Eric O Verger
email: eric.verger@ird.fr

Agnes Le Port

Augustin Borderon

Gabriel Bourbon

Mourad Moursi

Mathilde Savy

François Mariotti

Yves Martin-Prevel

Dietary Diversity Indicators and Their Associations with Dietary Adequacy and Health Outcomes: A Systematic Scoping Review

Keywords: 1-14 dietary diversity, indicators, nutrition, diet quality, health outcomes, body weight, noncommunicable diseases, adolescent, adult , high-income economy, LIE, low-income economy, LMIE, lower-middle-income economy, NCD, noncommunicable disease, OI, other indicator, PICOS, Population, Interventions, Comparators, Outcomes, and Study, PRISMA-ScR, Preferred

Dietary diversity has long been recognized as a key component of diet quality and many dietary diversity indicators (DDIs) have been developed. This systematic scoping review aimed to present a comprehensive inventory of DDIs and summarize evidence linking DDIs and dietary adequacy or health outcomes in adolescents and adults. Two search strategies were developed to identify peer-reviewed articles published in English up until June 2018 and were applied to Medline, Web of Science, and Scopus. A 2-stage screening process was used to select the studies to be reviewed. Four types of DDIs were identified among 161 articles, the majority of them belonging to the food group-based indicator type (n = 106 articles). Fifty studies indicated that DDIs were proxies of nutrient adequacy, but there was a lack of evidence about their relation with nutrients to limit. Associations between DDIs and health outcomes were largely inconsistent among 137 studies, especially when the outcomes studied were body weight (n = 60) and noncommunicable diseases (n = 41). We conclude that the ability of DDIs to reflect diet quality was found to be principally limited to micronutrient adequacy and that DDIs do not readily relate to health outcomes. These findings have implications for studies in low-and lower-middle-income economies where DDIs are often used to assess dietary patterns and overall diet quality.

Introduction

Food diversity has long been recognized as a key element of high-quality diets, based on the principle that no single food can provide the right amount of nutrients necessary to maintain optimal health. This theory has been historically documented on many occasions, such as the high prevalence of beriberi, as well as night blindness and scurvy, among the Imperial Japanese Army during the first half of the 20th century, due to rice-based rations that included little or no other foods [START_REF] Hawk | The great disease enemy, Kak'ke (beriberi) and the Imperial Japanese Army[END_REF]. Eating a variety of foods has been a longstanding recommendation of US dietary guidelines since 1980, initially phrased as "select foods each day from each of several major groups," then as "choose a variety of nutrient-dense foods across and within all food groups in recommended amounts" [START_REF]Nutrition and your health: dietary guidelines for Americans[END_REF][START_REF]2015-2020 Dietary guidelines for Americans[END_REF]. Many other national and international food-based dietary guidelines have included dietary diversity as a key feature, albeit with slightly different definitions depending on the country or countries and cultural dietary patterns [START_REF] Montagnese | European food-based dietary guidelines: a comparison and update[END_REF][START_REF]Preparation and use of food-based dietary guides: report of a joint FAO/WHO Expert Consultation, Nicosia, Cyprus. Preparation and use of food-based dietary guidelines: report of a joint FAO/WHO Consultation[END_REF]. One result of these historical evolutions and national differences was a lack of consensus about what dietary diversity represents and how to measure and operationalize it [START_REF] Ruel | Operationalizing dietary diversity: a review of measurement issues and research priorities[END_REF].

Dietary diversity indicators (DDIs) have been identified as promising measurement tools, particularly for use in developing countries, because of their simplicity of implementation and their potential to be used at a large scale compared with other food-consumption indicators involving the collection of complex quantitative information [START_REF] Ruel | Operationalizing dietary diversity: a review of measurement issues and research priorities[END_REF].

Thereafter, significant progress has been made in developing and validating simple DDIs with consistent and relevant meaning across different contexts and over time. As a result, many DDIs have been developed and used in the literature, either as proxies of nutritional adequacy of the diet or as recommendations to maintain optimal health (6-10). The most recent example is the Minimum Dietary Diversity for Women of Reproductive Age, which is calculated based on a single 24-h recall [START_REF]Minimum dietary diversity for women: a guide for measurement[END_REF] and has been shown to be effective in predicting adequacy for 11 micronutrients in 9 large datasets from different countries [START_REF]Women's Dietary Diversity Project (WDDP) Study Group. Development of a dichotomous indicator for population-level assessment of dietary diversity in women of reproductive age[END_REF].

While several comprehensive or systematic reviews have been carried out, the most recent ones focusing on obesity and body adiposity [START_REF] Vadiveloo | Associations between dietary variety and measures of body adiposity: a systematic review of epidemiological studies[END_REF][START_REF] Salehi-Abargouei | Dietary diversity score and obesity: a systematic review and meta-analysis of observational studies[END_REF][START_REF] De Oliveira Otto | Dietary diversity: implications for obesity prevention in adult populations: a science advisory from the American Heart Association[END_REF], there is a lack of comprehensive information about how dietary diversity is conceptualized and measured across contexts, and whether the proposed indicators are associated with dietary adequacy and health outcomes. Scoping reviews aim at identifying, mapping, and synthesizing the available evidence in a given field of interest [START_REF] Pham | A scoping review of scoping reviews: advancing the approach and enhancing the consistency[END_REF] and are particularly relevant for the following purposes: 1) clarify key concepts and definitions, 2) identify key characteristics or factors related to a concept, and 3) highlight knowledge gaps [START_REF] Munn | Systematic review or scoping review? Guidance for authors when choosing between a systematic or scoping review approach[END_REF]. The objectives of the present systematic scoping review are therefore as follows: 1) to present a comprehensive inventory of DDIs developed for adolescents and adults, 2) to summarize the evidence of the associations between DDIs and measures of dietary adequacy, and 3) to summarize the evidence of the associations between DDIs and health outcomes.

Methods

Search strategies

Based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses Extension for Scoping Reviews (PRISMA-ScR) guidelines [START_REF] Tricco | PRISMA Extension for Scoping Reviews (PRISMA-ScR): checklist and explanation[END_REF], 2 structured search strategies were developed to include title-abstract-keywords in 2 different search strings. The first search strategy focused on articles studying dietary diversity in association with measures of the dietary adequacy and included the titleabstract-keywords "diet diversity, diet variety, food diversity, food variety, nutrient intake, nutrient adequacy, diet quality," including relevant variations in keywords. The second search strategy focused on articles studying dietary diversity in association with health outcomes and included the title-abstractkeywords "diet diversity, diet variety, food diversity, food variety, health outcome, risk factor, life expectancy, mortality, morbidity, comorbidity, cancer, disease, overweight, obesity, adiposity, anthropometric status, diabetes, blood glucose, cardiometabolic, metabolic syndrome, hypertension, blood pressure, dyslipidemia, anemia, low birth weight, incidence, vascular," including relevant variations in keywords. The searches were limited to peer-reviewed articles published in English up until June 2018 and were run using 3 databases: Medline, Web of Science, and Scopus. Additionally, we examined reference lists in papers from the studies included to identify other relevant studies.

Data extraction

All studies identified as suitable were extracted using Zotero (version 4.0.28.7). We conducted a 2-stage screening process to select the studies to be fully reviewed. During the first stage, titles and abstracts were examined by 2 authors (EOV and AB) and irrelevant studies were excluded from further review. At the second stage, a full-text screen was performed by 2 authors (EOV and ALP) and evaluated using the Population, Interventions, Comparators, Outcomes, and Study design (PICOS) criteria for inclusion and exclusion [START_REF]Systematic reviews. CRD's guidance for undertaking reviews in health care[END_REF]. All disagreements regarding eligibility were resolved by discussion.

Inclusion and exclusion criteria

The PICOS criteria for inclusion and exclusion for title, abstract, and full-text screening are described in Table 1.

Because our intent was to present a comprehensive inventory of DDIs developed for adolescents and adults, we did not exclude articles based on their methodological quality. Furthermore, our scoping review was not meant to assess the validity or quality of the studies, nor of the indicators they used.

Synthesis of the results

Due to the wide heterogeneity among DDIs, measures of dietary adequacy, health outcomes, study designs, and statistical models, we used a qualitative and descriptive approach to review the available evidence regarding whether dietary diversity is associated with dietary adequacy and various health outcomes. The association between DDIs and any measure of dietary adequacy was described as "positive" (the higher the DDI, the higher the dietary adequacy), "mixed" (significance and direction of the association varied depending on subgroups or type of DDIs that were used), "null" (no association), or "negative" (the higher the DDI, the lower the dietary adequacy). The association between DDIs and any health outcome was described as "favorable" (e.g., the higher the DDI, the lower the risk for metabolic syndrome or the lower the risk for wasting), "mixed" (significance and direction of the association varied depending on subgroups or type of DDIs used), "null" (no association), or "unfavorable" (e.g., the higher the DDI, the higher the risk for obesity).

Results

Comprehensive inventory of dietary diversity indicators

Based on the 2 structured search strategies, 50 articles studying the association between dietary diversity and dietary adequacy and 137 articles studying the association between dietary diversity and any health outcomes were included (Figure 1). Cross-referencing the 2 sets of papers led to 161 unique studies published from 1989 to June 2018. From these, 4 types of DDI have been identified: the "food item-based indicators" (FIIs), the "food group-based indicators" (FGIs), the "dietary guidelines-based indicators" (DGIs) and the "other indicators" (OIs). Table 2 summarizes the characteristics of these 4 types of DDI, further described in the following sections.

FIIs of dietary diversity.

The FIIs were based on the number of different food items consumed over a reference period. FIIs were used in 56 studies and were usually a simple count of food items that had been consumed (n = 49). In 7 studies, the FII was also a simple count of food items but only those considered by the authors as healthy [START_REF] Kant | Measures of overall diet quality from a food frequency questionnaire: National Health Interview Survey[END_REF][START_REF] Kant | A comparison of three dietary pattern indexes for predicting biomarkers of diet and disease[END_REF][START_REF] Roberts | Dietary variety predicts low body mass index and inadequate macronutrient and micronutrient intakes in community-dwelling older adults[END_REF][START_REF] Gregory | Diet scores and cardio-metabolic risk factors among Guatemalan young adults[END_REF][START_REF] Masset | March 2021 be encouraged? Results from the Whitehall II cohort[END_REF][START_REF] Milte | Associations of diet quality with health-related quality of life in older Australian men and women[END_REF], unhealthy [START_REF] Roberts | Dietary variety predicts low body mass index and inadequate macronutrient and micronutrient intakes in community-dwelling older adults[END_REF][START_REF] Gregory | Diet scores and cardio-metabolic risk factors among Guatemalan young adults[END_REF][START_REF] Masset | March 2021 be encouraged? Results from the Whitehall II cohort[END_REF], or traditional [START_REF] Roche | Traditional food diversity predicts dietary quality for the Awajún in the Peruvian Amazon[END_REF]. We observed a large variability across studies in the number of different food items included in the FIIs (Figure 2), as well as variations in the reference periods (25 studies covered periods of 1-7 d, while 29 covered periods ranging from 7 d to 1 y).

FGIs of dietary diversity.

The FGIs were based on the number of different food groups consumed over a reference period, without allocating any weight to food groups. The way food groups were delineated varied greatly across the studies (resulting in varied numbers of food categories, of food items within categories, and of level of heterogeneity within the food groups). We decided to keep authors' food groups, even when they were debatable. FGIs were used in 106 studies and were usually a simple count of the different groups consumed over a reference period (n = 90). Another approach was to first assess the diversity of food consumed among 5 main food groups, weighted by intra-food-group diversity [START_REF] Mirmiran | Dietary diversity score in adolescents-a good indicator of the nutritional adequacy of diets: Tehran Lipid and Glucose Study[END_REF][START_REF] Azadbakht | Variety scores of food groups contribute to the specific nutrient adequacy in Tehranian men[END_REF][START_REF] Azadbakht | Dietary diversity score is favorably associated with the metabolic syndrome in Tehranian adults[END_REF][START_REF] Azadbakht | Dietary diversity score and cardiovascular risk factors in Tehranian adults[END_REF][START_REF] Mirmiran | Dietary diversity within food groups: an indicator of specific nutrient adequacy in Tehranian women[END_REF][START_REF] Azadbakht | Diet quality among Iranian adolescents needs improvement[END_REF][START_REF] Azadbakht | The association between dietary glycemic index, glycemic load and diet quality indices in Iranian adults: results from Isfahan Healthy Heart Program[END_REF][START_REF] Tavakoli | Is dietary diversity a proxy measurement of nutrient adequacy in Iranian elderly women[END_REF][START_REF] Nachvak | Dietary diversity score and its related factors among employees of Kermanshah University of Medical Sciences[END_REF][START_REF] Farhangi | Dietary diversity score is associated with cardiovascular risk factors and serum adiponectin concentrations in patients with metabolic syndrome[END_REF][START_REF] Karimbeiki | Higher dietary diversity score is associated with obesity: a case-control study[END_REF]. We observed a large variability across studies in the number of food groups considered (Figure 3). In the 55 studies that reported the rule to count a group in the indicator, we found large differences in the way to set the minimum amount (e.g., 15 or 25 g), or the serving size (e.g., half a serving or a serving), or the frequency of food consumption (e.g., once a week or once a day).

DGIs of dietary diversity.

The DGIs assessed the number of different food groups consumed over a reference period and allocated different weights to each food group according to national food-based dietary guidelines or international recommendations. DDIs were used in only 11 studies and the most frequently used was the Healthy Food Diversity (HFD) index. First developed for the German context [START_REF] Drescher | A new index to measure healthy food diversity better reflects a healthy diet than traditional measures[END_REF][START_REF] Truthmann | Associations of dietary indices with biomarkers of dietary exposure and cardiovascular status among adolescents in Germany[END_REF] and later adapted to the US context [START_REF] Vadiveloo | Development and evaluation of the US Healthy Food Diversity index[END_REF][START_REF] Vadiveloo | Greater healthful food variety as measured by the US Healthy Food Diversity index is associated with lower odds of metabolic syndrome and its components in US adults[END_REF][START_REF] Vadiveloo | Dietary variety is inversely associated with body adiposity among US adults using a novel food diversity index[END_REF][START_REF] Vadiveloo | Greater healthful dietary variety is associated with greater 2-year changes in weight and adiposity in the Preventing Overweight Using Novel Dietary Strategies (POUNDS Lost) Trial[END_REF], the HFD index is calculated by multiplying the Berry index (defined as 1 minus the sum of the squares of the share of each food in the total amount of energy intake) by the "health value" of the diet of each individual (calculated using health factors attributed to food groups according to the food-based dietary guidelines). Another type of DGI was based on the count of different groups consumed over a reference period, but in order for a food group to be counted in the index, individuals had to eat the minimum recommended number of servings according to national dietary guidelines (e.g., 3 servings daily for vegetables). This kind of DGI was used in the United States [START_REF] Song | Food group intake patterns in relation to nutritional adequacy of young adults[END_REF][START_REF] Schuette | Quantitative use of the Food Guide Pyramid to evaluate dietary intake of college students[END_REF], Sri Lanka [START_REF] Rathnayake | Use of dietary diversity score as a proxy indicator of nutrient adequacy of rural elderly people in Sri Lanka[END_REF][START_REF] Jayawardena | High dietary diversity is associated with obesity in Sri Lankan adults: an evaluation of three dietary scores[END_REF], and Malaysia [START_REF] Tiew | Factors associated with dietary diversity score among individuals with type 2 diabetes mellitus[END_REF].

OIs of dietary diversity.

The OIs, which relied on different concepts, were used in 12 studies (see Supplemental Results for more details). Briefly, 1 main type of OI was used in 6 studies to reflect the distribution of foods consumed, like the Berry (or Simpson) index [START_REF] Drescher | A new index to measure healthy food diversity better reflects a healthy diet than traditional measures[END_REF][START_REF] Otto Mc De | Everything in moderation-dietary diversity and quality, central obesity and risk of diabetes[END_REF][START_REF] Lachat | Dietary species richness as a measure of food biodiversity and nutritional quality of diets[END_REF], the QUANTIDD index [START_REF] Otsuka | Dietary diversity and 14-year decline in higher-level functional capacity among middle-aged and elderly Japanese[END_REF][START_REF] Otsuka | Dietary diversity decreases the risk of cognitive decline among Japanese older adults[END_REF], the Entropy index [START_REF] Tian | Dietary diversity and adiposity in Chinese men and women: an analysis of four waves of crosssectional survey data[END_REF], and the Dissimilarity index [START_REF] Otto Mc De | Everything in moderation-dietary diversity and quality, central obesity and risk of diabetes[END_REF]. The other main type of OI was based on the ratio between the "variety" (defined by the authors as the percentage of different food items consumed) within some food groups and the "variety" within other food groups [START_REF] Woo | Influence of dietary pattern on the development of overweight in a Chinese population[END_REF][START_REF] Sea | Associations between food variety and body fatness in Hong Kong Chinese adults[END_REF][START_REF] Woo | Diet and glucose tolerance in a Chinese population[END_REF][START_REF] Mccrory | Dietary variety within food groups: association with energy intake and body fatness in men and women[END_REF]. Another type of OI was a composite score similar to a DDI but with different weights arbitrarily attributed to food groups [START_REF] Masa | Socioeconomic correlates of dietary diversity and its association with adherence and psychosocial functioning of people living with HIV in rural Zambia[END_REF][START_REF] Benefice | Fatness and overweight in women and children from riverine Amerindian communities of the Beni River (Bolivian Amazon)[END_REF]. Last, 1 OI was called the Functional Diversity, a complex indicator reflecting the diversity in the nutrient composition of species (plant, livestock, and fish) consumed by each individual [START_REF] Lachat | Dietary species richness as a measure of food biodiversity and nutritional quality of diets[END_REF].

Use of indicators of dietary diversity over time and across contexts.

A first analysis indicated a growing use of DDIs with time (Figure 4A), with a higher use of these indicators occurring in the context of high-income economies (HIEs) as compared with low-, lower-middle-, and upper-middleincome economies (LIEs, LMIEs, and UMIEs, respectively; Figure 4B). A second analysis of the 161 articles that took the type of DDI into account showed that FIIs and FGIs were the most frequent types of indicators. While their use began at the same time, with a similar occurrence of use over time, a shift in 2010 resulted in FGIs becoming the current most frequently used type of indicator (Figure 4A). In terms of country income classification, studies in the contexts of LIEs, LMIEs, and UMIEs have mainly used FGIs over the other types of DDI, whereas the use of the 4 types of DDI was more balanced in HIEs (Figure 4B).

Review on the relation of DDIs with dietary adequacy

Fifty studies assessed the association between a DDI and a measure of dietary adequacy (Supplemental Table 1). Most of the studies used a cross-sectional design, were located in HIEs and UMIEs (Figure 5A), and calculated DDIs from either 24-h recalls or food-frequency questionnaires (FFQs; Figure 5B). The FGIs were the most frequently used indicators (n = 32), followed by FIIs (n = 24), DGIs (n = 5), and OIs (n = 4). There was a wide variation in terms of measures of dietary adequacy (Figure 5C) and in the number of nutrients used in the measures of dietary adequacy (Figure 5D). Among the 50 studies reviewed, all found some positive associations between the DDIs and the measures of dietary adequacy, except for 3 studies that found no associations with FIIs (57-59) and 3 others that found mixed associations with FIIs and OIs [START_REF] Roberts | Dietary variety predicts low body mass index and inadequate macronutrient and micronutrient intakes in community-dwelling older adults[END_REF][START_REF] Gregory | Diet scores and cardio-metabolic risk factors among Guatemalan young adults[END_REF][START_REF] Otto Mc De | Everything in moderation-dietary diversity and quality, central obesity and risk of diabetes[END_REF] (Figure 6A and Supplemental Figure 1A). Studies reporting mixed associations are those showing contradictory results (either significant or not and positive or negative associations) according to age groups [START_REF] Roberts | Dietary variety predicts low body mass index and inadequate macronutrient and micronutrient intakes in community-dwelling older adults[END_REF] or to the type of DDIs used [START_REF] Gregory | Diet scores and cardio-metabolic risk factors among Guatemalan young adults[END_REF][START_REF] Otto Mc De | Everything in moderation-dietary diversity and quality, central obesity and risk of diabetes[END_REF] (see Supplemental Results for more details).

We found 19 studies that investigated the relation between DDIs and dietary adequacy with accounting for energy intake. When energy intake was controlled for, the relations were attenuated but still significant in 7 studies [START_REF] Azadbakht | Variety scores of food groups contribute to the specific nutrient adequacy in Tehranian men[END_REF][START_REF] Mirmiran | Dietary diversity within food groups: an indicator of specific nutrient adequacy in Tehranian women[END_REF][START_REF] Arimond | March 2021 adequacy of women's diets in 5 diverse, resource-poor settings[END_REF][START_REF] Henjum | Low dietary diversity and micronutrient adequacy among lactating women in a peri-urban area of Nepal[END_REF][START_REF] Arsenault | Very low adequacy of micronutrient intakes by young children and women in rural Bangladesh is primarily explained by low food intake and limited diversity[END_REF][START_REF] Nguyen | Dietary diversity predicts the adequacy of micronutrient intake in pregnant adolescent girls and women in Bangladesh, but use of the 5-group cutoff poorly identifies individuals with inadequate intake[END_REF][START_REF] Foote | Dietary variety increases the probability of nutrient adequacy among adults[END_REF], became nonsignificant in 2 studies (58, 59), and were not attenuated in 2 studies [START_REF] Vadiveloo | Development and evaluation of the US Healthy Food Diversity index[END_REF][START_REF] Lachat | Dietary species richness as a measure of food biodiversity and nutritional quality of diets[END_REF]. However, while higher energy intake has long been recognized as a potential confounding factor when studying the relation between micronutrient intakes and indexes of overall diet quality [START_REF] Kant | Indexes of overall diet quality: a review[END_REF], it could also play a mediating role in that relation. Indeed, some studies have shown that higher food and energy intakes come along with higher variety of foods consumed [START_REF] Rolls | Variety in a meal enhances food intake in man[END_REF][START_REF] Rolls | Pleasantness changes and food intake in a varied four-course meal[END_REF][START_REF] Roe | Serving a variety of vegetables and fruit as a snack increased intake in preschool children[END_REF]. -Indicators reflecting how the foods consumed were distributed: Berry index [START_REF] Drescher | A new index to measure healthy food diversity better reflects a healthy diet than traditional measures[END_REF][START_REF] Otto Mc De | Everything in moderation-dietary diversity and quality, central obesity and risk of diabetes[END_REF][START_REF] Lachat | Dietary species richness as a measure of food biodiversity and nutritional quality of diets[END_REF], QUANTIDD index [START_REF] Otsuka | Dietary diversity and 14-year decline in higher-level functional capacity among middle-aged and elderly Japanese[END_REF][START_REF] Otsuka | Dietary diversity decreases the risk of cognitive decline among Japanese older adults[END_REF], Entropy index [START_REF] Tian | Dietary diversity and adiposity in Chinese men and women: an analysis of four waves of crosssectional survey data[END_REF], and Dissimilarity index (46) -Indicators calculated as a ratio between the "variety" (defined by the authors as percentage of different food items consumed) of some food groups and the variety of other food groups (51-54) -Composite score based on consumption of food groups and relative importance of each food group, with or without taking into account frequency of consumption (55, 56) -Functional Diversity: a complex indicator reflecting the diversity in nutrient composition of species (plant, livestock, and fish) consumed ( 47) 1 See Supplemental Results for more details about the "Other indicators". 2 A food group is a collection of foods that share similar nutritional properties or biological classifications.

Only 14 studies explored how DDIs were associated with nutrients that can be unhealthy if consumed in excess, like SFAs or added sugars (called excess nutrients in the rest of the article). Four studies found that DDIs were negatively related to excess nutrients (i.e., the higher the DDIs, the lower the intakes) (37, 57, 68, 69), 4 found positive associations (41, 70-72), and 6 found mixed [START_REF] Kant | Measures of overall diet quality from a food frequency questionnaire: National Health Interview Survey[END_REF][START_REF] Masset | March 2021 be encouraged? Results from the Whitehall II cohort[END_REF][START_REF] Drescher | A new index to measure healthy food diversity better reflects a healthy diet than traditional measures[END_REF][START_REF] Otto Mc De | Everything in moderation-dietary diversity and quality, central obesity and risk of diabetes[END_REF] or null (58, 73) associations. There was no clear pattern to explain these contrasting results (Figure 6B and Supplemental Figure 1B). Two DDIs provided interesting results. First, the Dissimilarity index was found to be negatively related to various food-based dietquality indicators, providing a specific measure of "unhealthy dietary diversity" due to its design which incorporated 12 different foods likely to have cardiometabolic effects [START_REF] Otto Mc De | Everything in moderation-dietary diversity and quality, central obesity and risk of diabetes[END_REF]. Next, the HFD index seemed to be the most suitable DDI to provide a specific measure of "healthy dietary diversity", being both positively related to measures of dietary adequacy and inversely related to excess nutrients [START_REF] Drescher | A new index to measure healthy food diversity better reflects a healthy diet than traditional measures[END_REF][START_REF] Vadiveloo | Development and evaluation of the US Healthy Food Diversity index[END_REF].

Review on the associations of DDIs with health outcomes

The 137 studies included in the review on the association between DDIs and health outcomes were further classified into 6 categories of health outcomes: 1) body weight and body composition (n = 60), 2) noncommunicable diseases (NCDs) and intermediate biomarkers of health (n = 41), 3) biomarkers of nutritional status (n = 19), 4) mental health and cognitive functions (n = 17), 5) mortality (n = 10), and 6) other health outcomes (n = 18).

Most studies used a cross-sectional design and were located in HIEs (Figure 7A). While body-weight and body-composition outcomes have been studied across different economical categories of countries, the number of studies investigating other health outcomes varied according to those categories (Figure 7C). For example, NCDs and intermediate biomarkers of health have been studied in HIEs more frequently than in UMIEs, and in UMIEs more than in LMIEs and LIEs, whereas biomarkers of nutritional status have been more frequently studied in LMIEs and LIEs than in UMIEs and HIEs. FGIs were by far the most frequently used indicators (n = 89), followed by FIIs (n = 43), DGIs (n = 8), and OIs (n = 10). The predominance of FGIs was noticeable across the 6 categories of health outcomes, except for NCDs and intermediate biomarkers of health, and for mental health and cognitive functions outcomes where FIIs were used just as much (Figure 7B). Thus, the analysis of the association between DDIs and health outcomes was driven by the economical context of the studies (Figure 8) rather than by the types of DDIs (Supplemental Figure 2). The following sections present a global analysis of each health outcome (except for the category "other health outcomes") but their detailed presentation can be found in the Supplemental Results and Supplemental Tables 234567.

DDIs and body weight and body composition.

Fifty-one studies evaluated the association between DDIs and outcomes that were related to excess body weight (weight gain, being overweight, or obesity); there was a similar proportion of studies finding favorable, mixed, null, or unfavorable associations. Of note, the proportion of studies finding an unfavorable association was higher in UMIEs compared with other contexts (Figure 8A). Only 6 studies used a longitudinal design, finding either a favorable [START_REF] Vadiveloo | Greater healthful dietary variety is associated with greater 2-year changes in weight and adiposity in the Preventing Overweight Using Novel Dietary Strategies (POUNDS Lost) Trial[END_REF][START_REF] Florêncio | Weight gain and reduced energy expenditure in low-income Brazilian women living in slums: a 4-year follow-up study[END_REF], mixed [START_REF] Otto Mc De | Everything in moderation-dietary diversity and quality, central obesity and risk of diabetes[END_REF][START_REF] Haws | Exploring the relationship between varieties of variety and weight loss: when more variety can help people lose weight[END_REF], null [START_REF] Lee | A simple food quality index predicts mortality in elderly Taiwanese[END_REF], or unfavorable (51) association. Furthermore, only 2 of them had a sample size >1000 participants and used multi-adjusted regressions [START_REF] Otto Mc De | Everything in moderation-dietary diversity and quality, central obesity and risk of diabetes[END_REF][START_REF] Lee | A simple food quality index predicts mortality in elderly Taiwanese[END_REF]. Nevertheless, 3 studies using a specific DDI provided interesting results that deserve to be highlighted. The food variety ratio could be considered as corresponding to some "(un)balanced dietary diversity": defined by the "variety" of snacks divided by the "variety" of grains and meats, it was found to be associated with an increased risk of becoming overweight [START_REF] Woo | Influence of dietary pattern on the development of overweight in a Chinese population[END_REF] or obese (52), while defined by the "variety" of vegetables divided by the "variety" of sweets, snacks, condiments, lunch and dinner entrées (e.g., beef, fried fish, pizza), and carbohydrates, it was found to be inversely associated with body fatness [START_REF] Mccrory | Dietary variety within food groups: association with energy intake and body fatness in men and women[END_REF].

There were only 9 studies related to being undernourished [defined as a BMI (kg/m 2 ) <18.5 among adults], with similar proportion of studies finding favorable, mixed, or null associations. The sole study using a longitudinal design found a favorable association of increased dietary diversity over undernourishment [START_REF] Savy | Dietary diversity scores and nutritional status of women change during the seasonal food shortage in rural Burkina Faso[END_REF]. These 9 studies represented about half of the studies conducted in LMIEs and LIEs (Figure 8A).

DDIs and NCDs and intermediate biomarkers of health.

Forty-one studies evaluated the association between DDIs and NCDs and intermediate biomarkers of health, with half of them finding a favorable association and the other half finding a mixed or null association. The number of studies and their types of results differed by country income classification (Figure 8B) and by type of DDI (Supplemental Figure 2B). Only 5 studies used a longitudinal design with large sample sizes and multi-adjusted regressions, of which 1 study found a favorable association with diabetes (78), 3 found null associations with diabetes [START_REF] Masset | March 2021 be encouraged? Results from the Whitehall II cohort[END_REF][START_REF] Otto Mc De | Everything in moderation-dietary diversity and quality, central obesity and risk of diabetes[END_REF][START_REF] Gicevic | Evaluating pre-pregnancy dietary diversity vs. dietary quality scores as predictors of gestational diabetes and hypertensive disorders of pregnancy[END_REF] and 1 study found a mixed association with cardiovascular disease [START_REF] Fung | International food groupbased diet quality and risk of coronary heart disease in men and women[END_REF].

DDIs and biomarkers of nutritional status.

Nineteen studies evaluated the association between DDIs and biomarkers of nutritional status, with about half of them finding a favorable association and the other half finding a mixed or null association. Most of these studies were conducted in LMIEs and LIEs (Figure 8C) and used FGIs (Supplemental Figure 2C). Only 3 studies used a longitudinal design with moderate sample sizes and multiadjusted regressions, finding either favorable [START_REF] Zerfu | Dietary diversity during pregnancy is associated with reduced risk of maternal anemia, preterm delivery, and low birth weight in a prospective cohort study in rural Ethiopia[END_REF], mixed [START_REF] Roba | Seasonal variation in nutritional status and anemia among lactating mothers in two agroecological zones of rural Ethiopia: a longitudinal study[END_REF] or null [START_REF] Rawat | Poor diet quality is associated with low CD4 count and anemia and predicts mortality among antiretroviral therapy-naive HIV-positive adults in Uganda[END_REF] associations with anemia.

DDIs and mental health and cognitive functions.

Seventeen studies evaluated the association between DDIs and mental health and cognitive functions, about two-third finding a favorable association and one-third finding a mixed or null association. Most of these studies were conducted in HIEs (Figure 8D). Only 3 studies used a longitudinal design with moderate sample sizes and multi-adjusted regressions, finding a favorable association with cognitive function [START_REF] Otsuka | Dietary diversity and 14-year decline in higher-level functional capacity among middle-aged and elderly Japanese[END_REF][START_REF] Otsuka | Dietary diversity decreases the risk of cognitive decline among Japanese older adults[END_REF][START_REF] Chen | Dietary quality may enhance survival related to cognitive impairment in Taiwanese elderly[END_REF].

DDIs and mortality.

Ten studies used a longitudinal design with medium to large sample sizes and multi-adjusted regressions to evaluate the association between DDIs and all-cause or cause-specific mortality. Half found a favorable association [START_REF] Rawat | Poor diet quality is associated with low CD4 count and anemia and predicts mortality among antiretroviral therapy-naive HIV-positive adults in Uganda[END_REF][START_REF] Chen | Dietary quality may enhance survival related to cognitive impairment in Taiwanese elderly[END_REF][START_REF] Kant | Dietary diversity and subsequent mortality in the 1st National-Health and Nutrition Examination Survey Epidemiologic Follow-up Study[END_REF][START_REF] Huang | Optimal dietary and plasma magnesium statuses depend on dietary quality for a reduction in the risk of all-cause mortality in older adults[END_REF][START_REF] Huang | Appetite predicts mortality in free-living older adults in association with dietary diversity: a NAHSIT cohort study[END_REF] and the other half a mixed [START_REF] Masset | March 2021 be encouraged? Results from the Whitehall II cohort[END_REF][START_REF] Lee | A simple food quality index predicts mortality in elderly Taiwanese[END_REF][START_REF] Wahlqvist | Dietary diversity no longer offsets the mortality risk of hyperhomocysteinaemia in older adults with diabetes: a prospective cohort study[END_REF] or null [START_REF] Kant | Dietary diversity and subsequent cause-specific mortality in the NHANES I epidemiologic follow-up study[END_REF][START_REF] Letois | Nutrition and mortality in the elderly over 10 years of follow-up: the Three-City Study[END_REF] association. The studies were mainly conducted in HIEs (Figure 8E) and mainly used FGIs (Supplemental Figure 2E).

Discussion

To the best of our knowledge, this is the first systematic scoping review presenting an extensive and comprehensive inventory of DDIs developed for adolescents and adults worldwide and summarizing the evidence of the associations between these indicators and 1) some measures of the dietary adequacy and 2) some health outcomes. The first finding of this review is that there is a large number of DDIs used in the literature, greatly varying in their structure. While almost all DDIs were found to be positively associated with some measures of dietary adequacy, their inconsistent relation with nutrients to limit was of concern, which underlines their limit to reflect overall diet quality. Overall, higher DDIs tended to be associated with benefits for various health outcomes, except in contexts such as HIEs and UMIEs where higher DDIs were found to be associated with higher risk of overweight and obesity. However, many studies found mixed or null results. In addition, only one-quarter of the studies used longitudinal designs.

Three decades of development of DDIs

The results of this review should be interpreted in the historical context of the evolution of DDIs. Originating in the late 1980s, DDIs have been extensively developed and used, as dietary diversity is recognized as a key feature of high-quality diets. Nevertheless, due to the lack of consensual definition of dietary diversity (or variety), a wide range of DDIs has been proposed with many more variations in terms of format (e.g., number of foods or food groups, based on single 24-h recall or FFQ) rather than concept (the vast majority of DDIs relied on counting foods or food groups consumed over a period of time).

A shift occurred in the late 2000s, with several research projects aiming to develop and validate simple FGIs based on single 24-h recalls for women of reproductive age that remain relevant and consistent across different contexts and over time [START_REF] Arimond | March 2021 adequacy of women's diets in 5 diverse, resource-poor settings[END_REF]. These methodological efforts are ongoing [START_REF]Women's Dietary Diversity Project (WDDP) Study Group. Development of a dichotomous indicator for population-level assessment of dietary diversity in women of reproductive age[END_REF][START_REF] Nguyen | Inventory on the dietary assessment tools available and needed in Africa: a prerequisite for setting up a common methodological research infrastructure for nutritional surveillance, research, and prevention of diet-related non-communicable diseases[END_REF].

Because some countries face a dramatic lack of expertise, infrastructure, and financial support (92), the Women's Dietary Diversity Score [START_REF]Guidelines for measuring household and individual dietary diversity[END_REF] and the Minimum Dietary Diversity for Women of Reproductive Age [START_REF]Minimum dietary diversity for women: a guide for measurement[END_REF] have paved the way for simple assessments of dietary diversity at the population level. Subsequently, they have favored the implementation of nutrition and health interventions, and also of nutrition-sensitive agriculture interventions, since these DDIs can be used to assess changes in the populations' diet before and after an intervention or to compare communities undergoing an intervention with control communities [START_REF] Herforth | Nutrition indicators in agriculture projects: current measurement, priorities, and gaps[END_REF][START_REF] Verger | Systematic review of use and interpretation of dietary diversity indicators in nutritionsensitive agriculture literature[END_REF]. Nevertheless, these 2 FGIs for women of reproductive age were validated as proxies of nutrient adequacy but not as proxies of moderation. While LIEs and LMIEs are undergoing an accelerated (although heterogeneous) nutrition transition characterized by increased intakes of unhealthy fats, refined carbohydrates, and added sugar [START_REF] Popkin | Dynamics of the double burden of malnutrition and the changing nutrition reality[END_REF], focusing solely on DDIs may be a major limitation in these contexts. Indeed, concerns regarding the excessive intake of certain nutrients and foods in LIEs and LMIEs were raised 20 y ago, questioning the need of a shift in the definition of dietary quality to include both concepts of nutrient deficiency and overnutrition [START_REF] Ruel | Operationalizing dietary diversity: a review of measurement issues and research priorities[END_REF].

DDIs and diet quality

This review found that the ability of DDIs to reflect overall diet quality was limited. Only 14 out of 50 studies explored how DDIs were associated with nutrients to limit, and only 4 studies found that DDIs could be considered as a proxy of moderation [START_REF] Vadiveloo | Development and evaluation of the US Healthy Food Diversity index[END_REF][START_REF] Drewnowski | The Dietary Variety Score: assessing diet quality in healthy young and older adults[END_REF][START_REF] Vandevijvere | Overall and within-food group diversity are associated with dietary quality in Belgium[END_REF][START_REF] Murphy | Simple measures of dietary variety are associated with improved dietary quality[END_REF].

In many HIEs, the food-based dietary guidelines changed from presenting separately the traditional concepts of dietary diversity, adequacy, moderation, and balance to including all these dimensions in each food-group recommendation [START_REF] Schneeman | Evolution of dietary guidelines[END_REF]. This shift was therefore also noticeable in the diet quality indices constructed from food-based dietary guidelines. For example, while US dietary guidelines evolved and specified the most advantageous types of variety, the original Healthy Eating Index (HEI), featuring dietary variety as a separate component, evolved into the HEI-2005, which no longer recognizes dietary variety as a separate component but instead includes new components that reflect the types of variety deemed to be the most beneficial [START_REF] Guenther | Development and evaluation of the Healthy Eating Index-2005: Dietary diversity indicators, nutrition, and health[END_REF].

A recent systematic review focusing on LIEs and LMIEs reported that individual DDIs were good proxies of nutrient adequacy, but also highlighted the necessity of accounting for moderation dimensions [START_REF] Trijsburg | Diet quality indices for research in low-and middle-income countries: a systematic review[END_REF]. The authors recommended evaluating healthy and unhealthy diet components separately, since using a single score for both components might reduce their ability to reflect diet quality and underestimate their associations with health outcomes [START_REF] Trijsburg | Diet quality indices for research in low-and middle-income countries: a systematic review[END_REF]. The development of a targeted systematic review and meta-analysis focusing on the strength of associations between DDIs and measures of diet quality would be of interest to better understand to what extent DDIs could reflect overall diet quality.

The use of simple DDIs may be convenient and relevant in many contexts, but such indicators should not be overinterpreted as reflecting other dimensions of dietary quality like moderation. Several DDIs providing more specific/detailed measurements of dietary diversity have been flagged throughout this review. The HFD index provides a specific measure of "healthy dietary diversity" [START_REF] Drescher | A new index to measure healthy food diversity better reflects a healthy diet than traditional measures[END_REF][START_REF] Vadiveloo | Development and evaluation of the US Healthy Food Diversity index[END_REF], the Dissimilarity index a specific measure of "unhealthy dietary diversity" [START_REF] Otto Mc De | Everything in moderation-dietary diversity and quality, central obesity and risk of diabetes[END_REF], and the food variety ratio a specific measure of "(un)balanced dietary diversity" [START_REF] Woo | Influence of dietary pattern on the development of overweight in a Chinese population[END_REF][START_REF] Sea | Associations between food variety and body fatness in Hong Kong Chinese adults[END_REF][START_REF] Mccrory | Dietary variety within food groups: association with energy intake and body fatness in men and women[END_REF]. However, these indicators were only used in specific contexts (Germany and United States for the HFD index, United States for the Dissimilarity index, and United States and Hong Kong for the food variety ratio) and their performances in other contexts would need to be tested. Furthermore, these indicators require intensive quantitative dietary data collection and sometimes demand high-skilled resources for data processing (HFD index and Dissimilarity index), thus limiting their use.

Dietary diversity, food-group diversity, and health outcomes

This review found that the associations between DDIs and health outcomes were largely inconsistent. Less than onequarter of the studies included in this review were based on a longitudinal design, which is more conducive than crosssectional or case-control designs to establish the relation with health-related outcomes. When considering the sole studies based on a longitudinal design with a large sample size and multi-adjusted regression analysis, most of them found mixed or null associations between DDIs and health outcomes. Also, DDIs were mostly assessed from a single 24-h recall, multiple 24-h recalls, or FFQs. Therefore, some studies explored the relation with health outcomes using a 1-d dietary diversity while others used a "usual" dietary diversity. These differences could affect the nature and magnitude of the associations.

Although the design and context of the studies are important to take into account, it is also important to consider the conceptual framework linking the dietary diversity to health outcomes. In most studies, it is quite unclear whether the authors used a DDI because they hypothesized a benefit of dietary diversity in their particular study setting or because they simply took a DDI as a general proxy for diet quality.

About half of the studies analyzing the associations between DDIs and NCDs, intermediate biomarkers of health, or mortality found mixed or null results. For these health outcomes, the consumption of specific food groups seemed to be more important than the overall diversity of the diet. For example, fruits and vegetables contain numerous nutrients, phytochemicals, and other unidentified compounds that are likely to act synergistically via several biological mechanisms in reducing the risk of chronic diseases and premature mortality. Some studies found that vegetable diversity was more strongly associated with a decreased risk of cancer than total dietary diversity (see Supplemental Results) (100-105). A recent dose-response meta-analysis of 95 studies found that the consumption of several types of fruits and vegetables was individually and inversely associated with coronary artery disease, stroke, cardiovascular diseases, total cancer, and all-cause mortality (106).

Regarding the associations between DDIs and body weight and body composition, the results were highly heterogeneous, but a majority of studies found mixed or null results. Two previous reviews reported that dietary diversity was inconsistently associated with body adiposity in diverse populations [START_REF] Vadiveloo | Associations between dietary variety and measures of body adiposity: a systematic review of epidemiological studies[END_REF] or not significantly associated with BMI status [START_REF] Salehi-Abargouei | Dietary diversity score and obesity: a systematic review and meta-analysis of observational studies[END_REF], and both questioned the definition of dietary diversity and the construction of the DDIs. According to Vadiveloo et al. [START_REF] Vadiveloo | Associations between dietary variety and measures of body adiposity: a systematic review of epidemiological studies[END_REF], associations with body adiposity were more consistent when dietary diversity focused on recommended and low-energy foods alone (i.e., foods that do not increase the odds of overweight and obesity) or when dietary diversity focused on less healthful, energy-dense foods alone (i.e., foods increasing the odds of overweight and obesity). This suggests that the diversity within specific food groups is of higher importance than the overall diversity of the diet. Recently, the American Heart Association stated that existing evidence does not support greater dietary diversity as an effective strategy to promote healthy body weight, and emphasized the need for further data to formulate adequate recommendations on dietary diversity [START_REF] De Oliveira Otto | Dietary diversity: implications for obesity prevention in adult populations: a science advisory from the American Heart Association[END_REF].

Limitations

Some limitations of this review have to be mentioned. Despite the use of the PRISMA-ScR guidelines, multiple structured search strategies, and PICOS criteria, this systematic scoping review may not be exhaustive due to the broad nature of the initial objective to provide an inventory of the DDIs and their associations with the dietary adequacy and/or various health outcomes. Additional and more focused structured search strategies may have led to greater completeness. However, we believe the method we used struck the right balance between feasibility and completeness. Another limitation is that the review only included articles published in English. Scoping reviews usually provide a descriptive overview without critically appraising individual studies, and the need for quality assessment of included studies in the scoping review process is still debated [START_REF] Pham | A scoping review of scoping reviews: advancing the approach and enhancing the consistency[END_REF]. Because this systematic scoping review encompasses very heterogeneous studies in terms of objectives, outcomes, designs, and statistical models, it would have been difficult to provide a consistent quality assessment and we decided not to assess the validity or the quality of the studies nor that of the indicators used. However, when focusing on health outcomes, we chose to describe the results of studies that used a longitudinal design with moderate/large sample sizes and multi-adjusted regressions. Nevertheless, only rigorous systematic reviews and metaanalysis would enable drawing conclusions as to what extent DDIs are associated with measures of diet quality and specific health outcomes.

Conclusions

The ability of DDIs to reflect diet quality was found to be principally limited to micronutrient adequacy. Furthermore, DDIs do not readily relate to health outcomes. Echoing the appeals from different authors, our findings call for the development and rigorous evaluation of a global diet quality index for use in LIEs and LMIEs [START_REF] Trijsburg | Diet quality indices for research in low-and middle-income countries: a systematic review[END_REF]107,108). Developing sound, easy-to-collect, and easy-to-use indicators of "healthy dietary diversity", "unhealthy dietary diversity", and "(un)balanced dietary diversity" (which could be analyzed in conjunction or combined into a global diet quality index) could be a way forward to measuring the impact of nutrition policies and programs aiming to tackle malnutrition in all its forms and track progress made to achieve Sustainable Development Goal number 2 by 2030.

FIGURE 1

 1 FIGURE 1 Systematic literature review flowchart for article selection. (A) Flowchart for selection and inclusion of studies in the systematic review of the evidence of dietary diversity and its relation with measures of dietary adequacy. (B) Flowchart for selection and inclusion of studies in the systematic review of the evidence of dietary diversity and its relationship with health outcomes.

FIGURE 2

 2 FIGURE 2 Distribution of studies according to the range of the theoretical maximum number of food items used in the food item-based indicators (when information available: n = 27 out of 56 studies).

FIGURE 3

 3 FIGURE 3 Distribution of studies according to the number of food groups used in the food group-based indicators (when information available: n = 102 out of 106 studies).

FIGURE 4

 4 FIGURE 4 Number of studies using the different types of dietary diversity indicators for adolescents and adults across the 161 articles included in this review. (A) Number of studies per type and per year. (B) Number of studies per type and per country income classification. DGI, dietary guidelines-based indicator; FGI, food group-based indicator; FII, food item-based indicator; HIE, high-income economies; LIE, low-income economies; LMIE, lower-middle-income economies; OI, other indicator; UMIE, upper-middle-income economies.

FIGURE 5

 5 FIGURE 5 Studies investigating the relation between dietary diversity indicators and dietary adequacy (n = 50) by country income classification (A), type of dietary assessment (B), and measure of dietary adequacy(C). (D) Number of nutrients used in the measures of dietary adequacy. DGI, dietary guidelines-based indicator; FGI, food group-based indicator; FII, food item-based indicator; HIE, high-income economies; LIE, low-income economies; LMIE, lower-middle-income economies; MAR, mean adequacy ratio; MPA, mean probability of adequacy; NAR, nutrient adequacy ratio; OI, other indicator; PA, probability of adequacy; UMIE, upper-middle-income economies.

FIGURE 6

 6 FIGURE 6 Results of studies investigating the relation between dietary diversity indicators and measures of dietary adequacy (n = 50) (A) or of excess nutrients (n = 14) (B), according to the type of indicator. DGI, dietary guidelines-based indicator; FGI, food group-based indicator; FII, food item-based indicator; OI, other indicator.

FIGURE 7

 7 FIGURE 7 Studies investigating the associations between dietary diversity indicators and health outcomes (n = 137) by country income classification (A) or health outcomes (B). (C) Number of health outcomes studied by country income classification. DGI, dietary guidelines-based indicator; FGI, food group-based indicator; FII, food item-based indicator; HIE, high-income economies; LIE, low-income economies; LMIE, lower-middle-income economies; NCD, noncommunicable diseases; UMIE, upper-middle-income economies.

FIGURE 8

 8 FIGURE 8 Results of studies investigating the associations between dietary diversity indicators and body composition (n = 60) (A), noncommunicable diseases and intermediate biomarkers of health (n = 41) (B), biomarkers of nutritional status (n = 19) (C), mental health and cognitive functions (n = 17) (D), mortality (n = 10) (E), and other health outcomes (n = 18) (F), according to country income classification. HIE, high-income economies; LIE, low-income economies; LMIE, lower-middle-income economies; UMIE, upper-middle-income economies.

TABLE 1

 1 PICOS criteria for inclusion and exclusion of studies1

	Parameter	Description
	Population	Inclusion criteria: adults and adolescents (age ≥10 y)
		Exclusion criteria: children (age <10 y)
	Interventions	Inclusion criteria: any study measuring participants' dietary variety or dietary diversity using an
		indicator based on the number of foods or food groups 2 consumed over a reference period,
		regardless of the mathematical operation required to compute this information
	Comparators	Inclusion criteria: participants with higher dietary diversity compared with participants with
		lower dietary diversity
	Outcomes	Inclusion criteria:
		1) Any measure of dietary adequacy, including nutrient intake, nutrient adequacy index, and
		food-based diet quality index
		2) Any health outcome, including (but not restricted to) body weight and body
		composition,
		noncommunicable diseases and intermediate biomarkers of health, biomarkers of
		nutritional status, mental health and cognitive functions, and mortality
	Study design	Inclusion criteria: all study designs
		Exclusion criteria: reviews, expert opinion, comments, letters to the editor, studies on animals,
		conference reports
	1 PICOS, Population, Interventions, Comparators, Outcomes and Study design criteria.
	2 A food group is a collection of foods that share similar nutritional properties or biological classifications.

TABLE 2

 2 Summary of the characteristics of the 4 types of dietary diversity indicators identified from the 161 articles included in the systematic literature review 1 the different food items consumed. Consuming the same food item 1 or more times scored 1; not consuming a food item scored 0. Most of the time, any food item was counted, except in 7 studies where only food items considered by the authors as healthy, unhealthy, or traditional were counted.

	Type of dietary diversity	Number of
	indicator	studies	Description
	Food item-based indicators (FIIs) Simple count of Food group-based indicators 56 106 Simple count of the different food groups 2 consumed. Most of the time, foods were
	(FGIs)		classified in 5, 9, 10, or 12 groups. Most of the time, consuming some foods from the
			same group 1 or more times scored 1; not consuming a food group scored 0. In a few
			cases, intra-food-group diversity was taken into account (24-34).
	Dietary guidelines-based	11	Two subtypes:
	indicators (DGIs)		-Healthy Food Diversity (HFD): multiplication of the Berry index by the health value of
			the individual's diet (33-38)
			-Count of different food groups consumed with the minimum recommended number
			of servings consumed to be included in the count (39-43)
	Other indicators (OIs)	12	Four subtypes:

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Acknowledgments

We thank Mary Arimond and Megan Deitchler for their constructive feedback. We also thank the 2 anonymous reviewers whose valuable comments and suggestions helped improve and clarify this manuscript. The authors' responsibilities were as follows-EOV, FM, and YM-P: designed the study; EOV, ALP, and AB: conducted the literature search and selected relevant articles; EOV, ALP, and GB: cross-checked data extracted from articles included in the review; EOV and ALP: drafted the figures, tables, and manuscript; FM, MM, MS, and YM-P: provided critical review; and all authors: read and approved the final manuscript.

convened by Intake-Center for Dietary Assessment, at which YM-P was an invited speaker and Intake-funded participant. Open-access charges were supported by the Bill & Melinda Gates Foundation, Seattle, Washington. Author disclosures: The authors report no conflicts of interest.

table of contents at https://academic.oup.com/advances/.


E Dartois

F Langlet

Ethane clathrate hydrate infrared signatures for solar system remote sensing

Keywords: Planetary ices, IR spectroscopy, Clathrate hydrate, Ethane, Remote sensing

Hydrocarbons such as methane and ethane are present in many solar system objects, including comets, moons and planets. The interaction of these hydrocarbons with water ice at low temperatures could lead to the formation of inclusion compounds, such as clathrate hydrates (water based host cages trapping hydrocarbons guest molecules), modifying their retention, stability and therefore evolution. The occurrence of =clathrate hydrates on solar system surfaces could be established by remote sensing of their spectroscopic signatures. In this study, we measure and analyse ethane clathrate hydrate spectra recorded in the temperature range from 5.3 to 160K, covering most of the temperature range of interest for solar system objects. Specific infrared band signatures are identified for the ethane encaged guest. We provide evidence that ethane clathrate hydrate outcrops can be detected by remote sensing on the surface of planetary bodies.

Introduction

Hydrocarbons are present in many solar system objects. The most abundant hydrocarbons species include gaseous methane or ethane present in the atmosphere of giant planets (e.g. [START_REF] Melin | Jupiter in the Ultraviolet: Acetylene and Ethane Abundances in the Stratosphere of Jupiter from Cassini Observations between 0.15 and 0.19 µm[END_REF][START_REF] Guerlet | Vertical and meridional distribution of ethane, acetylene propane in Saturn's stratosphere from CIRS/Cassini limb observations[END_REF][START_REF] Sada | 13C-Ethane in the Atmospheres of Jupiter and Saturn[END_REF][START_REF] Tokunaga | The detection of ethane on Saturn[END_REF], satellites atmospheres [START_REF] Cours | The 3 . 4 µm absorption in Titan's stratosphere: Contribution of ethane, propane, butane and complex hydrogenated organics[END_REF][START_REF] Lombardo | Ethane in Titan's Stratosphere from Cassini CIRS Far-and Mid-infrared Spectra[END_REF][START_REF] Niemann | Composition of Titan's lower atmosphere and simple surface volatiles as measured by the Cassini-Huygens probe gas chromatograph mass spectrometer experiment[END_REF], comets [START_REF] Villanueva | Ethane in planetary and cometary atmospheres: Transmittance and fluorescence models of the ν 7 band at 3.3 µm[END_REF]Crovisier et al. 2004;[START_REF] Mumma | A Survey of Organic Volatile Species in Comet C/1999 H1 (Lee) Using NIRSPEC at the Keck Observatory[END_REF][START_REF] Mumma | Detection of CO and Ethane in Comet 21P/Giacobini-Zinner: Evidence for Variable Chemistry in the Outer Solar Nebula[END_REF], in the liquid =phase on Titan [START_REF] Farnsworth | Constraining Ethane Concentration in Titan's Lakes and Seas[END_REF][START_REF] Clark | Detection and mapping of hydrocarbon deposits on Titan[END_REF][START_REF] Cordier | An Estimate of the Chemical Composition of Titan's Lakes[END_REF][START_REF] Lunine | The methane cycle on Titan[END_REF], solid =phase on Pluto and Triton [START_REF] Demeo | A search for ethane on Pluto and Triton[END_REF], or Kuiper Belt objects [START_REF] Brown | Methane and Ethane on the Bright Kuiper Belt Object 2005 FY9[END_REF]. The coexistence of hydrocarbons with water ice at low temperatures in some of these environments =raises the question about their ability to form clathrate hydrates. Clathrate hydrates are made of a 3-dimensional watermolecule connected network, linked via hydrogen bonds. To be stabilized, the clathrate network hosts cavities encapsulating guest molecules ("clathrate" meaning closure). Small molecules can be trapped in two main =crystalline clathrate hydrate cubic structures named type I and type II. The type I structure's unit cell (e.g. [START_REF] Sloan | Clathrate hydrates of Natural Gases[END_REF] is made of two dodecahedral (5 12 ) water cages and six larger cages containing twelve pentagonal and two hexagonal faces (5 12 6 2 ) per unit cell. Another structure, the type II structure, possesses sixteen dodecahedral (5 12 ) cages for eight large cages with twelve pentagonal and four hexagonal faces (5 12 6 4 ) per unit cell. =For each structure, the cage's number ratio and the filling ratio with guest molecules influence the spectroscopic signatures of the trapped molecules.

When the guests are relatively volatile species, like hydrocarbons such as methane and ethane, clathrate hydrates will modify their retention time scales in solar system bodies, and also modify their release conditions. =The hydrate term is sometimes used as a semantic shortcut to designate clathrate hydrates but must not be confused neither with hydrates nor with ice mixtures where a molecule is interacting with water ice and not necessarily mediated via an ordered crystalline cage.

Many models do include clathrate hydrates in the evolution or geophysical structure of solar system bodies, (e.g. [START_REF] Combe | Nature, distribution and origin of CO 2 on Enceladus[END_REF][START_REF] Marounina | Role of the global water ocean on the evolution of Titan's primitive atmosphere[END_REF][START_REF] Castillo-Rogez | Insights into Ceres's evolution from surface composition[END_REF][START_REF] Fu | The interior structure of Ceres as revealed by surface topography[END_REF][START_REF] Luspay-Kuti | The presence of clathrates in comet 67P/Churyumov-Gerasimenko[END_REF][START_REF] Marboeuf | A cometary nucleus model taking into account all phase changes of water ice: amorphous, crystalline, and clathrate[END_REF]. A better understanding of clathrate kinetics and their spectroscopic signatures is needed to continue addressing constraints on these clathrate hydrate models. A prerequisite for the identification of clathrate hydrates in the solar system is a thorough characterisation of the vibrational spectroscopic signatures in the infrared, or the specific spectral fingerprints, and their evolution with the ice structure and temperature. For small guest molecules, clathrate hydrates can crystallise in two different cubic structures (I and II), that will affect the filling of the ice cages and therefore the interactions and spectroscopy of the trapped species. Methane is the main hydrocarbon found in cold solar system environments =(e.g. Glein and Zolotov 2020; Guzmán-Marmolejo and Segura 2015, and citations above). Dedicated experiments [START_REF] Dartois | Methane clathrate hydrate infrared spectrum. II. Near-infrared overtones, combination modes and cages assignments[END_REF][START_REF] Dartois | Carbon dioxide clathrate hydrate FTIR spectrum. Near infrared combination modes for astrophysical remote detection[END_REF]Dartois and Deboffle 2008, and references therein) have recorded the clathrate hydrate infrared signatures in the 4K to 140K range, in the 2-4 µm (5000-2500 cm -1 ) range covering the fundamental stretching modes as well as the strongest combinations/overtones.

In addition to methane, ethane has been detected =on Titan and contributes to the hydrocarbon cycle [START_REF] Brown | The identification of liquid ethane in Titan's Ontario Lacus[END_REF][START_REF] Mousis | Sequestration of Ethane in the Cryovolcanic Subsurface of Titan[END_REF][START_REF] Barth | Methane, ethane, and mixed clouds in Titan's atmosphere: Properties derived from microphysical modeling[END_REF][START_REF] Griffith | Evidence for a Polar Ethane Cloud on Titan[END_REF][START_REF] Lunine | Ethane Ocean on Titan[END_REF]. In some instances, such as the surface of Titan, the lower abundance of the ethane hydrocarbon with respect to methane can be compensated by ethane's lower vapour pressure, or its liquid state, and could favour the ethane inclusion in the formation of clathrate hydrates. Missions targeting Titan, such as Dragonfly should better =constrain the surface and lower atmosphere conditions (e.g. [START_REF] Turtle | Dragonfly: In Situ Exploration of Titan's Organic Chemistry and Habitability[END_REF][START_REF] Voosen | NASA to fly drone on Titan[END_REF][START_REF] Lorenz | Dragonfly: A rotorcraft lander concept for scientific exploration at titan[END_REF]. In this article we explore the infrared spectra of the ethane clathrate hydrate in the 5.3-160K range, and provide the spectroscopic signature and band frequencies of the guest ethane trapped molecules.

Experiments

To form the ethane clathrate hydrate we followed a previously proven protocol in evacuated cryogenic cells [START_REF] Dartois | Methane clathrate hydrate infrared spectrum. II. Near-infrared overtones, combination modes and cages assignments[END_REF][START_REF] Dartois | Carbon dioxide clathrate hydrate FTIR spectrum. Near infrared combination modes for astrophysical remote detection[END_REF][START_REF] Dartois | Methane clathrate hydrate FTIR spectrum. Implications for its cometary and planetary detection[END_REF]. The cell was built around two ZnSe windows facing each other, for infrared transmission analysis, sealed to an oxygen-free high thermal conductivity (OFHC), gold coated, copper closed cell. It was thermally coupled to a cold finger whose temperature can be lowered using a liquid He transfer, balanced by a surrounding Minco polyimide thermofoil heater, =which maintains a constant temperature. A high vacuum evacuated cryostat (P < 10 -7 mbar) surrounded the cell. Gases were injected =into the cell (or evacuated) with a stainless steel injection tube brazed at the bottom of the cell. In these experiments, a water ice film was formed first, by injecting water vapour =into the cell maintained just below the water ice freezing point, forming an Ih ice. Deionized water was used. Several freeze-pump-thaw degassing cycles were applied to remove any dissolved gases. The cell temperature was then lowered to 267 K for the clathrate formation.

The cell was pressurised with ethane gas at about 25 bars. This {pressure,temperature} couple is well above the stability curve for ethane clathrate hydrate, which is about 3.5 bars at 267 K.

The system was kept under pressure =for approximately fifteen days, much above the expected diffusion kinetics time scale. If one assumes a typical diffusion coefficient around 10 -12 m 2 /h at 267K (e.g. Falenty et al. 2013, and references therein), in fifteen days the diffusion pervaded ∼20µm. The deposited water ice film thickness was several microns thick (the film deposited on each face of the cell is about 3±1µm thick), thus fully penetrated by diffusion by the ethane gas to make the clathrate. The temperature was then progressively lowered (at a rate of ∼1K/min) while evacuating the ethane gas. During this operation, we maintained the system just below the sublimation/vaporisation curve of pure ethane, and above the ethane clathrate hydrate expected stability curve [START_REF] Roberts | Constitution diagrams and composition of methane and ethane hydrates[END_REF]).

When the system was at a temperature sufficiently low enough so that the kinetics of the clathrate destabilisation becomes very long (typically below 100 K), the system was fully evacuated while the temperature continued to be lowered to its minimum of about 5.3K. The infrared spectra were then recorded with steps of 20K, which allowed us to follow the evolution of the spectral signatures, up to the clathrate hydrate rapid dissociation occurring above 160 K over an hour under our experimental conditions. (In between each temperature stabilised step, the temperature was raised at a rate of ∼1K/min, allowing for proper thermalisation of the clathrate hydrate.) The spectra were recorded with a Bruker Fourier transform infrared spectrometer covering the 5000-700 cm -1 spectral range at a resolution of 0.5 cm -1 , with a globar source, KBr beamsplitter and an HgCdTe detector cooled with liquid N 2 .

Results

The ethane clathrate hydrate transmittance spectrum, at 5.3K, after baseline correction, is shown in Fig. 1. The ethane clathrate hydrate bands in the infrared recorded from 5.3 to 160K are shown in Fig. 2 for the fundamental vibrational modes range (3000-2700 and 1500-1100 cm -1 ), and in Fig. 3 for the combinations/overtones (4470-3600 cm -1 ). These spectra are compared to the spectra of pure ethane ice recorded in the same cell at 77K, =crystalline ethane recorded at 15K [START_REF] Hudson | Infrared spectra and optical constants of astronomical ices: II. Ethane and ethylene[END_REF], and an amorphous H 2 O:C 2 H 6 (20:1) ice mixture from the Cosmic Ice Laboratory 1 in the fundamental modes regions. A spectrum of an ethane:oxirane (7:3) mixed clathrate from [START_REF] Richardson | FT-IR spectra of vacuum deposited clathrate hydrate of oxirane H_2S, THF, and ethane[END_REF] recorded at 90K, is shown above the spectra in the mid-infrared. The oxirane vibrational mode contribution is identified with asterisks. Oxirane is known to form and induce a clathrate hydrate type I structure. Its clathrate type I and II spectral positions are well known, helping to confirm the structure formed and thus assign the vibrational spectrum for other guests trapped in mixed oxirane =clathrate hydrates. A tentative attribution of the vibrational modes and combinations/overtones is over-plotted on these figures. The assignments are based on the gas phase rovibrational analysis presented by [START_REF] Hepp | RESEARCH NOTE Vibration-rotation bands in ethane[END_REF], 1999b[START_REF] Hepp | The jet cooled spectrum of ethane between 4000 and 4500cm-1[END_REF]; [START_REF] Hepp | The v 6 + v 10 band of ethane[END_REF], and assumes a bathochromic shift (a few wavenumbers for fundamental vibrations and up to ten to twenty for the combination modes regions) induced by the ethane clathration in a clathrate hydrate large cage (see Table 1). We also report the band position evolution as a function of temperature in Fig. 4 for selected intense transitions, and compare these band transitions with positions from the ethane:oxirane mixed clathrate spectrum from [START_REF] Richardson | FT-IR spectra of vacuum deposited clathrate hydrate of oxirane H_2S, THF, and ethane[END_REF] for the mid-infrared modes.

Discussion

Pure ethane clathrate hydrate is expected to form a type I clathrate hydrate. =The positions of the ethane bands in our experiment, when compared to the [START_REF] Richardson | FT-IR spectra of vacuum deposited clathrate hydrate of oxirane H_2S, THF, and ethane[END_REF] mixed ethane:oxirane band positions (shown with green diamond in Fig. 4) coincide well with the expected type I clathrate hydrate positions. [START_REF] Richardson | FT-IR spectra of vacuum deposited clathrate hydrate of oxirane H_2S, THF, and ethane[END_REF] however point toward unusual relative intensities of the oxirane band intensities in this experiment, requiring further analysis. It may suggest that the presence of ethane in this mixed clathrate may deform the structure more than for smaller guest species. Peak positions and tentative assignments are reported in Table 1 for the two measured extreme temperatures, 5.3 and 160 K, respectively.

The main outcome of this study is that the formation of an ethane clathrate hydrate gives rise to a recorded very unique band pattern, distinct from the other observed features for ethane in other possible phases. In particular the band splitting in the fundamental ν 7 degenerate mode region around 2970 cm -1 (already observed by [START_REF] Richardson | FT-IR spectra of vacuum deposited clathrate hydrate of oxirane H_2S, THF, and ethane[END_REF]), with a splitting amplitude of a bit more than 10 cm -1 ) is characteristic of the ethane clathrate hydrate, and not observed in other pure ethane or mixed ethane/water ice phases. In the combinations/overtone near infrared region, many bands observed in the pattern are also characteristic (in particular the ∼4400, 4320, 4170, 3980 cm -1 combinations modes splittings). They are clearly distinctive from the other possible solid ethane or ethane simple hydrate phases, pointing toward the uniqueness of the identification of a clathrate hydrate through the observation of these modes.

In planetary environments such as Jupiter, Saturn and its satellite Titan, Pluto and other TNOs, as well as comets, ethane is less abundant than methane. When type I clathrate hydrate formers are mixed, they may induce the formation of a type II hydrate, under specific ratios. [START_REF] Subramanian | Structural Transition Studies in Methane + Ethane Hydrates Using Raman and NMR[END_REF] report that in mixed methane and ethane clathrate hydrate studied by Raman spectroscopy, both type I formers taken individually, formed a type II clathrate hydrate under specific composition ranges, typically starting above 72 to 75% of methane. =The structure will go back to type I clathrate hydrate when ethane becomes a trace species, above the upper bound of 95% methane in these experiments. The mixed methane/ethane clathrate hydrate is metastable in some cases =as shown by, e.g., [START_REF] Takeya | Coexistence of structure I and II hydrates formed from a mixture of methane and ethane gases[END_REF]. [START_REF] Takeya | Lattice Expansion of Clathrate Hydrates of Methane Mixtures and Natural Gas[END_REF] measured the lattice constants of mixed methane and ethane clathrate hydrate at 113 K as a function of CH 4 gas content. The mixed system forms the type II clathrate hydrate for about 60 to 80% methane content and type I above and below, with values close to the pure methane hydrate lattice parameters of type I at high methane content. =Type I and type II mixed methane+ethane clathrate hydrates can coexist. The type II has been shown to be a metastable kinetically favoured stage during some mixed clathrate hydrate nucleation experiments, with a slow transformation into sI, the type I being the stable phase to long time scales [START_REF] Kida | Dissociation behavior of methane-ethane mixed gas hydrate coexisting structures i and ii[END_REF][START_REF] Ohno | Raman studies of methane-ethane hydrate metastability[END_REF][START_REF] Murshed | Kinetic studies of methane-ethane mixed gas hydrates by neutron diffraction and raman spectroscopy[END_REF]. In both type I and II clathrates, the ethane molecules occupies the large cage (the 5 12 6 2 in type I and 5 12 6 4 in type II), as ethane is too large to fit into the small cage. The proportions at which this change occurs will vary with the formation temperature of the clathrate hydrate because of the difference in fugacity of these two species. The ratio of small to large cages in each unit of the two clathrate ice structures favours type I when only the large cages are filled. The band positions are expected to shift by a few wavenumbers in between type I and type II clathrate hydrate large cages, being about 4 cm -1 redder for type II with respect to type I in the stretching modes, based on Raman spectroscopy [START_REF] Subramanian | Structural Transition Studies in Methane + Ethane Hydrates Using Raman and NMR[END_REF]. Apart from the shift specific to each clathrate hydrate structure, the pattern observed in the present experiments should be representative. =Several splittings for some vibrational modes/combinations, distinct from the known crystalline phase splittings, characteristic of ethane trapped in the large cages of a clathrate hydrate of type I (or II with an expected moderate shift) should be actively searched for to establish such clathrate hydrates occurence.

=Saturn's moon Titan, with an atmospheric temperature in the 70-180K range [START_REF] Hörst | Titan's atmosphere and climate[END_REF][START_REF] Niemann | Composition of Titan's lower atmosphere and simple surface volatiles as measured by the Cassini-Huygens probe gas chromatograph mass spectrometer experiment[END_REF][START_REF] Mckay | The thermal structure of Titan's atmosphere[END_REF], hosts conditions for hydrocarbon rains, and, with a surface temperature around 90K, harbours liquid hydrocarbons, including methane and ethane lakes (e.g. [START_REF] Mastrogiuseppe | Deep and methane-rich lakes on Titan[END_REF][START_REF] Hayes | Hydrocarbon lakes on Titan: Distribution and interaction with a porous regolith[END_REF][START_REF] Stofan | The lakes of Titan[END_REF]). The stability zone for the formation of methane and ethane clathrate hydrate falls in this temperature range [START_REF] Kalousová | The Insulating Effect of Methane Clathrate Crust on Titan's Thermal Evolution[END_REF][START_REF] Tobie | Evolution of Titan and implications for its hydrocarbon cycle[END_REF][START_REF] Lunine | The methane cycle on Titan[END_REF][START_REF] Thomas | A theoretical investigation into the trapping of noble gases by clathrates on Titan[END_REF][START_REF] Thomas | Clathrate hydrates as a sink of noble gases in Titan's atmosphere[END_REF][START_REF] Atreya | Titan's methane cycle[END_REF][START_REF] Osegovic | Compound clathrate hydrate on Titan's surface[END_REF]. [START_REF] Vu | Rapid Formation of Clathrate Hydrate From Liquid Ethane and Water Ice on Titan[END_REF] recently showed that the kinetics of formation at low temperature of an ethane clathrate hydrate is kinetically possible under Titan conditions, using Raman spectroscopy. These authors report that with a surface temperature of 90K, a full clathration of ice in contact with ethane will occur in about four (Earth) years, i.e. within a time scale shorter than Titan's seasons and summer solstices are separated by about 15 years, directly related to Saturn's orbital period of slightly more than 29 years). An alternative formation at the surface invoked in this study is the contact of ethane rain directly on exposed ice slabs, a situation for which the clathrate hydrate kinetics is more difficult to estimate. However, for such exposed fields, the spectroscopic signatures obtained by remote sensing are directly accessible, and would provide constraints on =clathrates occurrence. In Titan's lakes, the density of liquid ethane being higher than liquid methane (e.g., about 462.7 kg/m 3 (melting line) and 662.8 kg/m 3 (melting line) at 100K for methane and ethane, respectively [START_REF] Younglove | Thermophysical Properties of Fluids. II. Methane, Ethane, Propane, Isobutane, and Normal Butane[END_REF]), a methane/ethane phase separation should occur. =The full nitrogen, methane and ethane system must be investigated under Titan conditions (e.g. [START_REF] Hanley | Titan: Bubbles in focus[END_REF]. At the bottom of these lakes, ethane may therefore be in direct contact with an ice bedrock like the one observed elsewhere on Titan (e.g. [START_REF] Griffith | A corridor of exposed ice-rich bedrock across Titan's tropical region[END_REF]), but residing well below the lake's surface. =Additionally, if the temperature at the bottom of the lakes is higher than the surface temperature, the formation kinetics should be thermally enhanced. [START_REF] Vu | Rapid Formation of Clathrate Hydrate From Liquid Ethane and Water Ice on Titan[END_REF] consider the domain of formation at greater depths if ethane percolates deeper through the surface, with corresponding higher temperatures and favourable formation kinetics, but hardly accessible to spectroscopic means. Many experiments following the cage evolution and spectral signatures of clathrate hydrates are performed using Raman spectroscopy. =In the spectral range considered here, if both Raman and infrared spectrometers can be integrated in space probes that would land on solar system objects, and perform an analysis of the local field, a vast majority of the spectroscopic information is still obtained using infrared only remote sensing by space probes using on-board spectrometers. An outcrop on the surface of icy bodies, or a terrain recently exposed when there is a space probe fly-by may allow for the identification of clathrate hydrates by infrared spectroscopic means. Such a direct spectroscopic detection would considerably anchor our view on the geophysical evolution of these objects.

Conclusion

We measured the temperature dependence, in the 5.3 to 160 K range, of the near and mid-infrared spectral signatures of ethane trapped in a type I clathrate hydrate structure, identified by comparison to literature spectra of mixed oxirane:ethane clathrate hydrate. The =ethane molecule occupies the large cages of the ice crystal structure formed by the host water molecules. The large number of individual transitions observed in the fundamental modes of vibration and the numerous combinations/harmonics represent distinctive spectroscopic fingerprints that will allow remote identification if ethane is present in a clathrate hydrate in solar system ices. Further experiments are foreseen to explore the type I and II clathrate hydrate differences in the infrared over a large range of temperatures. When ethane occupies the large cage of type I or II clathrate hydrates, only a mild shift of about four wavenumbers between ethane bands in each structure is expected, =and, apart from a shift of such magnitude, the measured spectra in this study will be similar to those of both structures. These signatures can be used to analyse planetary remote sensing data and may be used for future proposed missions exploring the icy worlds of the solar system, in particular, ones targeting Saturn's moon Titan, such as the Dragonfly mission.

Fig. 1 .

 1 Fig.1. Baseline corrected ethane clathrate hydrate transmittance spectrum recorded at 5.3K. Note the imperfect cancelation of the Fabry-Perot fringes in the space between the ZnSe windows, leading to small waves observed superimposed on the =spectrum (e.g. in the 2500-1700 cm -1 interval). Scattering effects deform the water ice bands because of imperfect film surface roughness once clathration is achieved.

Fig. 3 .Fig. 4 .

 34 Fig. 3. Temperature dependent infrared spectra of the ethane clathrate in the combination/overtone regions. The crystalline pure ethane spectrum of Hudson et al. (2014) recorded at 15K is shown above. The pure ethane spectrum recorded in the cell at 77K is shown above too. Tentative assignments of the implied vibrational modes are given (see text for details). Spectra are offset for clarity.

Table 1 .

 1 The ethane centroid vibrational positions for an ethane:oxirane (7:3) mixed clathrate spectrum from[START_REF] Richardson | FT-IR spectra of vacuum deposited clathrate hydrate of oxirane H_2S, THF, and ethane[END_REF] recorded at 90K, are shown with green diamonds. Oxirane is known to form and induce a clathrate hydrate type I structure, helping to confirm the structure formed and also assign the C 2 H 6 vibrational bands in this mixed oxirane clathrate hydrate.

Hudson et al., https://science.gsfc.nasa.gov/691/cosmicice/spectra.html

Acknowledgments

This work was supported by the CNRS/INSU and CNRS/INP. The authors want to thank M. Bouzit, B. Crane, for their technical support to the initial design of the cell.