Strengthening the Reporting of Observational Studies in Epidemiology—Nutritional Epidemiology (STROBE-nut): An Extension of the STROBE Statement

<jats:title>Abstract</jats:title><jats:p>Concerns have been raised about the quality of reporting in nutritional epidemiology. Research reporting guidelines such as the Strengthening the Reporting of Observational Studies in Epidemiology (<jats:styled-content style="fixed-case">STROBE</jats:styled-content>) statement can improve quality of reporting in observational studies. Herein, we propose recommendations for reporting nutritional epidemiology and dietary assessment research by extending the <jats:styled-content style="fixed-case">STROBE</jats:styled-content> statement into Strengthening the Reporting of Observational Studies in Epidemiology – Nutritional Epidemiology (<jats:styled-content style="fixed-case">STROBE</jats:styled-content>‐nut). Recommendations for the reporting of nutritional epidemiology and dietary assessment research were developed following a systematic and consultative process, co‐ordinated by a multidisciplinary group of 21 experts. Consensus on reporting guidelines was reached through a three‐round Delphi consultation process with 53 external experts. In total, 24 recommendations for nutritional epidemiology were added to the <jats:styled-content style="fixed-case">STROBE</jats:styled-content> checklist. When used appropriately, reporting guidelines for nutritional epidemiology can contribute to improve reporting of observational studies with a focus on diet and health.</jats:p>

section_content: This study aims to improve the quality of reporting food intake studies through developing a checklist that can be used when researchers report a food intake data. 

Poorly reported food intake studies are unsuccessful in providing accurate description of the methods and findings, and cause heterogeneity that complicates data analysis in systematic reviews (Burrows et al. 2012 ). Readers of poorly reported studies may reach the erroneous conclusions or implement the results improperly in clinical settings, or in new research projects resulting in ineffective use of resources (Moher et al. 2011). 

A research reporting guideline is a simple tool that leads to a better reporting quality and more consistent research literature, without restricting the research creativity. A guideline is mainly a checklist, explicit text, a flow diagram or a combination between these three elements that specifies the items to be reported during a study. 

Implementing the checklist as a guideline, and improving the quality of reporting by journals and researchers would enable better management of resources and more accurate evidence-based decisions by stakeholders, health professionals and clinicians, leading to increased returns of investments (Simera et al. 2010). 

As diet and food intake is an important driver of health, development and use of natural resources, reporting food intake data accurately is a matter of concern. A search identified following checklists for food intake studies:  A guideline for describing nutritional epidemiological study designs developed for information required for all dietary assessment (Michael Nelson and Margetts 1997),  A scoring system developed by Serra-Majem et al. to evaluate the quality of the dietary intake validation studies (Serra-Majem et al. 2009),  A checklist developed by Burrows et al. for systematic reviews to assess the quality of dietary intake methodology and reporting in child and adolescent obesity intervention trials (Burrows et al. 2012), and  A checklist called STROFI "Strengthening the Reporting Of Food Intake" developed by Faber et al. inspired by the STROBE "Strengthening the Reporting of observational studies in Epidemiology" statement (Faber et al. 2013). 

None of the checklists however, were developed following a systematic and acceptable methodology for them to be used widely and endorsed by journals, researchers and other stakeholders internationally. As these checklists lack external validity, there is a recognized need for a checklist to be developed. None of these checklists are registered on the EQUATOR "Enhancing the QUAlity and Transparency of health Research" database of reporting guidelines. 

The present study follows a valid recognized method for developing a checklist. The checklist will be pre-tested before it is finalized and will be accompanied with an explanatory document. An expected outcome of this initiative is a new and pre-tested universal checklist that will be recognized, published, and endorsed by multiple journals and used by researchers. This protocol and checklist will be registered on the EQUATOR Network to increase its recognition, and utilization once developed, also to avoid duplication of efforts with other research groups that might consider developing a similar checklist.
section_name: Background and objectives

section_content: This study will use "The Guidance for Developers of Health Research Reporting Guidelines" method (Moher et al. 2010) with two types of consensus activities:

1. A formal activity to guide the development process of the checklist. A steering committee composed of researchers from three research institutions will manage the study in the face-to-face (video and Skype conferencing) online meetings. 

2. An Informal activity with participants consisting of a large body of international stakeholders of different disciplines (i. e. include methodologists, journal editors, statisticians, epidemiologists, and content experts) will be involved in 3 Delphi rounds. These participants will provide the essential input for the checklist and will be contacted through email.
section_name: Methods

section_content: To develop the checklist eight main activities will be carried out (Figure 1 ).
section_name: Design

section_content: The protocol of the study and the pre-tested questionnaires will be registered on the EQUATOR website after ethical clearance has been obtained (Step 2).
section_name: Registration on the EQUATOR website

section_content: A search for articles concerning food intake studies will be conducted during the development of the checklist to assess the quality of the reporting (Step 3). Information related to sources of bias in these studies will then be identified to have an insight into the items that need to be included in the checklist (Moher et al. 2010). The step will also consider emerging empirical data that reflects current practices.
section_name: Literature review

section_content: A reporting checklist needs to be developed with a multi-disciplinary set of participants. 

The Delphi method is a structured group process that is used to collect and understand the opinions of a group of experts in a specific field. It is a practical way to collect information and to reach consensus between experts that are unable to convene physically. The Delphi technique is also flexible as it allows disagreements between participants. Participants are able to express dissenting views, allowing the collection of diverse opinions without causing conflicts. Participants are not influenced by the ideas of others as they are not exposed to them (Cross 1999). For the present study, the Delphi rounds will be constructed according to the recommendation proposed by (Sinha et al. 2011). Although the Delphi process can continue endlessly until there is agreement between all participants, usually three rounds suffice to reach consensus and collect the needed information (Chia-Chien and Brian 2007);(Yousuf 2007). We will conduct a three-stage Delphi process with following specific objectives:

-Delphi round I (Step 4) is a quantitative method and will include open-ended questions, to facilitate getting as many ideas and opinions as possible on the items that need to be included in the checklist. This round is essential as it provides the basic input for the first draft of the checklist. Annex 1 contains the question of the Delphi round I. Prior to dissemination, the questionnaire will be pre-tested with a sample of ten volunteering researchers. 

-Delphi round II (Step 7) will be carried out after the first face-to-face meeting and based on the developed checklist. It will mainly contain dichotomous questions, to check the level of agreement on the items included within the developed checklist. The items will be answered online. The content of the checklist will depend on input from the first Delphi round and information brought up in the first face-to-face meeting. Annex 1 shows how the second round of the Delphi will probe for answers for the various items. An example of similar items that could be included in our checklist is the STROFI checklists (Faber et al. 2013, Vandenbroucke et al. 2007 ) (Annex 2). 

-Delphi round III (step 10) will be the last round and will be carried out after the second face-to-face meeting. This round allows the researchers to reach acceptable consensus and stability of answers within the group, within a considerable timeframe. The questions in this round will be similar to the questions asked during round two, however they will be based on the refined checklist that generates from Delphi round II and face-to-face meeting II. The Delphi round III questions are included as Annex 1. 

Invitation letters together with the informed consent will be sent and participants will be given a period of two weeks to reply, they will be sent a reminder once during the data collection period. The invitation letter and informed consent are included as Annex
section_name: Delphi rounds

section_content: Based on the answers obtained from the first Delphi round and the items considered important from the literature review, a large number of items are expected. A reduction to a concise, more manageable number of items for the checklist will be carried out by the steering committee. Two research groups of the steering committee will carry out the data reduction independently. The third group will serve as moderator and resolve conflicts and disagreements. Using consensus, the steering committee appointed experts of National Institute for Public Health and the environment in the Netherlands (RIVM) as moderator for the first round, the WHO International Agency for Research on Cancer, France (IARC) for the second round and Gent University, Belgium (UGent)

for the last round. 

The two checklists prepared from the Delphi rounds will be discussed during the first face-to-face meeting. During this meeting agreement will be reached on a final version as an output of this meeting. Items retrieved during the extensive literature review that were not brought up in the Delphi round might also be added to this version. 

Consensus at this stage is pre-defined and will follow the recommendation of (Sinha et al. 2011) and is set to be achieved as agreement of > 70% for each item on the checklist included. In the second and third Delphi round more consensus is expected and a threshold of >80% agreement will be used. 

To promote transparency, substantial disagreement, reasons and incorporating the reasons for disagreement will be identified and reported in the minutes of the meeting and exploratory document that complements the checklist.
section_name: Generating a list of items for consideration during the face-to-face meeting

section_content: Steering committee meetings will be organized through a videoconference. A conference room with the needed resources for every meeting, and a suitable time to allow maximum participation will be foreseen. No meals will be provided and participants will not need to travel. 

In each meeting, there will be an introductory phase, and an overall summary of the agenda. The Delphi round results, results of the data reduction, empirical evidence from literature, background topics and some glossary such as what could be considered as an item on the list will be presented in the meeting. An alternating moderator will be assigned. 

The discussions will revolve around the items and information in the checklist and the rational, evidence and consensus behind it. In order to reach consensus, a classification scheme for selecting items to include in the checklist will be used, similar to the one used in developing the Consort checklist (Moher et al. 2010). Each meeting has specific objectives to achieve:

-Face-to-face meeting I (step 6):

 Developing the first food intake checklist, based on the items received from Delphi round I and the items found from the literature, through discussions to reach consensus. 

 This meeting will be chaired and moderated by RIVM. 

-Face to face meeting II (Step 9):

 Discussing the findings of Delphi round II, and using these findings to improve the developed checklist, where items with consensus below 70% on valid responses will be excluded from the refined version of the checklist. 

 Discussing whether it is advisable to develop a flow diagram together with the checklist or not. 

 This meeting will be chaired and moderated by IARC. 

-Face to face meeting III (Step 12):

 Discussing the findings of Delphi round III, where items with consensus below 80% on valid responses will be excluded from the first draft of the checklist that will be pre-tested. 

 Discussing the development of the explanation and elaboration document, and authorship model that needs to be adapted. 

 Discussing the dissemination plan including, publication strategies and journals endorsement. 

 This meeting will be chaired and moderated by UGent.
section_name: The face-to-face consensus meetings

section_content: After drafting and finalizing the checklist, strategies to implement the dissemination plan will be considered by the steering committee.
section_name: Post-meeting activities

section_content: In this step, the focus will be on drafting the checklist with several attempts to come out with the best version. Notes from the face-to-face meeting will be taken into account when developing and organizing concisely worded checklist items. The checklist will be supported by a document that explains the rationale and the development process.
section_name: Developing the guidance statement

section_content: The checklist will be tested through developing a scoring system to assess the quality of reporting of food intake studies. Items on the list will be given a certain weight of the final score depending on the importance of inclusion during reporting, based on consensus of the checklist developers. 

The aim of this test is to check measurement agreement and the reliability of the checklist. Two food intake studies will be selected for scoring by two different groups:

the checklist developers and 30 external participants from the nutrition field. The score of the checklist developers will serve as a basis for comparison with the results obtained by the second group of participants to assess the checklist inter-rater validity and reliability. 

An information letter and informed consent will be distributed before the test (Annex 4 and 5). The scoring checklist together with two chosen studies will be sent and participants will be asked to submit the scores for the two papers back in a week. In case of unwillingness of many invitees to participate in this exercise, a list of additional participants will be developed and they will be contacted to join this part of the research.
section_name: Pilot test the checklist

section_content: An explanatory and elaboration document will be developed and signed by the steering committee. This document will explain the rationale and evidence for the inclusion of each item together with an elaboration on the details of each item. The document will also contain anonymous critical comments and dissenting views on particular items on the checklist to trigger feedback from users and facilitate future efforts in this area.
section_name: Developing the explanation and elaboration document

section_content: To support the use and dissemination of the checklist and for it to be more influential, publishing it in as many journals as possible will be of high priority. The first step will be to contact the editors who took part in the Delphi round to discuss the publication strategy, as well as implementing the publication strategies discussed during the last meeting.
section_name: Developing a publication strategy

section_name: Post-publication activities

section_content: Criticism and feedback will be encouraged from all stakeholders as a way to improve and update the checklist. Contact details and relevant information will be provided in the manuscripts and online.
section_name: Seeking and dealing with feedback and criticism

section_content: The support of journals to endorse and use the developed checklist will be sought. The journal editors that were involved in the checklist development will be first contacted, followed by as many journals as we can contact. Strategies discussed during the last meeting concerning endorsement will be implemented.
section_name: Encouraging endorsement of the checklist

section_content: To ensure that the checklist will have its intended impact, issues concerning adherence to the checklist will be addressed. A clear statement of how authors should use the checklist and what level of adherence is required will be developed, together with some recommendations to the journals that will be endorsing the checklist.
section_name: Supporting adherence to the checklist

section_content: An evaluation round will take place five years after successful endorsement and publication with a review paper.
section_name: Evaluating the impact of reporting checklist

section_content: Putting the checklist on a Gent University website as well as IARC and RIVM will be negotiated, together with issuing a copyright of both the checklist and the explanation and elaboration document.
section_name: Developing a web site

section_content: If the checklist proves to be successful after publications, and other researchers ask to translate it, active involvement in the translation phase will be sought to make sure translation is carried out appropriately.
section_name: Translating the checklist

section_content: The checklist will be updated on a needs basis after a few years, to make sure it reflects current practices of journals and researchers.
section_name: Updating the checklist

section_name: Participants

section_content: An executive group consisting of international multidisciplinary experts from (i) Gent

University in Belgium, (ii) the nutrition and metabolism sector at IARC, and (iii) RIVM will constitute the steering committee. They will guide the development of the checklist and prepare a separate explanatory report that will serve as a new reporting guidance for all study designs that use food intake tools in their data collection. 

Meetings will be organized in advance to ensure the presence of everyone. 

Researchers will be asked to confirm their attendance two weeks before each meeting. 

Two reminders will be sent, one, a week before and one a day before. 

Moreover, in order for all participants in the meeting to have current knowledge about the progress of the study, background information will be sent to them at least one week prior to the meeting to enable informed discussions.
section_name: Participants in the face-to-face meetings

section_content: According to the Delphi technique by (Chia-Chien and Brian 2007) there are no specific criteria to select the participants for the Delphi round. However, participants should be the most appropriate and could be chosen through nomination of the respected and well-known individuals. We aim for least 20 international stakeholders of different disciplines involved in the Delphi rounds and at least three methodologists, three Delphi rounds. Dropout rate will be calculated after each round and unresponsive participants will be contacted to understand the reason behind their dropout of the study. The dropouts for pilot testing the checklist will be managed in the same manner.
section_name: Participants in the Delphi rounds

section_content: The milestones for all steps within this research as following (Table 1 ).
section_name: Timeline

section_content: Participants' confidentiality will be ensured, since only the researcher and principal investigator will have access to aspects like the origin of the feedback opinions, responses during the Delphi rounds and checklist piloting. All participants will remain anonymous, as none of their statements will be attributed to them by name even after the completion of the final report. Each participant will receive an invitation letter with information about the study and an informed consent form. Participation and informed consent will be filled and sent back by email to the researchers.
section_name: Ethical considerations

section_content: There was no outside funding for this study Sections are consistent with those of the Strobe statement for cross-sectional, case-control, cohort and observational studies http://www. strobe-statement. org. We added "supplementary material" and "other".
section_name: Funding

section_content: The checklist will be developed based on the responses from Delphi round I and the face-to-face meeting after the Delphi, therefore the questions in this round will be based on the checklist and they will mainly assess whether the participant agree on each item on the list, therefore agreement on the item, its description and ranking will be assessed using the following format
section_name: Round II Delphi

section_content: The checklist will be further improved based on the responses from Delphi round II and the face-to-face meeting that will follow, therefore the questions in this round will be based on the refined checklist and they will mainly assess whether the participant agree on each item on the list, therefore agreement on the item, its description and ranking will be assessed using the same format used in Delphi round 2 Example 2: STROFI (STrengthening the Reporting Of Food Intake)*: checklist of items that can be addressed in reports of food intake Faber, M., et al. (2013). "Presentation and interpretation of food intake data: Factors affecting comparability across studies. " Nutrition.
section_name: Round III Delphi

section_content: Dear Sir/Madam, We contact you as an expert in dietary assessment methods to participate in the development of a food intake checklist to improve the quality of reporting food intake data. We aim to develop a checklist that is endorsed by journals and helpful to researchers internationally. The study is coordinated by Dr. Carl Lachat (Ugent, Belgium), Dr Inge Huybrechts (IARC, France) and Dr. Marga Ocké (RIVM, Netherlands). 

The checklist will be developed with a multi-disciplinary group of people including methodologists, journal editors, statisticians, epidemiologists, and content experts. For this purpose, we organize a Delphi consultation by e-mail. A steering committee will discuss and summarize the input from the different participants to develop the checklist. This mail initiates the first of three Delphi round. It includes open-ended questions to facilitate getting as many ideas and opinions as possible about items needed to be included in the checklist. This round is essential, as it will serve as the basic input for a first draft of the checklist. If you provide input, we will consider your suggestions during the update of the checklist and disseminate an updated draft of the checklist until consensus is reached. 

We propose a deadline of two weeks for each of the Delphi rounds to receive your input and will send one reminder. 

This study obtained Ethical clearance from Gent University on 10/12/2013 (B670201319178) and did not receive outside funding. The full protocol is available from the EQUATOR website. 

Your privacy and anonymity will be guaranteed. Only the project promoter assisting in the review of the data and a researcher) will have access to raw information gathered. 

Therefore, if you choose to participate in this study please return the informed consent signed by e-mail.  You can revise your answers to the questions if you wish so. 

 Your input will be stored anonymously; researchers not involved in the data collection will not have access to your personal data and name. 

 You can contact the researcher or the coordinator of the project at any time if you wish to obtain more information regarding this study. 

 There are no risks related to your participation in this study. However, in accordance to the Directive concerning experiments on humans (07/05/2004), an insurance with faultless responsibility has been foreseen for the unlikely event that you receive any injury or damage due to the participation in this study. 

I declare that I have been informed about the purpose of this study and understand that I can refuse to answer a particular question and withdraw when I like. My name won't be associated in any publication with the collected information. I accept that there is neither remuneration nor direct benefit for me. 

My consent will be confirmed by returning following statement by email:

"I hereby consent to participate in the Delphi round consultation for the development of a food intake checklist and understand that my views and opinions will be treated confidentially. "
section_name: Annex 3: Invitation letter for Delphi participants

section_content: Project coordinator Dr. Carl Lachat dana. hawwash@UGent. be carl. lachat@UGent. be Annex 5: Invitation letter for a validation study of a food intake guideline Dear Sir, Madam,

We like to invite to participate in the validation of a checklist for reporting food intake studies. The development of the checklist is aims to improve the quality of reporting food intake studies through developing a guideline statement that can be used when researchers report a food intake study. 

This study is a collaboration project between researchers from: Gent University in Belgium, the nutrition and metabolism section at the WHO International Agency for Research on Cancer (IARC) in France, and the National Institute for Public Health and the environment (RIVM) in the Netherlands. A valid recognized method was used to develop a guideline report for food intake studies, using consensus activities. Agreement regarding the checklist was reached in both formal and informal consensus. Formal included face-to-face meetings while informal was limited to Delphi rounds through web communications. The study is already registered on the EQUATOR network. An expected outcome of this initiative is the development of a universal checklist that will be published and endorsed by multiple journals. 

At this stage of the research, the newly developed checklist must be tested before its dissemination. The aim of the testing is to check measurement agreement and the reliability of the checklist. One valid method to verify this is by developing a scoring system for the checklist to assess the quality of already reported food intake studies. Items on the list are given a certain weight of the final score depending on the importance of inclusion during reporting. This scoring system will be used to score two selected food intake studies. 

You have been identified as a potential participant to take part in the checklist pretesting activity and therefore the present letter seeks to provide information about the research so that you become well aware of its implication in the case you decide to participate in it. 

Two selected food intake studies will be emailed to you together with the scoring checklist as soon as you sign the informed consent. You will be given duration of two weeks to read the studies, and assess the quality of their reporting, through giving a certain score for items mentioned on the checklist depending on whether they are reported and if so, the quality of the reporting. Then you have to send the two-scored checklists back with a score for each study. 

The length of scoring the studies depends on the effort and time you put into it, and your willingness to reply. 

The piloting of the checklist will start on the 10 th of April, and we would appreciate if you could submit your answers before the 25 th of April 2014. 

You are not obligated to participate in this study and you may withdraw at any time. Nevertheless, it is very important to participate to have representative data for analysis, and for you to contribute to the development of a better checklist that will be endorsed and published where you can also benefit from it as this guideline should assist in
section_name: Researcher Dana Hawwash

section_name: 1-Journal editors

section_content: journal editors, three statisticians, three epidemiologists, and three content experts. To account for no reply and dropouts, the invitation will be circulated widely to a larger number of experts. Snowballing will be encouraged and invitees will be asked to suggest additional names of participants. To minimize selection bias, a systematical procedure is used to select participants. Two different approaches will be used:

section_content: The criteria of selection are based on journals ranked under the in nutrition and dietetics category of the web of knowledge. The top twenty-five journals in this category were listed and grouped them by publisher. Each group of editors per one publisher will be contacted with one email and invited to take part of the Delphi rounds. One reminder will be sent.
section_name: 1-Journal editors

section_content: A systematic approach will be used to select these participants. First, corresponding authors that have been publishing relevant papers on these matters will be invited (see introduction for examples). If they are unwilling to participate, then the last author will be contacted. Second, work package leaders and principal investigators of large and well-known international dietary assessments projects will be invited. Specifically, the principal investigators of following projects will be contacted: EFCOVAL, EFCOSUM, OPEN STUDY, EU MENU, PANCAKE, ASPADAM.
section_name: 2-The methodologists, statisticians, epidemiologists and the content experts

section_content: Testing the checklist would be done through asking a sample of 30 researchers within the nutrition field to assess two different food intake studies using the scoring checklist developed by the researchers, and comparing their results with the results of the checklist developers obtained when doing the same exercise. These participants will be identified through convenience sampling using personal contacts.
section_name: Participants in the checklist piloting

section_content: The Delphi method is repetitive in nature, and the risk of dropouts during the second and third round usually increases (Cross 1999 ). This will be taken under consideration in this study. The invitation letter will highlight the importance of participating in all Details of the research team Member of the steering committee are listed in table 2. improving the quality of reporting food intake data. The results will be given at the end of the study and we will still be able to discuss it at that time if you wish. 

In accordance to the Directive concerning experiments on humans (07/05/2004), insurance with faultless responsibility has been foreseen for the unlikely event that you receive any injury or damage due to the participation in this study. 

It is important to note that privacy and anonymity will be guaranteed. Only the project promoter assisting in the review of the data and myself will have access to raw information gathered.
section_name: Rigor, validity and reliability