Prevention of Maternal Low-Grade Chronic Inflammation: The Diet’s Inflammatory Potential in Pregnant Women in Southern Benin ()
1. Introduction
An adequate maternal nutritional intake is a fundamental factor for a healthy pregnancy and the child’s optimal development. The hypothesis of “developmental origins of diseases” assumes that the nutritional status of the mother during the preconception and pregnancy period can influence the development of offspring and the onset of diseases, from childhood to old age [1] .
Epidemiological studies have shown a strong correlation between inflammatory markers and hyperinsulinemia, hypertriglyceridemia, body mass index and hypertension [2] [3] . Through pro-and anti-inflammatory bioactive compounds contained in food, diet has been shown to play a role in the occurrence of chronic inflammation [4] [5] , which paves way for the development of metabolic syndrome and diabetes [6] [7] .
Chronic inflammation in pregnant women leads to elevated blood pressure [8] and pre-eclampsia [9] , which can endanger the course of pregnancy for both mother and fetus and expose the unborn child to chronic diseases [10] [11] . Sen et al. [12] reported that inflammation was associated with a high risk of low birthweight in infants and a high risk of low breast milk production at birth. According to Hemaltha [11] , chronic inflammation in pregnant women is associated with vasculo-renal syndrome with a negative impact on the fetal growth and its development.
A pro-inflammatory diet during pregnancy is associated with chronic maternal systemic inflammation [8] . A study in America showed that the level of inflammation was higher in the second trimester of pregnancy and was associated with increased risk of gestational diabetes mellitus in African-American women [13] . In 2012, the cross-sectional study by Golzarand et al. [14] , observed that protein C-Reactive (CRP) was strongly associated with a high carbohydrate intake with saturated fatty acid and there were significant associations between food carbohydrate intakes, saturated fatty carbohydrates and the CRP.
In Benin, the rate of eclampsia and low weight at birth were respectively 12% and 9.1% [15] [16] in 2014. Maternal nutrition needs to be improved in Benin. From 2006 to 2017-2018, according to Demographic and health surveys, the percentage of women aged 15 - 49 presenting a state of thinness (body mass index less than 18.5) increased slightly, from 9% to 11%. During the same period, the percentage of overweight or obese women (BMI greater than or equal to 25) also increased, but more significant, going from 19% to 26%. The food inflammatory in pregnant women is not much documented. The objective was to determine the diet inflammatory index (DII) in pregnant women.
2. Methods
2.1. Settings
The study was conducted in the city of Ouidah, 40 kilometers from Cotonou. The total population of the city was estimated at 187,064 inhabitants with 5833 pregnancies expected [17] . Ouidah is a coastal city, traditional fishing is practiced.
2.2. Study Design and Population
The study was cross-sectional. The study population was pregnant women municipality. Any pregnant woman residing in the Ouidah municipality for at least six months was included in the study. Pregnant woman who was absent, sick, who has been prescribed a special diet for treatment were not included. Any woman who has declared herself pregnant and whose pregnancy has not been certified by a health worker was not selected.
2.3. Sampling
Sampling method and technique
The probabilistic sampling method with the cluster sampling technique adapted from World Health Organization were used to select pregnant women.
Sample size
The sample size was determined from the Schwartz formula.
where the risk of error α that we assume is 5% for a 95% confidence interval. Since we don’t have a prevalence of low-intensity inflammation in the general population in Benin, the prevalence of low-grade inflammation measured by ultra-sensitive CRP in a study carried out in Ouagadougou (39.4%) was considered [18] . By setting the aimed precision “i” at 7% and the cluster effect 1.5, the minimum size was 256 pregnant women. A minimum sample of 300 pregnant women was retained.
2.4. Variables
The dependent variable was “the Diet Inflammatory Index (DII) in pregnant women”. It was calculated for each participant from these dietary intakes of 22 nutrients according to the method described below.
1st step: Estimation of average nutrient intake from 24 h reminders
From two 24-hour non-consecutive food recalls carried out among pregnant women, the West African food composition table and the “Alimenthèque R” software were used to determine nutrient intakes. Dietary intakes have been adjusted and normalized with Multiple Source Methods [19] .
2nd step: Calculation of the inflammatory weight of nutrients
The average intake of each nutrient was multiplied by its inflammatory weight predetermined by Shivappa et al. [2] to obtain the inflammatory weight of each nutrient (Table 1).
3rd step: Calculation of the diet inflammatory index
To determine this index, the sum of the inflammatory weights of each nutrient was performed. When DII was positive, the diet was considered pro-inflammatory and when negative, the diet was as considered anti-inflammatory [2] .
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Table 1. Inflammatory coefficients of nutrients and energy.
Source: Designing and developing a literature-derived, population-based dietary inflammatory index [2] .
The independent variables were:
Dietary factors: energy, carbohydrates, fat, protein, micronutrients (fibers, thiamine, niacin, riboflavin, vitamin A, D, E, C, B6, B9, B12, iron, zinc, magnesium,)
Food groups;
Socio-demographic and economic factors: age, ethnicity, religion, education, occupation and socio-economic status.
2.5. Data Collection
Nine teams including a dietician and a community member fluent in French and local languages were formed and trained on the 24-hour multiple-pass recall technique described by Conway et al. [20] .
2.6. Data Analysis
Dietary intakes were adjusted and normalized with Multiple Sources Meth software. Data were analyzed using the SPSS software version 18.0 (SPSS Inc., Chicago, IL). A weighting variable was created and used in the analyses to take into consideration the sample design. The averages and standard deviation were estimated for the normally distributed quantitative variables and the medians with the percentiles 25 and 75 were calculated for the asymmetric ones. Proportions were calculated for the qualitative variables. On one hand, a correlation analysis was performed to investigate the relationship between DII and nutrients and between DII and food group intakes on the other hand. The significance threshold was set at p < 0.05.
3. Results
3.1. Participants’ Characteristics
The average age of participants was 27.20 ± 5.99 years. The most represented age group was 30 to 42 years with 34.84% (95% CI [28.98; 40.71]). Illiterate pregnant women and those with a high socio-economic level were also frequent and represented respectively 39.18% and 36.80%. Table 2 summarizes the sociodemographic characteristics of pregnant women.
3.2. Diet Inflammatory Index of Pregnant Women
The median diet inflammatory index was −3.026 with for Q1 (−16.59) and Q3 (1.86). Among the 310 pregnant women, 35 (11.30%) had a pro-inflammatory diet and 275 (88.70%) had an anti-inflammatory diet.
3.3. Association of Food Groups with Diet Inflammatory Index
Table 3 shows that only cereals, fruits, vegetables, legumes, fish, roots and tubers and sweets and sweet products were significantly correlated with the diet inflammatory index of pregnant women’s diet.
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Table 2. Socio-demographic and economic characteristics of pregnant women in Ouidah, Benin, (n = 310).
Maize was the main cereal in staple foods in the city. Vegetables consumed were namely tomatoes, onion, okra, pepper, leafy vegetables. Legums consumed were cowpea and beans. Mutton, goat, pork and poultry were protein source. Fruit consumption is limited as shown table III. Fish was part of the population’s daily diet.
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Table 3. Correlation coefficients between the overall diet inflammatory index and food group consumed in pregnant women, Ouidah, Benin (n = 310).
3.4. Association of Nutrient Intakes with Diet Inflammatory Index
Table 4 shows that only carbohydrate intake was positively correlated with the diet inflammatory index at the 5% threshold. That is, there is a link between carbohydrates and the index. But, lipids, proteins, fibers, monounsaturated fatty acids, polyunsaturated fatty acids, iron, vitamin B9, niacin, riboflavin, thiamine, vitamin B6, B12, C, E, D and zinc were negatively correlated with the diet inflammatory index. Only magnesium and vitamin A resulted in an inflammatory index negatively correlated with the diet inflammatory index.
4. Discussion
The study showed that the diet was pro-inflammatory in 11.30% of pregnant women. Vitamin A and zinc were negatively correlated with the diet inflammatory index. Intakes of tubers and sugary drinks were positively correlated with the diet inflammatory index while intakes of cereals, vegetables, legumes and fish were negatively correlated with DII.
4.1. Diet Inflammatory Index of Pregnant Women
Previous studies on the prevalence of pro-inflammatory diet in pregnant women are scarce. Instead, studies have focused on measuring chronic inflammation using CRP. Therefore, Zéba et al. in Burkina Faso [18] reported that 39.4% of the apparently healthy pregnant women of both sexes in their sample had low-intensity chronic inflammation, while Golzarand [14] in Iran reported that 24.6% of patients hospitalized at the endocrinology clinic had chronic inflammation. Chronic inflammation during pregnancy is particularly critical because during its development, the human embryo and fetus undergo a complex series
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Table 4. Correlation coefficients between the overall diet inflammatory index and nutrient intake in pregnant women, Ouidah, Benin (n = 310).
of changes in cell type and cell number. Each of these changes takes place in a strictly well chronological sequence and the disruption of the process by chronic inflammation can lead to dramatic and lasting consequences for the fetus and sustainable and dramatic consequences for the mother [13] .
4.2. Nutrients Associated with the Diet Inflammatory Index
Carbohydrates and fibers
The correlation weighting between carbohydrate intake and the dietary inflammatory index was higher than that obtained by Golzarand (r = 0.19) [14] . Other studies have reported the relationship between carbohydrate intake and CRP values [8] [21] [22] , between glycemic index and/or glycemic load and hs-CRP concentrations [23] [24] . In this regard, a recent meta-analysis covering randomized controlled intervention studies suggests that diets with a low glycemic index/load should be favored over diets with a high glycemic index/load in order to reduce pro-therapeutic biomarker concentrations inflammatory as hs-CRP [25] . Indeed, it is recognized that variations in blood sugar, including dysglycemia, contribute by at least two mechanisms to chronic inflammation, namely excessive glycation of proteins and activation of oxidative stress [26] .
Fiber intakes are inversely correlated with the diet inflammatory index. Several cross-sectional studies reported this inverse association between fiber consumption and hs-CRP concentrations [27] . A recent literature review including seven intervention studies concluded, based on six of the seven studies, that hs-CRP concentrations could be reduced by 25% - 54% after increasing dietary fiber intakes (3.3 - 7.8 g/MJ) [28] . One should note that these decreases in hs-CRP were reported as part of weight loss in most studies considered.
Fatty acids
Lipids such as monounsaturated and polyunsaturated fatty acids were negatively correlated with the diet inflammatory index as Golzarand et al reported in a study [14] of the lifestyles of smokers and non-smokers and Shivappa et al. [29] in another one about CRP among diabetic and cancer patients. In fact, fatty acids have the capacity to inhibit or activate certain stages of the inflammatory process [30] [31] . Consequently, saturated fatty acids can be linked to immune system receptors and activate the signaling pathway that regulates the expression of pro-inflammatory genes [32] [33] .
Proteins
Protein consumption increases the inflammatory index. Hung et al. [34] and Keogh et al. [35] reported opposite results in studies concerning followed hemodialysis patients and obese. Cavicchia et al. [22] found no link between protein intake and inflammatory index. However, other studies reported results similar to the present study [23] . According to Lavoie, protein-rich diets do not appear to be suitable for relieving inflammation, due to their likely deleterious effects on liver and kidney functions [36] [37] .
We should note that energy was not correlated with the diet inflammatory index. Contrary results were reported between energy and the inflammatory index of diet [23] . This may be due to the fact that energy results from macronutrients whose sources influence the inflammatory index differently.
Magnesium and Vitamin A
Micronutrients such as magnesium and vitamin A were inversely associated with the inflammatory index. The results are like those of Golzarand et al. [14] and Shivappa et al. [8] . Bo et al. reported that dietary magnesium intakes were strongly and inversely associated with pro-inflammatory marker concentrations [27] . Evidence indicates that flavonoids are able to act to interfere with inflammation by modulating intracellular signaling cascades that control neuronal survival, death and differentiation and can have impact on gene expression and interaction with mitochondria [26] .
4.3. Food Groups Associated with the Diet Inflammatory Index
Intakes of cereals, vegetables, legumes, and fish were negatively correlated with the diet inflammatory index. These results are like those of Ruiz et al. [38] . A recent literature review suggests, based on epidemiological studies, that each serving of whole grain cereal products consumed is associated with a 7% decrease in hs-CRP levels after adjustment for other nutritional factors [39] .
The anti-inflammatory effects of vitamins C and E of provitamins A and fiber may explain that fruits and vegetables have beneficial impacts on the inflammatory profile. In a study dealing with non-smoking men, Watzl et al. [40] reported that consuming 8 portions per day of carotenoid-rich fruits and vegetables for 4 weeks resulted in the reduction of hs-CRP as compared to eating 2 portions per day.
Fish intakes were inversely associated with the diet inflammatory index. This result is identical to those of Labonte et al. which showed that erythrocyte concentrations of docosapentaenoic acid (DPAn-3) were inversely associated with hs-CRP and inflammatory score. This result implies that high concentrations of DPAn-3 are associated with a lower risk of systemic inflammation in the population [41] .
Intake of sweetened beverages was positively associated with the diet inflammatory index. In fact, it has been shown that the consumption of sugary drinks (with added sugar, including among others soft drinks with or without caffeine, fruit drinks and lemonade) was positively associated with the concentrations of hs-CRP, interleukin-6 and tumor necrosis factors type 1 and 2 receptors in participants of the Health Professionals Follow-Up Study [42] . Studies carried out on patients suffering from coronary artery disease, and randomized nutritional intervention, crossover, carried out on 29 healthy men, established that consumption of 600 ml per day of sugary drinks containing different amounts (40 or 80 g) of fruits, glucose or sugar during 3 weeks increased by 60% to 109% the concentrations of CRP as compared to initial values at the beginning of this study [43] [44] .
The 24-hour recall data is memory-based; therefore, it is likely to be influenced through a memory lapse. However, the use of the five-step transition techniques minimizes the magnitude of this bias.
5. Conclusion
The study shows that more than one pregnant woman out of ten had a pro-inflammatory diet. Intakes of certain foods and nutrients were associated with the diet inflammatory index. The reduction of the inflammatory potential of the diet of pregnant women could be beneficial. This implies promoting the consumption of potentially anti-inflammatory foods and reduction of consumption of identified pro-inflammatory foods.
Acknowledgements
The authors would like to express their heartfelt thanks to the staff of the Ouidah health zone, the teams of the Regional Institute of Public Health.