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University of Groningen

Gaining insight in factors associated with successful ageing: body composition, nutrition, and

cognition

Nijholt, Willemke

DOI:

10.33612/diss.102704591

IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below.

Document Version

Publisher's PDF, also known as Version of record

Publication date: 2019

Link to publication in University of Groningen/UMCG research database

Citation for published version (APA):

Nijholt, W. (2019). Gaining insight in factors associated with successful ageing: body composition, nutrition, and cognition. Rijksuniversiteit Groningen. https://doi.org/10.33612/diss.102704591

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Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum.

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Response to:

“The use of ultrasound for

the estimation of muscle

mass: one site fits most?”

2

Willemke Nijholt, Harriët Jager-Wittenaar, Aldo Scafoglieri, Hans Hobbelen,

Cees P. van der Schans

J Cachexia Sarcopenia Muscle. 2018;9(3):627-628 DOI:10.1002/jcsm.12293

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Chapter 2B

46

The use of ultrasound for the estimation of muscle

mass: one site fits most?

Takashi Abe1, Jeremy P. Loenneke1 and Robert S. Thiebaud2

1 Kevser Ermin Applied Physiology Laboratory, Department of Health, Exercise Science, & Recreation Management, The University of Mississippi, University, MS, 38677, USA. 2 Department of Kinesiology, Texas Wesleyan University, 1201 Wesleyan St, Fort Worth, TX, 76105, USA Corresponding author: Takashi Abe (t12abe@gmail.com) During the last two decades, DXA-derived appendicular lean soft tissue mass has served as a major criterion for diagnosing the age-related loss of skeletal muscle mass (i.e. sarcopenia).1 From a

clinical perspective, however, DXA measurements are costly, and the device has limitedavailability. A possible alternative method for measuring muscle size (e.g. muscle thickness) in humans may be B-mode ultrasound. It is well known that ultrasound is a non-invasive, quick, valid, and reliable imaging technique to estimate muscle thickness in muscles of the extremity and trunk.2,3

With this in mind, we read with great interest the article by Nijholt and colleagues,4 where they

reported the validity and reliability of ultrasound to quantify musculature in older adults. The authors also reported on two prediction equations for estimating DXA-derived muscle mass. Although not reported within this paper, we previously noted that two of those prediction equations selected by Nijholt et al. included systematic error.5 Over the last couple of years,

we have published several prediction equations for estimating DXA-derived appendicular lean mass in older adults.6–8 Unfortunately, those equations were not included in the article by

Nijholt et al.4 Interestingly, a single site measurement of forearm muscle thickness was found

to be good predictor of DXA-derived lean soft tissue mass in older Caucasian adults,6 and the

equation was also found to be accurate in older Japanese adults.7 Notably, the standard error

of the estimate was 1.95 kg for the equation that used a single muscle thickness site, whereas the standard error of the estimate of the equation that included eight predictors was 1.13 kg.6

The amount of time required for a single ultrasound measurement is generally less than 1 min per person, so this estimate appears both valid and pragmatic.

In summary, our previous studies6,7 suggest that forearm muscle thickness measurements are

a tolerable and less demanding assessment to use for older adults, and ultrasound estimated appendicular lean mass from the forearm muscle thickness may be a useful indicator for evaluating muscularity in older adults. Although additional research is needed, our recent work along with others noted within the Nijholt et al.4 review may be useful with the development of

ultrasound evaluation for health screenings as well as for the primary diagnosis of sarcopenia.

Acknowledgements

The authors certify that they comply with the ethical guidelines for authorship and publishing of the Journal of Cachexia, Sarcopenia and Muscle.9

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References

1. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010;39:412–423.

2. Abe T, Loenneke JP, Thiebaud RS, Loftin M. Morphological and functional relationships with ultrasound measured muscle thickness of the upper extremity and trunk. Ultrasound. 2014;22:229–235.

3. Abe T, Loenneke JP, Thiebaud RS. Morphological and functional relationships with ultrasound measured muscle thickness of the lower extremity: A brief review. Ultrasound. 2015;23:166–173.

4. Nijholt W, Scafoglieri A, Jager-Wittenaar H, Hobbelen JS, van der Schans CP. The reliability and validity of ultrasound to quantify muscles in older adults: a systematic review. J Cachexia

Sarcopenia Muscle. 2017;8:702–712.

5. Abe T, Loenneke JP, Young KC, Thiebaud RS, Nahar VK, Hollaway KM, et al. Validity of ultrasound prediction equations for total and regional muscularity in middle-aged and older men and women. Ultrasound Med Biol. 2015;41:557–564.

6. Abe T, Thiebaud RS, Loenneke JP, Young KC. Prediction and validation of DXA-derived appendicular lean soft tissue mass by ultrasound in older adults. Age. 2015;37:114.

7. Abe T, Fijita E, Thiebaud RS, Loenneke JP, Akamine T. Ultrasound-derived forearm muscle thickness is a powerful predictor for estimating DXA-derived appendicular lean mass in Japanese older adults. Ultrasound Med Biol. 2016;42:2341–2344.

8. Abe T, Loenneke JP, Thiebaud RS, Fujita E, Akamine T, Loftin M. Prediction and validation of DXA-derived appendicular fat-free adipose tissue by a single ultrasound image of the forearm in Japanese older adults. J Ultrasound

Med. 2018;37(2):347-353.

9. von Haehling S, Morley JE, Coats AJS, Anker SD. Ethical guidelines for publishing in the Journal of Cachexia, Sarcopenia and Muscle: update 2015. J

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Chapter 2B

48

Response to: “The use of ultrasound for the

estimation of muscle mass: one site fits most?”

Willemke Nijholt1,2, Harriët Jager-Wittenaar1,3, Aldo Scafoglieri4, Hans Hobbelen1,5 and

Cees P. van der Schans CP1,2,6

1 Research Group Healthy Ageing, Allied Health Care and Nursing, Hanze University of Applied Sciences, Groningen, The Netherlands

2 Department of Rehabilitation Medicine, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands

3 Department of Maxillofacial Surgery, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands 4 Faculty of Medicine and Pharmacy, Vrije Universiteit Brussel, Brussels, Belgium

5 Department of General Practice and Elderly Care Medicine, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands

6 University of Groningen University Medical Center Groningen, Department of Health Psychology Research, Groningen, The Netherlands

We thank Takashi Abe, Jeremy P. Loenneke and Robert S. Thiebaud for their valuable response to our systematic review in their Letter entitled “The use of ultrasound for the estimation of muscle mass: one site fits most?”.1

We feel encouraged by their response that ultrasound has the potential to play an important role in assessing muscle mass in daily practice in the future. The authors remarked that we included only two studies in our systematic review that evaluated the validity of ultrasound-derived prediction equations for the prediction of muscle mass in older adults.2 The authors

elaborate on three other studies that indicate that forearm muscle thickness measurements could be used for the prediction of muscle mass in older adults. Although these articles provide additional information on the possibilities of muscle ultrasound for the prediction of muscle mass, we did not include these three articles in our systematic review because these articles were published later than the period included in our search,3,4 or did not meet

our inclusion criterion for age.5

The authors’ suggestion of using forearm muscle thickness measurements for the prediction of muscle mass is interesting for daily practice. It is very promising that the size of peripheral muscles is associated with (whole body) muscle mass. However, we do not fully agree with the statement that one site fits most. Despite the fact that the current definitions of sarcopenia and malnutrition focus on the assessment of (whole body) muscle mass,6,7 we would like

to emphasize that the assessment of peripheral muscles is of utmost importance. It has previously been observed that the loss of muscle mass is not uniform across all muscles.8 In

general, the loss of muscle mass of the lower limbs is a consequence of inactivity, whereas the loss of muscle mass in the upper limbs is more prone to nutritional depletion.9 This illustrates

the importance of assessing peripheral muscles. Peripheral muscles can be quantified using muscle ultrasound, but muscle ultrasound can also be used to qualify the muscle,

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e.g., to assess the amount of intramuscular fat. This intramuscular fat results in increased echogenicity, i.e., the reflectance of the emitted ultrasound signal,10 and is associated with

decreased muscle function in older adults.11 These findings implicate that not only the size of

the muscle matters, but also the composition of muscles needs to be assessed.

In summary, we agree with Abe, Loenneke and Thiebaud that ultrasound has high potential for the assessment of muscles in daily practice. However, we believe that assessing peripheral muscles is equally, or may be even more, important than the prediction of muscle mass. Therefore, we propose a paradigm shift from the assessment of (whole body) muscle mass to quantifying and qualifying peripheral muscles. Acknowledgements The authors certify that they comply with the ethical guidelines for publishing in the Journal of Cachexia, Sarcopenia and Muscle: update 2015.12

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Chapter 2B

50

References

1. Abe T, Loenneke JP, Thiebaud RS. The use of ultrasound for the estimation of muscle mass: one site fits most? J Cachexia Sarcopenia Muscle. 2018;9(1):213.

2. Nijholt W, Scafoglieri A, Jager-Wittenaar H, Hobbelen JSM, van der Schans CP. The reliability and validity of ultrasound to quantify muscles in older adults: A systematic review. J Cachexia

Sarcopenia Muscle. 2017;8:702-712.

3. Abe T, Fujita E, Thiebaud RS, Loenneke JP, Akamine T. Ultrasound-derived forearm muscle thickness is a powerful predictor for estimating DXA-derived appendicular lean mass in Japanese older adults. Ultrasound Med Biol. 2016;42:2341-2344.

4. Abe T, Loenneke JP, Thiebaud RS, Fujita E, Akamine T, Loftin M. Prediction and validation of DXA-derived appendicular fat-free adipose tissue by a single ultrasound image of the forearm in Japanese older adults. J Ultrasound

Med. 2018;37(2):347-353.

5. Abe T, Thiebaud RS, Loenneke JP, Young KC. Prediction and validation of DXA-derived appendicular lean soft tissue mass by ultrasound in older adults. Age. 2015:37:114.

6. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age

Ageing. 2010;39:412-423.

7. Cederholm T, Bosaeus I, Barazzoni R, et al. Diagnostic criteria for malnutrition–an ESPEN consensus statement. Clin Nutr. 2015:34(3):335-340. 8. Janssen I, Heymsfield SB, Wang Z, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol. 2000;89(1):81-88.

9. Heymsfield SB, Tighe A, Wang ZM. Nutritional assessment by anthropometric and biochemical methods. Modern nutrition in health and disease. 1994;8:812.

10. Arts IM, Pillen S, Schelhaas HJ, Overeem S, Zwarts MJ. Normal values for quantitative muscle ultrasonography in adults. Muscle &

nerve. 2010;41(1):32-41.

11. Watanabe Y, Yamada Y, Fukumoto Y, Ishihara T, Yokoyama K, Yoshida T, et al. Echo intensity obtained from ultrasonography images reflecting muscle strength in elderly men.  Clin

Interv Aging. 2013;8:993.

12. von Haehling S, Morley JE, Coats AJS, Anker SD. Ethical guidelines for publishing in the Journal of Cachexia, Sarcopenia and Muscle: update 2015. J

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