Lack of knowledge and availability of diagnostic equipment could hinder the diagnosis of sarcopenia and its management

Abstract

Objectives
Sarcopenia is an emerging clinical challenge in an ageing population and is associated with serious negative health outcomes. This study aimed to assess the current state of the art regarding the knowledge about the concept of sarcopenia and practice of the diagnostic strategy and management of sarcopenia in a cohort of Dutch healthcare professionals (physicians, physiotherapists, dietitians and others) attending a lecture cycle on sarcopenia.

Material and methods
This longitudinal study included Dutch healthcare professionals (n = 223) who were asked to complete a questionnaire before, directly after and five months after (n = 80) attending a lecture cycle on the pathophysiology of sarcopenia, diagnostic strategy and management of sarcopenia, i.e. interventions and collaboration.

Results
Before attendance, 69.7% of healthcare professionals stated to know the concept of sarcopenia, 21.4% indicated to know how to diagnose sarcopenia and 82.6% had treated patients with suspected sarcopenia. 47.5% used their clinical view as diagnostic strategy. Handgrip strength was the most frequently used objective diagnostic measure (33.9%). Five months after attendance, reported use of diagnostic tests was increased, i.e. handgrip strength up to 67.4%, gait speed up to 72.1% and muscle mass up to 20.9%. Bottlenecks during implementation of the diagnostic strategy were experienced by 67.1%; lack of awareness among other healthcare professionals, acquisition of equipment and time constraints to perform the diagnostic measures were reported most often. Before attendance, 36.4% stated not to consult a physiotherapists or exercise therapists (PT/ET) or dietitian for sarcopenia interventions, 10.5% consulted a PT/ET, 32.7% a dietitian and 20.5% both a PT/ET and dietitian. Five months after attendance, these percentages were 28.3%, 21.7%, 30.0% and 20.0% respectively.

Conclusion
The concept of sarcopenia is familiar to most Dutch healthcare professionals but application in practice is hampered, mostly by lack of knowledge, availability of equipment, time constraints and lack of collaboration.

Full text

RESEARCH ARTICLE
Lack of knowledge and availability of
diagnostic equipment could hinder the
diagnosis of sarcopenia and its management
Esmee M. Reijnierse
1,2
, Marian A. E. de van der Schueren
3,4
, Marijke C. Trappenburg
1,5
,
Marjan Doves
6
, Carel G. M. Meskers
7,8
, Andrea B. Maier
2,8
*
1Department of Internal Medicine, Section of Gerontology and Geriatrics, VU University Medical Center,
Amsterdam, The Netherlands, 2Department of Medicine and Aged Care, Royal Melbourne Hospital, The
University of Melbourne, Melbourne, Australia, 3Department of Internal Medicine, Section of Nutrition and
Dietetics, VU University Medical Center, Amsterdam, The Netherlands, 4Department of Nutrition, Sports and
Health, Faculty of Health and Social Studies, HAN University of Applied Sciences, Nijmegen, The
Netherlands, 5Department of Internal Medicine, Amstelland Hospital, Amstelveen, The Netherlands,
6Institute of Human Movement Studies, Faculty of Health Care, University of Applied Sciences Utrecht,
Utrecht, The Netherlands, 7Department of Rehabilitation Medicine, VU University Medical Center,
Amsterdam, The Netherlands, 8Department of Human Movement Sciences, MOVE Research Institute
Amsterdam, Vrije Universiteit, Amsterdam, The Netherlands
*andrea.maier@mh.org.au
Abstract
Objectives
Sarcopenia is an emerging clinical challenge in an ageing population and is associated with
serious negative health outcomes. This study aimed to assess the current state of the art
regarding the knowledge about the concept of sarcopenia and practice of the diagnostic
strategy and management of sarcopenia in a cohort of Dutch healthcare professionals (phy-
sicians, physiotherapists, dietitians and others) attending a lecture cycle on sarcopenia.
Material and methods
This longitudinal study included Dutch healthcare professionals (n = 223) who were asked
to complete a questionnaire before, directly after and five months after (n = 80) attending a
lecture cycle on the pathophysiology of sarcopenia, diagnostic strategy and management of
sarcopenia, i.e. interventions and collaboration.
Results
Before attendance, 69.7% of healthcare professionals stated to know the concept of sarco-
penia, 21.4% indicated to know how to diagnose sarcopenia and 82.6% had treated patients
with suspected sarcopenia. 47.5% used their clinical view as diagnostic strategy. Handgrip
strength was the most frequently used objective diagnostic measure (33.9%). Five months
after attendance, reported use of diagnostic tests was increased, i.e. handgrip strength up
to 67.4%, gait speed up to 72.1% and muscle mass up to 20.9%. Bottlenecks during imple-
mentation of the diagnostic strategy were experienced by 67.1%; lack of awareness among
other healthcare professionals, acquisition of equipment and time constraints to perform the
PLOS ONE | https://doi.org/10.1371/journal.pone.0185837 October 2, 2017 1 / 10
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OPEN ACCESS
Citation: Reijnierse EM, de van der Schueren MAE,
Trappenburg MC, Doves M, Meskers CGM, Maier
AB (2017) Lack of knowledge and availability of
diagnostic equipment could hinder the diagnosis of
sarcopenia and its management. PLoS ONE 12
(10): e0185837. https://doi.org/10.1371/journal.
pone.0185837
Editor: Masaki Mogi, Ehime University Graduate
School of Medicine, JAPAN
Received: May 22, 2017
Accepted: September 20, 2017
Published: October 2, 2017
Copyright: ©2017 Reijnierse et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All data files are
available from the Figshare database (https://
figshare.com/s/301a62c24c4a44ece727).
Funding: This study was supported by the
European Union’s Horizon 2020 research program
PreventIT (No 689238) to Andrea B. Maier and the
Marie Curie, Sklodowska, Innovative Training
Network PANINI (No 675003) to Andrea B. Maier.
The funders had no role in the study design, data

diagnostic measures were reported most often. Before attendance, 36.4% stated not to con-
sult a physiotherapists or exercise therapists (PT/ET) or dietitian for sarcopenia interven-
tions, 10.5% consulted a PT/ET, 32.7% a dietitian and 20.5% both a PT/ET and dietitian.
Five months after attendance, these percentages were 28.3%, 21.7%, 30.0% and 20.0%
respectively.
Conclusion
The concept of sarcopenia is familiar to most Dutch healthcare professionals but application
in practice is hampered, mostly by lack of knowledge, availability of equipment, time con-
straints and lack of collaboration.
Introduction
The clinical relevance of sarcopenia is increasingly being recognized and a clinical challenge in
our ageing population. Sarcopenia is associated with negative health outcomes such as falls [1,
2], impaired standing balance [3], physical disability [4,5] and mortality [6,7]. Sarcopenia is a
public health burden and entails high healthcare costs associated with hospitalization, outpa-
tient clinic visits and home healthcare expenditure [8,9]. According to survey data from the
United States, direct costs of sarcopenia may be up to 1.5% of the total healthcare costs [9].
Prevalence rates of sarcopenia vary up to 34% in geriatric outpatients dependent on the used
definition [10]. To date, no consensus definition of sarcopenia has been reached, however,
most recent definitions are based on measures of muscle mass, muscle strength and gait speed
[11–13].
Combined intervention of physical exercise and adequate protein intake is more effective in
increasing muscle mass and muscle strength compared to either physical exercise or nutritional
intervention alone [14–17]. Therefore, a multidisciplinary approach is required in which different
healthcare professionals play a key role in the diagnostic strategy and management of sarcopenia.
This requires common knowledge about the concept of sarcopenia, a diagnostic strategy and
optimal management of sarcopenia including consultation and collaboration between diverse
healthcare professionals. To date, the current knowledge and practice of healthcare professionals
regarding the diagnostic strategy and management of sarcopenia is unknown. This information
is highly needed to properly implement and strengthen the diagnostic strategy and management
of sarcopenia in clinical practice.
The primary aim of this study was to assess the current state of knowledge about the con-
cept of sarcopenia and the current practice of the diagnostic strategy and management of sar-
copenia. Secondary aims were to assess the intentions to implement the diagnostic strategy
and management of sarcopenia and to identify bottlenecks during implementation of the diag-
nostic strategy and management in a cohort of Dutch healthcare professionals attending the
Sarcopenia Road Show, a postgraduate, multidisciplinary lecture cycle for healthcare profes-
sionals with different backgrounds (physicians, physiotherapists, dietitians and others).
Materials and methods
Study design
This longitudinal study included 223 medical and allied Dutch healthcare professionals attend-
ing the lecture cycle ‘Sarcopenia Road Show’. Healthcare professionals worked either in
Current state of the art on the knowledge and practice of sarcopenia
PLOS ONE | https://doi.org/10.1371/journal.pone.0185837 October 2, 2017 2 / 10
collection and analysis, decision to publish, or
preparation of the manuscript.
Competing interests: The authors have declared
that no competing interests exist.

primary care, nursing homes or hospitals. Medical healthcare professionals included physi-
cians (geriatricians, internists, internist-geriatricians, nursing home physicians, general practi-
tioners (GP) and residents, considered as one group), nurses and GP assistants; allied
healthcare professionals included physiotherapists (PT), exercise therapists (ET) (PT and ET
considered as one group) and dietitians.
The Sarcopenia Road Show visited four lecture locations spread over the Netherlands (‘s
Hertogenbosch, Haarlem, Dordrecht, Texel) between February 2015 and September 2015.
Before and directly after the lectures, attending healthcare professionals were asked to com-
plete a printed questionnaire. Of all attending healthcare professionals, 95% completed these
questionnaires. Five months after attendance, an online questionnaire was sent by e-mail to a
subgroup of 147 healthcare professionals who gave permission to be contacted at a later stage,
of which n = 80 (54.4%) responded. Ethical approval was not required for this study and com-
pletion of the questionnaire was taken as consent.
Sarcopenia Road Show
The Sarcopenia Road Show comprised three lectures and three workshops in one session with
the aim to transfer knowledge about the concept of sarcopenia, diagnostic strategy and man-
agement of sarcopenia. Evidence-based lectures and workshops were developed by the authors
and based on the current literature due to the absence of guidelines for sarcopenia. Lectures
and workshops were presented by senior lecturers (internist-geriatrician, geriatric physiother-
apist and dietician) and were focused on the pathophysiology of sarcopenia, diagnostic strategy
and interventions, both from exercise and nutritional perspective. Lectures were presented in
a plenary session of one and a half hour, followed by three different parallel workshops
whereby each healthcare professional attended one type of workshop, focusing on either the
medical, exercise or nutritional aspects of sarcopenia. To diagnose sarcopenia, the definition
of the European Working Group on Sarcopenia in Older People (EWGSOP) [11] was pre-
sented, including muscle mass measured by bioelectrical impedance analysis (BIA), handgrip
strength measured by a hand dynamometer and gait speed measured by the four-meter walk
test at normal pace. Management aimed at increasing muscle mass and muscle strength by
exercise i.e. progressive resistance training [18] requiring a PT/ET and adequate protein intake
[19] as well as optimal division of protein over the day [20] requiring a dietitian. Importance
of collaboration between healthcare professionals for both the diagnostic strategy and manage-
ment was stressed.
Questionnaires
Questionnaires were developed by the authors. The first questionnaire was to be completed
before attendance and aimed at assessing the current knowledge and clinical practice regard-
ing sarcopenia. The second questionnaire was to be completed directly after attendance and
aimed at inquiring about intentions related to the diagnostic strategy and management. The
third questionnaire was to be completed five months after attendance and aimed at assessing
the level of implementation. Questions related to the current occupation, working affiliation,
current state of knowledge about the concept of sarcopenia, diagnostic strategy and manage-
ment of sarcopenia. The complete questionnaires are enlisted in S1 Table.
Statistical analyses
Descriptive statistics were used to calculate numbers and percentages. Analyses were stratified
by group of healthcare professionals and/or analyzed as the total group of healthcare profes-
sionals. Statistical analyses were performed using the Statistical Package for the Social Sciences
Current state of the art on the knowledge and practice of sarcopenia
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22.0 (SPSS Inc, Chicago, Illinois, USA). Visualization was performed using GraphPad Prism
(version 6.3).
Results
Table 1 shows the current occupation and working affiliation of attending healthcare profes-
sionals. Of the 223 healthcare professionals, 30.9% was physician, 14.3% nurse, 9.9% GP assis-
tant, 37.2% PT/ET and 7.6% dietitian. In total, 45.3% of the healthcare professionals were
working in primary care, 22.9% in nursing homes and 31.8% in hospitals.
Table 2 shows the current state of knowledge about the concept of sarcopenia and diagnos-
tic strategy of healthcare professionals before and directly after attendance. Before attendance,
69.7% of the healthcare professionals stated to know the concept of sarcopenia and 82.6% had
treated patients with suspected sarcopenia in the previous month before attendance. In total,
21.4% indicated to know how to formally diagnose sarcopenia. In routine clinical practice,
47.5% used their clinical view to diagnose sarcopenia. Of the healthcare professionals using
diagnostic measures, handgrip strength was the most frequently used measurement (33.9%),
mostly performed by PT/ET (50% of the PT/ET). PT/ET also measured gait speed most fre-
quently (30.5% of the PT/Et) compared to other healthcare professionals. Documentation of
the diagnosis of sarcopenia in clinical records was reported by 10.5% of the healthcare profes-
sionals. Fig 1A visualizes the management of sarcopenia depicted as percentages of consulted
healthcare professionals for interventions for the total group of healthcare professionals. In
case sarcopenia is diagnosed, 36.4% stated not to consult a PT/ET or dietitian, 10.5% consulted
a PT/ET, 32.7% a dietitian and 20.5% both a PT/ET and dietitian. Results stratified by groups
of healthcare professionals are shown in S2 Table. Of the medical healthcare professionals,
29.7% reported a lack of collaboration with PT/ET and 13.5% with dietitians. Of the PT/ET,
41.1% reported a lack of collaboration with medical healthcare professionals and 12.3% with
dietitians. Of the dietitians, 26.7% reported a lack of collaboration with medical healthcare
professionals and 33.3% with PT/ET.
Directly after attendance, 97.3% of the healthcare professionals indicated to know how to
diagnose sarcopenia (Table 2). Regarding the diagnostic strategy, 88.2% of the dietitians indi-
cated to intend to measure muscle mass. This percentage was lower in the other groups of
healthcare professionals. The intention to use handgrip strength and gait speed as diagnostic
measures was the highest in PT/ET (94.0% and 98.8% respectively). Healthcare professionals
stated in 80.9% to intend to document the diagnosis sarcopenia in clinical records (Table 2).
Fig 1B visualizes the intended management of sarcopenia. In case sarcopenia is diagnosed,
5.0% did not intend to consult a PT/ET or dietitian, 4.1% intended to consult a PT/ET, 34.4%
a dietitian and 56.6% both a PT/ET and dietitian. This did not differ between groups of health-
care professionals (S2 Table).
Table 1. Current occupation and working affiliation of attending healthcare professionals (n = 223).
Total Medical group Allied Health
Physician Nurse GP assistant PT/ET Dietitian
n = 223 n = 69 n = 32 n = 22 n = 83 n = 17
Primary care 101 (45.3) 15 (21.7) 10 (31.3) 22 (100) 43 (51.8) 11 (64.7)
Nursing homes 51 (22.9) 9 (13.0) 3 (9.4) NA 33 (39.8) 6 (35.3)
Hospitals 71 (31.8) 45 (65.2) 19 (59.4) NA 7 (8.4) 0
All variables are presented as n (%).
GP General practitioner, PT physiotherapist, ET exercise therapist, NA not applicable
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Of the healthcare professionals who completed the questionnaire five months after atten-
dance, 15.0% were physician, 13.8% nurse, 10.0% GP assistant, 50.0% PT/ET and 11.3% dieti-
tian; of whom 61.3% worked in primary care, 21.3% in nursing homes and 17.5% in hospitals.
Table 3 shows the diagnostic strategy and management of sarcopenia of healthcare profession-
als. In total, 53.8% of the healthcare professionals indicated to have implemented the diagnos-
tic strategy in clinical practice as suggested during the Sarcopenia Road Show. The criteria
were said to be most frequently applied to older adults with mobility problems (37.2%). The
median percentage of the patients screened for sarcopenia using the diagnostic strategy in the
previous working week were indicated to be 0% (IQR 0–4.5). In routine clinical practice,
13.9% of the healthcare professionals indicated to use muscle mass as diagnostic measure,
50.6% handgrip strength and 54.4% gait speed. Bottlenecks during the implementation of the
diagnostic strategy were experienced by 67.1%; lack of awareness among other healthcare pro-
fessionals, the acquisition of equipment and time constraints to perform the diagnostic test
were most often reported. Fig 1C visualizes the management of sarcopenia five months after
attendance. In case sarcopenia was diagnosed, 28.3% stated not to consult a PT/ET or dietitian,
21.7% consulted a PT/ET, 30.0% a dietitian and 20.0% both a PT/ET and dietitian. A lack of
collaboration was experienced by 36.8%.
Discussion
This study reports on the current state of knowledge about sarcopenia, diagnostic strategy and
management of sarcopenia among a cohort of Dutch healthcare professionals, attending a post
Table 2. Current state of knowledge about the concept of sarcopenia and diagnostic strategy of healthcare professionals before and directly after
attendance.
Total Medical group Allied health
Physician Nurse GP assistant PT/ET Dietitian
n = 223 n = 69 n = 32 n = 22 n = 83 n = 17
Knowledge about the concept
Before Knows the concept
a
154 (69.7) 39 (57.4) 23 (71.9) 13 (59.1) 63 (76.8) 23 (71.9)
Suspected sarcopenia
b,e
181 (82.6) 60 (89.6) 22 (68.8) 15 (71.4) 68 (82.9) 16 (94.1)
Knows how to diagnose
c
46 (21.4) 17 (26.2) 4 (12.5) 1 (4.5) 18 (22.8) 6 (35.3)
Directly after Knows how to diagnose
d
214 (97.3) 63 (94.0) 31 (100) 21 (95.5) 82 (98.8) 17 (100)
Diagnostic strategy–Diagnostic measures
Before None
a
83 (37.6) 18 (26.5) 13 (40.6) 15 (68.2) 34 (41.5) 3 (17.6)
Clinical view
a
105 (47.5) 41 (60.3) 17 (53.1) 5 (22.7) 32 (39.0) 10 (58.8)
Nutritional status
a
82 (37.1) 30 (44.1) 15 (46.9) 6 (27.3) 18 (22.0) 13 (76.5)
Muscle mass
a
20 (9.0) 6 (8.8) 1 (3.1) 0 9 (11.0) 4 (23.5)
Handgrip strength
a
75 (33.9) 22 (32.4) 6 (18.8) 1 (4.5) 41 (50.0) 5 (29.4)
Gait speed
a
43 (19.5) 15 (22.1) 3 (9.4) 0 25 (30.5) 0
Diagnostic strategy–Diagnostic measures
Directly after Intention to use muscle mass
d
64 (29.1) 16 (23.9) 6 (19.4) 4 (18.2) 23 (27.7) 15 (88.2)
Intention to use handgrip strength
d
175 (79.5) 51 (76.1) 19 (61.3) 15 (68.2) 78 (94.0) 12 (70.6)
Intention to use gait speed
d
167 (75.9) 50 (74.6) 21 (67.7) 10 (45.5) 82 (98.8) 4 (23.5)
Diagnostic strategy–Documentation of diagnosis
Before Yes
d
23 (10.5) 6 (8.8) 1 (3.1) 0 13 (16.0) 3 (17.6)
Directly after Intention to do
d
174 (80.9) 51 (78.5) 20 (64.5) 18 (81.8) 70 (87.5) 15 (88.2)
All variables are presented as n (%).
GP General practitioner, PT physiotherapist, ET exercise therapist
Data available in a subgroup of
a
n = 221,
b
n = 219,
c
n = 215,
d
n = 220
e
Question was asked the following: “Have you seen patients in the previous month in which you suspected that there could be presence of sarcopenia?”
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graduate lecture cycle on sarcopenia. Although healthcare professionals with a specific interest
in sarcopenia attended the lecture cycle, before attendance only a fifth indicated to know how
to formally diagnose sarcopenia and only a third used at least one of the proposed diagnostic
Fig 1. Management of sarcopenia depicted as percentages of consulted healthcare professionals for interventions: (a) before attendance (n = 223);
(b) directly after attendance (intention to consult) (n = 223) and (c) five months after attendance (data available in n = 60). PT physiotherapist, ET exercise
therapist.
https://doi.org/10.1371/journal.pone.0185837.g001
Table 3. Diagnostic strategy and management of sarcopenia of healthcare professionals five months
after attendance (n = 80).
Total n = 80
Diagnostic strategy
Implementation of diagnostic strategy 43 (53.8)
Application of diagnostic strategy
All older adults
a
12 (15.4)
Older adults with comorbidity
a
18 (23.1)
Older adults with mobility problems
a
29 (37.2)
Older adults with malnutrition
a
22 (28.2)
Screening percentage, median [IQR]
b
0 [0–4.5]
Diagnostic measures
c
No measures 56 (70.9)
Muscle mass 11 (13.9)
Handgrip strength 40 (50.6)
Gait speed 43 (54.4)
Experienced bottlenecks
b
49 (67.1)
Lack of awareness among other healthcare professionals 23 (31.9)
Not convinced or motivated about sarcopenia 5 (6.9)
Acquisition of a device to measure muscle mass 22 (30.6)
Acquisition of handgrip strength device 8 (11.1)
No space for walking test to assess gait speed 3 (4.2)
Time constrains to perform the diagnostic tests 22 (30.6)
No funding source specific for sarcopenia 9 (12.5)
Management–Collaboration
d
Lack of collaboration 25 (36.8)
All variables are presented as n (%) unless indicated otherwise.
IQR interquartile range. Data available in a subgroup of
a
n = 78,
b
n = 72,
c
n = 79,
d
n = 68
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measures in routine clinical practice if objective tests were used (mostly: handgrip strength).
Five months after attendance, approximately 50% indicated to use at least one diagnostic mea-
sure. Lack of awareness among other healthcare professionals, availability of equipment and
time constraints to perform the diagnostic measures were most often reported as bottlenecks
during implementation of the diagnostic strategy. For the management of sarcopenia, only
one out of five healthcare professionals consulted both a PT/ET and a dietitian before atten-
dance; this did not change after five months.
Knowledge about the concept of sarcopenia
Although healthcare professionals stated to be familiar with the concept of sarcopenia, only a
small percentage used diagnostic measures in clinical practice. Almost all healthcare profes-
sionals stated to have the intention to diagnose sarcopenia and the use of diagnostic measures
had increased five months after attendance. However, hardly any patients were screened for
sarcopenia in the working week prior to the five months evaluation. It could be presumed that
the current state of knowledge and application of the diagnostic strategy is even much lower
among healthcare professionals with no specific interest in sarcopenia. This implies that there
is a major challenge in educating different healthcare professionals working in the field of age-
ing to create the required level of awareness and common knowledge. A survey among dieti-
tians showed also that the term sarcopenia is used in only 12% of the dietitians [21]. To the
best of our knowledge, there are no other studies describing the current knowledge and prac-
tice of sarcopenia among healthcare professionals. Educational lectures for healthcare profes-
sionals, like the Sarcopenia Road Show, aimed at transferring knowledge on the
aforementioned topics, are a first step to create more awareness and knowledge among health-
care professionals, but further steps are necessary to facilitate implementation.
Diagnostic strategy
Handgrip strength and gait speed were the most frequently used diagnostic measures before
attendance. Healthcare professionals intended to use these diagnostic measures more fre-
quently and their use had increased significantly five months after attendance. Muscle mass
was least used as diagnostic measure and the intention to implement was much lower than
handgrip strength and gait speed, but its use had increased five months after attendance. The
acquisition of a device to measure muscle mass was one of the most reported bottlenecks.
Clearly, financial aspects such as the acquisition of even a relatively cheap bioelectrical imped-
ance analysis (BIA) device, creates huge barriers for implementation. Upon implementing the
diagnostic measures for sarcopenia, healthcare professionals reported different bottlenecks;
lack of awareness among other healthcare professionals, availability of equipment and time
constraints of diagnostic measures were most often reported. Anticipating on these experi-
enced bottlenecks is an important step to make the implementation of the diagnostic strategy
more effective and eventually to improve care in older adults with sarcopenia. Note that only
80 healthcare professionals completed the questionnaire five months after attending and this
subgroup could have over- or underestimated the results.
Management of sarcopenia
The optimal treatment of sarcopenia requires a combined physical and nutritional interven-
tion [14–17]. Before attendance, the combined consultation of a PT/ET and a dietitian was
reported by one out of five healthcare professionals and this had not changed five months after
attendance while half of the healthcare professionals had the intention to consult a PT/ET and
a dietitian. This result indicates a gap between clinical practice and research which can be
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explained by the experienced bottlenecks also hindering the implementation of the manage-
ment of sarcopenia, but probably also by organizational aspects such as availability, knowing
where to find other healthcare professionals, and reimbursement strategies. Ideally, there
should be a collaborative triangle between the physician, PT/ET and dietitian to diagnose and
manage sarcopenia. However, this ideal collaboration was often absent; a lack of collaboration
was experienced between the medical healthcare professionals and allied healthcare profes-
sionals before attendance and approximately a third of the healthcare professionals experi-
enced a lack of collaboration five months after attendance.
Implementation
Effective implementation of the diagnostic strategy and management of sarcopenia in daily
practices requires many factors such as acquisition of diagnostic measurement devices, re-
organization of care, collaboration between healthcare professionals, perceived needs and ben-
efits of innovation and organizational factors [22,23]. This study has highlighted some bottle-
necks that were experienced in the implementation phase. Finally, for an effective
implementation, all potential bottlenecks should be addressed in each phase of the implemen-
tation. Furthermore, a funding source specific for sarcopenia recognized by health insurance
companies and the development of national and international guidelines by different profes-
sionals associations would be helpful for the implementation. Sarcopenia is recently recog-
nized as an independent condition by the International Classification of Disease, Tenth
Revision, Clinical Modification (ICD-10-CM) [24]. This will have advantages for both research
and clinical practice such as the improvement of diagnosis and management, increasing
awareness among other healthcare professionals and access to more epidemiological data
regarding sarcopenia.
Strengths and limitations
This study is, to the best of our knowledge, the first study assessing the current state of knowl-
edge about the concept of sarcopenia, diagnostic strategy and management of sarcopenia
among healthcare professionals with different working affiliations. Another strength is the spe-
cially developed multidisciplinary lecture cycle based on the translation from recent evidence
into clinical practice. Selection bias is likely because the included healthcare professionals were
the ones most interested and motivated to attend a postgraduate program. In addition, the
healthcare professionals who responded to the questionnaire five months after attendance
were probably the most motivated ones, in comparison to the non-responders. Other limita-
tions of the study are the relative small group of dietitians while dietitians play an important
role in the diagnostic strategy and management of sarcopenia. A final limitation is the use of
questionnaires, which may have led to possible socially desirable responding.
Conclusion
The concept of sarcopenia is familiar to most Dutch healthcare professionals but application
in practice is hampered, mostly by lack of formal knowledge, availability of equipment and
time constraints. For the management of sarcopenia, collaboration between healthcare profes-
sionals should be improved. Educational lectures regarding sarcopenia could be a first step to
create more awareness among healthcare professionals, but more steps are required for suc-
cessful implementation.
Current state of the art on the knowledge and practice of sarcopenia
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Supporting information
S1 Table. Complete questionnaires before, directly after and five months after attendance.
(DOCX)
S2 Table. Management of sarcopenia depicted as consulted healthcare professionals for
interventions before and directly after attendance, total and stratified by group of health-
care professionals.
(DOCX)
Acknowledgments
The authors thank the healthcare professionals for their contribution to the study.
Author Contributions
Conceptualization: Esmee M. Reijnierse, Marian A. E. de van der Schueren, Marijke C. Trap-
penburg, Marjan Doves, Carel G. M. Meskers, Andrea B. Maier.
Data curation: Esmee M. Reijnierse.
Formal analysis: Esmee M. Reijnierse.
Methodology: Esmee M. Reijnierse, Marian A. E. de van der Schueren, Marijke C. Trappen-
burg, Marjan Doves, Carel G. M. Meskers, Andrea B. Maier.
Project administration: Esmee M. Reijnierse.
Resources: Esmee M. Reijnierse.
Supervision: Marian A. E. de van der Schueren, Marijke C. Trappenburg, Carel G. M. Mes-
kers, Andrea B. Maier.
Visualization: Esmee M. Reijnierse.
Writing – original draft: Esmee M. Reijnierse.
Writing – review & editing: Esmee M. Reijnierse, Marian A. E. de van der Schueren, Marijke
C. Trappenburg, Marjan Doves, Carel G. M. Meskers, Andrea B. Maier.
References
1. Landi F, Liperoti R, Russo A, Giovannini S, Tosato M, Capoluongo E, et al. Sarcopenia as a risk factor
for falls in elderly individuals: results from the ilSIRENTE study. Clin Nutr. 2012; 31(5):652–8. https://
doi.org/10.1016/j.clnu.2012.02.007 PMID: 22414775
2. Scott D, Hayes A, Sanders K, Aitken D, Ebeling PR, Jones G. Operational definitions of sarcopenia and
their associations with 5-year changes in falls risk in community-dwelling middle-aged and older adults.
Osteoporos Int. 2014; 25(1):187–93. https://doi.org/10.1007/s00198-013-2431-5 PMID: 23800748
3. Bijlsma AY, Pasma JH, Lambers D, Stijntjes M, Blauw GJ, Meskers CG, et al. Muscle Strength Rather
Than Muscle Mass Is Associated With Standing Balance in Elderly Outpatients. J Am Med Dir Assoc.
2013; 14(7):493–8. https://doi.org/10.1016/j.jamda.2013.02.001 PMID: 23540951
4. Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, et al. Epidemiology
of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998; 147(8):755–63. PMID:
9554417
5. Janssen I, Heymsfield SB, Ross R. Low relative skeletal muscle mass (sarcopenia) in older persons is
associated with functional impairment and physical disability. J Am Geriatr Soc. 2002; 50(5):889–96.
PMID: 12028177
6. Batsis J, Mackenzie T, Barre L, Lopez-Jimenez F, Bartels S. Sarcopenia, sarcopenic obesity and mor-
tality in older adults: results from the National Health and Nutrition Examination Survey III. Eur J Clin
Nutr. 2014; 68(9):1001–7. https://doi.org/10.1038/ejcn.2014.117 PMID: 24961545
Current state of the art on the knowledge and practice of sarcopenia
PLOS ONE | https://doi.org/10.1371/journal.pone.0185837 October 2, 2017 9 / 10

7. Bunout D, de la Maza MP, Barrera G, Leiva L, Hirsch S. Association between sarcopenia and mortality
in healthy older people. Australas J Ageing. 2011; 30(2):89–92. https://doi.org/10.1111/j.1741-6612.
2010.00448.x PMID: 21672118
8. Beaudart C, Rizzoli R, Bruyère O, Reginster J-Y, Biver E. Sarcopenia: burden and challenges for public
health. Arch Public Health. 2014; 72(1):45. https://doi.org/10.1186/2049-3258-72-45 PMID: 25810912
9. Janssen I, Shepard DS, Katzmarzyk PT, Roubenoff R. The healthcare costs of sarcopenia in the United
States. J Am Geriatr Soc. 2004; 52(1):80–5. PMID: 14687319
10. Reijnierse EM, Trappenburg MC, Leter M, Blauw G, Sipila
¨S, Sillanpa
¨a
¨E, et al. The Impact of Different
Diagnostic Criteria on the Prevalence of Sarcopenia in Healthy Elderly Participants and Geriatric Outpa-
tients. Gerontology. 2015; 61(6):491–6. https://doi.org/10.1159/000377699 PMID: 25871733
11. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia:European
consensus on definition and diagnosis Report of the European Working Group on Sarcopenia in Older
People. Age Ageing. 2010; 39(4):412–23. https://doi.org/10.1093/ageing/afq034 PMID: 20392703
12. Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, et al. Sarcopenia: an undiagnosed
condition in older adults. Current consensus definition: prevalence, etiology, and consequences. Inter-
national working group on sarcopenia. J Am Med Dir Assoc. 2011; 12(4):249–56. https://doi.org/10.
1016/j.jamda.2011.01.003 PMID: 21527165
13. Studenski SA, Peters KW, Alley DE, Cawthon PM, McLean RR, Harris TB, et al. The FNIH Sarcopenia
Project: Rationale, Study Description, Conference Recommendations, and Final Estimates. J Gerontol
A Biol Sci Med Sci. 2014; 69(5):547–58. https://doi.org/10.1093/gerona/glu010 PMID: 24737557
14. Bonnefoy M, Cornu C, Normand S, Boutitie F, Bugnard F, Rahmani A, et al. The effects of exercise and
protein–energy supplements on body composition and muscle function in frail elderly individuals: a
long-term controlled randomised study. Br J Nutr. 2003; 89(05):731–8.
15. Bunout D, Barrera G, de la Maza P, Avendaño M, Gattas V, Petermann M, et al. The impact of nutri-
tional supplementation and resistance training on the health functioning of free-living Chilean elders:
results of 18 months of follow-up. The Journal of nutrition. 2001; 131(9):2441S–6S. PMID: 11533291
16. Tieland M, Dirks ML, van der Zwaluw N, Verdijk LB, van de Rest O, de Groot LC, et al. Protein supple-
mentation increases muscle mass gain during prolonged resistance-type exercise training in frail elderly
people: a randomized, double-blind, placebo-controlled trial. J Am Med Dir Assoc. 2012; 13(8):713–9.
https://doi.org/10.1016/j.jamda.2012.05.020 PMID: 22770932
17. Kim HK, Suzuki T, Saito K, Yoshida H, Kobayashi H, Kato H, et al. Effects of Exercise and Amino Acid
Supplementation on Body Composition and Physical Function in Community-Dwelling Elderly Japa-
nese Sarcopenic Women: A Randomized Controlled Trial. J Am Geriatr Soc. 2012; 60(1):16–23.
https://doi.org/10.1111/j.1532-5415.2011.03776.x PMID: 22142410
18. Montero-Fernandez N, Serra-Rexach J. Role of exercise on sarcopenia in the elderly. Eur J Phys Reha-
bil Med. 2013; 49(1):131–43. PMID: 23575207
19. Bauer J, Biolo G, Cederholm T, Cesari M, Cruz-Jentoft AJ, Morley JE, et al. Evidence-based recom-
mendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE
Study Group. J Am Med Dir Assoc. 2013; 14(8):542–59. https://doi.org/10.1016/j.jamda.2013.05.021
PMID: 23867520
20. Paddon-Jones D, Rasmussen BB. Dietary protein recommendations and the prevention of sarcopenia:
protein, amino acid metabolism and therapy. Curr Opin Clin Nutr Metab Care. 2009; 12(1):86. https://
doi.org/10.1097/MCO.0b013e32831cef8b PMID: 19057193
21. Ter Beek L, Vanhauwaert E, Slinde F, Orrevall Y, Henriksen C, Johansson M, et al. Unsatisfactory
knowledge and use of terminology regarding malnutrition, starvation, cachexia and sarcopenia among
dietitians. Clin Nutr. 2016; 35(6):1450–6. https://doi.org/10.1016/j.clnu.2016.03.023 PMID: 27075318
22. Durlak JA, DuPre EP. Implementation matters: A review of research on the influence of implementation
on program outcomes and the factors affecting implementation. Am J Community Psychol. 2008; 41(3–
4):327–50. https://doi.org/10.1007/s10464-008-9165-0 PMID: 18322790
23. Green LW. Making research relevant: if it is an evidence-based practice, where’s the practice-based
evidence? Fam Pract. 2008; 25(suppl 1):i20–i4.
24. Cao L, Morley JE. Sarcopenia Is Recognized as an Independent Condition by an International Classifi-
cation of Disease, Tenth Revision, Clinical Modification (ICD-10-CM) Code. J Am Med Dir Assoc. 2016;
17(8):675–7. https://doi.org/10.1016/j.jamda.2016.06.001 PMID: 27470918
Current state of the art on the knowledge and practice of sarcopenia
PLOS ONE | https://doi.org/10.1371/journal.pone.0185837 October 2, 2017 10 / 10