Original Communication

Journal of Parenteral and Enteral

Nutrition
AGREEing on Guidelines for Nutrition Management of Adult Volume 0 Number 0
xxxx 2018 1–7
Severe Burn Patients 
C 2018 American Society for

Parenteral and Enteral Nutrition

DOI: 10.1002/jpen.1452
wileyonlinelibrary.com

Maria G. Grammatikopoulou, PhD1,2,3 ; Xenophon Theodoridis, MS2 ;

3
Konstantinos Gkiouras, MS ; Eleni-Maria Stamouli, PharmD4 ;
Myrsini-Eleni Mavrantoni, MS ; Theodore Dardavessis, PhD3 ;
3

and Dimitrios P. Bogdanos, PhD5,6

Abstract
Background: Severe burns are associated with a plethora of profound metabolic, immunologic, and physiologic responses,
demanding prompt and adequate management. The objective of the present study was to review, compare, and critically appraise
medical nutrition therapy guidelines for adult patients with severe burns, and produce salient points for the future update of relevant
guidelines. Methods: A total of 8 clinical practice guidelines developed by the American Burn Association (ABA), the European
Burn Association (EBA), the European Society for Parenteral and Enteral Nutrition (ESPEN), the Midlands National Health
Service, the Society for Critical Care Medicine (SCCM)/American Society for Parenteral and Enteral Nutrition (ASPEN), the
Spanish Society of Intensive Care Medicine and Coronary Units and Spanish Society of Parenteral and Enteral Nutrition, the
Indian Association for Parenteral and Enteral Nutrition (IAPEN), and the International Society for Burn Injury regarding medical
nutrition therapy in burn patients was independently reviewed by a team of 4 multidisciplinary researchers using the Appraisal
of Guidelines for Research & Evaluation (AGREE II) instrument. Results: From the appraised guidelines, the SCCM/ASPEN
guidelines received the greatest scoring in the majority of AGREE domains compared with ABA, EBA, and IAPEN, which obtained
the lowest scores. On the other hand, the ESPEN guidelines provided the majority of information concerning nutrition support
and medical nutrition therapy. Conclusion: Our study identified gaps in most nutrition guidelines and emphasized methodologic
issues that could improve the quality of future guidelines concerning nutrition support among adult severe burn patients. (JPEN J
Parenter Enteral Nutr. 2018;0:1–7)

Keywords
clinical practice guidelines; critical appraisal; critically ill; diet; enteral nutrition; ICU; injury; medical nutrition therapy; nutrition;
nutrition intervention; trauma

Clinical Relevancy Statement However, research shows that the degree of adherence to
the clinical practice guidelines is low among health profes-
Nutrition support in major burns is an important con- sionals. A review and critical appraisal of the guidelines
stituent of therapy, as well as a pivotal outcome effector. for the nutrition management of severe burn patients using

From the 1 Department of Nutrition and Dietetics, Alexander Technological Educational Institute, Thessaloniki, Greece; 2 Department of
Medicine, Faculty of Health Sciences, University of Thessaly, Larissa, Greece; 3 Department of Medicine, Faculty of Health Sciences, Aristotle
University of Thessaloniki, Thessaloniki, Greece; 4 Department of Pharmacy, Faculty of Health Sciences, Aristotle University of Thessaloniki,
Thessaloniki, Greece; 5 Department of Rheumatology and Clinical Immunology, Faculty of Medicine, School of Health Sciences, University of
Thessaly, Larissa, Greece; and the 6 Division of Transplantation, Immunology and Mucosal Biology, MRC Centre for Transplantation, King’s
College London Medical School, London, UK.
Financial disclosure: None declared.
Conflicts of interest: None declared.
Received for publication July 26, 2018; accepted for publication September 11, 2018.
Corresponding Author:
Maria G. Grammatikopoulou, PhD, Department of Nutrition and Dietetics, Alexander Technological Educational Institute, Sindos, PO Box 141,
GR57400, Thessaloniki, Greece.
Email: maria@nutr.teithe.gr
2 Journal of Parenteral and Enteral Nutrition 0(0)

validated tools such as the Appraisal of Guidelines for the European Burn Association (EBA),16 the European
Research & Evaluation is needed for: 1) identifying gaps Society for Parenteral and Enteral Nutrition (ESPEN),17
in the provided recommendations; and 2) highlighting the the Midlands National Health Service (NHS),18 Society
issues reducing the quality of guidelines. Comprehensive for Critical Care Medicine (SCCM)/the American Society
guidelines of high quality are expected to increase adherence for Parenteral and Enteral Nutrition (ASPEN),19,20 the
among health professionals, reduce individual decisions Spanish Society of Intensive Care Medicine and Coronary
lacking evidence, and improve the provision of care. Units and the Spanish Society of Parenteral and Enteral
Nutrition (SEMICYUC-SENPE),21 the Indian Association
Introduction for Parenteral and Enteral Nutrition (IAPEN),22 and the
International Society for Burn Injury (ISBI).23 Table 1
Severe burns are associated with a plethora of profound
details the guidelines suggested by each body, their main
metabolic, immunologic, and physiologic responses, de-
focus, and characteristics.
manding prompt support and adequate management, with
their effects lasting 2 years post-injury.1,2 The nutrition
support provided aims to mitigate the stress response3 and
to manage hypermetabolism4 and the associated increased Guidelines Appraisal
energy expenditure.3 Ultimate goals include correcting
A team of 4 multidisciplinary researchers, including a dieti-
for protein catabolism and muscle wasting, promoting
tian/nutritionist, 2 medical doctors, and a pharmacist, inde-
wound healing, and providing all essential micronutrients
pendently appraised the guidelines based on the Appraisal
to combat inflammation and distorted cell membrane
of Guidelines for Research & Evaluation (AGREE II)
homeostasis.1 Overcoming feeding complications,5 while
instrument.24 The AGREE tool examines 6 main domains
managing the induced hyperinsulinemia6 and sepsis, are
and a total of 23 items evaluating quality of the guidelines.
additional issues of key importance.7
The reviewers independently assigned a score to each item
Despite the importance of implementing evidence-
ranging from 1 (strongly disagree) to 7 (strongly agree),
based nutrition strategies for the management of severe
and the total scoring of each domain for each guideline
burns patients,8 the degree of adherence to the guide-
was calculated as a percentage (0%–100%) of the maximum
lines appears low,9,10 and the pragmatic clinical approach
possible score in each domain, minus the minimum possible
varies greatly from what is recommended.11 This prob-
score, based on the items and the number of reviewers.24,25
lem might stem from inadequate dissemination of the
Finally, each reviewer expressed their overall recommen-
guidelines,12 insufficient education or interest by health
dation for suggesting the use of the guidelines according
professionals,13 disagreement among health providers with
to AGREE,24 as “recommend without modifications,” “rec-
some recommendations,12 gaps and inconsistencies in
ommend with modifications,” or “not recommend.”
the provided guidelines, perceived low quality of the
guidelines,12 and/or lack of detailed suggestions concern-
ing dose and administration of the provided care for
each domain of the medical nutrition therapy (MNT). Results
With the suggested guidelines providing generic population
Table 2 details the percent scores of the selected guidelines
recommendations,14 decision making and patient-tailored
according to the 4 reviewers. The SCCM/ASPEN19,20 guide-
care become essential components of MNT. However,
lines received the highest scoring in the majority of AGREE
adherence to the guidelines is still required to minimize
domains, the overall quality, and recommendations without
independent and personal behaviors concerning therapy,
modification by the reviewers. The lowest scores were mainly
which may entail clinical risks.12
demonstrated by ABA,15 EBA,16 and IAPEN.22 The ABA15
The aim of the present study was to review, compare, and
and EBA16 guidelines were the least recommended by the
critically appraise guidelines for the nutrition management
reviewers, and received the lowest quality ratings overall.
of adult severe burn patients and produce salient points for
Table 3 displays an overview of the nutrition recommen-
the update of future relevant guidelines.
dations for severe burn patients, based on the selected guide-
lines. The majority of information concerning MNT and
Methods
nutrition support was provided by the ESPEN17 guidelines,
A total of 8 advising bodies was retrieved from followed by the UK18 and the Spanish guidelines.21 The
PubMed/Medline, Google, and the Guidelines International least nutrition-related information was incorporated in the
Network, providing professional practice guidelines for ABA15 guidelines.
the MNT of adult severe burn patients, published in Supplementary Table 1 details the nutrition recommen-
the English language, during the last 10 years. Advising dations provided by each advising body and highlights the
bodies included the American Burn Association (ABA),15 between-guidelines differences in adult severe burn MNT.
Grammatikopoulou et al 3

Table 1. General Description of Guidelines Included, and Their Scope.

Scope Organization

Nutrition Support
in Critically Ill
Burn Care With Patients With
Enclosed MNT Enclosed Total
Nutrition in Burn Recommendations Number
Advising Body Country Recommendations Patients for Burn Patients Professional Government of Pages

ABA15 USA   13
EBA16 Europe   95
ESPEN17 Europe   6
IAPEN22 India   18a
ISBI23 International   69
NHS18 UK   52
SCCM/ASPEN19,20 USA   53
SEMICYUC- Spain    4
SENPE21

, included; ABA, American Burn Association; EBA, European Burn Association; ESPEN, European Society for Parenteral and Enteral
Nutrition; IAPEN, Indian Association for Parenteral and Enteral Nutrition; ISBI, International Society for Burn Injury; MNT, medical nutrition
therapy; NHS, National Health Service; SCCM/ASPEN, Society of Critical Care Medicine/American Society for Parenteral and Enteral
Nutrition; SEMICYUC: Spanish Society of Intensive Care Medicine and Coronary Units; SENPE: Spanish Society of Parenteral and Enteral
Nutrition.
a With links to additional recommendations provided online, by other advising bodies.

Discussion Unlike SCCM/ASPEN19,20 and ISBI,23 ESPEN17 failed to

clearly define target users. Target population preferences
The present study highlighted the inadequate quality and
and views were not accounted for by the ESPEN17 or
gaps in nutrition guidelines for severe burn patients. Differ-
SCCM/ASPEN19,20 guidelines, whereas NHS18 reported a
ent guidelines scored better in distinct AGREE domains,
scheduled future audit process for updating the guidelines.
with the SCCM/ASPEN19,20 recommendations receiving
As far as rigor, guidelines grading the evidence of
the greatest scores in the majority of domains, overall qual-
the suggested recommendations while providing detailed
ity, and recommendation by the review panel. However, the
reference sources scored better on AGREE. Additionally,
ESPEN17 guidelines appeared to present more information
those with detailed search methods and criteria for evidence
concerning hands-on burn-specific MNT.
selection (SCCM/ASPEN19,20 and ISBI23 ) were in greater
Scope and purpose of the SCCM/ASPEN19,20 guidelines
compliance with the AGREE standards and, subsequently,
were in total agreement with AGREE (Table 2). Questions
received better appraisal scores. Benefits and harms were
addressed by the guidelines were not explicitly reported by
not reported in EBA,16 ABA,15 or SEMICYUC-SENPE.21
ESPEN,17 with the majority being scattered throughout the
ESPEN17 reported few harms, but side effects/risks were
manuscript text. Questions were also inadequately reported
not thoroughly mentioned. The external review process
by IAPEN22 and NHS,18 but ABA15 and EBA16 had the
of ESPEN17 involved non-experts, whereas IAPEN22
lowest scoring on the scope and purpose domain.
employed burn surgeons for the procedure. Post-discharge
The greater stakeholder involvement in scoring was
and outpatient care recommendations were only provided
observed in the ISBI23 recommendations. ESPEN17 lacked
by NHS.18
involvement of dermatologists and plastic surgeons; how-
As far as reviewer recommendation is concerned, the
ever, they are rarely involved in the nutrition management
SCCM/ASPEN19,20 guidelines were unanimously recom-
of severe burn patients in Europe, and their guidelines were
mended without modifications based on the AGREE tool,
MNT-specific, instead of having a general burn manage-
by all reviewers (Table 2). The ESPEN17 and ISBI23
ment scope. Instead, ESPEN17 focused on employing in-
guidelines were recommended without modifications by
tensivists specialized in burn care with nutrition experience;
75% of the panel, with the remaining 25% suggesting the
however, the lack of dietitians was also apparent. Similarly,
implementation of modifications. Additionally, reviewers
EBA16 did not include any dietitians, not even for the more
unanimously suggested the need for revising the NHS18
detailed nutrition issues, whereas ABA15 employed only
guidelines, with the majority of the panel (75%) additionally
1 dietitian for the MNT-specific part of their guidelines.
4 Journal of Parenteral and Enteral Nutrition 0(0)

Table 2. AGREE II Scores of Guidelines for Nutrition Management of Burn Patients (% of Maximum Scoring for Each Domain
and Subcategory).

Guidelines From Advising Bodies

SCCM/ SEMICYUC-
AGREE II Domains ABA15 EBA16 ESPEN17 IAPEN22 ISBI23 NHS18 ASPEN19,20 SENPE21

1. Scope and purpose 63.9 54.2 73.6 52.8 68.1 81.9 100 68.1
1a. Objectives 79.2 79.2 75.0 66.7 83.3 95.8 100 62.5
1b. Questions 29.2 29.2 70.8 54.2 62.5 70.8 100 70.8
1c. Population 83.3 54.2 75.0 37.5 58.3 79.2 100 70.8
2. Stakeholder involvement 30.6 36.1 15.3 37.5 84.7 59.7 45.8 18.1
2a. Group membership 83.3 75.0 29.2 70.8 79.2 50.0 100 37.5
2b. Target population 4.2 4.2 0 16.7 79.2 41.7 0 4.2
preferences and views
2c. Target users 4.2 29.2 16.7 25.0 95.8 87.5 100 12.5
3. Rigor 9.4 20.8 49.5 19.8 76.6 51.0 95.3 57.3
3a. Search methods 0 12.5 62.5 25.0 95.8 50.0 100 100
3b. Evidence criteria 4.2 0 62.5 4.2 95.8 54.2 100 95.8
3c. Evidence strengths and 4.2 4.2 50.0 4.2 54.2 20.8 95.8 58.3
limitations
3d. Recommendations 0 4.2 66.7 0 83.3 37.5 95.8 79.2
formulation
3e. Benefits and harms 4.2 4.2 33.3 29.2 100 20.8 100 29.2
consideration
3f. Recommendations and 62.5 45.8 87.5 45.8 70.8 70.8 87.5 66.7
evidence link
3g. External review 0 12.5 33.3 33.3 70.8 66.7 83.3 29.2
3h. Updating procedures 0 83.3 0 16.7 41.7 87.5 100 0
4. Clarity of presentation 61.1 36.1 91.7 52.8 95.8 81.9 100 70.8
4a. Specific, unambiguous 58.3 37.5 83.3 54.2 95.8 79.2 100 70.8
recommendations
4b. Management options 45.8 45.8 91.7 37.5 95.8 70.8 100 70.8
4c. Identifiable key 79.2 25.0 100 66.7 95.8 95.8 100 70.8
recommendations
5. Applicability 36.5 27.1 22.6 15.6 63.5 45.8 41.7 24.0
5a. Application 45.8 16.7 12.5 29.2 83.3 37.5 50.0 29.2
facilitators and barriers
5b. Implementation of 41.7 4.2 0 20.8 50.0 29.2 0 4.2
advice/tools
5c. Resource implications 45.8 16.7 0 12.5 70.8 45.8 33.3 0
5d. Monitor/audit criteria 12.5 70.8 0 0 50.0 70.8 83.3 62.5
6. Editorial independence: 0 0 100 0 52.1 100 100 87.5
6a. Funding body 0 0 100 0 4.2 100 100 100
6b. Competing interests 0 0 100 0 100 100 100 75.0
Overall Quality 37.5 29.2 66.7 33.3 83.3 50.0 100 45.8
Recommendation
Without modifications 0 0 75.0 0 75.0 0 100 0
With modifications 0 0 25.0 75.0 25.0 100 0 75.0
Not recommended 100 100 0 25.0 0 0 0 25.0

Highest scoring in each domain is presented in bold.

ABA, American Burn Association; AGREE, Appraisal of Guidelines for Research and Evaluation24 ; EBA, European Burn Association; ESPEN,
European Society for Parenteral and Enteral Nutrition; IAPEN: Indian Association for Parenteral and Enteral Nutrition; ISBI, International
Society for Burn Injury; NHS, National Health Service; SCCM/ASPEN, Society of Critical Care Medicine/American Society for Parenteral and
Enteral Nutrition; SEMICYUC: Spanish Society of Intensive Care Medicine and Coronary Units; SENPE, Spanish Society of Parenteral and
Enteral Nutrition.
Grammatikopoulou et al 5

Table 3. Overview of Recommendations for Nutrition Management of Severe Burn Patients.

SCCM/ SEMICYUC-
Recommendation ABA15 EBA16 ESPEN17 IAPEN22 ISBI23 NHS18 ASPEN19,20 SENPE21

Dietitian needed -  -  -  - -
MNT aim -  -  -  - -
Nutrition screening on admissiona - - - -    -
Routine screening -  - -   - -
Patient nutrition education -  - - - - - -
Nutrition care plan - - - - -  - -
Fluid needs -  - - - - - -
Fluid resuscitation -   -  - - -
Feeding initiation time point - -      -
Feeding route  -      
Feeding solution recommendations - -  - - - - -
Indirect calorimetry use - -  - - -  
Specific predictive EER equations    -    
Goal protein intake  -  -    
Amino acid supplementation - -  - -  - 
Goal carbohydrate intake - -  - - - - 
Preferred carbohydrate type - - - - - - - 
Goal fiber intake - -  - - - - -
Glucose control tactics - -  - - - Not burn- 
specific
Goal lipid intake - -  - - - - 
Lipid emulsion suggestions 
Vitamin C recommendations - -  - -  - -
Vitamin D recommendations - -  - -  - -
Vitamin E recommendations - -  - - - -
Vitamin A recommendations - - - - -  - -
Copper, selenium, zinc recommendations - -  - -  - 
Nursing temperature for metabolic modulation - -  - - - - -
rhGH administration - -  - - - - -
Monitoring MNT guidelines - - - - -  - -
Outpatient care - - - - -  - -
Dietitian follow-up post-discharge and home care - - - - -  - -

, included; -, lacking; ABA, American Burn Association; EBA, European Burn Association; EER, estimated energy requirements; ESPEN,
European Society for Parenteral and Enteral Nutrition; IAPEN, Indian Association for Parenteral and Enteral Nutrition; ISBI, International
Society for Burn Injury; MNT, medical nutrition therapy; NHS, National Health Service; rhGH, recombinant human growth hormone;
SCCM/ASPEN, Society of Critical Care Medicine/American Society for Parenteral and Enteral Nutrition; SEMICYUC, Spanish Society of
Intensive Care Medicine and Coronary Units; SENPE, Spanish Society of Parenteral and Enteral Nutrition.
a Nutrition screening including weight monitoring.

voting for an update of the SEMICYUC-SENPE21 and
IAPEN22 guidelines.
The present study also indicates discrepancies between
the AGREE domains scoring (Table 2) and the amount
of information provided in the guidelines (Table 3 and
supplementary table). For instance, the ESPEN17 guidelines
were the most informative in terms of burn-specific MNT;
however, they failed to fulfill many of the AGREE stan-
dards. Considering these domains in future updates will un-
doubtedly increase the validity of the ESPEN17 guidelines
and their use, given that they present a more thorough and
comprehensive aspect of burn-specific MNT. On the other
hand, inclusion of more information concerning hands-on
burn-specific MNT might ameliorate the overall content of
the SCCM/ASPEN19,20 guidelines.
Of note, the current appraisal also delineates the for-
gotten role of dietitians in the provision of burn care.
The ABA,15 SCCM/ASPEN,19,20 ESPEN,17 and Spanish21
guidelines failed to stress the need for a multidisciplinary
team in the management of severe burns patients, including
a dietitian. Nutrition screening on admission was only sug-
gested by few advising bodies,18-20,23 and routine nutrition
assessment was left out by the majority.15,17,19-22 Specific
MNT aims were only mentioned in 3 of the reviewed
guidelines,16,18,22 and the implementation of a detailed
nutrition care plan was considered by NHS18 alone. As far
6 Journal of Parenteral and Enteral Nutrition 0(0)
as energy and protein recommendations, they are missing in
both the ABA15 and the IAPEN22 guidelines, with protein
goals also lacking in the EBA16 suggestions. Percent of
feeding adequacy achieved during hospitalization was only
mentioned by few bodies. Additionally, patient-tailored
energy provision assessed by indirect calorimetry was sug-
gested by ESPEN,17 SCCM/ASPEN,19,20 and SEMICYUC-
SENPE,21 with the remaining advising bodies proposing the
use of predictive equations, a considerable a weakness for
the provision of adequate care of burn patients. Optimal
carbohydrate and lipid intake ranges were reported solely
by ESPEN17 and SEMICYUC-SENPE.21 Only NHS18
provided information for nutrition support post-discharge
and outpatient care. However, it should be noted that only
the ESPEN,17 IAPEN,22 and NHS18 guidelines were MNT-
specific for severe burn patients. The remaining guidelines
were either aiming to provide overall recommendations for
burn care, or to provide recommendations for the nutrition
support in critically ill patients.
According to Fischer,26 guideline non-adherence can be
divided into personal factors, including physician culture,
guideline-related reasons, and external determinants. The
inadequate presentation of some topics included in the
guidelines has also been suggested as a barrier for non-
adherence to the guidelines.12 Resistance of health pro-
fessionals toward guideline adherence appears unanimous
in the literature.27-29 Health professionals are in need of
simple, current, reliable, and accessible guidelines,28 while,
in parallel, the demand for training health professionals
in guideline usage becomes a priority.30 Additionally, a
recent systematic review31 highlighted the issue of sus-
tainability of professionals’ adherence to clinical practice
guidelines, with the majority of professionals abandon-
ing guideline usage, a year after being familiar with the
recommendations.
Strengths of the study include the individual evaluation
of each guideline by a multidisciplinary panel of reviewers,
and the use of a validated tool. On the other hand, limi-
tations stem from the inclusion of guidelines published in
the English language only. It should be noted, however, that
the aim of the present study was not to criticize the existing
guidelines, but rather to critically appraise them, in order to
aid in the development of future guidelines with less bias,
and more rigor.
Guidelines serve to promote evidence-based decisions in
the clinical practice area,32 bridging health services research,
with provided care. At the same time, non-adherence to
guidelines results in insufficient healthcare, great discrepan-
cies in the provided care, worse disease outcomes, and in-
creased medical costs.30 The present study identified gaps in
the current guidelines and highlighted several methodologic
issues that could increase the quality of the recommenda-
tions for the provision of nutrition support among adult
severe burn patients.
Acknowledgement
Given that this work was submitted in July 2018, the authors
dedicate it to the victims of the July 23, 2018, wildfires in
Marathon, Greece.
Statement of Authorship
M. G. Grammatikopoulou, T. Dardavessis, and D. P. Bog-
nadons equally contributed to the conception and design
of the research; M. G. Grammatikopoulou, X. Theodoridis
E.-M. Stamouli, K. Gkiouras, and M.-E. Mavrantoni con-
tributed to the acquisition and analysis of the data; M. G.
Grammatikopoulou, T. Dardavessis, K. Gkiouras, and X.
Theodoridis contributed to the interpretation of the data; and
M. G. Grammatikopoulou and D. P. Bogdanos drafted the
manuscript. All authors critically revised the manuscript, agree
to be fully accountable for ensuring the integrity and accuracy
of the work, and read and approved the final manuscript.
Supplementary Information
Additional supporting information may be found online in the
Supporting Information section at the end of the article.
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