Adaptation and validation of a food frequency questionnaire (FFQ) to assess dietary intake in Moroccan adults

The burden of chronic non-communicable diseases (NCD) in African countries continues to rise [1]. The epidemiological profile of North Africa increasingly mirrors that of more developed societies, where cancer, cardiovascular, and respiratory diseases represent a major societal and health burden. Prevalence of these, and other NCDs related to diet, has continuously increased in the last two decades [2–4], but there is scant scientific evidence on the role of dietary habits on disease risk and prevalence in the Moroccan population [5, 6].

Food frequency questionnaires (FFQs) are a helpful instrument to ascertain usual dietary intake and its relationship with health and disease outcomes [7, 8]. Although FFQs are widely used in Europe and America [9, 10], nutritional epidemiology in Morocco remains hindered by the lack of locally representative dietary questionnaires, particularly FFQs. We are only aware of one FFQ recently developed to ascertain usual fruit and vegetable intake in Moroccan adults [11]. To date, the vast majority of what we know about dietary habits and chronic disease in this country relates to their association with Ramadan and obesity [2, 12].

The rapid socio-economic transition in North Africa has been accompanied by changes in the way the population eat, which are not easily captured with dietary questionnaires from, for example, high income countries. Morocco is a fast-growing developing country with a diet characterised by intake of vegetable-based dish, spices, and meat [11–13], and a rich combination of very traditional dishes with a more modern cuisine. Having FFQs that reflect such transitions and cultural features are urgently needed to identify regionally and locally relevant dietary risk factors for health and disease outcomes. To implement these FFQs, the validity and reproducibility of the instrument needs to be assessed [14, 15].

Our study was aimed at adapting the international GA²LEN FFQ to include staple foods consumed in Morocco, and at validating it in a sample of health Moroccan adults.

The final version of the adapted FFQ contained 255 foods, which were classified into 32 groups as follows: (1) bread, (2) breakfast with grains, (3) couscous, (4) pasta, (5) cake, (6) rice, (7) sugar, (8) sweets without chocolate, (9) chocolate, (10) vegetable oil, (11) margarine and vegetable fat, (12) butter and animals fat, (13) dried fruit, (14) legumes, (15) vegetables, (16) potatoes, (17) fruits, (18) juice, (19) non-alcoholic beverages, (20) coffee/tea, (21) beer, (22) wine, (23) other-alcoholic beverages, (24) red meat, (25) poultry, (26) sekat (offal), (27) fish, (28) eggs, (29) milk of cow/milk of soya, (30) cheese, (31) other dairy products, and (32) miscellaneous foods (Table 1).

The mean intake of TEI, macro-nutrients and micro-nutrients measured by FFQ1, FFQ2, and the 24-h recall questionnaires are presented in Tables 3. For TEI and nutrients intakes, the means reported in the FFQ1 were higher than the means reported using the average of the three 24-h recall questionnaires. The Bland-Altman plots for energy, and macronutrients (carbohydrates, proteins, and fat) are shown in Fig. 2. The Bland Altman plots confirmed an over-estimation of nutrient intakes consumptions by the FFQ.

Nutrients	FFQ1	FFQ2	24 Hour Recalls
	Mean ± SD	Mean ± SD	Mean ± SD
Energy (kcal)	2546.5 ± 719.5	2392.5 ± 738.9	1926.2 ± 589.6
Carbohydrates(g)	452.1 ± 149.7	430.4 ± 148.6	321.9 ± 103.3
Proteins (g)	135.3 ± 61.6	128.9 ± 57.4	87.1 ± 38.2
Fat (g)	108.2 ± 39.9	103.9 ± 44.3	71.8 ± 39.0
Total MUFA(g)	110.2 ± 64.0	104.6 ± 57.8	45.8 ± 32.9
Total PUFA(g)	78.3 ± 53.8	72.5 ± 47.1	31.1 ± 29.9
Total SFA(g)	80.9 ± 55.6	75.6 ± 54.3	41.4 ± 33.1
Vitamin A (μg)	445.1 ± 220.9	439.9 ± 259.2	533.1 ± 680.8
Vitamin C (mg)	221.6 ± 141.6	196.3 ± 114.0	129.3 ± 93.4
Vitamin E (mg)	73.4 ± 53.1	70.1 ± 48.7	28.0 ± 30.2
Selenium (μg)	138.4 ± 74.0	144.7 ± 67.2	91.1 ± 63.7
Magnesium (mg)	567.3 ± 237.0	556.7 ± 230.3	324.7 ± 143.7
Calcium (mg)	1241.6 ± 600.6	1188.7 ± 576.2	755.0 ± 408.2
Iron (mg)	28.5 ± 22.4	26.7 ± 20.6	16.9 ± 11.4
Fiber (g)	49.4 ± 58.5	44.9 ± 52.1	26.3 ± 37.4

Our study described the process of adaptation of the international GA²LEN FFQ for use in Moroccan adults, and its relative validity and reproducibility to estimate usual food intake. The adapted FFQ contained 255 items, including staple foods consumed by the Moroccan population. The FFQ was classified into 32 food groups or sections, to mirror the structure of the GA²LEN FFQ, which facilitates international comparability. To our knowledge, this is the first FFQ in Morocco to include a comprehensive list of both traditional and ‘modern’ foods, providing a reasonable assessment of relative dietary intake over a 1-year period. We are aware of another FFQ developed in Morocco by Landais et al., but it is limited to intake of fruits and vegetables only [11]. The energy adjusted Pearson correlation between the FFQ and the mean 24-HRs showed that the relative validity findings were moderately consistent across the majority of nutrients, they ranged between 0.19 for fat to 0.86 for total MUFA, and these observed values were comparable to other FFQs validation studies [26–28].

The nutrient intakes reported with the use of the FFQ were higher than those reported using the 24-h recall questionnaires. This over-reporting is not uncommon when validating an FFQ with a relatively large number of food items [26, 29–33]. We used the average of three 24-h recall questionnaires, which is considered an acceptable number of days to capture usual intake [34]. A systematic review found that 75% of validation studies use the 24-h recall questionnaires as reference method against FFQs [35], preferred for the accuracy to capture daily consumption of a varied diet, and for their relatively easier administration and analysis compared to other dietary questionnaires. The FFQ and the 24-h recall questionnaire have some differences in their error sources, which make them sufficiently independent [36]. Both instruments are prone to memory bias (long-term vs short term in the FFQ vs the 24-h recall questionnaire, respectively) and have differences in the perception of portion sizes (usually pre-defined in the FFQ) [35, 37, 38]. The 24-h recall questionnaire method is based on open-ended questions; while the FFQ is usually designed to have close-ended questions.

The acceptable correlations between the the FFQs and 24-HRs and the overestimation of energy and nutrient intakes between the two methods were confirmed by the Bland-Altman plots. These figures indicated a positive mean difference for TEI and macronutrients. These results are in agreement with those reported by other studies [39–41].

Since no dietary method can assess nutrient intake without error [35], we used energy adjusted nutrient estimates in our analyses as a way to reduce correlated errors between the two dietary methods [22, 38]. Energy-adjustment decreased correlation coefficients for all nutrients, which often happens when variability is more related to systematic errors of under/overestimation than to energy intake [42–44]. Similarly, other studies have not reported that energy-adjusted estimates improved crude correlations [45–47]. The de-attenuated correlations were increased because of the correction for the day to day variation in intakes.

The reproducibility of the FFQ was examined by the administration of the questionnaire in two occasions, 1 month apart. As reported in other studies [48, 49], we found that the estimates observed in FFQ1 were slightly higher than in the second FFQ. This could be partly explained by the level of engagement of the participants and the attention required to complete the FFQ in full. The ICCs showed a good level of agreement for the reporting of macro- and micronutrients, ranging from 0.69 (fat) to 0.75 (proteins for macro-nutrients, and over 0.7 for most micro-nutrients, suggesting that the FFQ has a good repeatability and reproducibility [50].

Our study has several strengths. The structure of the FFQ was adapted from the international GA²LEN FFQ, whose applicability has been demonstrated in multinational studies in high [9] and low income countries [51]. In order to make the FFQ representative of the Moroccan population, we endeavored to identify traditional foods that are part of the staple diet of the country, while also maintaining the international structure of the food classification to facilitate international comparisons. We followed a strict protocol to ensure the FFQ was correctly translated into Moroccan Arabic, which is different from the written and spoken Arabic in other North African countries. The FFQ also takes into account seasonal variations in food consumption, an important feature in North Africa where seasonality strongly influences dietary choices.

We acknowledge this validation study has some limitations. The FFQ captures usual intake of foods over a longer period of time than a 24-h recall questionnaire, which could lead to errors in the results. We compared the FFQ to the average intake reported in three 24-h recall questionnaires. Although this is an acceptable number of interviews, several studies recommend seven recall days (replicates) to capture a better estimate of the habitual intake. However, three recording days per subject are considered feasible and sufficient to estimate within-person variability (day-to-day variability). Due to the length of the validation study (1 month), some seasonal variations might not have been captured accurately with the 24-h recall questionnaire. This may negatively impact the correlation results, reflecting differences between the two instruments, rather than limitations of the FFQ. The length of the FFQ (255 food items) might have discouraged the participants to respond it fully. We designed the FFQ bearing in mind the current gap in nutritional epidemiology in North Africa, creating a tool that captures the usual diet of Morocco, and that it estimates intake of other foods that are associated with the nutritional transition of the region. Finally, the majority of the study sample was comprised of women with a high level of education. This does not represent the general population of Morocco, where illiteracy and poverty are common. The use of the FFQ in the general population would probably require a close interaction between an interviewer and the participant to overcome communication and educational limitations.

This adaptation and validation study showed that the FFQ has a good relative validity and a good reproducibility for most nutrients. It is the first complete and validated tool to assess usual dietary intake in the Moroccan population that includes a wide range of traditional, as well as more ‘modern’ food items. Given its representativeness of local foods and habits, it can be used as an instrument to assess the relation of dietary habits and diseases in which diet might play a role.