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Does dietary total antioxidant capacity relate to oxidative stress levels in water immersion during labor? A case-control study

SUMMARY

OBJECTIVE:

The aim of this study was to investigate the effect of water immersion during the first stage of labor on maternal and neonatal oxidative stress and the association between serum and dietary total antioxidant capacity.

METHODS:

Women were divided into two groups: those immersed in water during the first stage of labor (n=30) and those who had conventional birth (n=33). Total oxidative stress and total antioxidant status levels were examined in antepartum and postpartum maternal serum and neonatal cord blood samples. Dietary total antioxidant capacity was determined by the food frequency questionnaire.

RESULTS:

Vitamin C and dietary total antioxidant capacity consumption were found to be higher in the water immersion group (106.92 mg/day and 18.94 mmol/gün, respectively) than the conventional birth group (92.69 mg/day and 15.99 mmol/gün, respectively) (p<0.05). Women immersed in water during the first stage of labor had lower total oxidative stress levels in antepartum and postpartum maternal serum and neonatal cord blood samples than those who had conventional birth (5.43±2.42 mmol/L and 5.59±3.35 mmol/L vs. 8.58±5.53 mmol/L and 12.68±16.58 mmol/L; p<0.05). Dietary total antioxidant capacity was found to be negatively correlated with total oxidative stress levels in antepartum and postpartum maternal serum and neonatal cord blood samples (p=0.012, p=0.047, p=0.035, and p<0.05).

CONCLUSION:

Women immersed in water during the first stage of labor had lower total oxidative stress levels in their postnatal maternal serum and neonatal cord blood samples and dietary total antioxidant capacity was also a factor associated with low total oxidative stress levels.

KEYWORDS:
Labor; Antioxidant; Oxidative stress

INTRODUCTION

Pregnancy is a physiological process that increases tissue oxygen and metabolic demands. Increased oxygen demand leads to increased production of free oxygen radicals, leading to increased oxidative stress and lipid peroxidation in pregnant women compared to nonpregnant women11 Moore TA, Ahmad IM, Schmid KK, Berger AM, Ruiz RJ, Pickler RH, et al. Oxidative stress levels throughout pregnancy, at birth, and in the neonate. Biol Res Nurs. 2019;21(5):485-94. https://doi.org/10.1177/1099800419858670
https://doi.org/10.1177/1099800419858670...
. The balance between oxidative and antioxidant systems plays a role in maintaining normal metabolic processes and preventing negative outcomes22 Argüelles S, Machado MJ, Ayala A, Machado A, Hervías B. Correlation between circulating biomarkers of oxidative stress of maternal and umbilical cord blood at birth. Free Radic Res. 2006;40(6):565-70. https://doi.org/10.1080/10715760500519834
https://doi.org/10.1080/1071576050051983...
.

Water immersion during labor (WIDL) is a nonpharmacological conjugate of epidural analgesia. It is becoming a popular choice in contemporary obstetrics because it moves the birthing women from a passive role compliant of authority to an active participant in the whole event, giving a sense of achievement and satisfaction. Both the Royal College of Obstetricians and Gynecologists and the American College of Nurse–Midwives support water immersion in a healthy term "uncomplicated pregnancies"33 Vanderlaan J, Kamanga FC, Garcia LM. Challenges to interdisciplinary consensus for evidence-based practice with water immersion for labor and birth: a systematic review of scholarly references. Health Sci Rev. 2022;2:100013.. The 2018 Cochrane review states moderate- to low-quality evidence concerning water immersion during the first stage of labor on the mode of birth (spontaneous, instrumental and cesarean section) and no evidence for adverse neonatal outcomes44 Cluett ER, Burns E, Cuthbert A. Immersion in water during labour and birth. Cochrane Database Syst Rev. 2018;5(5):CD000111. https://doi.org/10.1002/14651858.CD000111.pub4
https://doi.org/10.1002/14651858.CD00011...
.

The literature has investigated immersion practices during labor in terms of their effects on labor pain, anxiety, duration of delivery, and the newborn55 Liu Y, Liu Y, Huang X, Du C, Peng J, Huang P, et al. A comparison of maternal and neonatal outcomes between water immersion during labor and conventional labor and delivery. BMC Pregnancy Childbirth. 2014;14:160. https://doi.org/10.1186/1471-2393-14-160
https://doi.org/10.1186/1471-2393-14-160...

6 Eberhard J, Stein S, Geissbuehler V. Experience of pain and analgesia with water and land births. J Psychosom Obstet Gynaecol. 2005;26(2):127-33. https://doi.org/10.1080/01443610400023080
https://doi.org/10.1080/0144361040002308...
-77 Lee SL, Liu CY, Lu YY, Gau ML. Efficacy of warm showers on labor pain and birth experiences during the first labor stage. J Obstet Gynecol Neonatal Nurs. 2013;42(1):19-28. https://doi.org/10.1111/j.1552-6909.2012.01424.x
https://doi.org/10.1111/j.1552-6909.2012...
. Also, studies have investigated the level of oxidative stress associated with immersion during labor and has been shown to be associated with lower oxidative stress levels. However, they have examined only postpartum values and attributed any differences in oxidative stress between groups to immersion during labor88 Sert UY, Ozel S, Neselioglu S, Erel O, Engin Ustun Y. Water ımmersion during the labour and effects on oxidative stress. Fetal Pediatr Pathol. 2020;39(3):185-93. https://doi.org/10.1080/15513815.2019.1651801
https://doi.org/10.1080/15513815.2019.16...
,99 Ibanoglu MC, Köse C, Yilmaz-Ergani S, Arslan B, Akpınar F, Engin-Ustun Y. A prospective study of myeloperoxidase levels in water immersion. Placenta. 2022;123:1-4. https://doi.org/10.1016/j.placenta.2022.04.005
https://doi.org/10.1016/j.placenta.2022....
.

The present study investigated antepartum, postpartum, and neonatal TOS and TAS and evaluated dietary TAC of maternal diet. We hypothesized that WIDL is associated with lower TOS levels than CB and dietary TAC is a contributing factor to this situation.

METHODS

Participants

The study included pregnant women who met the following inclusion criteria: 18–35 years of age; primigravid; term pregnancy (37–41 weeks); no abnormal laboratory findings; no comorbidities; nonsmokers; spontaneous onset of labor; and women with singleton pregnancies, with newborns in vertex presentations and an estimated fetal weight of 2500–4000 g. Pregnant women were excluded if they presented with a ruptured membrane, had a body mass index (BMI) of ≥30 kg/m2, or needed labor augmentation.

Sample size was calculated using Student's t-test with 0.80 power at a significant level of 0.05 as described by Sert et al.88 Sert UY, Ozel S, Neselioglu S, Erel O, Engin Ustun Y. Water ımmersion during the labour and effects on oxidative stress. Fetal Pediatr Pathol. 2020;39(3):185-93. https://doi.org/10.1080/15513815.2019.1651801
https://doi.org/10.1080/15513815.2019.16...
. The calculation showed that samples should comprise a minimum of 60 pregnant individuals (30 per group) and their newborns.

Pregnant women who met the inclusion criteria were randomly divided into two groups: those immersed in water during the first stage of labor (n=30) (WIDL) and those who were on land during all stages of labor (n=33) (CB).

Data collection

Maternal and neonatal demographic and obstetric data were extracted from medical records, and data related to mothers’ frequency of food intake in the antenatal period were collected via face-to-face interviews.

Water immersion conditions

Mothers in the WIDL group had their labors monitored in bathtubs, as described by Ibanoglu et al99 Ibanoglu MC, Köse C, Yilmaz-Ergani S, Arslan B, Akpınar F, Engin-Ustun Y. A prospective study of myeloperoxidase levels in water immersion. Placenta. 2022;123:1-4. https://doi.org/10.1016/j.placenta.2022.04.005
https://doi.org/10.1016/j.placenta.2022....
.

Biochemical analyses

Total oxidative stress and TAS levels were analyzed using a commercial enzyme-linked immunosorbent assay kit (Relassay, Turkey)1010 Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005;38(12):1103-11. https://doi.org/10.1016/j.clinbiochem.2005.08.008
https://doi.org/10.1016/j.clinbiochem.20...
,1111 Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem. 2004;37(4):277-85. https://doi.org/10.1016/j.clinbiochem.2003.11.015
https://doi.org/10.1016/j.clinbiochem.20...
. The oxidative stress index (OSI) was calculated as the ratio of the TOS level to the TAS level according to the following formula: TOS (μmol H2O2 equivalent/L)/TAS (μmol Trolox equivalent/L). The OSI is an objective indicator of the balance between TOS and TAS levels1212 Eren Y, Dirik E, Neşelioğlu S, Erel Ö. Oxidative stress and decreased thiol level in patients with migraine: cross-sectional study. Acta Neurol Belg. 2015;115(4):643-9. https://doi.org/10.1007/s13760-015-0427-y
https://doi.org/10.1007/s13760-015-0427-...
.

Dietary analyses

To determine the daily nutrient intake (energy, macronutrient, and micronutrient intake), a semiquantitative food frequency questionnaire (FFQ) was used and analyzed via the Bebis version 7.2 software (Ebispro, Stuttgart, Germany)1313 Bebis (Beslenme Bilgi Sistemi), Nutrition Database Software. Database: the German food code and nutrient data base (BLS II.3, 1999) with additions from USDA-sr and other sources. Istanbul; 2004.. The dietary TAC of the participants was calculated using the antioxidant food database created by Carlsen et al.1414 Carlsen MH, Halvorsen BL, Holte K, Bøhn SK, Dragland S, Sampson L, et al. The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr J. 2010;9:3. https://doi.org/10.1186/1475-2891-9-3
https://doi.org/10.1186/1475-2891-9-3...
based on the ferric-reducing antioxidant power assay.

Ethical approval

Approval from the ethics committee to conduct this study was obtained from the Clinical Research Ethics Committee of the Etlik Zubeyde Hanim Women's Health Training and Research Hospital (no. 2020/129, dated 09/09/2020). The study was conducted in accordance with the Declaration of Helsinki and followed the ethical standards of the country of origin.

Statistical analyses

Statistical analysis was performed using the Statistical Package for the Social Sciences (SPSS) version 22.0 for Mac (SPSS Inc., Chicago, IL), and the data distribution was evaluated using the Kolmogorov-Smirnov test and found to be nonnormally distributed. The Mann-Whitney U test and multiple linear regression analysis were used. The level of significance was set at p<0.05.

RESULTS

There was no difference between the groups in pregnant women's mean age; gestational week; body mass index (BMI); cervical dilatation at the time of admission; estimated fetal weight; duration of the first stage of labor; and newborns’ Apgar scores, birth weights, and neonatal intensive care status. The groups had similar sociodemographic and obstetric characteristics.

Women in the WIDL group had a higher intake of vitamin C (106.92±15.88 mg/day) and dietary TAC than women in the CB group (93.69±16.53 mg/day) (p<0.05) (Table 1).

Table 1
Daily energy and nutrient intake of the water immersion during labor and conventional birth groups.

Women who had CB had higher postpartum maternal serum TOS levels (8.58±5.53 μmol/L) and neonatal cord blood TOS levels (12.68±16.58 μmol/L) than those who were immersed in water during the first stage of labor (5.43±2.42 μmol/L, 5.59±3.35 μmol/L, and 0.02±0.01, respectively) (p<0.05) (Table 2).

Table 2
Biochemical findings in antepartum and postpartum maternal serum samples as well as neonatal cord blood samples.

In the WIDL group, dietary TAC was negatively correlated with antepartum (p=0.000) and postpartum (p=0.014) maternal serum and neonatal cord blood (p=0.001) TOS levels; morever, it was negatively correlated with antepartum (p=0.000) and postpartum (p=0.030) maternal serum OSI levels (p<0.05). Also, dietary TAC was positively correlated with antepartum (p=0.015) and neonatal cord blood (p=0.029) TAS levels (Table 3).

Table 3
Multiple linear regression analysis of the effect of dietary total antioxidant capacity on antepartum and postpartum maternal serum and neonatal cord blood samples of total oxidant status, total antioxidant status, and oxidative stress index levels based on birth status.

DISCUSSION

In the current study, we found that postpartum maternal serum and neonatal cord blood TOS levels were found to be lower in the WIDL group than the CB group, and dietary TAC was correlated with antepartum and postpartum maternal serum and neonatal cord blood TAS levels.

Few studies in the literature have investigated the association between immersion during labor and oxidative stress88 Sert UY, Ozel S, Neselioglu S, Erel O, Engin Ustun Y. Water ımmersion during the labour and effects on oxidative stress. Fetal Pediatr Pathol. 2020;39(3):185-93. https://doi.org/10.1080/15513815.2019.1651801
https://doi.org/10.1080/15513815.2019.16...
,99 Ibanoglu MC, Köse C, Yilmaz-Ergani S, Arslan B, Akpınar F, Engin-Ustun Y. A prospective study of myeloperoxidase levels in water immersion. Placenta. 2022;123:1-4. https://doi.org/10.1016/j.placenta.2022.04.005
https://doi.org/10.1016/j.placenta.2022....
,1515 Uzunlar Ö, Sert ÜY, Kadıoğlu N, Çandar T, Engin Üstün Y. The effects of water immersion and epidural analgesia on cellular immune response, neuroendocrine, and oxidative markers. Turk J Med Sci. 2021;51(3):1420-7. https://doi.org/10.3906/sag-2009-181
https://doi.org/10.3906/sag-2009-181...
. From these studies, Sert et al.88 Sert UY, Ozel S, Neselioglu S, Erel O, Engin Ustun Y. Water ımmersion during the labour and effects on oxidative stress. Fetal Pediatr Pathol. 2020;39(3):185-93. https://doi.org/10.1080/15513815.2019.1651801
https://doi.org/10.1080/15513815.2019.16...
investigated the serum levels of disulfide, disulfide/total thiol ratio, native thiol, total thiol, and albumin and Ischemia-modified albumin levels in neonatal cord blood. Ibanoglu et al.99 Ibanoglu MC, Köse C, Yilmaz-Ergani S, Arslan B, Akpınar F, Engin-Ustun Y. A prospective study of myeloperoxidase levels in water immersion. Placenta. 2022;123:1-4. https://doi.org/10.1016/j.placenta.2022.04.005
https://doi.org/10.1016/j.placenta.2022....
examined the association between WIDL and oxidative stress based on the myeloperoxidase levels in cord blood samples. Assessment of the level of oxidative stress, measuring different oxidant and antioxidant molecules separately, is not recommended because it may cause overlapping and imprecise values as well as high costs; instead, TOS and TAS are advised to be more reliable, sensitive, and stable measures1010 Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005;38(12):1103-11. https://doi.org/10.1016/j.clinbiochem.2005.08.008
https://doi.org/10.1016/j.clinbiochem.20...
,1111 Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem. 2004;37(4):277-85. https://doi.org/10.1016/j.clinbiochem.2003.11.015
https://doi.org/10.1016/j.clinbiochem.20...
. The method of measuring serum TAS and TOS levels in this study has high linearity, and the results are highly reproducible1111 Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem. 2004;37(4):277-85. https://doi.org/10.1016/j.clinbiochem.2003.11.015
https://doi.org/10.1016/j.clinbiochem.20...
. Also, Uzunlar et al.1515 Uzunlar Ö, Sert ÜY, Kadıoğlu N, Çandar T, Engin Üstün Y. The effects of water immersion and epidural analgesia on cellular immune response, neuroendocrine, and oxidative markers. Turk J Med Sci. 2021;51(3):1420-7. https://doi.org/10.3906/sag-2009-181
https://doi.org/10.3906/sag-2009-181...
used TAS and TOS levels as measures of oxidative and antioxidative stress in relation to immersion and examined these values only in cord blood samples postbirth; they attributed the difference in oxidative stress between the groups to immersion during labor. Our study, unlike the three studies mentioned above, determined antepartum serum TOS and TAS levels and found no difference between the groups. Thus, the present study clearly demonstrated that immersion was the only factor that resulted in low postpartum TOS levels in pregnant women of the WIDL group.

Diet has been the most important contributing factor for the regulation of oxidative stress levels1616 Gantenbein KV, Kanaka-Gantenbein C. Mediterranean diet as an antioxidant: the ımpact on metabolic health and overall wellbeing. Nutrients. 2021;13(6):1951. https://doi.org/10.3390/nu13061951
https://doi.org/10.3390/nu13061951...
. Maternal dietary TAC (17.32±4.71 mmol/day) of women included in this study was found to be higher than those reported in a study from Brazil that evaluated the dietary TAC of 733 pregnant women (4.3 mmol/day)1717 Sartorelli DS, Carvalho MR, Silva Santos I, Crivellenti LC, Souza JP, Franco LJ. Dietary total antioxidant capacity during pregnancy and birth outcomes. Eur J Nutr. 2021;60(1):357-67. https://doi.org/10.1007/s00394-020-02251-y
https://doi.org/10.1007/s00394-020-02251...
but were similar to those reported in another study from Spain (17 mmol/day)1818 Henríquez-Sánchez P, Sánchez-Villegas A, Ruano-Rodríguez C, Gea A, Lamuela-Raventós RM, Estruch R, et al. Dietary total antioxidant capacity and mortality in the PREDIMED study. Eur J Nutr. 2016;55(1):227-36. https://doi.org/10.1007/s00394-015-0840-2
https://doi.org/10.1007/s00394-015-0840-...
. The similarity of the data in the present study to that in the study conducted in Spain can be explained by the Mediterranean diet in both countries. The Mediterranean diet, owing to its abundance of fruits, vegetables, and oilseeds, is high in antioxidants1919 Barbouti A, Goulas V. Dietary antioxidants in the mediterranean diet. Antioxidants (Basel). 2021;10(8):1213. https://doi.org/10.3390/antiox10081213
https://doi.org/10.3390/antiox10081213...
.

It has been reported that dietary antioxidants, such as vitamin C, vitamin E, beta-carotene, and flavonoids, might reduce oxidative stress2020 Czlapka-Matyasik M, Gramza-Michalowska A. The total dietary antioxidant capacity, ıts seasonal variability, and dietary sources in cardiovascular patients. Antioxidants (Basel). 2023;28:12(2):292.. In our study results, vitamin C consumption was determined to be higher in the water immersion group than the CB group. This contributes to higher dietary TAC and lower TOS levels determined in the water immersion group.

Instead of analyzing each nutrient with antioxidant properties separately, we preferred to determine the dietary TAC, an indicator of the cumulative ability of diet antioxidants2020 Czlapka-Matyasik M, Gramza-Michalowska A. The total dietary antioxidant capacity, ıts seasonal variability, and dietary sources in cardiovascular patients. Antioxidants (Basel). 2023;28:12(2):292., effect on serum TOS and TAS levels. In addition, our study results showed that there was a relationship between dietary TAC and serum TOS and TAS levels in the WIDL group. In the CB group, a relationship (between dietary TAC and TOS levels) was shown only in the antepartum period. It is thought that this may be related to higher dietary TAC in the water immersion group. Consumption of the recommended amount for dietary TAC has not been reported, and our findings suggest that there may be a threshold for interaction with serum TAS and TOS levels.

CONCLUSION

This is the first study in which serum oxidative stress levels were determined in prenatal, postnatal, and neonatal cord blood, and their relationship with serum TAS and dietary TAC was evaluated in WIDL.

In this study and other studies, it has been shown that WIDL results in low serum TOS levels. However, in previous studies, dietary TAC, which highly affects serum TOS levels, has not been evaluated. According to our results, dietary TAC also contributes significantly to the provision of low TOS levels.

In conclusion, considering the relationship between dietary TAC and serum TOS levels, an increase in dietary antioxidant intake in the maternal diet can reduce both postpartum maternal serum and cord blood TOS levels.

  • Funding: none.

REFERENCES

  • 1
    Moore TA, Ahmad IM, Schmid KK, Berger AM, Ruiz RJ, Pickler RH, et al. Oxidative stress levels throughout pregnancy, at birth, and in the neonate. Biol Res Nurs. 2019;21(5):485-94. https://doi.org/10.1177/1099800419858670
    » https://doi.org/10.1177/1099800419858670
  • 2
    Argüelles S, Machado MJ, Ayala A, Machado A, Hervías B. Correlation between circulating biomarkers of oxidative stress of maternal and umbilical cord blood at birth. Free Radic Res. 2006;40(6):565-70. https://doi.org/10.1080/10715760500519834
    » https://doi.org/10.1080/10715760500519834
  • 3
    Vanderlaan J, Kamanga FC, Garcia LM. Challenges to interdisciplinary consensus for evidence-based practice with water immersion for labor and birth: a systematic review of scholarly references. Health Sci Rev. 2022;2:100013.
  • 4
    Cluett ER, Burns E, Cuthbert A. Immersion in water during labour and birth. Cochrane Database Syst Rev. 2018;5(5):CD000111. https://doi.org/10.1002/14651858.CD000111.pub4
    » https://doi.org/10.1002/14651858.CD000111.pub4
  • 5
    Liu Y, Liu Y, Huang X, Du C, Peng J, Huang P, et al. A comparison of maternal and neonatal outcomes between water immersion during labor and conventional labor and delivery. BMC Pregnancy Childbirth. 2014;14:160. https://doi.org/10.1186/1471-2393-14-160
    » https://doi.org/10.1186/1471-2393-14-160
  • 6
    Eberhard J, Stein S, Geissbuehler V. Experience of pain and analgesia with water and land births. J Psychosom Obstet Gynaecol. 2005;26(2):127-33. https://doi.org/10.1080/01443610400023080
    » https://doi.org/10.1080/01443610400023080
  • 7
    Lee SL, Liu CY, Lu YY, Gau ML. Efficacy of warm showers on labor pain and birth experiences during the first labor stage. J Obstet Gynecol Neonatal Nurs. 2013;42(1):19-28. https://doi.org/10.1111/j.1552-6909.2012.01424.x
    » https://doi.org/10.1111/j.1552-6909.2012.01424.x
  • 8
    Sert UY, Ozel S, Neselioglu S, Erel O, Engin Ustun Y. Water ımmersion during the labour and effects on oxidative stress. Fetal Pediatr Pathol. 2020;39(3):185-93. https://doi.org/10.1080/15513815.2019.1651801
    » https://doi.org/10.1080/15513815.2019.1651801
  • 9
    Ibanoglu MC, Köse C, Yilmaz-Ergani S, Arslan B, Akpınar F, Engin-Ustun Y. A prospective study of myeloperoxidase levels in water immersion. Placenta. 2022;123:1-4. https://doi.org/10.1016/j.placenta.2022.04.005
    » https://doi.org/10.1016/j.placenta.2022.04.005
  • 10
    Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005;38(12):1103-11. https://doi.org/10.1016/j.clinbiochem.2005.08.008
    » https://doi.org/10.1016/j.clinbiochem.2005.08.008
  • 11
    Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem. 2004;37(4):277-85. https://doi.org/10.1016/j.clinbiochem.2003.11.015
    » https://doi.org/10.1016/j.clinbiochem.2003.11.015
  • 12
    Eren Y, Dirik E, Neşelioğlu S, Erel Ö. Oxidative stress and decreased thiol level in patients with migraine: cross-sectional study. Acta Neurol Belg. 2015;115(4):643-9. https://doi.org/10.1007/s13760-015-0427-y
    » https://doi.org/10.1007/s13760-015-0427-y
  • 13
    Bebis (Beslenme Bilgi Sistemi), Nutrition Database Software. Database: the German food code and nutrient data base (BLS II.3, 1999) with additions from USDA-sr and other sources. Istanbul; 2004.
  • 14
    Carlsen MH, Halvorsen BL, Holte K, Bøhn SK, Dragland S, Sampson L, et al. The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr J. 2010;9:3. https://doi.org/10.1186/1475-2891-9-3
    » https://doi.org/10.1186/1475-2891-9-3
  • 15
    Uzunlar Ö, Sert ÜY, Kadıoğlu N, Çandar T, Engin Üstün Y. The effects of water immersion and epidural analgesia on cellular immune response, neuroendocrine, and oxidative markers. Turk J Med Sci. 2021;51(3):1420-7. https://doi.org/10.3906/sag-2009-181
    » https://doi.org/10.3906/sag-2009-181
  • 16
    Gantenbein KV, Kanaka-Gantenbein C. Mediterranean diet as an antioxidant: the ımpact on metabolic health and overall wellbeing. Nutrients. 2021;13(6):1951. https://doi.org/10.3390/nu13061951
    » https://doi.org/10.3390/nu13061951
  • 17
    Sartorelli DS, Carvalho MR, Silva Santos I, Crivellenti LC, Souza JP, Franco LJ. Dietary total antioxidant capacity during pregnancy and birth outcomes. Eur J Nutr. 2021;60(1):357-67. https://doi.org/10.1007/s00394-020-02251-y
    » https://doi.org/10.1007/s00394-020-02251-y
  • 18
    Henríquez-Sánchez P, Sánchez-Villegas A, Ruano-Rodríguez C, Gea A, Lamuela-Raventós RM, Estruch R, et al. Dietary total antioxidant capacity and mortality in the PREDIMED study. Eur J Nutr. 2016;55(1):227-36. https://doi.org/10.1007/s00394-015-0840-2
    » https://doi.org/10.1007/s00394-015-0840-2
  • 19
    Barbouti A, Goulas V. Dietary antioxidants in the mediterranean diet. Antioxidants (Basel). 2021;10(8):1213. https://doi.org/10.3390/antiox10081213
    » https://doi.org/10.3390/antiox10081213
  • 20
    Czlapka-Matyasik M, Gramza-Michalowska A. The total dietary antioxidant capacity, ıts seasonal variability, and dietary sources in cardiovascular patients. Antioxidants (Basel). 2023;28:12(2):292.

Publication Dates

  • Publication in this collection
    15 Mar 2024
  • Date of issue
    2024

History

  • Received
    01 Aug 2023
  • Accepted
    30 Aug 2023
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