Quality Appraisal of Nutritional Guidelines to Prevent, Diagnose, and Treat Malnutrition in All Its Forms during Pregnancy

This work aimed to identify clinical practice guidelines (CPGs) that include recommendations for the prevention, diagnosis, and treatment of women’s malnutrition during pregnancy and to evaluate the quality of these guidelines using the Appraisal of Guidelines for Research and Evaluation (AGREE II) instrument. We conducted a literature review using PubMed and different websites from January 2009 to February 2021. The quality of the CPGs was independently assessed by reviewers using the AGREE II instrument, which defines guidelines scoring >70% in the overall assessment as “high quality”. The analysis included 43 guidelines. Among the main findings, we identified that only half of the CPGs (51.1%) obtained a final “high quality” evaluation. AGREE II results varied widely across domains and categories. The two domains that obtained the highest scores were scope and purpose with 88.3% (range 39 to 100%) and clarity of presentation with 87.2% (range 25 to 100%). Among the “high quality” CPGs, the best scores were achieved by the three guidelines published by the National Institute of Health and Care Excellence (NICE) and the World Health Organization (WHO). Due to the importance of maternal nutrition in pregnancy, it is essential to join forces to improve the quality of the guidelines, especially in CPGs that do not meet the reference standards for quality.


Introduction
Maternal nutrition crucially contributes to the offspring's health and future generations. Studies in animals and humans have observed adverse developmental processes selection; (iv) charting the data; and (v) collating, summarizing, and reporting results. We added an extra step of (vi) critical appraisal using the AGREE II instrument [16].
The inclusion criteria considered international and national CPGs, consensus, expert opinion based on evidence, and standard references with recommendations on nutritional assessment (behavior, anthropometric, biochemical, clinical evaluation, and lifestyle), healthy diet, dietary modifications, nutritional supplementation, or any nutritional or lifestyle recommendation given in primary healthcare facilities. We excluded opinions, editorials, articles published as communication tools, and CPGs with lifestyle and nutrition recommendations oriented to a specific pathology or associated complications.

Search Strategy and Studies Selection
We performed a systematic literature search in the database PubMed (https://ncbi.nlm. nih.gov/pubmed, accessed on 10 February 2021) and a manual search of guideline-related websites, limiting the search to studies published between January 2009 and February 2021. The selection of this time frame considered the review and update of the Institute of Medicine (IOM) recommendations for weight gain during pregnancy that included ways to encourage their adoption through strategies to assist practitioners with the publication of the "Weight Gain During Pregnancy: Reexamining the Guidelines" in 2009 [17].
For the PubMed search, we used keywords such as pregnancy; pregnancy trimester, first; nutrition assessment; prevention and control; and malnutrition. We followed a Boolean search using search filters to identify any guidelines in English or Spanish (see Table 1). For the guideline-related websites, we selected international agencies and gynecology, obstetrics, and maternal nutrition societies as well as databases from the National Institute of Health and Care Excellence (NICE; UK) and Guidelines International Network (GIN). Key terms of the algorithm were used alone or in combination. We imported all studies identified through the database and the website search to Excel. We checked for and removed duplicates.

Quality Assessment
Authors, including dietitians and physicians, participated in the evaluation process. Two authors (CMM and MAM) independently assessed each study's title and abstract to determine the references' eligibility. In case of disagreement, another author (SBM) evaluated the guide. Several health professionals (CMA, GAC, JMC, KMS, LIG, LTC, MAM, MPC, NSG, SES, AT, BSM, CMM, FAA, and SHC) conducted a peer review to assess the full text of the potentially eligible documents in order to determine if they meet the inclusion criteria. In case of disagreement, a third author (AT, BSM, CMM, GAC, MPC, and SBM) was responsible to decide whether or not to include it.
We used the AGREE II tool to assess the quality of the selected CPGs. This instrument aims to identify the quality guidelines and their strengths and limitations and consists of 23 key items grouped into six domains: (1) scope and purpose (related to the overall aim of the guideline); (2) stakeholder involvement (measures the extent to which the appropriate stakeholders developed the guideline); (3) rigor of development (concerned with the process used to gather and synthesize the evidence); (4) clarity of presentation (appraises the language, structure, and format of the guideline); (5) applicability (related to the implications of applying the guideline); and (6) editorial independence (evaluates that the formulation of recommendations is unbiased with competing interests) followed by 2 global rating items ("overall assessment"). The evaluation of each item uses a 7-point Likert rating scale (from 1 = "strongly disagree" to 7 = "strongly agree), as defined in the AGREE II user's manual [16].
The overall scores of each domain were calculated by adding their corresponding items and scaling the total as a proportion of the maximum possible score for that domain (max score = 100). The overall assessment requires the user to make a judgment as to the quality of the guideline, taking into account the criteria considered in the assessment process. The user is also asked whether he/she would recommend use of the guideline. A score of >70% indicates "high quality" in the guidelines as determined by the AGREE II user's manual [16].
Due to time restrictions, only two authors (BSM, LTC, NRM, SES, AT, FAA, JMC, LIG, and MAM) independently evaluated the quality of each CPG using the online AGREE platform, "My AGREE PLUS", which is suggested by the AGREE II methodology.

Data Analysis
Means and median scores were calculated in each AGREE II domain to identify the most critical domains across the different guidelines. The overall quality evaluation of each guideline used a threshold of 70% for the final score of each domain. We used Microsoft Excel 2021, version 16.57, for data collection and extraction. Figure 1 provides the PRISMA flow diagram [18] with a detailed summary of the research results. We identified 82 records through the search. After removing duplicated studies, the abstracts of 79 records were screened, leading to 54 CPGs for full review and, finally, 43 for quality assessment.   Table 2 shows the general characteristics of the analyzed CPGs. Regarding geographical distribution, 35% of the reviewed guidelines corresponded to the North America Region, with guidelines from Canada (n = 9) and the USA (n = 6), while 37% were from Europe and the Central Asia region, with contribution from the United Kingdom (n = 9), Poland (n = 2), Italy (n = 1), Spain (n = 1), France (n = 1), and Europe region (n = 2). The regions with the lowest number of CPGs reviewed were East Asia and the Pacific, with two CPGs from Australia and the Middle East and North Africa and one CPG from the United Arab Emirates. Finally, we included nine international CPGs (21%).

Results
Concerning the type of recommendations in the reviewed CPGs, 86% had recommendations related to prevention, 56% corresponded to diagnosis, and 27% related to treatment ( Table 2) of any form of malnutrition during pregnancy. Table 3 reports the total score (mean and median) for each domain and the final quality evaluation of all CPGs. Only 51.1% of CPGs obtained a final evaluation of "high quality" with four or more domains reaching a score higher than 70%. Among the "high quality" CPGs, "Antenatal care for uncomplicated pregnancies" (NICE, 2019) [44] had the best score with >90% in all domains, while "Guideline: daily iron supplementation in adult women and adolescent girls" (World Health Organization (WHO), 2016) [54] and "Guideline: vitamin A supplementation in pregnant women" (WHO,2011) [58] both scored >80%  Table 2 shows the general characteristics of the analyzed CPGs. Regarding geographical distribution, 35% of the reviewed guidelines corresponded to the North America Region, with guidelines from Canada (n = 9) and the USA (n = 6), while 37% were from Europe and the Central Asia region, with contribution from the United Kingdom (n = 9), Poland (n = 2), Italy (n = 1), Spain (n = 1), France (n = 1), and Europe region (n = 2). The regions with the lowest number of CPGs reviewed were East Asia and the Pacific, with two CPGs from Australia and the Middle East and North Africa and one CPG from the United Arab Emirates. Finally, we included nine international CPGs (21%).   Concerning the type of recommendations in the reviewed CPGs, 86% had recommendations related to prevention, 56% corresponded to diagnosis, and 27% related to treatment ( Table 2) of any form of malnutrition during pregnancy. Table 3 reports the total score (mean and median) for each domain and the final quality evaluation of all CPGs. Only 51.1% of CPGs obtained a final evaluation of "high quality" with four or more domains reaching a score higher than 70%. Among the "high quality" CPGs, "Antenatal care for uncomplicated pregnancies" (NICE, 2019) [44] had the best score with >90% in all domains, while "Guideline: daily iron supplementation in adult women and adolescent girls" (World Health Organization (WHO), 2016) [54] and "Guideline: vitamin A supplementation in pregnant women" (WHO,2011) [58] both scored >80% in all six domains.

Quality of Guidelines According to the AGREE II Domains
On the other hand, a CPG published by Bomba-Opoń (2017) [23] and another one published by the American Dietetic Association (ADA), American Society of Nutrition (ASN), Siega-Riz, A.M., King, J.C. (2019) [21] obtained the lowest scores with 17 and 25% of total average, respectively.
When looking more thoroughly at domain scores, the highest domain scores were for "scope and purpose" (domain 1) with a mean score of 88.3% (range 39 to 100%) and "clarity of presentation" (domain 4) with a mean score of 87.2% (range 25 to 100%). Meanwhile, the lowest values were for "applicability" (domain 5) with a mean score of 67.8% (range 4 to 100%) and "rigor and development" (domain 3) with a mean score of 74.3% (range 10 to 100%). Figures 2 and 3 show the mean and median quality scores of each domain in the guidelines graded as high and low quality.  [21] obtained the lowest scores with 17 and 25% of total average, respectively.
When looking more thoroughly at domain scores, the highest domain scores were for "scope and purpose" (domain 1) with a mean score of 88.3% (range 39 to 100%) and "clarity of presentation" (domain 4) with a mean score of 87.2% (range 25 to 100%). Meanwhile, the lowest values were for "applicability" (domain 5) with a mean score of 67.8% (range 4 to 100%) and "rigor and development" (domain 3) with a mean score of 74.3% (range 10 to 100%). Figures 2 and 3 show the mean and median quality scores of each domain in the guidelines graded as high and low quality.    [21] obtained the lowest scores with 17 and 25% of total average, respectively.
When looking more thoroughly at domain scores, the highest domain scores were for "scope and purpose" (domain 1) with a mean score of 88.3% (range 39 to 100%) and "clarity of presentation" (domain 4) with a mean score of 87.2% (range 25 to 100%). Meanwhile, the lowest values were for "applicability" (domain 5) with a mean score of 67.8% (range 4 to 100%) and "rigor and development" (domain 3) with a mean score of 74.3% (range 10 to 100%). Figures 2 and 3 show the mean and median quality scores of each domain in the guidelines graded as high and low quality.

Scope and Purpose Domain
Domain 1 had the highest results with a mean of 88.3% (range 39 to 100%) and a median of 89% (range 39 to 100%). Moreover, 30.2% (n = 13) of the guidelines had a maximum score of 100%. Only one guideline presented a score below 50%, which was the Bomba-Opoń (2017) guideline [23] with 39%.

Clarity of Presentation
The mean score in domain 4 was the second highest with 87.2% (range 25 to 100%). Only 27.9% (n = 12) of the guidelines had a high score (100%). In contrast, the guidelines of Cetin, I. [24] and Donnay, S. [30] obtained the lowest scores of 25 and 42%, respectively.

Discussion
The current study presents a rigorous review that explores the quality of 43 CPGs designed to prevent, diagnose, and treat malnutrition in pregnancy using the AGREE II tool. Among the main findings, we identified that only half of the CPGs (51.1%) obtained a final "high quality" evaluation with four or more domains reaching a score higher than 70%. The guidelines classified as high and low quality had a higher evaluation in the classifications of domain 1 "scope and purpose" (mean = 88.3%, range = 39-100%) and domain 4 "clarity of presentation" (main = 87.2%, range = 25-100%). The domains with the lowest score in both groups were "applicability" (mean = 67.8%, range = 4-100%), "rigor of development" (mean = 74.3.3%, range = 10-100%), and "editorial independence" (mean = 75.0%, range = 4-100%).
To our knowledge, there are few systematic reviews that have evaluated the quality of nutrition care guidelines in this population [62][63][64]. These systematic reviews focused mainly on the assessment of weight management guidelines. The findings published by all of them are consistent with ours. The quality of the guidelines regarding the "rigor of development" and "applicability" domains is poor. These observations impact the failure to establish recommendations in clinical practice and, consequently, to address malnutrition in all its forms in pregnant women. As international organizations recognize them, all the guidelines identified the objective and purpose of care in clinical practice. However, it is necessary to go beyond the purpose because clinical practice guidelines are developed to improve the medical decision-making process among health professionals [65]. Likewise, considering other nutrition indicators, such as food intake, diet quality, and nutrition biomarkers, to assess clinical nutrition guidelines may improve patient-centered antenatal care.
Pregnancy is a unique time for identifying, preventing, and correcting any form of malnutrition in women, which may impact the health of the next generation. This opportunity is of utmost importance as this is a sensitive time, and most countries integrate antenatal care into universal health access. Dietary interventions to promote a healthy diet during pregnancy are part of the double-duty actions suggested by a group of experts to end malnutrition in all its form by 2030 [66]. However, from a nutrition care approach, it is recommended that the nutrition care process be followed to establish specific and evidence-based dietary interventions for each person. In this context, researchers and professionals should strengthen the nutrition methodology in research studies and consider the best evidence-based clinical nutrition practice guidelines.
Assessment of the quality of CPGs is relevant in the clinical field and for formulating and implementing programs and interventions to improve the quality of care and the population's nutritional status. We recommend that guideline developers, clinicians, researchers, and policymakers consider and use the AGREE II instrument as it is detailed and easy to apply in situations of poor nutrition in pregnant women and other clinical conditions [64]. In addition, this tool allows critical evaluation before implementation, which would support decision-making around the health system of a country or region and even during emergencies.
Maternal nutritional status during pregnancy plays a critical role in fetal growth and development, contributing to the offspring's health and future maternal health; therefore, improving the quality of the domains with lower scores is essential. Enhancing the quality of CPGs could improve nutritional care during this life stage and the health of mothers and their offspring across generations. Due to the importance of maternal nutrition in pregnancy, it is essential to join forces to improve the quality of the guidelines, especially CPGs that need to meet the reference standards for quality.

Conflicts of Interest:
The authors declare no conflict of interest.