Accepted Manuscript Title: Ultrasonographic Evaluation of the Calf Muscle Mass and Architecture in Elderly Patients With and Without Sarcopenia ¨ ur Kara Author: Mehmet Emin Kuyumcu Meltem Halil Ozg¨ Bledjan C ¸ uni G¨okhan C ¸ a˘glayan Serdar G¨uven Yusuf Yes¸il G¨unes¸ Arık Burcu Balam Yavuz Mustafa Cankurtaran Levent ¨ ¸ akar Ozc PII: DOI: Reference:
S0167-4943(16)30067-X http://dx.doi.org/doi:10.1016/j.archger.2016.04.004 AGG 3313
To appear in:
Archives of Gerontology and Geriatrics
Received date: Revised date: Accepted date:
4-11-2015 4-4-2016 7-4-2016
Please cite this article as: Kuyumcu, Mehmet Emin, Halil, Meltem, Kara, ¨ ur, C Ozg¨ ¸ uni, Bledjan, C ¸ a˘glayan, G¨okhan, G¨uven, Serdar, Yes¸il, Yusuf, ¨ ¸ akar, Levent, Arik, G¨unes¸, Yavuz, Burcu Balam, Cankurtaran, Mustafa, Ozc Ultrasonographic Evaluation of the Calf Muscle Mass and Architecture in Elderly Patients With and Without Sarcopenia.Archives of Gerontology and Geriatrics http://dx.doi.org/10.1016/j.archger.2016.04.004 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Ultrasonographic Evaluation of the Calf Muscle Mass and Architecture in Elderly Patients With and Without Sarcopenia Mehmet Emin Kuyumcu MD1*
[email protected], Meltem Halil MD1, Özgür Kara MD1, Bledjan Çuni MD2 Gökhan Çağlayan MD2, Serdar Güven MD2, Yusuf Yeşil MD1, Güneş Arık MD1, Burcu Balam Yavuz MD1, Mustafa Cankurtaran MD1, Levent Özçakar MD2 1
Hacettepe University Medical School, Department of Internal Medicine
Division of Geriatric Medicine, 06100 Sıhhıye, Ankara, Turkey 2
Hacettepe University Medical School, Department of Physical and Medicine Rehabilitation
06100 Sıhhıye, Ankara, Turkey *
Corresponding author at: Hacettepe University Medical School, Department of Internal
Medicine, Division of Geriatric Medicine, 06100 Sıhhıye, Ankara, Turkey, Tel : 0090 312 305 15 38, Fax: 0090 312 309 76 20.
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Highlights Only calf circumference measurements may not be appropriate for assessing sarcopenia. Thickness and fascicle length values of musculus gatrocnemius are lower in sarcopenic elderly and these two parameters can serve as alternative measurements for diagnosing/quantifying sarcopenia. Ultrasound imaging can safely/conveniently be used to evaluate different compartments of the musculoskelal system in elderly.
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Abstract BACKGROUND/OBJECTIVES: To sonographically assess the muscle mass and architecture of sarcopenic elderly subjects, and to explore the utility of ultrasound (US) measurements in predicting sarcopenia. METHODS: One hundred elderly subjects were enrolled in this cross-sectional study. Mean age value of our study population was 73.08 ± 6.18 years. The diagnosis of sarcopenia was confirmed by measuring fat-free mass index (using bioelectrical impedance analysis) and handgrip strength. Calf circumference was measured and US evaluations comprised bilateral gastrocnemius muscle (MG) thickness, fascicle length and pennate angles; subcutaneous fat and dermis thicknesses in the calf. RESULTS: Bilateral muscle thickness and fascicle length values were significantly lower in patients with sarcopenia (both p<0.05). Sarcopenic and nonsarcopenic subjects had similar pennate angles, subcutaneous fat and dermis thicknesses. Median thickness ratio (100 × t (MG) / [t (subcutaneous tissue) + t (dermis) + t (MG)]) values were 64% (40-88%) in the right and 64% (38-86%) in the left calf. Bilateral MG thickness and fascicle length values showed high sensitivity in predicting sarcopenia (all values > 76.92%). CONCLUSIONS: Gastrocnemius muscle thickness and fascicle length values are lower in sarcopenic elderly and these two parameters can serve as alternative measurements for predicting/quantifying sarcopenia. Calf circumference measurements alone may not be appropriate for assessing sarcopenia. Instead, US imaging can conveniently be used to evaluate different compartments of the musculoskelal system in (sarcopenic) elderly.
Keywords: Older adult; sarcopenia; gastrocnemius; fat; ultrasound; architecture
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1. INTRODUCTION Sarcopenia is a geriatric syndrome characterised by progressive and generalised loss of skeletal muscle mass and strength, with a risk of adverse outcomes such as physical disability, falls, poor quality of life and death(Cruz-Jentoft et al., 2010; Visser and Schaap, 2011). The prevalence of sarcopeniais 5-13% amongelderly aged 60-70years and11-50% after the age of80 years(Morley, 2008).The current diagnosis of sarcopenia depends on the measurement of muscle mass and function(Abellan van Kan et al., 2012; Chien et al., 2008). There are different methods for evaluating muscle mass and function but the challenge is to decide which one is the best(Cruz-Jentoft et al., 2010). Muscle architecture plays an important role in muscle functions(Blazevich et al., 2007; Mahlfeld et al., 2004). Pennation angle, fascicle length and muscle thickness are the pertinent parameters measured to assess the structural properties of muscles(Kaya et al., 2013; Scanlon et al., 2014). Further, ultrasound (US) imaging has been shown to be suitable in this regard(Blazevich et al., 2007; Thomaes et al., 2012).There are only a few studies reporting on the evaluation of muscle architecture in sarcopenic subjects and they mainly comprise comparisons between young and elderly subjects (whom were accepted to be sarcopenic without any relevant assessments)(Narici et al., 2003; Strasser et al., 2013). On the other hand, differences between sarcopenic and non-sarcopenic elderly has not been studied yet. Accordingly, the purpose of this study was two-fold; first we aimed tosonographicallyassess the muscle mass and architecture ofsarcopenic elderly subjects; and second we aimed to explore the utilityofsuch measurements in predictingsarcopenia.
2. MATERIALS AND METHODS 2.1. Study Design And Subjects
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In this cross-sectional study, 100 elderly subjects (41 M, 59 F; aged 73.08 ± 6.18 years) who admitted to the outpatient clinic of geriatric medicine were consecutively enrolled. All subjects were evaluated with medical history and standardized clinical examinations. Co-morbidities (diabetes mellitus, hypertension, coronary heart disease, osteoporosis, hyperlipidemia, hypothyroidism, lung disease, depression, atrial fibrillation) were defined reviewing current medications, using patients’ self-report and comprehensive geriatric assessment and laboratory tests. Patients with pacemaker, prosthesis, severe edema and electrolyte imbalance (owing to the possibility of incorrect measurements of bioelectrical impedance analysis (BIA)) and patients with advanced dementia and severe mobility problems (owing to the difficulties during the tests/measurements) were excluded from study. This study was approved by the local ethical committee. Subjects were informed about the study procedure and they consented participate were taken.
2.2. Comprehensive Geriatric Assessment Tests Katz index of independence in activities of daily living (ADL)(Katz, 1983), Lawton-Brody instrumental activities of daily living (IADL)(Lawton and Brody, 1969), Mini-Mental State Examination (MMSE)(Folstein et al., 1975), Mini Nutritional Assessment Tool-short form (MNA-SF)(Cohendy et al., 2001), Yesavage geriatric depression scale-short form (GDSSF)(Burke et al., 1991)and Tinetti balance test (Tinetti, 1986; Tinetti et al., 1986) were used.
2.3. Anthropometric Parameters Current weight, height, body mass index (BMI), waist, hip, bilateral mid-upper arm (MAC) and calf circumferences (CC) of all participants were measured. Body weight and height were
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measured to the nearest 0.1 kg and 0.1 cm using standardized equipment and procedures. BMI was calculated as weight (kg) divided by height squared (m2)(Janssen et al., 2002). Waist circumference (WC) was measured at mid-point between the borders of lowermost rib and the uppermost lateral border of the ilium to the nearest 0.1 cm at the end of normal expiration(Ryu et al., 2013). Hip circumference (HC) was measured horizontally at the point of largest lateral extension at the hips or over the buttocks(Carlsson et al., 2014). Mid-arm circumference (MAC) was measured to the nearest cm at the midpoint between the acromion and the olecranon process.CC was measured at the level of the largest circumference of bilateral calf, to the nearest cm (Ulger et al., 2013).
2.4. Muscle Strength Measurement Handgrip strength was evaluated with the Takei TKK 5401 Digital Handgrip Dynamometer. Three measurements of maximum strength were taken in the dominant hand, in three repetitions with a hand dynamometer, and the highest value was recorded as maximal grip strength (Halil et al., 2014).
2.5. Body Composition Bioelectrical impedance analysis (BIA) was performed by a geriatrician (MD) with a Body stat quadscan 4000 device (Florida, USA) using a multi-frequency, tetrapolar technique on the right side of the body in supine position on a non-conducting surface, with arms slightly abducted from the trunk and the legs slightly separated. Electrodes were placed on the right side of the body on the dorsal surface of the metacarpal-phalangeal and metatarsal-phalangeal joints and also medially between the distal prominences of the radius and ulna and between the medial and lateral malleoli at the ankle (Chien et al., 2008; Janssen et al., 2000).
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2.6. Defining of Sarcopenia Fat-free mass index (FFMI) for evaluation of muscle mass and handgrip strength test for muscle strength measurement were used for the diagnosis of sarcopenia. Fat-free mass index (FFMI)was measured by BIA. To estimate the cut-off value of low muscle mass, the mean and standard deviation (SD) of FFMI pertaining to young adults from our population (32 M, 29 F, aged 18-40 years) were used. These data were acquired from healthy subjects (physicians and medical personnel from our center) using the same technical methodology (i.e. BIA, timing of the day, etc.).Participants with a FFMI below 2 SD of young adults were recorded to have low muscle mass (Chien et al., 2008; Krause et al., 2012). The cut-off FFMI values of low muscle mass in our population were <17.51 kg/m2 for men and <14.52 kg/m2 for women. Poor grip strength was defined according to Cardiovascular Hearth Survey Study (CHS) criteria. For men with BMI ≤ 24, between 24.1 and 28, and>28 the cut-offpoints were 29, 30 and 32 kg respectively; and for women with BMI ≤ 23, between 23.1 and 26, between 26.1 and 29, and>29 thecut-offpointswere 17, 17.3, 18 and 21 kg respectively (Bastiaanse et al., 2012; Fried et al., 2001). Sarcopenia was defined as having both low muscle mass and poor handgrip strength after collection of all the data.
2.7. Ultrasonographic Evaluation Ultrasound (US )evaluations were performed using a 5-12 MHz linear probe (Logiq P5, General ElectricsMedicalSystems) by the same physiatrist (having a 15-year experience in musculoskeletal US), who was blinded to the study results. Measurements were performed bilaterally on the medial head of the gastrocnemius muscle (MG). Participants lied in prone position with their legs extended and their feet hanging on the side of the examination table.
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Images were obtained at the most bulky area of the MG. Muscle thickness was measured as the distance between the upper and deeper aponeurosis, pennation angle was measured as the angle of insertion of muscle fascicles into the deep aponeurosis, and fascicle length was measured as the length of the fascicular path between the superficial and deep aponeurosis (Kaya et al., 2013; Strasser et al., 2013). Additionally, thicknesses for the subcutaneous fat tissue and dermiş were measured without compression (Figure 1A-B).
2.8. LaboratoryTests Bloods were obtained from the antecubital vein between 8.30 and 10.00 am, after an over night fasting of at least 8h. Laboratory tests including complete blood count, erythrocyte sedimentation rate (ESR), alanine amino transferase (ALT), total protein, albumin, sodium (Na), potassium (K),triglyceride (TG), low-density lipoprotein (LDL), fasting plasma glucose (FPG), blood urea nitrogen (BUN), creatinine, calcium (Ca), phosphorus (P) were evaluated by a hospital auto analyzer.
2.9. Statistical Analysis SPSS (Statistical Package for Social Sciences) for Windows 15.0 program was used for statistical analysis. The variables were investigated using visual (histograms, probability plots) and analytical methods to determine whether or not they were normally distributed. Data are presented as mean±SDfor normally distributed variables and as median, (minimummaximum) for skew distributed continuous variables. Categorical variables are shown as frequencies. Pearson’s x2 method for categorical, Mann-Whitney U test for skew distributed parameters were performed for univariateanalysis. Correlation analyses were performed with Spearman
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test for not normally distributed parameters. Two-sided values of p < 0.05 were considered as statistically significant. Thickness and fascicle length of bilateral MG in predicting sarcopenia were analyzed using Receiver Operating Characteristics (ROC) curve analysis. When a significantcut-off value was observed, the sensitivity, specificity, positive predictive values(PPV) and negative predictive values (NPV) were presented. While evaluating theare aunder the curve, a 5% type1 error level was used to accept a statistically significant predictive value of the test variables. We also developed a thickness ratio (TR) as follows: 100 × t (MG) / [t (subcutaneous tissue) + t (dermis) + t (MG)]
3. RESULTS The study population was aged 73.08 ± 6.18 years. The prevalence of sarcopenia was16.0% (19.5% in males, 13.6% in females). The demographic properties, anthropometric measurements, comprehensive geriatric assessment tests and US parameters of the study population are presented in Table 1.The median age was significantly higher, body weight, BMI, handgrip, bilateral MAC and calf CC were significantly lower in patients with sarcopenia. The prevalence of osteoporosis was higher (p=0.045) and Tinetti balance test scores were significantly lower (p=0.004) in subjects with sarcopenia when compared with those without. The two groups were otherwise similar as regards co-morbidities, geriatric assessment and laboratory test results. Thickness and fascicle length of bilateral MG were significantly lower in patients with sarcopenia. There were no significant differences between the groups regarding pennate angles, subcutaneous tissue and dermis thicknesses. Median TR values were 64 % (40-88%) in the right calf and 64% (38-86%) in the left calf. These ratios were negatively correlated with body FMI (right; r:-0.537, p<0.001, left; r:-
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0.517, p<0.001), and positively correlated with handgrip strength (right; r:0.538, p<0.001, left; r:0.556, p<0.001). Optimal cut-off point for TR was found not to be able to predict sarcopenia by using ROC analyse. Fat-free mass index (FFMI) was significantly and positively correlated with handgrip strength (r:0.580, p<0.001). Correlation analyses results between parameters acquired from US evaluation with FFMI and handgrip strength are presented in Table 2. FFMI was significantly correlated with bilaterally MG and dermis thicknesses, left pennate angle and fascicle lengths. Handgrip strength was significantly correlated with bilaterally MG and subcutaneous tissue thicknesses and fascicle lengths. ROC curve analyses are given in Table 3 and Figure 2. Both MG thickness and fascicle length(but not TR ratio) values showed high sensitivity in predicting sarcopenia.
4. DISCUSSION The aim of our study was to sonographically evaluate muscular and nonmuscular calf compartments in sarcopenic elderly subjects. Our results have shown that nonmuscular compartments might constitute significant proportion of the calf thickness and that the thickness and fascicle length of MG were significantly lower in elderly with sarcopenia. To the best knowledge of the authors, this is the first study whereby US imaging has been used to substantially assess the calf of elderly subjects who had sarcopenia according to European Working Group on Sarcopenia in Older People (EWGSOP) criteria. Sarcopenia is a common clinical problem in elderly and leads to severe adverse outcomes(Janssen et al., 2002; Ryu et al., 2013).It has been defined as the loss of skeletal muscle mass and strength with aging. However, until recently, there has been no widely accepted definition. EWGSOP proposed that sarcopenia is diagnosed using the criteria of low muscle mass and low muscle function (either low strength and/or low physical
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performance)(Cruz-Jentoft et al., 2010).Similarly, in the relevant literature, there are various ways (based on cut-off values) to diagnose sarcopenia. Owing to the differences among populations, these values might not be used uniformly worldwide. For instance, while according to the CHS criteria, 16 subjects were diagnosed with sarcopenia; only 8 could have been diagnosed as such according to Foundation for the National Institutes of Health (FNIH) criteria (Dam et al., 2014; Studenski et al., 2014). Even this difference alone can indicate the need for more precise definitions for cut-off values –or the necessity for better methods (e.g. imaging) in the diagnosis of sarcopenia. The function of skeletal muscle is directly determined by its architecture 31, 32. In this regard, muscle thickness, fascicle length and pennation angle are used to evaluate the structural properties of muscular tissues(Scanlon et al., 2014; Strasser et al., 2013).Although magnetic resonance imaging and computed tomography (CT) are the gold standards to measure cross sectional area and composition of muscles, the aforementioned parameters can not be assessed by these imaging methods. Further, cost and radiation exposure might be the other challenging issues for the imaging of elderly subjects. As such, owing to its advantages i.e. cost-effective, convenient, patient/physician-friendly, US imaging has appeared in the recent years for prompt and detailed evaluation of various musculoskeletal tissues (Blazevich et al., 2007; Kaya et al., 2013; Malas et al., 2014).In this regard, we have used sonographic evaluation for measuring the thickness of the skin, subcutaneous fat and the thickness and architectural parameters of the MG. The reason why we have used the calf area was to diligently compare the US measurements with those of commonly applied/suggested anthropometric parameters for predicting sarcopenia. Previously, Narici et al.(Narici et al., 2003)evaluated the effect of aging on human MG architecture by comparing morphometric measurements on 14 young (aged 27-42 year) and 16 older (aged 70-81 year) physically active men using CT and US imaging. They have found
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that the cross-sectional area, volume, fascicle length and pennation angle of MG were significantly lower in the older group. In another study, Strasser et al.(Strasser et al., 2013)compared US parameters (quadriceps femoris muscle thickness, pennation angle and echogenicity) in 26 young (aged 24.2±3.7 years) and 26 old (aged 67.8±4.8 years) patients. They have found decreased muscle thickness and pennation angles with increased muscle echogenicity. Inboth studies, young adults and elderly subjects were compared and the elderly were considered/accepted to have sarcopenia. On the other hand, we have used EWGSOP criteria for diagnosis of sarcopenia and compared the two groups of sarcopenic vs nonsarcopenic elderly. Since bilateral MG thickness and fascicle length values were found to be lower in the sarcopenic group, our preliminary results indicate that these two parameters seem to be predominantly affected during the process of sarcopenia in the elderly. Further, we propose that those values can also be used to predict sarcopenia with high sensitivity. Concerning the CC measurements, previous studies have reported that they can be used as indirect ways of muscle assessment (Baumgartner et al., 1998; Rolland et al., 2003). However, depending on the country and population, the results and the cut-off values can vary, and actually be quite conflicting (Halil et al., 2014; Kawakami et al., 2014). Herewith, our findings of calf thickness measurements provide another strong argument not to use these values for predicting muscle mass. Yet, the TR in the calf region was decreased as low as 38%. Overall, considering the fact that the increased fat tissue or edema in the subcutaneous fat layer might well contribute to fallacious CC values, we strongly deem the use of such a ratio in light of our US measurements that are noteworthy for actual assessment of the calf compartment. On the other hand, in contrast to above quoted muscle architecture values, TRs were found not to be able to predict sarcopenia. Another interesting finding of our study is the fact that handgrip strength values were correlated more strongly with subcutaneous fat when compared with MG thicknesses. At this
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point, one speculation would be that fat deposition might be more uniform throughout the body and better reflecting a subject’s overall activity (thus possibly performance at another region as well)than single/another region’s muscle strength. One limitation of our study might be attributed to the relatively small sample size of our study population. Herewith, a more important concern would be the definite need for larger samples in order to describe sensitivity/specificity values for sarcopenia prediction. Another relative limitation could be the lack of other measures for Daily activities which would have possibly reflected low values in sarcopenic subjects (while Katz did not). 5. CONCLUSION To summarize, in the light of our first and preliminary findings, we arrive in the following conclusions. First, CC measurements may not be appropriate for assessing sarcopenia; second, thickness and fascicle length values of MG are lower in sarcopenic elderly and these two parameters can serve as alternative measurements for diagnosing/quantifying sarcopenia. Third, ratios calculated by the use of US measurements might better serve to evaluate the calf muscle mass. Last but not least, US imaging can safely/conveniently be used to evaluate different compartments of the musculoskeletal system in (sarcopenic) elderly.
CONFLICT OF INTEREST The authors have no financial or any other kind of personal conflicts with this paper and any relation with a funding.
Author Contributions: MEK, designed the study, supervised the data collection, carried out the statistical analysis and wrote the paper. MH, designed the study, supervised the data collection, carried out the statistical analysis and wrote the paper. OK, supervised the data
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collection, carried out the statistical analysis. BC, GC and SG, supervised the data collection and protocol development. YY, carried out the statistical analysis, perfromed figures. GA, supervised the data collection. BBY and MC, designed the study and assisted with writing the paper. LÖ, designed the study, performed the ultrasonographic evaluation and assisted with writing the paper. Sponsor’s Role: None.
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REFERENCES Abellan van Kan, G., Houles, M., Vellas, B., 2012. Identifying sarcopenia. Curr Opin Clin Nutr Metab Care 15, 436-441. Bastiaanse, L.P., Hilgenkamp, T.I., Echteld, M.A., Evenhuis, H.M., 2012. Prevalence and associated factors of sarcopenia in older adults with intellectual disabilities. Res Dev Disabil 33, 2004-2012. Baumgartner, R.N., Koehler, K.M., Gallagher, D., Romero, L., Heymsfield, S.B., Ross, R.R., Garry, P.J., Lindeman, R.D., 1998. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147, 755-763. Blazevich, A.J., Cannavan, D., Coleman, D.R., Horne, S., 2007. Influence of concentric and eccentric resistance training on architectural adaptation in human quadriceps muscles. J Appl Physiol (1985) 103, 1565-1575. Burke, W.J., Roccaforte, W.H., Wengel, S.P., 1991. The short form of the Geriatric Depression Scale: a comparison with the 30-item form. J Geriatr Psychiatry Neurol 4, 173178. Carlsson, A.C., Wändell, P., Riserus, U., Arnlöv, J., Borné, Y., Engström, G., Leander, K., Gigante, B., Hellénius, M.L., de Faire, U., 2014. Differences in anthropometric measures in immigrants and Swedish-born individuals: Results from two community-based cohort studies. Prev Med 69C, 151-156. Chien, M.Y., Huang, T.Y., Wu, Y.T., 2008. Prevalence of sarcopenia estimated using a bioelectrical impedance analysis prediction equation in community-dwelling elderly people in Taiwan. J Am Geriatr Soc 56, 1710-1715. Cohendy, R., Rubenstein, L.Z., Eledjam, J.J., 2001. The Mini Nutritional Assessment-Short Form for preoperative nutritional evaluation of elderly patients. Aging (Milano) 13, 293-297. Cruz-Jentoft, A.J., Baeyens, J.P., Bauer, J.M., Boirie, Y., Cederholm, T., Landi, F., Martin, F.C., Michel, J.P., Rolland, Y., Schneider, S.M., Topinková, E., Vandewoude, M., Zamboni, M., People, E.W.G.o.S.i.O., 2010. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 39, 412-423. Dam, T.T., Peters, K.W., Fragala, M., Cawthon, P.M., Harris, T.B., McLean, R., Shardell, M., Alley, D.E., Kenny, A., Ferrucci, L., Guralnik, J., Kiel, D.P., Kritchevsky, S., Vassileva, M.T., Studenski, S., 2014. An evidence-based comparison of operational criteria for the presence of sarcopenia. J Gerontol A Biol Sci Med Sci 69, 584-590. Folstein, M.F., Folstein, S.E., McHugh, P.R., 1975. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12, 189-198. Fried, L.P., Tangen, C.M., Walston, J., Newman, A.B., Hirsch, C., Gottdiener, J., Seeman, T., Tracy, R., Kop, W.J., Burke, G., McBurnie, M.A., Group, C.H.S.C.R., 2001. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 56, M146-156. Halil, M., Ulger, Z., Varlı, M., Döventaş, A., Oztürk, G.B., Kuyumcu, M.E., Yavuz, B.B., Yesil, Y., Tufan, F., Cankurtaran, M., Saka, B., Sahin, S., Curgunlu, A., Tekin, N., Akçiçek, F., Karan, M.A., Atlı, T., Beger, T., Erdinçler, D.S., Arıoğul, S., 2014. Sarcopenia assessment project in the nursing homes in Turkey. Eur J Clin Nutr. Janssen, I., Heymsfield, S.B., Baumgartner, R.N., Ross, R., 2000. Estimation of skeletal muscle mass by bioelectrical impedance analysis. J Appl Physiol 89, 465-471. Janssen, I., Heymsfield, S.B., Ross, R., 2002. Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 50, 889-896. Katz, S., 1983. Assessing self-maintenance: activities of daily living, mobility, and instrumental activities of daily living. J Am Geriatr Soc 31, 721-727. 15
Kawakami, R., Murakami, H., Sanada, K., Tanaka, N., Sawada, S.S., Tabata, I., Higuchi, M., Miyachi, M., 2014. Calf circumference as a surrogate marker of muscle mass for diagnosing sarcopenia in Japanese men and women. Geriatr Gerontol Int. Kaya, A., Kara, M., Tiftik, T., Tezcan, M.E., Ozel, S., Ersöz, M., Göker, B., Haznedaroğlu, S., Ozçakar, L., 2013. Ultrasonographic evaluation of the muscle architecture in patients with systemic lupus erythematosus. Clin Rheumatol 32, 1155-1160. Krause, K.E., McIntosh, E.I., Vallis, L.A., 2012. Sarcopenia and predictors of the fat free mass index in community-dwelling and assisted-living older men and women. Gait Posture 35, 180-185. Lawton, M.P., Brody, E.M., 1969. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist 9, 179-186. Mahlfeld, K., Franke, J., Awiszus, F., 2004. Postcontraction changes of muscle architecture in human quadriceps muscle. Muscle Nerve 29, 597-600. Malas, F., Kara, M., Kaymak, B., Akıncı, A., Özçakar, L., 2014. Ultrasonographic evaluation in symptomatic knee osteoarthritis: clinical and radiological correlation. Int J Rheum Dis 17, 536-540. Morley, J.E., 2008. Sarcopenia: diagnosis and treatment. J Nutr Health Aging 12, 452-456. Narici, M.V., Maganaris, C.N., Reeves, N.D., Capodaglio, P., 2003. Effect of aging on human muscle architecture. J Appl Physiol (1985) 95, 2229-2234. Rolland, Y., Lauwers-Cances, V., Cournot, M., Nourhashémi, F., Reynish, W., Rivière, D., Vellas, B., Grandjean, H., 2003. Sarcopenia, calf circumference, and physical function of elderly women: a cross-sectional study. J Am Geriatr Soc 51, 1120-1124. Ryu, M., Jo, J., Lee, Y., Chung, Y.S., Kim, K.M., Baek, W.C., 2013. Association of physical activity with sarcopenia and sarcopenic obesity in community-dwelling older adults: the Fourth Korea National Health and Nutrition Examination Survey. Age Ageing 42, 734-740. Scanlon, T.C., Fragala, M.S., Stout, J.R., Emerson, N.S., Beyer, K.S., Oliveira, L.P., Hoffman, J.R., 2014. Muscle architecture and strength: adaptations to short-term resistance training in older adults. Muscle Nerve 49, 584-592. Strasser, E.M., Draskovits, T., Praschak, M., Quittan, M., Graf, A., 2013. Association between ultrasound measurements of muscle thickness, pennation angle, echogenicity and skeletal muscle strength in the elderly. Age (Dordr) 35, 2377-2388. Studenski, S.A., Peters, K.W., Alley, D.E., Cawthon, P.M., McLean, R.R., Harris, T.B., Ferrucci, L., Guralnik, J.M., Fragala, M.S., Kenny, A.M., Kiel, D.P., Kritchevsky, S.B., Shardell, M.D., Dam, T.T., Vassileva, M.T., 2014. The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci 69, 547-558. Thomaes, T., Thomis, M., Onkelinx, S., Coudyzer, W., Cornelissen, V., Vanhees, L., 2012. Reliability and validity of the ultrasound technique to measure the rectus femoris muscle diameter in older CAD-patients. BMC Med Imaging 12, 7. Tinetti, M.E., 1986. Performance-oriented assessment of mobility problems in elderly patients. J Am Geriatr Soc 34, 119-126. Tinetti, M.E., Williams, T.F., Mayewski, R., 1986. Fall risk index for elderly patients based on number of chronic disabilities. Am J Med 80, 429-434. Ulger, Z., Halil, M., Cankurtaran, M., Yavuz, B.B., Yesil, Y., Kuyumcu, M.E., Gungor, E., İzgi, H., İskit, A.T., Abbasoglu, O., Ariogul, S., 2013. Malnutrition in Turkish nursing homes: a correlate of short term mortality. J Nutr Health Aging 17, 305-309. Visser, M., Schaap, L.A., 2011. Consequences of sarcopenia. Clin Geriatr Med 27, 387-399.
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Figure captions
Figure 1. Comparative ultrasound imaging of the calf region. On the axial view (A); dermis (a), subcutaneous fat (b) and medial head of the gastrocnemius muscle thickness measurements are illustrated. On the longitudinal view (B); fascicle length and pennation angle measurements are exemplified from the medial head of the gastrocnemius muscle.
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Figure 2. ROC analyses results of bilateral gastrocnemius muscle thickness (MGT) and fascicle length (FL) values in predicting sarcopenia. (L: Left, R: Right)
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Tables Table 1. Demographic properties, anthropometric measurements, comprehensive geriatric assessment tests and US parameters of the study population Parameters Demographic and
Sarcopenic (n:16)
Non-sarcopenic(n:84)
p
Age (year)
77.50 (71-88)
70.50 (65-85)
<0.001*
Gender (M/F)
8 (%19.50)/ 8(%13.60)
33 (%39.30) /51 (%60.70)
0.425
Height (cm)
156 (141-174)
159 (141-180)
0.402
Weight (kg)
65 (49-87)
73 (44-115)
0.002*
BMI (kg/m2)
24.50 (20.20-41.40)
28.75 (21.20-45.70)
0.006*
Handgripstrenght
20.25 (14.40-28.50)
24.60 (13.50-48.80)
0.004*
WC (cm)
92 (59-110)
101 (55-125)
0.009*
HC (cm)
108 (51-129)
107 (87-133)
0.576
Right MAC (cm)
26.75 (22-34)
29 (22-42.50)
0.027*
Left MAC (cm)
26.25 (21-35)
29 (21-43.50)
0.045*
Right CC (cm)
34 (26-42)
37 (27-47)
0.014*
Left CC (cm)
33 (25-40)
36.50 (27.50-47)
0.009*
Katz-ADL
6 (2-6)
6 (4-6)
0.597
LB-IADL
17 (0-17)
17 (7-17)
0.403
MNA-SF
14 (2-14)
14 (8-14)
0.230
MMSE GDS-SF
29 (18-30) 0 (0-9)
29 (11-30) 0 (0-11)
0.149 0.354
Tinetti Number of drugusage
16 (0-16) 4 (1-11)
16 (4-16) 4 (0-12)
0.004* 0.352
R-DermisThickness (cm) L-DermisThickness (cm) R-SCT Thickness (cm) L-SCT Thickness (cm) R-MG Thickness (cm)
0.12 (0.07-0.18)
0.12 (0.06-0.18)
0.617
0.11 (0.07-0.18)
0.12 (0.07-0.22)
0.802
0.71 (0.58-1.87)
0.75 (0.14-1.78)
0.307
0.72 (0.57-1.90)
0.75 (0.19-2.13)
0.442
1.50 (1.16-1.69)
1.80 (1.12-2.56)
<0.001*
L-MG Thickness (cm)
1.53 (1.08-1.79)
1.75 (1.01-2.64)
0.001*
R-MG FL (cm)
3.46 (2.11-4.55)
4.07 (2.98-5.94)
0.002*
L-MG FL (cm)
3.19 (2.72-4.49)
3.99 (2.85-6.21)
0.001*
R-PennateAngle
23.40 (18-37.50)
25.40 (18.30-38.20)
0.116
L-PennatAngle
24.30 (15.80-42.30)
22.90 (14.70-40.00)
0.386
Anthropometric Parameters
(kg)
Comprehensive Geriatric Assessment Tests
US parameters
M/F: Male/Female, BMI: Body mass index, WC: Waist circumference, HC: Hip circumference, MAC: Mid-arm circumference, CC: Calf circumference, ADL: Activities of Daily living, IADL: Lawton-Brody instrumental
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activities of daily living, MNA-SF: Mini Nutritional Assessment Tool-short form, MMSE: Mini-Mental State Examination, GDS-SF: Yesavage geriatric depression scale-short form, R: Right, L: Left, SCT: Subcutaneustissue, MG: Musculus gastrocnemius, FL: Fascicle length, * Statistically significant differences
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Table 2. Correlation analysis results between US parameters with FFMI and handgrip strength US Parameters
FFMI
R-MG Thickness L-MG Thickness R-MG FL L-MG FL R-PennateAngle L-PennateAngle R-DermisThickness L-DermisThickness R-SCT Thickness L-SCT Thickness
r 0.590 0.454 0.522 0.438 -0.061 -0.231 0.297 0.267 -0.211 -0.214
Handgripstrength P <0.001* <0.001* <0.001* <0.001* 0.587 0.035* 0.009* 0.019* 0.065 0.061
r 0.363 0.355 0.422 0.349 0.001 -0.097 0.180 0.196 -0.471 -0.465
P 0.001* 0.001* <0.001* 0.001* 0.996 0.381 0.118 0.085 <0.001* <0.001*
US: Ultrasound, FFMI: Fat-free mass index, R: Right, L: Left, SCT: Subcutaneus tissue, MG: Musculus gastrocnemius, FL: Fascicle length, * Statistically significant differences
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Table 3. ROC analysis results of US parameters in predicting sarcopenia Parameters
AUC
Sensitivity
Specificity
PPV
NPV
R-MG Thickness (1.69 cm)
0.833
100.00
64.56
31.70
100.00
L-MG Thickness (1.71 cm)
0.784
92.31
52.56
24.50
97.60
R-MG FL (3.62 cm)
0.775
76.92
70.51
30.30
94.80
L-MG FL (3.47 cm)
0.799
76.92
80.77
24.50
97.60
R: Right, L: Left, SCT: Subcutaneus tissue, MG: Musculus gastrocnemius, FL: Fascicle length, AUC: Area under curve, PPV: Positive predictive value, NPV: Negative predictive values
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