assessment and skeletal muscle A recent study showed that after gastric sleeve surgery, index or lean mass. patients lost an average of 10% lean mass (LM) in the first * A. Simó‑Servat month and 17% loss after 1 year. However, the change in andreusimoservat@gmail.com weight and the subsequent change in the BMI do not reflect * MJ. Barahona the changes in FM and LM, the two main compartments of body composition [6]. Among the many relevant techniques Extended author information available on the last page of the article 13 Vol.:(0123456789) 1212 Obesity Surgery (2023) 33:1211–1217 for measuring muscle mass, muscle ultrasonography the differences in electric impedance among biological (MUS) is an emerging tool in clinical practice. MUS is a tissues using Janssen’s equation: SM (kg) = [(height − 2 simple, real-time, noninvasive, radiation-free, low-cost, (cm)/BIA resistance (ohms) × 0.401) + (gender (men = 1, and easily transportable, as well as valid and reliable, women = 0) × 3.825) + (age (years) × −0.071)] + 0.5102. method to estimate muscle mass. There are clinical trials We used the SMI of Baumgartner to identify sarcopenia in exploring MUS assessment for the diagnosis of sarcopenia people with obesity, which was calculated using SMI = SM [7, 8], but there is a lack of research on the role of MUS kg/height2 [14]. The ­BodyStat® 1500 MDD model was used in diagnosing sarcopenic obesity (SO) and in evaluating as previously described [12]. the changes in LM after BS [9]. MUS would allow an US measurements were made with a sonographic US Logiq accessible and useful assessment of sarcopenia in patients P9 (GE Healthcare) equipment muscle-skeleton B-model with obesity after BS and could be used as an alternative or using a linear multifrequency transducer (4–11 Hz) with complementary method to the conventionally used skeletal adequate use of contact gel and minimal pressure to avoid muscle mass index (SMI) measured by BIA or DEXA [10]. excessive compression of the muscle. Patient positioning was Moreover, MUS can detect regional sarcopenia of a specific done in accordance with what is reported in the literature [12, group of muscles as the quadriceps. This muscle group 15–19] (Fig. 1). Sarcopenia mainly affects lower limbs, so is essential to carry out basic functions for the autonomy the rectus femoris plus vastus intermedius were specifically of an individual since it is essential for walking [11] and selected to evaluate it [20], and its US evaluation was carried consequently for QoL. On this basis, thigh muscle thickness out according to the recommendations of the European Union (TMT) and subcutaneous fat (SF) measurements obtained Geriatric Medicine Society Sarcopenia Special Interest Group by ultrasound (US) of quadriceps are new, easily accessible and in accordance with the previous literature [19]. A set of parameters that we can introduce in clinical practice to three consecutive measurements was performed, and the improve the study of body composition of our patients. In average value was reported as the TMT or SF. Data were fact, morphological characteristics based on US measures of reported in centimeters (cm) as means ± standard deviation. the quadriceps muscle could be used for the screening and To avoid interindividual variability, the same physician initial evaluation of SO in candidates for BS and, especially, (endocrinologist A. S-S) with 4 years of experience performed in their follow-up. This approach will allow us to gain new all measurements. To assess intra-observer reliability, we insights into the potential usefulness of MUS [12]. evaluated intraclass correlation coefficients (CVs) using 3 The aim of this longitudinal pilot study is to examine images taken on 3 separate days on 30 participants, and the whether MUS has an added value to BIA in terms of monitoring results of CVs were 0.93 for TMT and 0.87 for SF. the changes of body composition and QoL after BS. Statistical analysis Material and Methods STATA statistical software version 14 (College Station, TX) was used. Continuous variables are expressed as mean We performed a prospective observational pilot study ± standard deviation (SD) unless specified otherwise. carried out in our hospital. Subjects were recruited from Categorical variables are expressed with percentages. the outpatient Obesity Unit between February 2019 and T-test was used to assess the differences between groups in November 2020. Subjects were candidates for BS when their continuous variables, Fisher test was used for categorical BMI was higher than 35 kg/m2 with comorbidities or BMI> variables, and the Pearson’s correlation test was used to 40 kg/m2. The study follows the STROBE guidelines for explore the relation between different variables. All analyses prospective studies [13]. Exclusion criteria were age ≥65 were 2-tailed, with p <0.05 considered statistically significant. years, pregnancy, and patients with clinical or personal characteristics that make monitoring difficult: drug or alcohol addiction, severe psychological, or psychiatric Results disorders. BIA and MUS tests as well as Moorehead-Ardelt Quality of Life Questionnaire were conducted during the The baseline data of the participants are shown in Table 1. same visit. All these assessments were carried out 1 month A total of 32 subjects were included: 24 female participants before surgery and at 12-month follow-up. The Hospital’s (75%), mean age of 49.15 ± 1.9 years. The mean baseline Ethics Committee approved all the procedures carried out BMI was of 43.79 ± 4.95 kg/m2 and decreased 6.63 ± 1.25 in the study, and all subjects signed the informed consent kg/m2 (p=0.001). before their inclusion in the study. The anthropometric parameters (FM and LM) assessed The skeletal muscle mass (SM) was measured using BIA. by BIA and the measurements performed using US (SF This method measures the body composition according to and TMT) are displayed in Table 2. We found significant 13 Obesity Surgery (2023) 33:1211–1217 1213 Fig. 1  Measurement of subcuta- neous tissue and thigh muscles using US. SF, subcutaneous fat; A TMT, thigh muscle thickness; SF VI, vastus intermedius; RF, B SF rectus femoris. A Representa- tive image of participant (Id 17) before BS. B Representative RF image of participant (Id 17) RF after BS TMT TMT VI VI Femoral bone Femoral bone Table 1  The baseline characteristics of the patients p=0.0005). In Fig. 2, we can see the improvement of the TMT in a particular patient. Total sample size 32 We found a positive correlation between the FM and Female 24 (75%) SF (pre-surgical, r=0.42, p=0.01; post-surgical, r=0.52, Age (years) mean ± SD 49.15 ± 1.9 p=0.003) and between SMI and TMT (pre-surgical, BMI (kg/m2) mean ± SD 43.79 ± 4.95 r=0.35, p=0.04; post-surgical, r=0.38, p=0.03) (Fig. 3). A Gastric bypass Roux-en-Y (%) 26 (81.25) significant improvement in the Moorehead-Ardelt Quality Sleeve gastrectomy (%) 6 (18.74) of Life Questionnaire score (0.52 ± 0.27 vs 1.66 ± 0.17, Diabetes Mellitus II (%) 10 (31.25) p=0.001) was observed, and this increasing punctuation was Hypertension (%) 19 (59.4) better in the 12 subjects where the TMT rises (1.21 ± 0.21 vs Dyslipidemia (%) 11 (34.4) 1.09 ± 0.31). Notably, we found a strong correlation between TMT assessed post-BS and the QoL test (r=0.91, p=0.0192) *BMI body mass index (Fig. 3). However, we did not find any statistically significant correlation between the QoL questionnaire and SMI or LM. Table 2  Anthropometric parameters by BIA and US measurements pre- and post-BS Discussion Pre-surgery (mean Post-surgery (mean p* ± SD) ± SD) In the present study, changes in body composition were LM (kg) 66.05 ± 2.42 62.29 ± 2.42 0.001 evaluated with BIA and MUS in patients undergoing BS FM (%) 45.19 ± 1.34 37.92 ± 1.81 0.001 at baseline and after 12-month follow-up. The results SMI (kg/m2) 10.19 ± 0.39 9.85 ± 0.39 0.057 showed a loss of FM, LM, and SF but not of SMI and TMT (cm) 1.74 ± 0.09 1.79 ± 0.1 0.635 TMT. FM had the greatest relative and absolute change. SF (cm) 1.26 ± 0.1 1.06 ± 0.09 0.007 In particular, the significantly higher change in FM and SF SMI, skeletal muscle mass index; LM, lean mass; FM, fat mass; SF, compared with LM and TMT before BS and after 12 months subcutaneous fat; TMT, thigh muscle thickness confirm a significant change in body composition that was *p <0.05 considered statistically significant already found in other studies [21]. We demonstrate a good correlation between pre- and post-surgery using US and BIA reductions in FM (45.19 ± 1.34 vs 37.92 ± 1.81, p=0.001) for assessing body composition. These good correlations and SF (1.27 ± 0.11 vs 1.03 ± 0.09, p=0.007). A significant have been observed between FM and SF, as well as between reduction in LM (66.05 ± 2.42 vs 62.29 ± 2.42, p=0.001) the SMI calculated by BIA and the TMT, thus supporting the was also observed, but not in SMI (p=0.057) and TMT usefulness of US to assess the follow-up of these patients. (p=0.635). In fact, in 12 subjects, the TMT improved despite In addition, US revealed that 12 patients had a significant detecting a decrease in the LM. Specifically, the mean TMT improvement in TMT after surgery but not in LM and of these 12 subjects increased (1.28 ± 0.13 vs 2 ± 0.16, SMI. These 12 patients have a lower mean age (44 years) 13 1214 Obesity Surgery (2023) 33:1211–1217 Fig. 2  Measurement of subcuta- neous tissue and thigh muscles using US. SF, subcutaneous fat; A TMT, thigh muscle thickness; VI, vastus intermedius; RF, rectus femoris. A Representa- B tive image of participant (Id 25) SF before BS. B Representative SF image of participant (Id 25) after BS RF RF TMT TMT VI VI Femoral Bone Femoral Bone than the other 20 patients (52 years), with no differences of a muscle group, it could be a complementary technique to regarding sex. They did not present a different LM and both the BIA and the dynamometer that provide functional FM at baseline or greater weight reduction compared information. Overall, our results point to further exploring to the rest of the patients. So, this improvement in TMT the usefulness of US in this field and establishing cut-off could be due to increased physical activity after BS. points as a diagnostic method for regional sarcopenia. Since MUS measures the muscle mass of the quadriceps, The main limitation of our study is the small sample it provides relevant information about the specific group size and the lack of a control group of subjects with normal of muscles that the patient works out. By contrast, BIA weight. Nevertheless, the study was aimed to evaluate the does not show the same level of accuracy. Therefore, the evolution after surgery and the patients represented their patient could improve the QoL even if the total LM does not own control [22]. The disadvantages of US are principally show improvement by BIA, since the improvement of the the lack of standardization and its high dependence on the quadriceps can allow patient autonomy. In fact, we found a expertise and skills of the operator [23]. The interpretation strong positive correlation between the QoL test and TMT of muscle–fat interfaces is limited due to similar acoustic post-BS. In addition, the improvement of QoL questionnaire impedance of muscle and fat tissues. Another drawback punctuation (1.21 ± 0.21) in the 12 patients in whom TMT of the US technique is that the operator could cause enhanced after BS was higher than in those patients (1.09 measurement errors by applying the transducer to the skin ± 0.31) without TMT increase. These findings suggest that with excessive pressure as this may compress the muscle MUS could be useful and complementary in determining [24]. In addition, we did not have data on muscle function. regional sarcopenia, which directly affects their quality of However, given that the quadriceps is an important muscle life, opening another field of study about regional sarcopenia for mobility measurement, quadriceps thickness provides in determinate groups of muscles. a useful surrogate of force [25–27]. The same physician This prospective pilot study revealed that the changes in performed all measurements, and this precluded the test body composition produced by BS are also significant with reproducibility. Finally, this is a pilot study, and, therefore, US and that they correlate with BIA. The use of MUS to larger studies are needed to confirm our results. determine changes in body composition in SO population, and specifically in the candidates to for BS provides more insight into a correct evaluation of body composition Conclusions after the intervention. Currently, in most centers, no body composition study is performed in a systematic or Our results suggest that MUS can be complementary to BIA protocolized manner, probably due to a lack of resources. for the evaluation and the follow-up of body composition in DEXA, CT, and MRI are methods that are not only difficult patients operated on for BS. TMT of quadriceps rather than to access and expensive, but also have radioactive effects. LM is strongly correlated with QoL, and, therefore, MUS In contrast, MUS is an increasingly accessible tool in the is an easy, noninvasive, low-cost tool that provides relevant consultation that could guide us on body composition as a information about quadriceps sarcopenia, which is closely screening for SO. Since US can provide regional information related to QoL. 13 Obesity Surgery (2023) 33:1211–1217 1215 60 50 50 40 FM FM 40 30 30 20 10 20 .5 1 1.5 2 2.5 3 0 .5 1 1.5 2 SF SF Pre-surgery Post-surgery a) 16 14 14 12 12 SMI SMI 10 10 8 8 6 6 .5 1 1.5 2 2.5 3 0 1 2 3 4 TMT TMT Pre-surgery Post-surgery b) 4 Moorehead-Ardelt Quality of Life Questionnaire 3 2 1 0 0 1 2 3 4 c) TMT Fig. 3  a A significant correlation was observed between fat mass BIA and TMT assessed by US (pre-surgical, r=0.35, p=0.04; post- (FM) by bioelectrical impedance analysis (BIA) and thigh muscle surgical, r=0.38, p=0.03). c A significant correlation was observed thickness (TMT) by ultrasound (US) (pre-surgical, r=0.42, p=0.01; between the Moorehead-Ardelt Quality of Life Questionnaire and post-surgical, r=0.52, p=0.003). b A significant correlation was TMT assessed by US post-surgery (r=0.91, p=0.0192). observed between skeletal muscle mass index (SMI) assessed by 13 1216 Obesity Surgery (2023) 33:1211–1217 Acknowledgements The authors wish to express their gratitude 9. 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Ibarra1 · M. Libran1 · C. Quirós1 · N. Puértolas3 · N. Alonso1 · V. Perea1 · R. Simó4 · MJ. Barahona1 1 3 Department of Endocrinology and Nutrition, Hospital Department of General Surgery, Hospital Universitari Universitari MútuaTerrassa, Plaça del Doctor Robert, 5, MútuaTerrassa, Terrassa, Barcelona, Spain 08221 Terrassa, Barcelona, Spain 4 Diabetes and Metabolism Research Unit, Vall d’Hebron 2 Department of Medicine, Autonomous University Research Institute and CIBERDEM (ISCIII), Autonomous of Barcelona, Bellaterra, Barcelona, Spain University of Barcelona, Terrassa, Barcelona, Spain 13