Both acute injury or illness and chronic conditions (eg, chronic kidney disease, congestive heart failure, or cancer) are commonly associated with weight loss in dogs and cats.1 However, weight loss in these conditions is unlike weight loss in healthy animals. In healthy animals, weight loss is primarily attributable to loss of fat tissue, whereas lean body mass is the primary body compartment affected during weight loss associated with illness or injury. Muscle loss associated with disease is termed cachexia, whereas sarcopenia is a related condition involving muscle loss associated with aging in the absence of disease.1 Because muscle is functional tissue, cachexia and sarcopenia can adversely impact strength, immune function, wound healing, and mortality rates.1,2
One of the biggest challenges in addressing cachexia and sarcopenia is recognition and early diagnosis of the conditions. An MCS system has been validated for use in cats and dogs, and it is recommended by national and international organizations as a component of nutritional assessment for dogs and cats.3–5 Muscle condition scoring is ideal for clinical use in dogs and cats because it can be quickly and easily performed. However, it may not be precise enough as an outcome measure for research studies wherein quantification of muscle mass over time is needed, particularly when the changes in muscle mass are small.
Quantitative methods for assessment of lean body mass or muscle mass in humans include dual-energy x-ray absorptiometry and bioelectrical impedance,6 but inherent assumptions for each of these methods reduce their accuracy. Computed tomography is another method for measurement of muscle mass; however, companion animals must be sedated or anesthetized for both dual-energy x-ray absorptiometry and CT.7,8 Therefore, research on cachexia and sarcopenia in companion animals would benefit from more clinically relevant measures of muscle mass.
Ultrasonography is a method for quantification of muscle mass in dogs and cats that does not typically require that animals be sedated or anesthetized. Ultrasonographic measurement of muscle has been used to assess muscle loss in humans,9,10 healthy dogs,7,11 cats,12 and dogs with various degrees of cachexia and sarcopenia.13 However, ultrasonographic techniques have not been validated for assessment of muscle mass in cats with cachexia and sarcopenia. Therefore, the objectives of the study reported here were to assess the convergent validity between MCS and ultrasonographic measurements in cats with various degrees of muscle loss as well as to evaluate the repeatability and reproducibility of MCS assessment in this population of cats.
Materials and Methods
Animals
Forty cats with naturally acquired chronic medical conditions (eg, kidney disease, cardiac disease, cancer, and hepatic disease) were included in the study. Cats represented a wide range of ages, BCSs, and MCSs. The study was performed with cats that lived at the Nestlé Purina PetCare facility. The protocol was reviewed and approved by the Nestlé Purina PetCare Animal Care and Use Committee.
Experimental procedures
A prospective cross-sectional study was performed. Data regarding body weight, BCS, MCS, ultrasonographic measurement of epaxial muscle, thoracic radiographic findings, and forelimb circumference measurement were assessed for each cat.
Body weight and BCS—Body weight was recorded to the nearest 0.01 kg by use of a calibrated scale. The BCS was measured by use of a 9-point scoring system.14
MCS—Five raters (2 investigators [LMF and KEM], 1 additional veterinarian, and 2 animal technicians) participated in the study. The 2 investigators trained the other raters on use of the MCS system. This system was used to score muscle mass as normal muscle mass or mild, moderate, or severe muscle loss.15 Each of the 5 raters then evaluated and scored all 40 cats 3 separate times over a 1- to 2-day period. The order of evaluation was randomly assigned among raters and for each scoring session for each rater by use of an online random number generator.a
Ultrasonographic measurement of epaxial muscle—Ultrasonographic measurements were obtained at the level of T13 by use of an ultrasound machineb with a 5- to 12-MHz linear transducerc and a previously described method.11,12 Briefly, unsedated cats were manually restrained in a standing or crouching position (position was dependent on the preference of the cat; position does not affect the results12), the hair was shaved over the dorsum at the level of T13, and ultrasonography gel was applied to the shaved area. The transducer was placed at T13 with the beam angle perpendicular to the axis of the vertebral column; minimal pressure was used to avoid distorting the shape of the tissues. Measurements of EMH were obtained with the calipers of the ultrasound machine; the first cursor was placed at the junction of the 13th rib and T13 at the bone-muscle interface, and the second cursor was placed dorsolaterally at the muscle-subcutaneous tissue interface. The angle of this measurement was intended to provide the shortest distance between these 2 landmarks. Three measurements (a separate placement of the probe for each measurement) of the maximal height of the right epaxial muscle were obtained, and the mean of the 3 measurements was used as the final value for muscle height. Muscle height of all cats was measured by 1 investigator (JF).
Thoracic radiography and morphometric measurement—Lateral thoracic radiographs were obtained for all cats. Length of T4 was measured by a single investigator (JF) and used to calculate a ratio of the muscle height at T13 to T4 length (ie, VEMS). The VEMS was used to standardize muscle measurements across cats of various shapes and sizes, as described elsewhere.11–13 In addition, the forelimb circumference was measured by a single investigator (LMF) at the midpoint between the carpus and elbow joint. This technique has been validated for use in cats and dogs as an alternative to the use of T4 length, and the value is defined as the FLEMS.12,13
Statistical analysis
Data distributions were evaluated by means of visual inspection and the Shapiro-Wilk test. The data were normally distributed; thus, data are reported as mean ± SD. For analyses, MCS categories were converted to numeric values as follows: 3 = normal muscle mass, 2 = mild muscle loss, 1 = moderate muscle loss, and 0 = severe muscle loss. Relationships between MCS, VEMS, FLEMS, and body weight were tested with Spearman correlation analyses. Interrater agreement (reproducibility) and intrarater agreement (repeatability) were assessed with the κ statistic. Agreement on the basis of the κ coefficient was interpreted as fair (κ = 0.21 to 0.40), moderate (κ = 0.41 to 0.60), substantial (κ = 0.61 to 0.80), or almost perfect (κ = 0.81 to 1.00). Analyses were performed with commercially available software.d Results were considered significant at a value of P ≤ 0.05.
Results
Forty cats were enrolled in the study, including 28 males (all castrated) and 12 females (all spayed). Mean ± SD age was 10.3 ± 3.9 years. Of the 40 cats, 24 had at least 1 chronic medical condition, and 16 of these 24 cats had > 1 chronic medical condition.
Mean ± SD body weight was 3.99 ± 1.04 kg (range, 2.31 to 6.03 kg), and mean BCS was 5 ± 2 (range, 1 to 9). Eighteen (45%) cats had a BCS > 5; all 9 cats that weighed > 4.75 kg had a BCS > 5. The mean of the MCSs as assigned by 2 investigators (LMF and KEM) indicated normal muscle mass for 10 cats, mild muscle loss for 11 cats, moderate muscle loss for 8 cats, and severe muscle loss for 11 cats. Nine of the 30 (30%) cats with muscle loss had a BCS > 5. Cats with a medical condition were significantly (P = 0.03) more likely to have muscle loss. There was no significant difference between male and female cats with regard to muscle loss (P = 0.99), MCS (P = 0.56), or BCS (P = 0.55). A significant inverse correlation was identified between age and body weight (r = −0.43; P = 0.006), age and BCS (r = −0.60; P < 0.001), and age and MCS (r = −0.71; P < 0.001; Table 1); thus, with an increase in age, body weight and BCS decreased and MCS worsened. The BCS was significantly (P < 0.001) positively correlated with MCS (r = 0.78). Body weight was also significantly positively correlated with BCS (r = 0.76; P < 0.001) and MCS (r = 0.58; P < 0.001).
Correlations (r) between age, body weight, BCS, and variables used to assess muscle mass in 40 cats with various degrees of muscle loss.
Variable | Age | Body weight | BCS | MCS | EMH | VEMS | FLEMS |
---|---|---|---|---|---|---|---|
Age | — | r = −0.43 | r = −0.60 | r = −0.71 | r = −0.51 | r = −0.55 | r = −0.45 |
— | P = 0.006 | P < 0.001 | P < 0.001 | P = 0.001 | P < 0.001 | P = 0.004 | |
Body weight | r = −0.43 | — | r = 0.76 | r = 0.58 | r = 0.87 | r = 0.65 | r = 0.41 |
P = 0.006 | — | P < 0.001 | P < 0.001 | P < 0.001 | P < 0.001 | P = 0.009 | |
BCS | r = −0.60 | r = 0.76 | — | r = 0.78 | r = 0.69 | r = 0.64 | r = 0.35 |
P < 0.001 | P < 0.001 | — | P < 0.001 | P < 0.001 | P < 0.001 | P = 0.026 | |
MCS | r = −0.71 | r = 0.58 | r = 0.78 | — | r = 0.60 | r = 0.66 | r = 0.41 |
P < 0.001 | P < 0.001 | P < 0.001 | — | P < 0.001 | P < 0.001 | P = 0.009 | |
EMH | r = −0.51 | r = 0.87 | r = 0.69 | r = 0.60 | — | r = 0.88 | r = 0.68 |
P = 0.001 | P < 0.001 | P < 0.001 | P < 0.001 | — | P < 0.001 | P < 0.001 | |
VEMS | r = −0.55 | r = 0.65 | r = 0.64 | r = 0.66 | r = 0.88 | — | r = 0.79 |
P < 0.001 | P < 0.001 | P < 0.001 | P < 0.001 | P < 0.001 | — | P < 0.001 | |
FLEMS | r = −0.45 | r = 0.41 | r = 0.35 | r = 0.41 | r = 0.68 | r = 0.79 | — |
P = 0.004 | P = 0.009 | P = 0.026 | P = 0.009 | P < 0.001 | P < 0.001 | — |
— = Not applicable.
Mean ± SD EMH as measured ultrasonographically was 1.02 ± 0.15 cm, mean VEMS was 0.94 ± 0.12, and mean FLEMS was 1.28 ± 0.17. Mean values for EMH, VEMS, and FLEMS were determined for each MCS category (Table 2). Body weight was significantly positively correlated with EMH (r = 0.87; P < 0.001), VEMS (r = 0.65; P < 0.001), and FLEMS (r = 0.41; P = 0.009; Table 1). The VEMS and FLEMS were significantly (P < 0.001) positively correlated with each other (r = 0.79). Age was significantly inversely correlated with EMH (r = −0.51; P = 0.001), VEMS (r = −0.55; P < 0.001), and FLEMS (r = −0.45; P = 0.004). The BCS was significantly correlated with EMH (r = 0.69; P < 0.001), VEMS (r = 0.64; P < 0.001), and FLEMS (r = 0.35; P = 0.03). The MCS was significantly (P < 0.001) correlated with EMH (r = 0.60; Figure 1). The MCS was also significantly correlated with VEMS (r = 0.66; P < 0.001) and FLEMS (r = 0.41; P = 0.009).
Mean ± SD values for EMH, VEMS, and FLEMS for 40 cats with various degrees of muscle loss as assessed on the basis of the MCS.
MCS | |||||
---|---|---|---|---|---|
Variable | All cats (n = 40) | Normal muscle mass (n = 10) | Mild muscle loss (n = 11) | Moderate muscle loss (n = 8) | Severe muscle loss (n = 11) |
EMH (cm) | 1.02 ± 0.15 | 1.13 ± 0.14 | 1.07 ± 0.12 | 0.99 ± 0.13 | 0.89 ± 0.12 |
VEMS | 0.94 ± 0.12 | 1.02 ± 0.08 | 0.99 ± 0.09 | 0.91 ± 0.10 | 0.82 ± 0.09 |
FLEMS | 1.28 ± 0.17 | 1.34 ± 011 | 1.36 ± 0.19 | 1.22 ± 0.11 | 1.19 ± 0.19 |
Muscle condition scores were assigned in accordance with the World Small Animal Veterinary Association nutritional assessment guidelines.15
Interrater agreement (reproducibility) of MCS assessments among the 5 raters yielded an overall κ value of 0.43. Differences were observed for this value depending on the degree of muscle loss (normal muscle mass, κ = 0.58; mild muscle loss, κ = 0.25; moderate muscle loss, κ = 0.25; and severe muscle loss, κ = 0.62; all P < 0.001). Overall, the mean intrarater κ value (repeatability) for the 5 raters was 0.43 (range, 0.49 to 0.76), which indicated moderate agreement. The range of intrarater κ values was 0.53 to 0.89 for cats with normal muscle mass, 0.19 to 0.60 for cats with mild muscle loss, 0.36 to 0.63 for cats with moderate muscle loss, and 0.65 to 0.87 for cats with severe muscle loss (all P < 0.001).
Discussion
Epaxial muscle height, measured ultrasonographically, may be a suitable quantitative method for assessing muscle mass in cats with various MCSs, as has been determined for healthy dogs11 and cats12 as well as dogs with muscle loss with various MCSs.13 In the study reported here, as expected, EMH was significantly associated with body weight. However, normalization of EMH on the basis of T4 length (VEMS) and forelimb circumference (FLEMS) did not eliminate the correlation with body weight (ie, VEMS and FLEMS were significantly correlated with body weight), which suggested that the use of T4 length or forelimb circumference did not effectively normalize EMH among cats of various body weights. This was in contrast to results of studies of healthy dogs11 and cats12 as well as dogs with muscle loss13 in which VEMS and FLEMS were not significantly correlated with body weight.
One possible reason for these findings is that the sample of cats in the present study had a much narrower range of body weights, compared with the range of body weights for cats in a previous study12 involving use of this method, which may have been attributable to this population of cats with medical conditions. The 2 studies11,13 of dogs included subjects with a wide range of body weights (1.5 to 38.8 kg). Even in the previous study12 conducted to validate this method in healthy cats, investigators enrolled cats with a BCS between 4 and 6 (scale of 1 to 9) to avoid inclusion of thin or overweight cats, but those cats had a wider range in body weight (2.23 to 8.05 kg) than did the cats of the present study (2.31 to 6.03 kg).
In the present study, cats of any size or BCS were eligible for inclusion, but it appeared that the heaviest cats were overweight (all cats > 4.75 kg were overweight). This suggested that heavier cats were more overweight and that the true range of body sizes represented in the study was relatively narrow. In addition, in the studies11,13 of dogs, T4 length ranged from 0.69 to 2.71 cm, and in the previous study12 of healthy cats, T4 length ranged from 0.88 to 1.49 cm. In the study reported here, T4 length ranged from 0.95 to 1.23 cm. Therefore, EMH was divided by a denominator of approximately 1 cm, which did not normalize the EMH as effectively as in previous studies. The FLEMS in the study reported here was also associated with body weight, which suggested that dividing EMH by the forelimb circumference was not an effective method for normalizing the EMH across cats of various body weights. The reasons for this may have included many of the aforementioned reasons but also the imprecision of measurements of the forelimb circumference owing to the cats’ coats.
Also, in contrast to results of all 3 previous studies11–13 involving ultrasonography of muscle mass in dogs and cats, body weight in the present study was significantly positively correlated with measurements of muscle mass (MCS, EMH, VEMS, and FLEMS), which suggested that lighter cats were more likely to have muscle loss than were heavier cats. Lighter cats may be more likely to lose muscle because they have less fat to lose, which may be related to a phenomenon called the obesity paradox. The risk of death in humans with chronic heart failure is lowest for overweight patients and highest for underweight patients.16 A similar finding has been noted for cats with cardiac disease17 and cats with chronic kidney disease.18 It is thought that this beneficial effect is not due to the excess adipose tissue per se, but rather to the increased reserve of lean body mass typically associated with obesity (when a subject gains weight, approx 75% of the excess tissue is fat and approx 25% is lean). This is not always the case, as illustrated by the fact that 30% of the cats with muscle loss were overweight. However, overweight cats may have also had more lean tissue so that muscle loss did not impact them as markedly.
Given the large overlap of EMH, VEMS, and FLEMS data in the study reported here, use of these measurements would likely not be suitable for diagnosis of cachexia in cats, as opposed to results of a study13 involving dogs, in which cutoff values for VEMS and FLEMS were determined that could be used to identify mild muscle loss. Instead, EMH may be more appropriate for monitoring muscle mass in cats over time for care of individual animals or as an end point for clinical interventions targeting muscle. It may be that EMH alone is the most appropriate measurement to use for monitoring muscle mass in cats over time. However, prospective studies are needed to evaluate the use of EMH, VEMS, and FLEMS for monitoring muscle mass in cats over time.
Similar to results of comparable studies of dogs13 and cats3 with various degrees of muscle loss, results of the study reported here indicated good repeatability of MCS assessment but only moderate reproducibility. Repeatability and reproducibility of measurements were highest for cats with normal muscle mass or severe muscle loss, whereas measurements for cats with mild or moderate muscle loss had lower agreement. These findings were similar to those from previous studies conducted to validate use of the MCS system in dogs13 and cats.3 Additional training could increase reproducibility, which would be important for studies that involve the use of the MCS as an outcome variable as well as for clinical use of the MCS system. Although the originally validated MCS system was numeric,3 we and the World Small Animal Veterinary Association nutritional assessment guidelines15 currently recommend avoiding the use of numbers and instead recommend the terms used in the present study (ie, normal muscle mass, mild muscle loss, moderate muscle loss, or severe muscle loss.) Not all clinicians use the same numeric system (some use MCS = 3 as severe muscle loss, whereas others use MCS = 3 as normal muscle mass); therefore, the use of terms, rather than numbers, can help to avoid confusion. This was the approach used in the present study, although the descriptive terms were converted to numbers for statistical analysis.
Although the MCS is a subjective assessment of overall muscle mass and ultrasonographic EMH assessment measures the height of 1 specific muscle group, we found that the MCS was significantly correlated with the more quantitative ultrasonographic measurement of EMH. This suggested that the MCS system used in the present study was a reasonable, clinically relevant method for assessing overall muscle mass in cats.
In the present study, age was significantly and inversely correlated with various measurements of muscle mass (ie, MCS, EMH, VEMS, and FLEMS). This was consistent with findings in humans and companion animals that indicate a loss of lean body mass and muscle mass occurs with aging (sarcopenia).19,20 However, it is unclear whether the muscle loss is attributable to aging alone, diseases associated with aging (eg, chronic kidney disease, heart failure, or cancer), or a combination of these things.
Values obtained with the BCS system, which is an assessment of fat, and the MCS system, which is an assessment of muscle, were correlated in the present study, but they are not directly related. For example, a cat could be obese and have severe muscle loss, or a cat could be thin but have normal muscle condition. In the present study, 9 of 30 (30%) cats with muscle loss were overweight (BCS > 5/9), and muscle loss was seen among all BCSs. Although BCS was significantly associated with MCS, EMH, VEMS, and FLEMS, it is important to assess both BCS and MCS because overweight, ideal-weight, and thin cats can all have muscle loss.
The present study had several important limitations. First, no reference standard was used to measure muscle mass or lean body mass. Because general anesthesia was not an option for the study, we elected to compare 2 clinically relevant methods for assessment of muscle mass. Therefore, we only reported associations and not accuracy for the various methods. In addition, the included cats differed regarding BCS, age, and health status, which may have affected the results. The advantage of this heterogeneity was that it reflected cats seen in clinical practice, but additional studies of the MCS system and ultrasonographic measurement of muscle in more homogeneous populations (eg, cats with a single underlying disease or geriatric cats without underlying diseases) are warranted to further evaluate these muscle assessment methods.
A single investigator performed all ultrasonographic measurements in the study reported here, and these measurements were made in real time on live cats for logistic reasons (rather than making the measurements at a later time). Although this could have introduced bias because the investigator was able to see the cats, this person was unaware of each cat's body weight, BCS, or MCS. Nonetheless, the timing of measurements should be considered in future studies.
In addition, the present study did not provide information on repeatability and reproducibility of muscle ultrasonographic measurements in cats with various degrees of muscle loss. Although repeatability and reproducibility of this measurement have been evaluated in healthy dogs,11 these characteristics may not hold true for dogs and cats with muscle loss and this should be determined in a future study. Another limitation was that the EMH was assessed at a single location (ie, T13). Additional studies are needed to determine whether loss of muscle is consistent along the entire length of the epaxial muscles. Finally, studies of humans19–21 and dogs22 have revealed that cachexia and sarcopenia involve compositional changes in muscle (eg, conversion of type I to type II fibers and infiltration of muscles with lipid) as well as functional changes, so it will be important to determine whether similar muscle changes also occur in cats with cachexia and sarcopenia.
Regardless of these limitations, results of the present study indicated that ultrasonographic measurements of epaxial muscle can be used for quantitative assessment and that the MCS system can be used with substantial repeatability and moderate reproducibility as a subjective method for assessing muscle mass in cats. Prospective studies are warranted of the use of these measurements for serial assessment of patients and as end points in clinical trials.
Acknowledgments
Supported by Nestlé Purina PetCare Co.
Drs. Freeman, Michel, and Fages received reimbursement of travel expenses associated with conducting this study. Dr. Freeman has received research funding from or provided sponsored lectures or consulting services for Royal Canin, Nestlé Purina PetCare, Aratana Therapeutics, and Hill's Pet Nutrition Inc. Dr. Michel has received research funding from Royal Canin and Nestlé Purina PetCare Co and serves on an Advisory Council for Nestlé Purina PetCare Co. Drs. Zanghi and Vester Boler are employees of Nestlé Purina Research.
Presented in part at the 2019 American College of Veterinary Internal Medicine Forum, Phoenix, June 2019.
The authors thank Jim Ambrose, Dr. Melanie Barnes, Hallie Barnett, Brandy Panning, and Sarah Dionne for technical assistance and Dr. James Sutherland-Smith for assistance with development of the ultrasonographic method for measuring muscle mass and for valuable input on its use in cats.
ABBREVIATIONS
BCS | Body condition score |
EMH | Epaxial muscle height |
FLEMS | Forelimb epaxial muscle score |
MCS | Muscle condition score |
VEMS | Vertebral epaxial muscle score |
Footnotes
Random.org random integer generator, Randomness and Integrity Services Ltd, Dublin, Ireland.
Sonoscape S8 Expert, National Ultrasound, Duluth, Ga.
L752 5–12 MHz linear probe, National Ultrasound, Duluth, Ga.
Systat, version 13.0, Systat Inc, San Jose, Calif.
References
1. Freeman LM. Cachexia and sarcopenia: emerging syndromes of importance in dogs and cats. J Vet Intern Med 2012;26:3–17.
2. von Haehling S. Wasting away: how to treat cachexia and muscle wasting in chronic disease? Br J Clin Pharmacol 2017;83:2599–2601.
3. Michel KE, Anderson W, Cupp C, et al. Correlation of a feline muscle mass score with body composition determined by dual-energy x-ray absorptiometry. Br J Nutr 2011;106(suppl 1):S57–S59.
4. Baldwin K, Bartges J, Buffington T, et al. AAHA nutritional assessment guidelines for cats and cats. J Am Anim Hosp Assoc 2010;46:285–296.
5. Freeman L, Becvarova I, Cave N, et al. WSAVA nutritional assessment guidelines. J Small Anim Pract 2011;52:385–396.
6. Freeman LM, Kehayias JJ, Roubenoff R. Use of dual-energy x-ray absorptiometry (DEXA) to measure lean body mass, body fat, and bone mineral content (BMC) in dogs and cats (lett). J Vet Intern Med 1996;10:99–100.
7. Hutchinson D, Sutherland-Smith J, Watson AL, et al. Assessment of methods of evaluating sarcopenia in old dogs. Am J Vet Res 2012;73:1794–1800.
8. Bullen LE, Evola MG, Griffith EH, et al. Validation of ultrasonographic muscle thickness measurements as compared to the gold standard of computed tomography in dogs. Peer J 2017;5:e2926.
9. Sergi G, Trevisan C, Veronese N, et al. Imaging of sarcopenia. Eur J Radiol 2016;85:1519–1524.
10. Nijholt W, Scafoglieri A, Jager-Wittenaar H, et al. The reliability and validity of ultrasound to quantify muscles in older adults: a systematic review. J Cachexia Sarcopenia Muscle 2017;8:702–712.
11. Freeman LM, Sutherland-Smith J, Prantil LR, et al. Quantitative assessment of muscle in dogs using a vertebral epaxial muscle score. Can J Vet Res 2017;81:255–260.
12. Freeman LM, Sutherland-Smith J, Cummings C, et al. Evaluation of a quantitatively derived value for assessment of muscle mass in clinically normal cats. Am J Vet Res 2018;79:1188–1192.
13. Freeman LM, Michel KE, Zanghi BM, et al. Evaluation of the use of muscle condition score and ultrasonographic measurements for assessment of muscle mass in dogs. Am J Vet Res 2019;80:595–600.
14. Laflamme D. Development and validation of a body condition score system for cats. Feline Pract 1997;25(5/6):13–18.
15. World Small Animal Veterinary Association Global Nutrition Committee. Muscle condition score charts for cats. Available at: www.wsava.org/Guidelines/Global-Nutrition-Guidelines. Accessed Jul 21, 2019.
16. Sharma A, Lavie CJ, Borer JS, et al. Meta-analysis of the relation of body mass index to all-cause and cardiovascular mortality and hospitalization in patients with chronic heart failure. Am J Cardiol 2015;115:1428–1434.
17. Finn E, Freeman LM, Rush JE. The relationship between body weight, body condition, and survival in cats with heart failure. J Vet Intern Med 2010;24:1369–1374.
18. Freeman LM, Lachaud MP, Matthews S, et al. Evaluation of weight loss over time in cats with chronic kidney disease. J Vet Intern Med 2016;30:1661–1666.
19. Lang T, Streeper T, Cawthon P, et al. Sarcopenia: etiology, clinical consequences, intervention, and assessment. Osteoporos Int 2010;21:543–559.
20. Boutin RD, Yao L, Canter RJ, et al. Sarcopenia: current concepts and imaging implications. AJR Am J Roentgenol 2015;205:W255–W266.
21. Frontera WR. Physiologic changes of the musculoskeletal system with aging: a brief review. Phys Med Rehabil Clin North Am 2017;28:705–711.
22. Sutherland-Smith J, Hutchinson D, Freeman LM. Comparison of computed tomographic attenuation values for epaxial muscles in old and young dogs. Am J Vet Res 2019;80:174–177.