Effect of antenatal use of high energy nutritional supplements on cardio metabolic risk markers in underweight primi gravidas; a randomized controlled trial | BMC Pregnancy and Childbirth

BMC Pregnancy and Childbirth volume 24, Article number: 695 (2024) Cite this article

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Pregnancy is a state of increased metabolic demand, and poor maternal nutrition can exacerbate these changes, potentially increasing the risk of cardiometabolic disorders.This study is significant as it investigates the effect of high energy nutritional supplements on cardio metabolic risk markers in underweight primigravidas.

A single blinded randomized controlled trial was conducted from April 2018- August 2019 among the Pakistani tertiary care facilities of Khyber Pakhtunkhwa. A total of thirty six participants were randomized into two groups receiving either high energy nutritional supplement ‘MAAMTA’ or Placebo. They were instructed to take Placebo/Supplement alongside to their regular prenatal care and food from their first antenatal visit till a week postnatally. Anthropometric measurements and blood samples for biochemical parameters insulinlevels, fasting blood glucose & lipid profile were taken at baseline visit, between 16 and 20 weeks gestation and a post natal visit.

The two-way repeated measures ANOVA showed that there was a highly significant time effect on participant’s Insulin level (F (1.8, 53.6) = 10.64, P < 0 0.000, ηp2 = 0.269). A highly significant time effect on participant’s insulin resistance (F (2, 68) = 8.116,P < 0 0.001, ηp2 = 0.193) was also observed. There was a highly significant time effect on participant’s LDL level as well (F (2, 68) = 11.82, P < 0 0.000, ηp2 = 0.258).

Supplementation with high energy nutritional supplements may improve insulin levels and insulin sensitivity in underweight primigravidas.

https://www.ClinicalTrials.govClinicalTrials.gov Identifier: ISRCTN 10088578. Registered on 27 March 2018. https://www.isrctn.com/ISRCTN10088578.

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In low- and middle-income nations, malnutrition is extremely permeating and injurious condition. In these countries nutritional deficiencies in both the mother and the child is a growing problem, especially low body mass index (BMI) which is indicative of maternal under-nutrition [1].

The WHO reports that 155 million children under the age of five are stunted, 52 million are wasted, and 17 million are severely wasted. Additionally, 462 million adults are underweight [2].

Malnutrition a universal issue, is affecting each and every country of the world. Twenty million underweight infants are born each year, and one-third of women who are of reproductive age are anaemic [3].

Maternal malnutrition is a major issue in many nations. In many nations in South Asia and Sub-Saharan Africa, > 20% of women are under nourished having a BMI < 18.5 4. Up to 40% of women may be affected in certain of those nations. Over 10% of women in several South-Central Asian nations are shorter than 145 cm [5]. The burden of malnutrition also affects Pakistan’s adult population, with 52.1% of reproductive age women suffering from anaemia [6]. Of the 8,000 women of childbearing age (15–45 years old) who die each year, the majority of deaths about 20% are from pregnancy and childbirth-related problems [7].

Pregnant and lactating women require high quantity of nutrients [8]. Food-based treatments, such as nutritional counseling, food fortification, and bio fortification, have been used to reduce malnutrition in pregnant and lactating women [9]. Lipid based nutritional supplements (LNS) are a new way to boost the micronutrient and macronutrient content of home-cooked meals for pregnant and breastfeeding women and their children [10]. High energy supplements are products designed to provide a concentrated source of calories & nutrients, often used by individuals with high physical demands [11]. These supplements typically contain a mix of carbohydrates, fats and proteins along with vitamins & minerals to support energy production and overall health [12]. Common high energy supplements are energy bars, energy gels, carbohydrate drinks/powders, protein shakes with added carbohydrates and Nut butter & spreads [13]. MAAMTA used in this study is a peanut butter based paste, which can be consumed as such or as a spread. It is high in healthy fats & proteins with a moderate amount of carbohydrates. These are calorie dense and provide a moderate amount of sustained energy [14].

The alterations in lipid metabolism result in the build-up of fats, which operate as a store of calories for the foetus and the mother during every phase of pregnancy and lactation [15]. Triglycerides (TG) and cholesterol (TC) are also required for placental oxidation/membrane formation and placental steroid production [16]. Risk of preeclampsia is increased by metabolic syndrome (insulin resistance (IR), oxidative stress, central obesity, hyperglycemia, hypertension and dysregulation of lipoprotein lipase causing dyslipidemia, all of these inducing endothelial dysfunction [17].

As the high energy nutritional supplement given in this study was also LNS, so we wanted to see if it has any detrimental effect on the lipid profile and thus the cardio metabolic risk markers in underweight primigravidas.

Hypothesis; The use of high energy nutritional supplements by healthy underweight primigravida may affect their voluntary oral intake, lipid profile and insulin sensitivity.

Primary outcome: The primary outcomes of this study were Changes in Cardiometabolic Risk Markers: Measurement of specific markers such as blood glucose levels, lipid profiles (including LDL, HDL, triglycerides), blood pressure, secondly effect on insulin resistance which can occur in a pregnancy.

The Advanced Study and Research Board (ASRB) authorized (ASRB000669/EH/IBMS) and the Ethical Committee of Khyber Medical University approved this study under (DIR/KMU-EB/EH/000453) and permission was taken from the respective tertiary care hospitals. This trial is also registered in ISRCTN registry under (ISRCTN 10088578) dated 27/03/2018. Our study adheres to CONSORT guidelines. After obtaining the approval, recruitment was started from the province of Khyber Pakhtunkhwa tertiary care facilities and clinical trial room set up in those respective hospitals for the convenience of the participants. Simple random sampling was done and Open Epi software was used to calculate sample size. This sample size was calculated based on the difference in the main outcomes of this study (Insulin) from studies conducted by Stratton et al. 2008 and Fatima et al. 2015, considering 85% power and CI of 95%, 24 participants are required to conduct this study [18, 19]. Keeping in mind 20% dropout rate, Thirty six Primi underweight participants were selected from the OPDs of the concerned gynecology and obstetrics departments.

It was a single blinded randomized controlled trial in which participants are randomly assigned to either the intervention group (receiving the supplement) or the control group (receiving a placebo) using Computor randomizer(version3). Only the participants are unaware of which group they have been assigned to, while the researchers administering the treatment knew which participants are in the intervention or control groups.

Underweight primigravidas having a BMI < 18.5 kg/m2.

underweight primigravida having any major illness like hypertension, gestational diabetes mellitus, thyroid or liver disorders. Also those primigravidas already on long term supplementation or other medication or having allergy to supplements were excluded from this study.

The recruitment of the participants is shown in Fig. 1. The participants were informed about the objectives of this study and informed consent was asked for at the start of the study.Participant were requested to make three visits, one at baseline, second between 16 and 20 weeks gestation and a post natal visit. Nutritional counseling was given to the participants in addition to prenatal care.

recruitment of participants for this study

A high-energy nutritional supplement called “MAAMTA” with 400 kcal/75 gm of energy that was made with peanut butter was given to the HENS group, while the placebo consisted of 75 gm of wheat flakes, 40 ml of skimmed milk, and two tablets of artificial sweetener (Canderal). Per 75 grammes, it contains 137.8 calories (Fig. 2). The participants were asked not to discard the sachet s of their supplements/placebo, which were collected by the main researcher at the end of each week. Any leftovers in the sachet were measured and deducted from 75gms to make sure the exact amount taken by the participants.In addition to their regular diet and prenatal care, participants of both groups were instructed to take the HENS/placebo throughout the duration of their pregnancy as well as one week after giving birth.

For baseline visit the participants were invited to attend a trial in the trial room in a fasted state. After they were acclimatized to the environment, anthropometric measurements were taken and 5 ml blood was taken from them in a 5 ml BD syringe, then the plunger was removed (to avoid hemolysis) and 2 ml of this blood was put into an EDTA vacutainer TM tube, 2 ml in gel tube and 1 ml in an Eppendorf tube containing 200 µl of aprotonin (a bovine origin pancreatic inhibitor).The sample with EDTA and aprotonin were put in the refrigerator while the sample in gel tube was placed in a stand for serum to get separated. Afterwards were served with juice and light breakfast. They were given incentive of Rs.1000 and were also given nutritional counseling. The date for their next visit was calculated and written on their prescription from their antenatal visit. They were reminded of the second visit two days before the visit telephonically. The same procedure was repeated as on the first visit. Similarly, they were asked to make a post natal visit, after their condition was stabilized. Fasting blood samples and anthropometric measurements were taken.

The anthropometric measurements that were taken included, height using a seca Leicester 214 (portable standiometer) and weight, body fat, hydration and bone was calculated using bioelectrical impedance scale by (Beurer GmbH, Soflinger str.218 89077 Ulm, Germany Art._Nr.748.13, TypeBF220). The mid upper arm circumference (MUAC) was determined using a strip used was a validated World Food Programme strip. The same strip was used throughout the study.

Metabolic Syndrome Criteria (NCEP ATP III, IDF, WHO) [20] was used to assess cardiometabolic risk factors. Metabolic syndrome is a significant indicator of cardiometabolic risk. The criteria vary slightly between different guidelines, but typically include:

Waist circumference (Central Obesity)

NCEP ATP III: ≥102 cm (40 inches) for men, ≥ 88 cm (35 inches) for women.

IDF: ≥94 cm for men, ≥ 80 cm for women (values may differ by ethnicity).

Triglycerides

≥ 150 mg/dL (1.7 mmol/L) or on treatment for elevated triglycerides.

HDL cholesterol

< 40 mg/dL (1.03 mmol/L) for men, < 50 mg/dL (1.29 mmol/L) for women.

Blood pressure

≥ 130/85 mm Hg or on treatment for hypertension.

Fasting glucose

≥ 100 mg/dL (5.6 mmol/L) or on treatment for elevated glucose.

Having three or more of these factors typically indicates metabolic syndrome.

Biochemical parameters like Insulin was analysed by the electro chemi luminescent immunoassay “ECLIA"technique. Fasting blood glucose and lipid profile by enzymatic colorimetric method using cobas501 analyzer.

The HOMA model by Matthews et al.,1985 has shown to be a valid clinical and epidemiological technique for assessing insulin resistance. HOMA uses a basic nonlinear equations to describe glucose insulin homeostasis [21].

HOMAIR index is calculated according to the formula.

HOMAIR; fasting glucose in m mol/l × fasting insulin in mU/ml/22.5

Statistical analysis was performed using version 20 of IBM SPSS ®. Weight, height, age, and BMI were taken as mean ± standard deviation. Normality of the data was checked using Shapiro-Wilk test while the primary & secondary outcomes was analysed using repeated measure ANOVA. Mauchly sphericity test was employed for P value reporting, in case of sphericity was not significant then we used Greenhouse-Geisser test. Insulin resistance was calculated by HOMAR model.

Nutritional value of 75gms of MAAMTA and Placebo

Maternal 24 h. dietary intake was taken into account and as well as a whole day trial was conducted to see the effect of the supplement on daily intake, appetite and energy intake, which is already being published in JPMA [22].

A highly significant effect of time on participant’s BMI (F (2, 68) = 44.8, P < 0 0.01, ηp2 = 0.57) was calculated by two-way repeated measures ANOVA. Although no significant within group effect of supplementation on participant’s BMI (F (2, 68) = 0.45, P = 0 0.634, ηp2 = 0.013). Test of between subject effect of supplementation on BMI was only 3.9% (P = 0.25) and explained only 3.9% variation in BMI. Also a highly significant effect of time on participant’s weight (F (2, 68) = 36.32, P < 0 0.01, ηp2 = 0.51)was shown and a marginally significant within group effect of supplementation on participant’s weight (F (2, 68) = 3.180, P = 0 0.048, ηp2 = 0.086). Test of between subject effect of supplementation on weight was only 9.5% (P = 0.067) and explained only 9.5% variation in weight. A significant within group effect of supplementation on participant’s body mass (F (1.37, 46.7) = 3.63, P = 0.050, ηp2 = 0.096). A highly significant effect of time on participant’s MUAC (F (2, 68) = 9.70, P = 0 0.000, ηp2 = 0.222) was seen and no significant within group effect of supplementation on participant’s MUAC (F (2, 68) = 0.42, P = 0 0.65, ηp2 = 0.012) was seen, (Table 1).

A highly significant time effect on participant’s Insulin level (F (1.8,53.6) = 10.64, P = 0 0.000, ηp2 = 0.269) and no significant within group effect of supplementation on participant’s Insulin level (F (1.85,53.6) = 0.337, P = 0 0.112, ηp2 = 0.074) was seen by using the two-way repeated measure ANOVA. Test of between subject effect of supplementation on insulin was only 01% (P = 0.84) and explained that only 01% variation in Insulin level. There was a highly significant time effect on participant’s IR (F (2, 68) = 8.116, P = 0 0.001, ηp2 = 0.193) and a significant within group effect of supplementation on participant’s IR (F (2, 68) = 4.024, P = 0 0.022, ηp2 = 0.106) was seen. Test of between subject effect of supplementation on HOMAIR was only 1.5% (P = 0.484) and explained that only 1.5% variation in Insulin resistance level. There was a significant effect of time on participant’s fasting blood glucose level (F (1.7,58.1) = 5.730, P = 0 0.08, ηp2 = 0.144) and also a significant within group effect of supplementation on participant’s fasting blood glucose level (F (1.7,58.1) = 3.784, P = 0 0.035, ηp2 = 0.10) was seen by the two-way repeated measure ANOVA. Test of between subject effect of supplementation on weight is 8.4% (P = 0.087) and explained that only 8.4% variation in fasting blood glucose level (Table 2).

As shown by two-way repeated measures ANOVA, a highly significant time effect on participant’s low density lipoproteins (LDL) level (F (2,68) = 11.82, P = 0 0.000, ηp2 = 0.258) and no significant within group effect of supplementation on participant’s LDL level (F (2,68) = 0.510, P = 0 0.540, ηp2 = 0.015) was seen. Test of between subject effect of supplementation on LDL was 7.8% (P = 0.098) and explained that only 7.8% variation in LDL level. Although no significant effect of time or within group effect was seen on cholesterol, triglycerides and high density lipoproteins (HDL) (Table 3).

During a normal pregnancy, there is an upsurge in the lipid levels e.g. TG and TC as advancement in the gestational age [23]. Maternal hyperphagia and high insulin levels stimulate fat depot accumulation by increasing fatty acid synthesis throughout the first two trimesters. This research focuses on understanding how these supplements influence cardiometabolic markers like blood pressure, lipid profiles, and glucose levels, which are important for assessing long-term health risks.In the current study, a highly significant effect of time was observed on participant’s insulin level measured at three different visits. Also a significant time’s effect as well as within group effect of supplementation was seen on fasting glucose levels. The reason for this significant effect of time on insulin might be that during the second trimester of pregnancy, the human placental lactogen (HPL) rises and induces lipolysis to release mother free fatty acids, providing the mother with an alternate energy source while preserving glucose for the foetus. During pregnancy, HPL is a chief antagonist of insulin, and because of this a woman’s body requires more insulin [24].Our findings are in contrast to the study by Fatima et al. on intake of HENSD in underweight females in the evening. They concluded that short term supplementation with HENSD in the evening has no impact on fasting insulinaemia or glycaemia [25].

In this study, a significant effect of time and within group effect of supplementation on HOMAIR was seen. Our findings are in accordance with the Fatima et al.,2021 findings that short term supplementation with HENS in the late afternoon reduces insulin sensitivity and increased HOMAIR [26].

In this study, we investigated the impact of supplementation on lipid profile which was measured at baseline experimental day then at second visit made between week16th -20th and third visit made postnatally. The difference seen between the groups in regards of TC, TGs, LDL and HDL was not significant. These results of our study are similar to the study by Fatima et al.,2015, on intake of HENSD in underweight females in the evening. They also did not observe any effect of supplementation on fasting lipids and postprandial lipaemia [25]. Our results are in contrast to the results of a study by BM Oaks et al. done to explore the effect of lipid based nutritional supplements on plasma fatty acids level during pregnancy and lactation and lipid profile in Ghana and Malawi. Unlike our study, they found an increase in plasma ALA levels at 36 weeks in those receiving SQ-LNS in comparison with the control group. Breast milk ALA was increased by SQ-LNS in Ghana but not Malawi [27].

A Physiological increase in the TC, TGs and LDL is seen in the late second trimester and third trimester [28]. A highly significant effect of time was seen on LDL in the HENS group as well as the Placebo group. No significant increase was observed in the TC, TGs and HDL of the participants of our study in the second and third in contrast to a study done by Padama Leela et al.,2012 who noted that the values of TC, TGs, and VLDL in pregnant women were greater than those in non-pregnant women [29]. This maybe because the participants of our study groups were all pregnant in contrast to the above study in which the control group was non-pregnant women. This also shows that the supplementation by ‘MAAMTA’ has no effect on the cholesterol and LDL levels and is safe to be used by the pregnant women.

It has been shown that changes in blood lipid levels in the early stages of pregnancy enhance the likelihood of pregnancy-induced hypertension (PIH). When compared to normal pregnant women, pregnant women with hypertension have greater levels of TC, TGs, LDL, and VLDL, but their HDL levels are lower [30]. According to certain research, TG levels in the blood have no effect on PIH, although LDL does play a part. PIH risk increases if LDL levels exceeds than 117 mg/dl [31]. Preeclampsia can also be caused by primigravidity, as studies have shown that this condition is more common in primigravidas [32]. Although, all our study participants were primigravidas, having a mean blood pressure of 100/70 mm Hg. No case of eclampsia was reported in our study. There may be some role of supplementation and dietary counseling given to the participants of both the groups. However, the exact mechanism should be explored in future studies. Similarly, no significant increase in any fraction of lipids was observed in our study participants unlike in a study by Shivanagappa et al., 2015 done on lipid profile in pregnancy, which investigated the relationship between lipid levels and systemic blood pressure during pregnancy. The hypertension group had significantly higher levels of TC, LDL, VLDL, and TGs than the control group, but there was no discernible difference in HDL levels among the two groups [30].

This study concluded that supplementation with high-energy nutritional supplements may improve insulin levels and insulin sensitivity in underweight primigravidas. The robust study design, with its use of a randomized controlled approach and thorough assessment of various anthropometric and biochemical parameters, lends a high degree of credibility to our findings. The inclusion of a diverse, real-world sample of Pakistani women further enhances the generalizability of our results, making them highly relevant to addressing the pressing public health challenges faced by many developing countries.

In conclusion, this study represents a significant contribution to the growing body of evidence on the importance of maternal nutrition and its impact on cardiometabolic health. The promising results demonstrate the potential for high-energy nutritional supplements to serve as a simple, yet effective, intervention for improving the metabolic profile of underweight pregnant women, ultimately leading to better outcomes for both mother and child. This work paves the way for further research and implementation efforts aimed at optimizing maternal and child health in resource-limited settings.

The limitations of our study are the small sample size and shorter duration of the study as many studies have been continued till one year post natally.

All the data generated and analyzed has already been incorporated into the study.

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The authors extend their appreciation to the Researchers Supporting Project (RSPD2024R758), King Saud University, Riyadh, Saudi Arabia.

This work was funded by the Researchers Supporting Project (RSPD2024R758), King Saud University, Riyadh, Saudi Arabia. The publication charges for this article are partially borne by Khyber Medical University Publication Fund (No. DIR/ORIC/Ref/24/00076).

Biochemistry Department, Khyber Girls Medical College, Peshawar, Pakistan

Kalsoom Tariq, Nabila Sher & Bela Inayat

Biochemistry Department, Khyber Medical University, Peshawar, Pakistan

Hafsa Zafar, Mashal Zafar, Sofia Islam & Sadia Fatima

Department of Biochemistry, KMU Institute of Dental Sciences, Kohat, KP, 26000, Pakistan

Fozia Fozia

Department of Chemistry, Kohat University of Science and Technology, Kohat, 26000, Pakistan

Ijaz Ahmad

Department of Pharmacology and Toxicology, College of Pharmacy, King Saud University, P.O. Box 55760, Riyadh, 11451, Saudi Arabia

Mohamed Mohany & Salim S. Al-Rejaie

Jiangsu Key Laboratory of Sericultural Biology and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, 212100, China

Mingkun Zhu

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Conceptualization, SF, Formal analysis SF, FF, NS, MM, ASAR, IA, MZ; Funding acquisition, MM, FF; Investigation, KT, HZ; Methodology, KT, BI; Supervision, SF; Writing – original draft, KT, MZ, SI; Writing – review & editing, SF, MM, NS, IA, FF, SSAR, MZ.

Correspondence to Fozia Fozia or Sadia Fatima.

Written informed consent was obtained from all participants. Participants were informed about the purpose of the study, the voluntary nature of participation, and their right to withdraw at any time without consequence. Confidentiality and anonymity of participants were assured.

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Tariq, K., Zafar, H., Sher, N. et al. Effect of antenatal use of high energy nutritional supplements on cardio metabolic risk markers in underweight primi gravidas; a randomized controlled trial. BMC Pregnancy Childbirth 24, 695 (2024). https://doi.org/10.1186/s12884-024-06868-3

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Received: 21 July 2024

Accepted: 26 September 2024

Published: 23 October 2024

DOI: https://doi.org/10.1186/s12884-024-06868-3

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