Wed, Mar 19, 2025
[Archive]
Volume 10, Issue 1 (Feb 2025)
JNFS 2025, 10(1): 69-80 |
Back to browse issues page
Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
Taherkhani M, Montazerifar F, Hekmatdoost A, Rashidkhani B, Payandeh A, Karajibani M. Association between Dietary Total Antioxidant Capacity and Odds of Preeclampsia: A Case-control Study. JNFS 2025; 10 (1) :69-80
URL: http://jnfs.ssu.ac.ir/article-1-912-en.html
URL: http://jnfs.ssu.ac.ir/article-1-912-en.html
Mahshid Taherkhani 
, Farzaneh Montazerifar * , Azita Hekmatdoost , Bahram Rashidkhani , Abolfazl Payandeh , Mansour Karajibani
, Farzaneh Montazerifar * , Azita Hekmatdoost , Bahram Rashidkhani , Abolfazl Payandeh , Mansour Karajibani
Pregnancy Health Research Center, School of Medicine, Zahedan University of Medical Sciences, Zahedan, Iran
Keywords: Hypertension, Antioxidants, Oxidative stress, Preeclampsia, Oxygen radical absorbance capacity, Diet.
Full-Text [PDF 657 kb]
(142 Downloads)
| Abstract (HTML) (656 Views)
Introduction
Full-Text: (42 Views)
Association between Dietary Total Antioxidant Capacity and Odds of Preeclampsia: A Case-control Study
Mahshid Taherkhani; MSc1, Farzaneh Montazerifar; PhD *1, 2, Azita Hekmatdoost; MD, PhD3, Bahram Rashidkhani; MD, PhD4, Abolfazl Payandeh; PhD5 & Mansour Karajibani; PhD1, 6
Mahshid Taherkhani; MSc1, Farzaneh Montazerifar; PhD *1, 2, Azita Hekmatdoost; MD, PhD3, Bahram Rashidkhani; MD, PhD4, Abolfazl Payandeh; PhD5 & Mansour Karajibani; PhD1, 6
1 Department of Nutrition, School of Medicine, Zahedan University of Medical Sciences, Zahedan, Iran; 2 Pregnancy Health Research Center, School of Medicine, Zahedan University of Medical Sciences, Zahedan, Iran; 3 Department of Clinical Nutrition and Dietetics, Faculty of Nutrition and Food Technology, National Nutrition and Food Technology Research Institute, Shahid Beheshti University of Medical Sciences, Tehran, Iran; 4 Department of Community Nutrition, Faculty of Nutrition Sciences and Food Technology, National Nutrition and Food Technology Research Institute, Shahid Beheshti University of Medical Sciences, Tehran, Iran; 5 Department of Biostatistics and Epidemiology, School of Health, Genetics of Non-Communicable Disease Research Center, Zahedan University of Medical Sciences, Zahedan, Iran; 6 Health Promotion Research Center, School of Medicine, Zahedan University of Medical Sciences, Zahedan, Iran.
| ARTICLE INFO | ABSTRACT | |
| ORIGINAL ARTICLE | Background: Preeclampsia may cause maternal and child morbidity and mortality. Evidence suggests that oxidative stress may be involved in the development of preeclampsia; however, the role of dietary total antioxidant capacity (DTAC) on preeclampsia risk has not yet been elucidated. Thus, this study aims to assess the relationship between DTAC and odds of preeclampsia. Methods: This case-control study was conducted on 240 pregnant women (preeclampsia, n=60; controls, n=180) in Qazvin, Iran. Controls were 3:1 ratio matched with cases in terms of participants’ age and gestational age. Dietary intakes were assessed using a validated food frequency questionnaire evaluating the preceding year. DTAC was measured by two methods: ferric reducing antioxidant potential (FRAP) and oxygen radical absorbance capacity (ORAC). Multivariable logistic regression was employed to evaluate the association between preeclampsia and DTAC and also selected antioxidants. Results: After controlling for potential confounders, a significant inverse relationship was found between ORAC and preeclampsia; individuals in the highest tertile of ORAC were 67% less likely to have preeclampsia than those in the lowest tertile of ORAC (OR: 0.33; 95% CI: 0.11-0.97; P-trend<0.05). There was no significant relation between FRAP and preeclampsia. The risk of preeclampsia was 70% lower among subjects with the highest tertile of vitamin C intake compared to the lowest tertile of it. Conclusion: Pregnant women with the highest tertile of ORAC and vitamin C intake were at lower risk of preeclampsia. Therefore, prospective studies are needed to confirm the protective effects of dietary anti-oxidants on preeclampsia incidence. | |
| Article history: Received:20 Jun 2023 Revised: 25 Sep 2023 Accepted: 21 Oct 2023 |
||
| *Corresponding author: fmontazerifar@gmail.com Department of Nutrition, School of Medicine, Zahedan University of Medical Sciences, Zahedan, Iran. Postal code: 9816845827 Tel: +98 915 5416903 |
||
| Keywords: Hypertension; Antioxidants; Oxidative stress; Preeclampsia; Oxygen radical absorbance capacity; Diet. |
Introduction
Preeclampsia is a pregnancy complication, occurring after the 20th week of gestational age with increased blood pressure and proteinuria in women who previously had normal blood pressure (Ghulmiyyah and Sibai, 2012). Preeclampsia occurs in approximately 2% to 8% of pregnancies worldwide (Henderson et al., 2017). Prevalence is slightly higher in Iran, (about 4% to 10%) (Omani-Samani et al., 2019). Moreover, this disorder is one of the main reasons of maternal, fetal, and neonatal mortality and morbidity (Henderson et al., 2017).
Recent studies indicated an opposite association between Dietary Total Antioxidant Capacity (DTAC) and the odds of chronic diseases like type 2 diabetes (Mancini et al., 2018), breast cancer (Pantavos et al., 2015), gestational diabetes mellitus (Daneshzad et al., 2020), and fatty liver (Salavatizadeh et al., 2022).
Some studies showed maternal diet plays a significant role in incidence of preeclampsia (Cao et al., 2020, Grum et al., 2018). Moreover, according to previous studies, supplementation with folic acid (Wang et al., 2015), vitamins E, and C reduce incidence of preeclampsia (Lorzadeh et al., 2020). Other studies demonstrated that lower intake of vitamins E and C, fruits, fiber, carotenoids, and excessive intake of carbohydrates, fat, saturated fat, sodium, and calories may be associated with high risk of preeclampsia (Kang et al., 2022, Saputra et al., 2017, Yusuf et al., 2019). However, evidence is varied and inconsistent in this respect (Christiansen et al., 2022, Eshriqui et al., 2016, Kalpdev et al., 2011).
We consume different groups of food in our diet containing numerous nutrients and antioxidants that may have cumulative or synergic effects on each other (Mancini et al., 2018). Investigation of them individually may be misleading (Liu et al., 2022). Studies indicated that DTAC, as a summary of dietary anti-oxidants intake, is an effective tool for assessing odds of chronic diseases (Nascimento-Souza et al., 2018). This indicator represents the capacity of food antioxidants to neutralize free radicals (Mancini et al., 2018).
Pro-inflammatory diets corresponded to high inflammatory biomarkers that play critical role in incidence of preeclampsia (Liu et al., 2022). Evidence demonstrated that primary reduction of antioxidants and increases in oxidative stress products may induce a situation that plays an important role in pathogenesis of this disorder (Taravati and Tohidi, 2018). Unusually, high levels of free radicals and also a decline in enzymatic and non-enzymatic antioxidant defense can lead to damage of cellular organelles and enzymes, and an increase in lipid peroxidation products can promote endothelial cell dysfunction (Shehu et al., 2020, Taravati and Tohidi, 2018). Furthermore, some previous studies suggested adequate antioxidant intake may reduce the odds of preeclampsia by neutralizing free radicals and protecting endothelial cells from oxidative stress damage (Aminuddin et al., 2021, Lorzadeh et al., 2020).
According to the researchers’ knowledge, only one study analyzed the relationship between DTAC and preeclampsia (Sheikhi et al., 2017), while no study investigated this relationship using the Ferric Reducing Antioxidant Potential (FRAP) method. The Iranian traditional dietary pattern has specific features such as large size of food portion containing refined carbohydrates. Thus, examining the relationship between DTAC and the odds of preeclampsia in the Middle Eastern countries with their specific dietary patterns might add further information to the researchers’ knowledge. Therefore, the association between DTAC and preeclampsia was investigated by using the two most common methods (Oxygen Radical Absorbance Capacity (ORAC) and FRAP).
Materials and Methods
Study design and sample
This case-control study was conducted in two referral hospitals in Qazvin, Iran. Participants were selected from pregnant women whose gestational age was more than 20 weeks (Magee et al., 2022, Mol et al., 2016) by convenience sampling method between January and September 2021. A total of 240 pregnant women were examined and who had high blood pressure before pregnancy, incomplete Food Frequency Questionnaire (FFQ), and energy intake more than mean±3 standard deviation (SD) were excluded. Eventually, 218 participants remained (57 cases, 161 controls); the case-to-control ratio of 1:3 was considered.
Cases were chosen from pregnant women with blood pressure greater than 140/90 mmHg and presence of protein in urine (Mol et al., 2016). Controls were selected from outpatients or those who were referred for delivery. Furthermore, all controls were matched to cases in terms of age and gestational age at the same time to avoid bias.
Dietary assessment
The authors employed a semi-quantitative, valid, and reliable FFQ with 168 food items in an in-person interview to assess individuals' dietary consumption over the previous year (Mirmiran et al., 2010). An expert interviewer completed all questionnaires and asked participants about food items consumption frequency (daily, weekly or monthly). Participants who could not declare their dietary consumption based on standard serving size were asked based on their own portion size, and then, a dietitian converted these data to grams per day. The authors computed energy and nutrient composition of foods with the United States Department of Agriculture (USDA) food composition database. For some Iranian food items like traditional bread that did not exist in USDA database, the Iranian Food Composition Table (FCT) was used.
DTAC calculation
Two methods for DTAC measurement was used. FRAP estimates the capacity of dietary antioxidants to reduce ferric to ferrous ions (Carlsen et al., 2010), and ORAC evaluates inhibitory effect of dietary antioxidants on peroxy-radical-induced oxidation (Haytowitz and Bhagwat, 2010). The daily intake of each food item was multiplied by its related corresponding value, and then was used to calculate overall DTAC. The supplements in the DTAC calculation were not considered because the researchers did not access detailed data about them (frequency and dosage of supplements were not evaluated, and supplements that were used sporadically were not considered).
Assessment of other variables
Required data including age, gestational age, pre-pregnancy weight, gravidity, primiparous, abortion, pregnancy interval, oral contraceptive use, smoking, education, occupation, previous preeclampsia history, and family history of preeclampsia were gathered by structured questionnaire in a face-to-face interview. Additionally, participants were asked about dietary supplements (yes/no) commonly used in pregnancy and before pregnancy including folate, iron, multivitamins plus minerals, and vitamin D.
Anthropometric measures like weight and height were measured with accuracy of 0.1 kg and 0.1 cm, respectively. pre-pregnancy Body Mass Index (BMI) was calculated by dividing pre-pregnancy weight (kg) by square of height (m2), and gestational weight gain by the difference between current and pre-pregnancy weight. Measuring tape was placed between acromial process and olecranon in non-dominant hand for measurement of middle upper arm circumference with an accuracy of 0.1 cm. The hand flexed 90° from the elbow.
The authors used a reliable and valid questionnaire for estimation of physical activity levels (Klishadi et al., 2001). This questionnaire consisted of different physical activity levels, from resting or sleeping (Metabolic Equivalent (Mets)= 0.9) to heavy activities (Mets > 6). All participants were asked about the duration of all these activities in a day. These numbers were multiplied by the related Met coefficient. Finally, all numbers were added to calculate physical activity level (Met-h/day).
Ethical considerations
The study was conducted according to Helsinki declaration. The Ethics Committee of the Zahedan University of Medical Sciences authorized protocols of this study. (Approval ID: IR.ZAUMS.REC.1399.
438) All participants signed written knowledgeable consent.
Data analysis
Characteristics of participants were summarized using descriptive statistics. Kolmogorov-Smirnov test was employed for assessment of normal distribution of continuous variables. Student's t-test and Mann–Whitney U test were used for comparing two groups in continuous variables with normal and non-normal distribution, respectively. For comparing more than two groups, the authors employed Analysis of Variance (ANOVA) for continuous variables and Kruskal-Wallis test for non-normal continuous variables. Then, Chi-square test and Fisher exact test were employed to assess categorical variables. Finally, binary logistic regression was used to estimate odds ratio (OR) and 95% confidence interval (CI) in different models that adjusted for multiple covariates. P-values less than 0.05 were considered significant. Additionally, all tests were two sides. IBM SPSS statistical package (version 21) was employed for all analyses.
Results
General characteristics and dietary intake of participants are summarized in Table 1. Cases had higher pre-pregnancy weight, pre-pregnancy BMI, mid-upper arm circumference (MUAC), pregnancy interval, and previous preeclampsia history (P<0.05). In assessment of dietary intake between cases and controls, controls reported higher intake of fruits and nuts. Moreover, caffeine intake was lower in control group (P<0.05). ORAC and FRAP scores did not indicate significant differences between cases and controls (P>0.05). Additionally, not significant difference was found between cases and controls regarding the use of supplements (data not shown).
Table 2 presents general characteristics of study participants across tertiles of DTAC. There were significantly more primiparous individuals in the lowest tertile of FRAP compared to the highest tertile of it. Additionally, individuals in the highest tertile of ORAC had lower percentage of family history of preeclampsia (P<0.05) in comparison to the lowest tertile of it.
Table 3 indicated dietary intake of study participants across tertiles of DTAC. Pregnant women in the highest tertile of FRAP had significantly higher intakes of whole grains, fruits, nuts, energy, carbohydrate, protein, total fat, polyunsaturated fatty acid, vitamin C, caffeine, and fiber compared with individuals in the lowest tertile of it. Subjects in the top tertile of ORAC had higher consumption of whole grains, vegetables, fruits, dairy products, legumes, nuts, energy, carbohydrate, protein, total fat, polyunsaturated fatty acids, vitamin C, sodium, caffeine, and fiber (P<0.05) compared to the lowest tertile of it.
ORs and 95% CIs for the risk of developing preeclampsia across tertiles of DTAC are reported in Table 4. Results from modeling of FRAP did not show any significant relationship among cases and controls. A significant inverse association was found between ORAC and risk of preeclampsia; individuals in the highest ORAC tertile were 0.77 times less likely to have preeclampsia compared with those in the lowest tertile after controlling for potential confounders (ORT3–T1=0.33, 95% CI:0.11–0.97; P=0.04). The contribution of food groups in the FRAP score was as follows: tea (41%), fruit (26%), and vegetable (10%). While for ORAC scores, the most alteration was explained by consumption of fruits (49%), vegetables (22%), and tea (8%) (data not shown).
Recent studies indicated an opposite association between Dietary Total Antioxidant Capacity (DTAC) and the odds of chronic diseases like type 2 diabetes (Mancini et al., 2018), breast cancer (Pantavos et al., 2015), gestational diabetes mellitus (Daneshzad et al., 2020), and fatty liver (Salavatizadeh et al., 2022).
Some studies showed maternal diet plays a significant role in incidence of preeclampsia (Cao et al., 2020, Grum et al., 2018). Moreover, according to previous studies, supplementation with folic acid (Wang et al., 2015), vitamins E, and C reduce incidence of preeclampsia (Lorzadeh et al., 2020). Other studies demonstrated that lower intake of vitamins E and C, fruits, fiber, carotenoids, and excessive intake of carbohydrates, fat, saturated fat, sodium, and calories may be associated with high risk of preeclampsia (Kang et al., 2022, Saputra et al., 2017, Yusuf et al., 2019). However, evidence is varied and inconsistent in this respect (Christiansen et al., 2022, Eshriqui et al., 2016, Kalpdev et al., 2011).
We consume different groups of food in our diet containing numerous nutrients and antioxidants that may have cumulative or synergic effects on each other (Mancini et al., 2018). Investigation of them individually may be misleading (Liu et al., 2022). Studies indicated that DTAC, as a summary of dietary anti-oxidants intake, is an effective tool for assessing odds of chronic diseases (Nascimento-Souza et al., 2018). This indicator represents the capacity of food antioxidants to neutralize free radicals (Mancini et al., 2018).
Pro-inflammatory diets corresponded to high inflammatory biomarkers that play critical role in incidence of preeclampsia (Liu et al., 2022). Evidence demonstrated that primary reduction of antioxidants and increases in oxidative stress products may induce a situation that plays an important role in pathogenesis of this disorder (Taravati and Tohidi, 2018). Unusually, high levels of free radicals and also a decline in enzymatic and non-enzymatic antioxidant defense can lead to damage of cellular organelles and enzymes, and an increase in lipid peroxidation products can promote endothelial cell dysfunction (Shehu et al., 2020, Taravati and Tohidi, 2018). Furthermore, some previous studies suggested adequate antioxidant intake may reduce the odds of preeclampsia by neutralizing free radicals and protecting endothelial cells from oxidative stress damage (Aminuddin et al., 2021, Lorzadeh et al., 2020).
According to the researchers’ knowledge, only one study analyzed the relationship between DTAC and preeclampsia (Sheikhi et al., 2017), while no study investigated this relationship using the Ferric Reducing Antioxidant Potential (FRAP) method. The Iranian traditional dietary pattern has specific features such as large size of food portion containing refined carbohydrates. Thus, examining the relationship between DTAC and the odds of preeclampsia in the Middle Eastern countries with their specific dietary patterns might add further information to the researchers’ knowledge. Therefore, the association between DTAC and preeclampsia was investigated by using the two most common methods (Oxygen Radical Absorbance Capacity (ORAC) and FRAP).
Materials and Methods
Study design and sample
This case-control study was conducted in two referral hospitals in Qazvin, Iran. Participants were selected from pregnant women whose gestational age was more than 20 weeks (Magee et al., 2022, Mol et al., 2016) by convenience sampling method between January and September 2021. A total of 240 pregnant women were examined and who had high blood pressure before pregnancy, incomplete Food Frequency Questionnaire (FFQ), and energy intake more than mean±3 standard deviation (SD) were excluded. Eventually, 218 participants remained (57 cases, 161 controls); the case-to-control ratio of 1:3 was considered.
Cases were chosen from pregnant women with blood pressure greater than 140/90 mmHg and presence of protein in urine (Mol et al., 2016). Controls were selected from outpatients or those who were referred for delivery. Furthermore, all controls were matched to cases in terms of age and gestational age at the same time to avoid bias.
Dietary assessment
The authors employed a semi-quantitative, valid, and reliable FFQ with 168 food items in an in-person interview to assess individuals' dietary consumption over the previous year (Mirmiran et al., 2010). An expert interviewer completed all questionnaires and asked participants about food items consumption frequency (daily, weekly or monthly). Participants who could not declare their dietary consumption based on standard serving size were asked based on their own portion size, and then, a dietitian converted these data to grams per day. The authors computed energy and nutrient composition of foods with the United States Department of Agriculture (USDA) food composition database. For some Iranian food items like traditional bread that did not exist in USDA database, the Iranian Food Composition Table (FCT) was used.
DTAC calculation
Two methods for DTAC measurement was used. FRAP estimates the capacity of dietary antioxidants to reduce ferric to ferrous ions (Carlsen et al., 2010), and ORAC evaluates inhibitory effect of dietary antioxidants on peroxy-radical-induced oxidation (Haytowitz and Bhagwat, 2010). The daily intake of each food item was multiplied by its related corresponding value, and then was used to calculate overall DTAC. The supplements in the DTAC calculation were not considered because the researchers did not access detailed data about them (frequency and dosage of supplements were not evaluated, and supplements that were used sporadically were not considered).
Assessment of other variables
Required data including age, gestational age, pre-pregnancy weight, gravidity, primiparous, abortion, pregnancy interval, oral contraceptive use, smoking, education, occupation, previous preeclampsia history, and family history of preeclampsia were gathered by structured questionnaire in a face-to-face interview. Additionally, participants were asked about dietary supplements (yes/no) commonly used in pregnancy and before pregnancy including folate, iron, multivitamins plus minerals, and vitamin D.
Anthropometric measures like weight and height were measured with accuracy of 0.1 kg and 0.1 cm, respectively. pre-pregnancy Body Mass Index (BMI) was calculated by dividing pre-pregnancy weight (kg) by square of height (m2), and gestational weight gain by the difference between current and pre-pregnancy weight. Measuring tape was placed between acromial process and olecranon in non-dominant hand for measurement of middle upper arm circumference with an accuracy of 0.1 cm. The hand flexed 90° from the elbow.
The authors used a reliable and valid questionnaire for estimation of physical activity levels (Klishadi et al., 2001). This questionnaire consisted of different physical activity levels, from resting or sleeping (Metabolic Equivalent (Mets)= 0.9) to heavy activities (Mets > 6). All participants were asked about the duration of all these activities in a day. These numbers were multiplied by the related Met coefficient. Finally, all numbers were added to calculate physical activity level (Met-h/day).
Ethical considerations
The study was conducted according to Helsinki declaration. The Ethics Committee of the Zahedan University of Medical Sciences authorized protocols of this study. (Approval ID: IR.ZAUMS.REC.1399.
438) All participants signed written knowledgeable consent.
Data analysis
Characteristics of participants were summarized using descriptive statistics. Kolmogorov-Smirnov test was employed for assessment of normal distribution of continuous variables. Student's t-test and Mann–Whitney U test were used for comparing two groups in continuous variables with normal and non-normal distribution, respectively. For comparing more than two groups, the authors employed Analysis of Variance (ANOVA) for continuous variables and Kruskal-Wallis test for non-normal continuous variables. Then, Chi-square test and Fisher exact test were employed to assess categorical variables. Finally, binary logistic regression was used to estimate odds ratio (OR) and 95% confidence interval (CI) in different models that adjusted for multiple covariates. P-values less than 0.05 were considered significant. Additionally, all tests were two sides. IBM SPSS statistical package (version 21) was employed for all analyses.
Results
General characteristics and dietary intake of participants are summarized in Table 1. Cases had higher pre-pregnancy weight, pre-pregnancy BMI, mid-upper arm circumference (MUAC), pregnancy interval, and previous preeclampsia history (P<0.05). In assessment of dietary intake between cases and controls, controls reported higher intake of fruits and nuts. Moreover, caffeine intake was lower in control group (P<0.05). ORAC and FRAP scores did not indicate significant differences between cases and controls (P>0.05). Additionally, not significant difference was found between cases and controls regarding the use of supplements (data not shown).
Table 2 presents general characteristics of study participants across tertiles of DTAC. There were significantly more primiparous individuals in the lowest tertile of FRAP compared to the highest tertile of it. Additionally, individuals in the highest tertile of ORAC had lower percentage of family history of preeclampsia (P<0.05) in comparison to the lowest tertile of it.
Table 3 indicated dietary intake of study participants across tertiles of DTAC. Pregnant women in the highest tertile of FRAP had significantly higher intakes of whole grains, fruits, nuts, energy, carbohydrate, protein, total fat, polyunsaturated fatty acid, vitamin C, caffeine, and fiber compared with individuals in the lowest tertile of it. Subjects in the top tertile of ORAC had higher consumption of whole grains, vegetables, fruits, dairy products, legumes, nuts, energy, carbohydrate, protein, total fat, polyunsaturated fatty acids, vitamin C, sodium, caffeine, and fiber (P<0.05) compared to the lowest tertile of it.
ORs and 95% CIs for the risk of developing preeclampsia across tertiles of DTAC are reported in Table 4. Results from modeling of FRAP did not show any significant relationship among cases and controls. A significant inverse association was found between ORAC and risk of preeclampsia; individuals in the highest ORAC tertile were 0.77 times less likely to have preeclampsia compared with those in the lowest tertile after controlling for potential confounders (ORT3–T1=0.33, 95% CI:0.11–0.97; P=0.04). The contribution of food groups in the FRAP score was as follows: tea (41%), fruit (26%), and vegetable (10%). While for ORAC scores, the most alteration was explained by consumption of fruits (49%), vegetables (22%), and tea (8%) (data not shown).
| Table 1. General characteristics and dietary intake of preeclampsia cases and controls. | |||
| Variables | Case (n=57) | Control (n=161) | P-valuea |
| Quantitative variables | Mean ± SD | Mean ± SD | |
| Age (y) | 29.93 ± 6.83 | 29.02 ± 6.52 | 0.37 |
| Pre-pregnancy weight (kg) | 71.74 ± 14.48 | 62.90 ± 10.79 | <0.001 |
| Gestational weight gain (kg) | 12.20 ± 5.98 | 10.89 ± 5.15 | 0.11 |
| Height (cm) | 161.82 ± 6.84 | 160.49 ± 6.09 | 0.17 |
| MUAC (cm) | 29.65 ± 3.70 | 27.62 ±3.03 | <0.001 |
| Pre-pregnancy body mass index (kg/m2) | 27.33 ± 4.84 | 24.44 ± 4.12 | <0.001 |
| Physical activity (Met.h/day) | 29.65 ± 3.35 | 29.48 ± 3.33 | 0.74 |
| DTAC by ORAC (mmol/day) | 14.08 ± 3.86 | 15.21 ± 4.45 | 0.09 |
| Energy (kcal/day) | 2512.17 ± 546.06 | 2536.23 ± 493.25 | 0.75 |
| Carbohydrate (% of energy) | 56.49 ± 5.42 | 57.62 ± 5.52 | 0.18 |
| Protein (% of energy) | 12.80 ± 1.79 | 12.78 ± 1.61 | 0.94 |
| Fat (% of energy) | 33.06 ± 5.89 | 31.90 ± 5.95 | 0.20 |
| Fiber (g/day) | 29.73 ± 9.39 | 29.73 ± 8.56 | 0.99 |
| Refine grains (g/day) | 367.38 ± 151.38 | 385.84 ± 124.77 | 0.36 |
| Fruits (g/day) | 304.03 ± 130.81 | 374.87 ± 143.56 | 0.001 |
| Legumes (g/day) | 36.99 ± 20.82 | 40.37 ± 25.77 | 0.37 |
Nuts (g/day): |
Median (IQR) 5.22 (13.27) |
Median (IQR) 10.58 (13.50) |
0.004 |
| Vegetables (g/day) | 315.81 (213.29) | 323.27 (237.32) | 0.81 |
| Red meat (g/day) | 13.19 (23.21) | 11.85 (19.54) | 0.37 |
| Caffeine (mg/day) | 89.06 (72.04) | 47.14 (66.0) | 0.01 |
| DTAC by FRAP (mmol/day) | 10.07 (3.88) | 9.24 (3.83) | 0.14 |
| Qualitative variables | n (%) | n (%) | |
| Primiparous (yes) | 16 (28.1) | 41 (25.5) | 0.70 |
| Abortion history (yes) | 12 (29.3) | 46 (38.3) | 0.29 |
| Pregnancy interval (y) ≤4 >4 |
12 (29.3) 29 (70.7) |
61 (50.8) 59 (49.2) |
0.01 |
| Oral contraceptive use (yes) | 11 (19.3) | 23 (14.3) | 0.37 |
| Smoking (present smoker) | 1 (1.8) | 1 (0.6) | 0.45 |
| Education level Secondary school and less High school University |
25 (43.9) 23 (40.4) 9 (15.8) |
75 (46.6) 66 (41.0) 20 (12.4) |
0.80 |
| Occupation (yes) | 3 (5.3) | 11 (6.8) | 1.00 |
| Previous preeclampsia historyb | 9 (22.0) | 10 (8.3) | 0.02 |
| Family history of preeclampsia | 11 (19.3) | 17 (10.6) | 0.09 |
| a: Student t-test or Mann–Whitney U test was used for quantitative variables; and Chi-square or fisher exact test was used for qualitative variables; b: Among the 161 (73.8%) women with a previous pregnancy; MUAC: Mid upper arm circumference; DTAC: Dietary total antioxidant capacity; ORAC: Oxygen radical absorbance capacity; IQR: interquartile range. | |||
| Table 2. General characteristics of participants across tertiles of dietary total antioxidant capasity. | ||||||||
| Variable | Tertiles of DTAC by FRAP | P-valuea | Tertiles of DTAC by ORAC | P-valuea | ||||
| I | II | II | I | II | II | |||
| <8.31 (n = 67) |
8.31-10.78 (n = 74) |
>10.78 (n = 77) |
<12.98 (n =79) |
12.98-16.76 (n=72) |
>16.76 (n=67) |
|||
| Age (y) | 28.15 ± 6.92b | 30.11 ± 6.64 | 29.42 ± 6.19 | 0.20 | 28.32 ± 6.54 | 29.72 ± 6.79 | 29.88 ± 6.41 | 0.27 |
| Gestational age (weeks) | 35.73 ± 4.19 | 36.04 ± 3.68 | 36.51 ± 3.24 | 0.54 | 36.11 ± 3.46 | 36.31 ± 3.77 | 35.90 ± 3.93 | 0.72 |
| Pre pregnancy weight (kg) | 64.66 ± 13.13 | 64.51 ± 12.71 | 66.37 ± 11.64 | 0.60 | 66.82 ± 13.31 | 64.56 ± 12.04 | 64.00 ± 11.81 | 0.34 |
| Pre pregnancy BMI (kg/m2) | 25.24 ± 4.75 | 25.21 ± 4.76 | 25.14 ± 4.02 | 0.99 | 25.81 ± 4.66 | 25.21 ± 4.53 | 24.46 ± 4.18 | 0.19 |
| Physical activity (Met-h/day) | 28.82 ± 2.73 | 29.63 ± 3.77 | 30.03 ± 3.28 | 0.08 | 29.79 ± 3.44 | 29.32 ± 3.37 | 29.41 ± 3.18 | 0.66 |
| Primiparous (yes) | 26 (38.8) | 16 (21.6) | 15 (19.5) | 0.01 | 23 (29.1) | 19 (26.4) | 15 (22.4) | 0.65 |
| Family history of preeclampsia (yes) |
11 (16.4)c |
7 (9.5) |
10 (13.0) |
0.46 |
16 (20.3) |
5 (6.9) |
7 (10.4) |
0.04 |
| Education level Secondary school and less High school University |
35 (52.2) 25 (37.3) 7 (10.4) |
29 (39.2) 36 (48.6) 9 (12.2) |
36 (46.8) 28 (36.4) 13 (16.9) |
0.37 | 39 (49.4) 29 (36.7) 11 (13.9) |
32 (44.4) 31 (43.1) 9 (12.5) |
29 (43.3) 29 (43.3) 9 (13.4) |
0.92 |
| a: ANOVA-test or Kruskal-Wallis test was used for quantitative variables; Chi-square test was used for qualitative variables; b: Mean±SD; c: n (%); DTAC: Dietary total antioxidant capacity; ORAC: Oxygen radical absorbance capacity; FRAP: Ferric reducing antioxidant potential; BMI: Body mass index. | ||||||||
| Table 3. Dietary intake of participants across tertiles of dietary total antioxidan capacity. | ||||||||
| Variable | Tertiles of DTAC by FRAP | P-valuea | Tertiles of DTAC by ORAC | P-valuea | ||||
| I | II | II | I | II | II | |||
| Whole grains (g/day) | 72.87 ± 92.04b | 112.91 ± 105.93 | 133.23 ± 122.24 | 0.001 | 81.15 ± 100.10 | 107.61 ± 102.87 | 139.38 ± 122.57 | <0.001 |
| Refined grains (g/day) | 379.48 ± 129.94 | 404.50 ± 138.43 | 359.77 ± 125.64 | 0.11 | 395.27 ± 129.40 | 387.23 ± 134.43 | 357.52 ± 131.63 | 0.20 |
| Vegetables (g/day) | 347.90 ± 162.44 | 352.70 ± 156.84 | 376.26 ± 195.91 | 0.74 | 293.47 ± 136.87 | 381.62 ± 185.34 | 413.74 ± 174.57 | <0.001 |
| Fruits (g/day) | 289.76 ± 100.34 | 362.86 ± 139.01 | 408.03 ± 157.53 | <0.001 | 252.22 ± 88.87 | 357.06 ± 98.27 | 478.36 ± 140.97 | <0.001 |
| Dairy products (g/day) | 328.49 ± 196.54 | 332.33 ± 183.46 | 354.56 ± 213.38 | 0.69 | 259.55 ± 179.40 | 352.64 ± 157.66 | 418.04 ± 223.27 | <0.001 |
| Red meat (g/day) | 17.42 ± 15.57 | 16.06 ± 13.37 | 17.48 ± 17.96 | 0.90 | 15.82 ± 15.01 | 14.52 ± 13.19 | 20.98 ± 18.30 | 0.08 |
| Legumes (g/day) | 34.49 ± 20.58 | 41.64 ± 22.03 | 41.76 ± 29.29 | 0.13 | 30.86 ± 19.42 | 39.52 ± 22.72 | 49.63 ± 28.11 | <0.001 |
| Nuts (g/day) | 9.65 ± 8.04 | 11.67 ± 12.24 | 15.72 ± 15.29 | 0.04 | 6.00 ± 6.45 | 11.44 ± 8.08 | 21.24 ± 16.49 | <0.001 |
| Energy (kcal) | 2254.22 ± 396.92 | 2542.05 ± 428.94 | 2758.20 ± 546.57 | <0.001 | 2231.88 ± 419.58 | 2524.77 ± 427.08 | 2886.93 ± 450.74 | <0.001 |
| Carbohydrate (g/day) | 316.92 ± 62.37 | 367.93 ± 70.25 | 395.48 ± 78.58 | <0.001 | 315.25 ± 64.35 | 362.66 ± 63.66 | 416.37 ± 70.69 | <0.001 |
| Protein (g/day) | 71.93 ± 15.25 | 82.10 ± 15.99 | 86.84 ± 19.92 | <0.001 | 69.82 ± 15.26 | 80.25 ± 14.67 | 93.84 ± 16.51 | <0.001 |
| Total fat (g/day) | 82.53 ± 23.45 | 88.79 ± 23.54 | 100.33 ± 28.27 | 0.001 | 81.12 ± 24.48 | 90.04 ± 24.74 | 103.50 ± 24.89 | <0.001 |
| Polyunsaturated fatty acid (g/day) |
21.58 ± 7.73 |
22.57 ± 7.94 |
24.99 ± 8.60 |
0.03 |
21.35 ± 7.96 |
23.22 ± 8.62 |
25.10 ± 7.68 |
0.01 |
| Vitamin E (mg/day) | 20.13 ± 10.00 | 19.55 ± 9.01 | 21.69 ± 10.53 | 0.51 | 18.82 ± 9.41 | 21.68 ± 10.51 | 21.16 ± 9.56 | 0.10 |
| Vitamin C (mg/day) | 117.80 ± 39.94 | 149.03 ± 50.40 | 161.29 ± 66.26 | <0.001 | 109.67 ± 37.58 | 141.02 ± 42.45 | 186.91 ± 60.32 | <0.001 |
| Sodium (mg/day) | 3747.58 ± 1225.95 | 3958.46 ± 1037.97 | 4191.57 ± 1524.35 | 0.07 | 3844.82 ± 1273.53 | 3862.17 ± 1377.84 | 4252.94 ± 1185.84 | 0.01 |
| Caffein (mg/day) | 33.82 ± 25.72 | 62.34 ± 28.53 | 135.64 ± 67.68 | <0.001 | 71.06 ± 48.60 | 68.18 ± 54.88 | 101.51 ± 78.83 | 0.01 |
| Fiber (g/day) | 24.99 ± 6.68 | 30.56 ± 7.67 | 33.05 ± 9.60 | <0.001 | 23.45 ± 5.61 | 29.84 ± 6.78 | 37.01 ± 8.05 | <0.001 |
| Partially hydrogenate vegetable oils (g/day) |
9.59 ± 14.39 |
9.82 ± 17.13 |
11.47 ± 18.61 |
0.78 |
13.14 ± 17.72 |
8.86 ± 16.50 |
8.60 ± 15.94 |
0.08 |
| a: ANOVA-test or Kruskal-Wallis test was used for quantitative variables; Chi-square test was used for qualitative variables; b: Mean±SD; DTAC: Dietary total antioxidant capacity; ORAC: Oxygen radical absorbance capacity; FRAP: Ferric reducing antioxidant potential. | ||||||||
| Table 4. Odds ratios and 95% confidence intervals for the association between dietary total antioxidant capacity and preeclampsia. | ||||||
| Variable | I | II | III | Ptrend | ||
| OR | 95% CI | OR | 95% CI | |||
| Tertiles of FRAP | ||||||
| Crude | Reference | 1.19 | 0.55-2.60 | 1.47 | 0.69-3.13 | 0.31 |
| Model 1 | Reference | 1.23 | 0.55-2.77 | 1.62 | 0.71-3.71 | 0.24 |
| Model 2 | Reference | 0.96 | 0.36-2.52 | 0.59 | 0.15-2.27 | 0.47 |
| Tertiles of ORAC | ||||||
| Crude | Reference | 0.67 | 0.33-1.38 | 0.49 | 0.22-1.05 | 0.06 |
| Model 1 | Reference | 0.58 | 0.27-1.24 | 0.36 | 0.14-0.92 | 0.03 |
| Model 2 | Reference | 0.74 | 0.31-1.75 | 0.33 | 0.11-0.97 | 0.05 |
| Model 1: Adjusted for age and energy; Model 2: Further adjusted for gestational age, pre-pregnancy body mass index, primiparous, gravidity, abortion history, pregnancy interval, education, previous preeclampsia history, family history of preeclampsia, caffeine, gestational weight gain, status of physical activity, Oral contraceptive; FRAP: Ferric reducing ability of plasma; ORAC: Oxygen radical absorbance capacity. | ||||||
Table 5 provides multivariable-adjusted odds ratios for the association between some dietary components and preeclampsia. The risk of preeclampsia was 70% lower among subjects in the highest tertile of vitamin C compared to the first tertile (ORT3–T1=0.30, 95% CI:0.11–0.79). Furthermore, participants with moderate intake of vitamin A and beta carotene (second tertile) had respectively 61% (OR=0.39, 95% CI:0.17–0.88) and 62% (OR=0.38, 95% CI:0.17–0.86) lower risk of preeclampsia (these relationships existed only in the first adjusted models) than those in the lowest tertile.
| Table 5. Odds ratios and 95% confidence intervals for the association between some dietary components and preeclampsia. | ||||
| Variable | Tertials of components of dietary | Ptrend | ||
| I | II | III | ||
| Vitamin A Model 1 Model 2 |
Reference Reference |
0.39 (0.17-0.88) 0.45 (0.18-1.13) |
0.46 (0.20-1.04) 0.60 (0.24-1.48) |
0.05 0.24 |
| Vitamin E Model 1 Model 2 |
Reference Reference |
1.11 (0.51-2.45) 1.38 (0.55-3.42) |
1.39 (0.63-3.11) 1.54 (0.60-3.90) |
0.40 0.36 |
| Vitamin C Model 1 Model 2 |
Reference Reference |
0.36 (0.16-0.79) 0.44 (0.17-1.08) |
0.33 (0.14-0.76) 0.30 (0.11-0.79) |
0.01 0.01 |
| Folate Model 1 Model 2 |
Reference Reference |
0.54 (0.23-1.25) 0.50 (0.19-1.31) |
0.51 (0.18-1.40) 0.42 (0.13-1.37) |
0.19 0.14 |
| Beta carotene Model 1 Model 2 |
Reference Reference |
0.38 (0.17-0.86) 0.42 (0.17-1.05) |
0.51 (0.23-1.10) 0.54 (0.22-1.30) |
0.07 0.14 |
| Selenium Model 1 Model 2 |
Reference Reference |
0.96 (0.40-2.27) 0.85 (0.32-2.28) |
1.27 (0.49-3.29) 1.40 (0.44-4.42) |
0.58 0.52 |
| Model 1: Adjusted for age and energy; Model 2: Further adjusted for gestational age, pre-pregnancy body mass index, primiparous, gravidity, abortion history, pregnancy interval, education, previous preeclampsia history, family history of preeclampsia, caffeine, gestational weight gain, status of physical activity, Oral contraceptive. | ||||
Discussion
The authors discovered a significant inverse association between ORAC and preeclampsia. Although this relationship was not significant regarding FRAP models, in analysis of dietary intake of single antioxidants, dietary intake of vitamin C was significantly associated with lower risk of preeclampsia. To the best of the authors’ knowledge, this study was among the first investigations in the world (Sheikhi et al., 2017).
Previous studies highlighted an inverse association between DTAC and metabolic syndrome, abdominal obesity, hypertension (Fateh et al., 2022, Villaverde et al., 2019), and type 2 diabetes in adults (Mancini et al., 2018). Furthermore, dietary intake of individual antioxidants such as vitamin C, E, folate, and carotenoids were assessed in association to preeclampsia (Kang et al., 2022, Saputra et al., 2017, Wang et al., 2015). As DTAC evaluates total dietary antioxidants from a wide range of food items, focusing on DTAC seems to be better than examining dietary antioxidants individually.
Some previous studies reported a beneficial effect of DTAC in association with non-alcoholic fatty liver disease (Sohouli et al., 2020), polycystic ovary syndrome (Shoaibinobarian et al., 2022), gestational diabetes mellitus (Daneshzad et al., 2020), and hypertension (Fateh et al., 2022, Villaverde et al., 2019); however, another study did not find any relationship between DTAC and pre-eclampsia (Sheikhi et al., 2017). These discrepant results might be explained by different methods for measurement of DTAC, failure to control the effect of potential confounders, different study designs, subjects' health status, different dietary habits and cooking types, and different tools for assessment of dietary intake (FFQ and 24-hour dietary intake record).
In this study, the authors estimated ORAC mainly attributed to fruits (49%), vegetables (22%), and tea (8%), while FRAP was mainly attributed to tea (41%), fruits (26%), and vegetables (10%). Thus, the reverse association of DTAC and preeclampsia could be due to its healthy food components. A meta-analysis reported that high adherence to healthy dietary patterns reduced the risk of preeclampsia; this dietary pattern consisted of the consumption of vegetables, fruits, fish, and whole grains and a low intake of meat, processed foods, and sugar-sweetened foods (Traore et al., 2021). On the other hand, following western dietary patterns was related to the odds of preeclampsia; and simple sugars, refined grains, and saturated fatty acids were the main components of this dietary pattern related to oxidative stress, insulin resistance, and metabolic syndrome (Abbasi et al., 2021). Moreover, a case-control study of pregnant women found that participants in the highest quartile of dietary approach to stop hypertension (DASH) had 47% less risk of preeclampsia compared with the lowest quartile (ORQ4–Q1=0.53, 95% CI: 0.36–0.78, P trend=0.001); whole grains, fruits, vegetables, legumes, nuts, and dairy products were the main components of DASH diet (Cao et al., 2020). A prospective cohort study conducted in Norway on 32933 nulliparous women demonstrated that added sugar and sugar-sweetened beverages contributed significantly to the risk of preeclampsia; on the contrary, intake of food items containing natural sugars like fresh and dried fruit decreased risk of preeclampsia (Borgen et al., 2012). In another study conducted in the USA on 1538 pregnant women, findings showed that dietary fiber intake reduced the probability of preeclampsia. Besides, their results indicated that dietary fiber reduced triglyceride concentration and increased high-density lipoprotein cholesterol concentration, which might lead to attenuation of dyslipidemia, an important clinical feature of preeclampsia (Qiu et al., 2008). Thus, it seems that healthy diets with similar compositions can prevent preeclampsia.
Oxidative stress and inflammatory situation are attributed to impaired placenta implantation that result in an imbalance between pro-inflammatory and regulatory cytokines. Consumption of fruits, vegetables, and food items with a low dietary inflammatory index (DII) were associated with lower levels of inflammatory biomarkers such as interleukin (IL)-2, IL-4, and transforming growth factor beta (TGF-β). Moreover, increased antioxidants concentration in serum and placenta can prevent hypoperfusion, and might have a protective effect against preeclampsia development (Liu et al., 2022). In this study, the dietary intake of fruits and nuts, as anti-inflammatory and anti-oxidant food items, were higher in controls compared to cases (P value < 0.05). Besides, subjects in the highest tertile of ORAC consumed more whole grains, vegetables, fruits, dairy products, legumes, and nuts compared to the lowest tertile.
Vitamin C, beta-carotene, and polyphenols are the most important items in calculation of DTAC. Their presence in foods as exogenous antioxidants can reduce free radical production (Liu et al., 2022). The results showed that participants in the highest tertile of vitamin C intake had 70% fewer odds of preeclampsia (ORT3–T1 = 0.30, 95% CI: 0.11–0.79, Ptrend= 0.01) in comparison to the lowest tertile of it. This finding was in line with previous studies, which reported the beneficial effects of healthy dietary patterns, containing main sources of vitamin C in reducing preeclampsia risk (Cao et al., 2020).
Like other studies, this study had its strengths and limitations. Some strengths of the present study were using a validated and reliable questionnaire that specified for the Iranian population the total antioxidant capacity of the whole diet instead of single antioxidants beside some single components, controlling for a wide range of confounders, and matching controls to cases for two potential confounders, age, and gestational age.
This study also has some limitations that must be considered. Case-control design is susceptible to selection bias. Hence, the results cannot be extrapolated to society. Additionally, the FFQ questionnaire was based on memory; consequently, recall bias and measurement error were inevitable. All methods that measure DTAC mainly present in vitro potential antioxidant activity of food items; the bioavailability of these antioxidants might be variable in vivo (Carlsen et al., 2010). Furthermore, the majority of these values are reported for raw items that might have various values compared with cooked items or in combination with other foods (Carlsen et al., 2010, Haytowitz and Bhagwat, 2010). The database for measurement of ORAC and FRAP was based on the previously published database, not on Iranian food items. For some food items with no specific score, the authors considered the mean of similar food items for computing total scores, which might affect the findings.
In FRAP method, DTAC might be underestimated compared to the actual value because this assay cannot measure some antioxidants such as glutathione and small molecular weight antioxidant (Carlsen et al., 2010). Although the authors assessed supplement intake, they did not find significant difference between the two groups. Finally, they could not evaluate any antioxidant or inflammatory biomarkers to strengthen our findings.
Conclusion
Data showed that pregnant women with the highest tertile of ORAC and vitamin C intake are at lower risk of preeclampsia. Prospective studies are needed to confirm the protective effects of dietary anti-oxidants on preeclampsia incidence.
Acknowledgments
The authors would like to appreciate mothers who participated in this study and also Zahedan University of Medical Sciences. This research was approved by the Vice-Chancellor for Research and Information Technology of Zahedan University of Medical Sciences, Zahedan, Iran (Code: 2984).
Authors' contributions
Drafting of the manuscript was done by M Taherkhani and F Montazerifar, study concept and design by M Taherkhani, F Montazerifar and A Hekmatdoost, statistical analysis by B Rashidkhani and A Payandeh, data collection by M Taherkhani, Interpretation of data by M Taherkhani, F Montazerifar and A Hekmatdoost, and critical revision of the manuscript by M Taherkhani, F Montazerifar, A Hekmatdoost and M Karajibani. All authors have read and approved this article.
Conflict of Interest
The authors declared no conflict of interests.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
References
Abbasi R, Bakhshimoghaddam F & Alizadeh M 2021. Major dietary patterns in relation to preeclampsia among Iranian pregnant women: a case–control study. Journal of maternal-fetal & neonatal medicine. 34 (21): 3529-3536.
Aminuddin NA, Sutan R & Mahdy ZA 2021. Role of Palm Oil Vitamin E in Preventing Pre-eclampsia: A Secondary Analysis of a Randomized Clinical Trial Following ISSHP Reclassification. Frontiers in medicine. 7: 596405.
Borgen I, et al. 2012. Maternal sugar consumption and risk of preeclampsia in nulliparous Norwegian women. European journal of clinical nutrition. 66 (8): 920-925.
Cao Y, et al. 2020. Adherence to a Dietary Approaches to Stop Hypertension (DASH)-style diet in relation to preeclampsia: a case-control study. Scientific reports. 10 (1): 1-7.
Carlsen MH, et al. 2010. The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutrition journal. 9 (1): 1-11.
Christiansen CH, et al. 2022. Multivitamin use and risk of preeclampsia: A systematic review and meta‐analysis. Acta Obstetricia et Gynecologica Scandinavica. 01 (10): 1038-1047.
Daneshzad E, Tehrani H, Bellissimo N & Azadbakht L 2020. Dietary total antioxidant capacity and gestational diabetes mellitus: a case-control study. Oxidative medicine and cellular longevity. 1: 5471316.
Eshriqui I, et al. 2016. Gestational dietary patterns are not associated with blood pressure changes during pregnancy and early postpartum in a Brazilian prospective cohort. European journal of nutrition. 55 (1): 21-32.
Fateh HL, et al. 2022. Association between dietary total antioxidant capacity and hypertension in Iranian Kurdish women. BMC Women's health. 22 (1): 1-7.
Ghulmiyyah L & Sibai B 2012. Maternal mortality from preeclampsia/eclampsia. In Seminars in perinatology, pp. 56-59. Elsevier.
Grum T, Hintsa S & Hagos G 2018. Dietary factors associated with preeclampsia or eclampsia among women in delivery care services in Addis Ababa, Ethiopia: a case control study. BMC research notes. 11 (1): 1-5.
Haytowitz DB & Bhagwat S 2010. USDA database for the oxygen radical absorbance capacity (ORAC) of selected foods, Release 2. US Department of agriculture. 3 (1): 10-48.
Henderson JT, Thompson JH, Burda BU & Cantor A 2017. Preeclampsia screening: evidence report and systematic review for the US Preventive Services Task Force. JAMA. 317 (16): 1668-1683.
Kalpdev A, Saha SC & Dhawan V 2011. Vitamin C and E supplementation does not reduce the risk of superimposed PE in pregnancy. Hypertension in pregnancy. 30 (4): 447-456.
Kang T, et al. 2022. Dietary carotenoid intake and risk of developing preeclampsia: a hospital-based case–control study. BMC Pregnancy and childbirth. 22 (1): 1-13.
Klishadi R, Khosravi A, Famouri F, Sadeghi M & Shirani S 2001. Assessment of physical activity of adolescents in Isfahan. Journal of Shahrekord University of Medical Sciences. 3 (2): 55-66.
Liu Y-h, et al. 2022. Dietary inflammatory index, inflammation biomarkers and preeclampsia risk: A hospital-based case-control study. British journal of nutrition. 129 (9): 1528-1536.
Lorzadeh N, Kazemirad Y & Kazemirad N 2020. Investigating the preventive effect of vitamins C and E on preeclampsia in nulliparous pregnant women. Journal of perinatal medicine. 48 (6): 625-629.
Magee LA, Nicolaides KH & von Dadelszen P 2022. Preeclampsia. New England journal of medicine. 386 (19): 1817-1832.
Mancini FR, et al. 2018. Dietary antioxidant capacity and risk of type 2 diabetes in the large prospective E3N-EPIC cohort. Diabetologia. 61 (2): 308-316.
Mirmiran P, Esfahani FH, Mehrabi Y, Hedayati M & Azizi F 2010. Reliability and relative validity of an FFQ for nutrients in the Tehran lipid and glucose study. Public health nutrition. 13 (5): 654-662.
Mol BW, et al. 2016. Pre-eclampsia. Lancet. 387 (10022): 999-1011.
Nascimento-Souza MA, Paiva PG, Martino HSD & Ribeiro AQ 2018. Dietary total antioxidant capacity as a tool in health outcomes in middle-aged and older adults: a systematic review. Critical reviews in food science and nutrition. 58 (6): 905-912.
Omani-Samani R, et al. 2019. Adverse maternal and neonatal outcomes in women with preeclampsia in Iran. Journal of maternal-fetal & neonatal medicine. 32 (2): 212-216.
Pantavos A, et al. 2015. Total dietary antioxidant capacity, individual antioxidant intake and breast cancer risk: the R otterdam study. International journal of cancer. 136 (9): 2178-2186.
Qiu C, Coughlin KB, Frederick IO, Sorensen TK & Williams MA 2008. Dietary fiber intake in early pregnancy and risk of subsequent preeclampsia. American journal of hypertension. 21 (8): 903-909.
Salavatizadeh M, et al. 2022. Dietary total antioxidant capacity is inversely associated with the odds of non-alcoholic fatty liver disease in people with type-2 diabetes. Frontiers in nutrition. 9: 1037851.
Saputra NPK, Lipoeto NI & Machmud R 2017. Analyses of nutrients and body mass index as risk factor for preeclampsia. Journal of obstetrics and gynecology of india. 67 (6): 409-413.
Shehu CE, et al. 2020. A Comparative Study of Oxidative Stress in Preeclampsia and Normal Pregnancy. International journal of gynecology & obstetrics. 3: 127-133.
Sheikhi M, Sharifi-Zahabi E & Paknahad Z 2017. Dietary antioxidant capacity and its association with preeclampsia. Clinical nutrition research. 6 (1): 47-54.
Shoaibinobarian N, et al. 2022. Dietary total antioxidant capacity and risk of polycystic ovary syndrome: a case-control study. International journal of fertility and sterility. 16 (3): 200-205.
Sohouli MH, Fatahi S, Sayyari A, Olang B & Shidfar F 2020. Associations between dietary total antioxidant capacity and odds of non-alcoholic fatty liver disease (NAFLD) in adults: a case–control study. Journal of nutritional science. 9: e48.
Taravati A & Tohidi F 2018. Comprehensive analysis of oxidative stress markers and antioxidants status in preeclampsia. Taiwanese journal of obstetrics and gynecology. 57 (6): 779-790.
Traore SS, et al. 2021. A meta-analysis of maternal dietary patterns and preeclampsia. Clinical nutrition open science. 40: 15-29.
Villaverde P, et al. 2019. High dietary total antioxidant capacity is associated with a reduced risk of hypertension in French women. Nutrition journal. 18 (1): 1-10.
Wang Y, et al. 2015. Folic acid supplementation and dietary folate intake, and risk of preeclampsia. European journal of clinical nutrition. 69 (10): 1145-1150.
Yusuf H, Subih HS, Obeidat BS & Sharkas G 2019. Associations of macro and micronutrients and antioxidants intakes with preeclampsia: A case-control study in Jordanian pregnant women. Nutrition, metabolism and cardiovascular diseases. 29 (5): 458-466.
The authors discovered a significant inverse association between ORAC and preeclampsia. Although this relationship was not significant regarding FRAP models, in analysis of dietary intake of single antioxidants, dietary intake of vitamin C was significantly associated with lower risk of preeclampsia. To the best of the authors’ knowledge, this study was among the first investigations in the world (Sheikhi et al., 2017).
Previous studies highlighted an inverse association between DTAC and metabolic syndrome, abdominal obesity, hypertension (Fateh et al., 2022, Villaverde et al., 2019), and type 2 diabetes in adults (Mancini et al., 2018). Furthermore, dietary intake of individual antioxidants such as vitamin C, E, folate, and carotenoids were assessed in association to preeclampsia (Kang et al., 2022, Saputra et al., 2017, Wang et al., 2015). As DTAC evaluates total dietary antioxidants from a wide range of food items, focusing on DTAC seems to be better than examining dietary antioxidants individually.
Some previous studies reported a beneficial effect of DTAC in association with non-alcoholic fatty liver disease (Sohouli et al., 2020), polycystic ovary syndrome (Shoaibinobarian et al., 2022), gestational diabetes mellitus (Daneshzad et al., 2020), and hypertension (Fateh et al., 2022, Villaverde et al., 2019); however, another study did not find any relationship between DTAC and pre-eclampsia (Sheikhi et al., 2017). These discrepant results might be explained by different methods for measurement of DTAC, failure to control the effect of potential confounders, different study designs, subjects' health status, different dietary habits and cooking types, and different tools for assessment of dietary intake (FFQ and 24-hour dietary intake record).
In this study, the authors estimated ORAC mainly attributed to fruits (49%), vegetables (22%), and tea (8%), while FRAP was mainly attributed to tea (41%), fruits (26%), and vegetables (10%). Thus, the reverse association of DTAC and preeclampsia could be due to its healthy food components. A meta-analysis reported that high adherence to healthy dietary patterns reduced the risk of preeclampsia; this dietary pattern consisted of the consumption of vegetables, fruits, fish, and whole grains and a low intake of meat, processed foods, and sugar-sweetened foods (Traore et al., 2021). On the other hand, following western dietary patterns was related to the odds of preeclampsia; and simple sugars, refined grains, and saturated fatty acids were the main components of this dietary pattern related to oxidative stress, insulin resistance, and metabolic syndrome (Abbasi et al., 2021). Moreover, a case-control study of pregnant women found that participants in the highest quartile of dietary approach to stop hypertension (DASH) had 47% less risk of preeclampsia compared with the lowest quartile (ORQ4–Q1=0.53, 95% CI: 0.36–0.78, P trend=0.001); whole grains, fruits, vegetables, legumes, nuts, and dairy products were the main components of DASH diet (Cao et al., 2020). A prospective cohort study conducted in Norway on 32933 nulliparous women demonstrated that added sugar and sugar-sweetened beverages contributed significantly to the risk of preeclampsia; on the contrary, intake of food items containing natural sugars like fresh and dried fruit decreased risk of preeclampsia (Borgen et al., 2012). In another study conducted in the USA on 1538 pregnant women, findings showed that dietary fiber intake reduced the probability of preeclampsia. Besides, their results indicated that dietary fiber reduced triglyceride concentration and increased high-density lipoprotein cholesterol concentration, which might lead to attenuation of dyslipidemia, an important clinical feature of preeclampsia (Qiu et al., 2008). Thus, it seems that healthy diets with similar compositions can prevent preeclampsia.
Oxidative stress and inflammatory situation are attributed to impaired placenta implantation that result in an imbalance between pro-inflammatory and regulatory cytokines. Consumption of fruits, vegetables, and food items with a low dietary inflammatory index (DII) were associated with lower levels of inflammatory biomarkers such as interleukin (IL)-2, IL-4, and transforming growth factor beta (TGF-β). Moreover, increased antioxidants concentration in serum and placenta can prevent hypoperfusion, and might have a protective effect against preeclampsia development (Liu et al., 2022). In this study, the dietary intake of fruits and nuts, as anti-inflammatory and anti-oxidant food items, were higher in controls compared to cases (P value < 0.05). Besides, subjects in the highest tertile of ORAC consumed more whole grains, vegetables, fruits, dairy products, legumes, and nuts compared to the lowest tertile.
Vitamin C, beta-carotene, and polyphenols are the most important items in calculation of DTAC. Their presence in foods as exogenous antioxidants can reduce free radical production (Liu et al., 2022). The results showed that participants in the highest tertile of vitamin C intake had 70% fewer odds of preeclampsia (ORT3–T1 = 0.30, 95% CI: 0.11–0.79, Ptrend= 0.01) in comparison to the lowest tertile of it. This finding was in line with previous studies, which reported the beneficial effects of healthy dietary patterns, containing main sources of vitamin C in reducing preeclampsia risk (Cao et al., 2020).
Like other studies, this study had its strengths and limitations. Some strengths of the present study were using a validated and reliable questionnaire that specified for the Iranian population the total antioxidant capacity of the whole diet instead of single antioxidants beside some single components, controlling for a wide range of confounders, and matching controls to cases for two potential confounders, age, and gestational age.
This study also has some limitations that must be considered. Case-control design is susceptible to selection bias. Hence, the results cannot be extrapolated to society. Additionally, the FFQ questionnaire was based on memory; consequently, recall bias and measurement error were inevitable. All methods that measure DTAC mainly present in vitro potential antioxidant activity of food items; the bioavailability of these antioxidants might be variable in vivo (Carlsen et al., 2010). Furthermore, the majority of these values are reported for raw items that might have various values compared with cooked items or in combination with other foods (Carlsen et al., 2010, Haytowitz and Bhagwat, 2010). The database for measurement of ORAC and FRAP was based on the previously published database, not on Iranian food items. For some food items with no specific score, the authors considered the mean of similar food items for computing total scores, which might affect the findings.
In FRAP method, DTAC might be underestimated compared to the actual value because this assay cannot measure some antioxidants such as glutathione and small molecular weight antioxidant (Carlsen et al., 2010). Although the authors assessed supplement intake, they did not find significant difference between the two groups. Finally, they could not evaluate any antioxidant or inflammatory biomarkers to strengthen our findings.
Conclusion
Data showed that pregnant women with the highest tertile of ORAC and vitamin C intake are at lower risk of preeclampsia. Prospective studies are needed to confirm the protective effects of dietary anti-oxidants on preeclampsia incidence.
Acknowledgments
The authors would like to appreciate mothers who participated in this study and also Zahedan University of Medical Sciences. This research was approved by the Vice-Chancellor for Research and Information Technology of Zahedan University of Medical Sciences, Zahedan, Iran (Code: 2984).
Authors' contributions
Drafting of the manuscript was done by M Taherkhani and F Montazerifar, study concept and design by M Taherkhani, F Montazerifar and A Hekmatdoost, statistical analysis by B Rashidkhani and A Payandeh, data collection by M Taherkhani, Interpretation of data by M Taherkhani, F Montazerifar and A Hekmatdoost, and critical revision of the manuscript by M Taherkhani, F Montazerifar, A Hekmatdoost and M Karajibani. All authors have read and approved this article.
Conflict of Interest
The authors declared no conflict of interests.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
References
Abbasi R, Bakhshimoghaddam F & Alizadeh M 2021. Major dietary patterns in relation to preeclampsia among Iranian pregnant women: a case–control study. Journal of maternal-fetal & neonatal medicine. 34 (21): 3529-3536.
Aminuddin NA, Sutan R & Mahdy ZA 2021. Role of Palm Oil Vitamin E in Preventing Pre-eclampsia: A Secondary Analysis of a Randomized Clinical Trial Following ISSHP Reclassification. Frontiers in medicine. 7: 596405.
Borgen I, et al. 2012. Maternal sugar consumption and risk of preeclampsia in nulliparous Norwegian women. European journal of clinical nutrition. 66 (8): 920-925.
Cao Y, et al. 2020. Adherence to a Dietary Approaches to Stop Hypertension (DASH)-style diet in relation to preeclampsia: a case-control study. Scientific reports. 10 (1): 1-7.
Carlsen MH, et al. 2010. The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutrition journal. 9 (1): 1-11.
Christiansen CH, et al. 2022. Multivitamin use and risk of preeclampsia: A systematic review and meta‐analysis. Acta Obstetricia et Gynecologica Scandinavica. 01 (10): 1038-1047.
Daneshzad E, Tehrani H, Bellissimo N & Azadbakht L 2020. Dietary total antioxidant capacity and gestational diabetes mellitus: a case-control study. Oxidative medicine and cellular longevity. 1: 5471316.
Eshriqui I, et al. 2016. Gestational dietary patterns are not associated with blood pressure changes during pregnancy and early postpartum in a Brazilian prospective cohort. European journal of nutrition. 55 (1): 21-32.
Fateh HL, et al. 2022. Association between dietary total antioxidant capacity and hypertension in Iranian Kurdish women. BMC Women's health. 22 (1): 1-7.
Ghulmiyyah L & Sibai B 2012. Maternal mortality from preeclampsia/eclampsia. In Seminars in perinatology, pp. 56-59. Elsevier.
Grum T, Hintsa S & Hagos G 2018. Dietary factors associated with preeclampsia or eclampsia among women in delivery care services in Addis Ababa, Ethiopia: a case control study. BMC research notes. 11 (1): 1-5.
Haytowitz DB & Bhagwat S 2010. USDA database for the oxygen radical absorbance capacity (ORAC) of selected foods, Release 2. US Department of agriculture. 3 (1): 10-48.
Henderson JT, Thompson JH, Burda BU & Cantor A 2017. Preeclampsia screening: evidence report and systematic review for the US Preventive Services Task Force. JAMA. 317 (16): 1668-1683.
Kalpdev A, Saha SC & Dhawan V 2011. Vitamin C and E supplementation does not reduce the risk of superimposed PE in pregnancy. Hypertension in pregnancy. 30 (4): 447-456.
Kang T, et al. 2022. Dietary carotenoid intake and risk of developing preeclampsia: a hospital-based case–control study. BMC Pregnancy and childbirth. 22 (1): 1-13.
Klishadi R, Khosravi A, Famouri F, Sadeghi M & Shirani S 2001. Assessment of physical activity of adolescents in Isfahan. Journal of Shahrekord University of Medical Sciences. 3 (2): 55-66.
Liu Y-h, et al. 2022. Dietary inflammatory index, inflammation biomarkers and preeclampsia risk: A hospital-based case-control study. British journal of nutrition. 129 (9): 1528-1536.
Lorzadeh N, Kazemirad Y & Kazemirad N 2020. Investigating the preventive effect of vitamins C and E on preeclampsia in nulliparous pregnant women. Journal of perinatal medicine. 48 (6): 625-629.
Magee LA, Nicolaides KH & von Dadelszen P 2022. Preeclampsia. New England journal of medicine. 386 (19): 1817-1832.
Mancini FR, et al. 2018. Dietary antioxidant capacity and risk of type 2 diabetes in the large prospective E3N-EPIC cohort. Diabetologia. 61 (2): 308-316.
Mirmiran P, Esfahani FH, Mehrabi Y, Hedayati M & Azizi F 2010. Reliability and relative validity of an FFQ for nutrients in the Tehran lipid and glucose study. Public health nutrition. 13 (5): 654-662.
Mol BW, et al. 2016. Pre-eclampsia. Lancet. 387 (10022): 999-1011.
Nascimento-Souza MA, Paiva PG, Martino HSD & Ribeiro AQ 2018. Dietary total antioxidant capacity as a tool in health outcomes in middle-aged and older adults: a systematic review. Critical reviews in food science and nutrition. 58 (6): 905-912.
Omani-Samani R, et al. 2019. Adverse maternal and neonatal outcomes in women with preeclampsia in Iran. Journal of maternal-fetal & neonatal medicine. 32 (2): 212-216.
Pantavos A, et al. 2015. Total dietary antioxidant capacity, individual antioxidant intake and breast cancer risk: the R otterdam study. International journal of cancer. 136 (9): 2178-2186.
Qiu C, Coughlin KB, Frederick IO, Sorensen TK & Williams MA 2008. Dietary fiber intake in early pregnancy and risk of subsequent preeclampsia. American journal of hypertension. 21 (8): 903-909.
Salavatizadeh M, et al. 2022. Dietary total antioxidant capacity is inversely associated with the odds of non-alcoholic fatty liver disease in people with type-2 diabetes. Frontiers in nutrition. 9: 1037851.
Saputra NPK, Lipoeto NI & Machmud R 2017. Analyses of nutrients and body mass index as risk factor for preeclampsia. Journal of obstetrics and gynecology of india. 67 (6): 409-413.
Shehu CE, et al. 2020. A Comparative Study of Oxidative Stress in Preeclampsia and Normal Pregnancy. International journal of gynecology & obstetrics. 3: 127-133.
Sheikhi M, Sharifi-Zahabi E & Paknahad Z 2017. Dietary antioxidant capacity and its association with preeclampsia. Clinical nutrition research. 6 (1): 47-54.
Shoaibinobarian N, et al. 2022. Dietary total antioxidant capacity and risk of polycystic ovary syndrome: a case-control study. International journal of fertility and sterility. 16 (3): 200-205.
Sohouli MH, Fatahi S, Sayyari A, Olang B & Shidfar F 2020. Associations between dietary total antioxidant capacity and odds of non-alcoholic fatty liver disease (NAFLD) in adults: a case–control study. Journal of nutritional science. 9: e48.
Taravati A & Tohidi F 2018. Comprehensive analysis of oxidative stress markers and antioxidants status in preeclampsia. Taiwanese journal of obstetrics and gynecology. 57 (6): 779-790.
Traore SS, et al. 2021. A meta-analysis of maternal dietary patterns and preeclampsia. Clinical nutrition open science. 40: 15-29.
Villaverde P, et al. 2019. High dietary total antioxidant capacity is associated with a reduced risk of hypertension in French women. Nutrition journal. 18 (1): 1-10.
Wang Y, et al. 2015. Folic acid supplementation and dietary folate intake, and risk of preeclampsia. European journal of clinical nutrition. 69 (10): 1145-1150.
Yusuf H, Subih HS, Obeidat BS & Sharkas G 2019. Associations of macro and micronutrients and antioxidants intakes with preeclampsia: A case-control study in Jordanian pregnant women. Nutrition, metabolism and cardiovascular diseases. 29 (5): 458-466.
Type of article: orginal article |
Subject:
public specific
Received: 2023/06/20 | Published: 2025/02/4 | ePublished: 2025/02/4
Received: 2023/06/20 | Published: 2025/02/4 | ePublished: 2025/02/4
Send email to the article author
| Rights and permissions | |
 |
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
