Macronutrient Composition of Colostrum in Mothers with Gestational Diabetes Mellitus

Abstract

Background:

Infants fed breast milk are known to have lower rates of childhood obesity. However, there is evidence suggesting an increased risk of obesity in infants who receive milk from a diabetic mother. The aim of this study was to investigate the calorie and macronutrient content of colostrum in mothers with gestational diabetes mellitus (GDM).

Methods:

This prospective, controlled study included mothers who had diagnosis of GDM and a control group of mothers without GDM who delivered at term. Colostrum samples were analyzed for macronutrients (fat, protein, and carbohydrate) and calorie content using a human milk analyzer (Miris, Uppsala, Sweden).

Results:

A total of 92 colostrum samples were analyzed, 31 in the GDM group and 61 in the non-GDM group. The carbohydrate content of colostrum in the GDM group was higher compared with the non-GDM group (p = 0.004). The calorie, fat, and protein contents of colostrum were similar between the groups (p > 0.05). Multiple regression analysis indicated that having GDM was significantly related to carbohydrate content.

Conclusion:

The colostrum of GDM mothers had higher carbohydrate content. This might be one of the factors explaining the relationship between diabetic breast milk and infantile obesity.

Introduction

Breast milk, the ideal nutrient for infants, is a dynamic fluid whose composition is constantly changing to meet the physiological needs of the baby during the breastfeeding period.¹ Factors such as maternal age, dietary and somatometric characteristics, prematurity, and metabolic abnormalities may also affect the content of breast milk.^2–4

Infants who are fed breast milk are known to have lower rates of childhood obesity.⁵ However, there is evidence suggesting an increased risk of obesity in infants who receive milk from a diabetic mother.⁶ It was reported that the relationship between diabetic breast milk and risk of obesity was related to the timing of breastfeeding; receiving diabetic breast milk during the first week of life was associated with higher body weight at 2 years of age.⁷ Therefore, a detailed analysis of the milk of diabetic mothers is necessary to fully understand the relationship between breastfeeding and obesity in children of diabetic mothers.

A small number of studies investigating the breast milk content of mothers with insulin-dependent diabetes mellitus (IDDM) indicated that total protein and lactose content did not differ from the milk of healthy mothers.^8–10 Three studies examining total fat content showed no difference in the fat content of breast milk from IDDM and healthy mothers,^8,10,11 whereas the results of one study suggested that total fat content was lower in IDDM mothers.⁹

Gestational diabetes mellitus (GDM), defined as hyperglycemia with onset or recognition during pregnancy, is an increasingly common complication of pregnancy.¹² Although glycemic control in GDM mothers normalizes soon after delivery, metabolic changes in this period might be reflected in colostrum composition, as the production of colostrum begins in late pregnancy.¹³ Moreover, previous studies have revealed differences in macronutrients not only in colostrum but also in the transitional milk and mature milk of mothers with GDM.^3,14

Few studies have reported macronutrient content in the colostrum of GDM mothers, and these studies yielded contradictory results.^3,14,15 This study aimed to evaluate the calorie and macronutrient content of colostrum produced by mothers with GDM. Our hypothesis was that GDM may alter the macronutrient content of colostrum.

Materials and Methods

This prospective controlled study was conducted between August 2018 and January 2019 at Zekai Tahir Burak Maternal Health Training and Research Hospital. Ethical approval was obtained from Clinical Research Ethics Committee No. 7 (159/2017) before the study.

Study population

Of the mothers who attended pregnancy follow-up in the antenatal outpatient clinic and gave birth in the same hospital at 37 weeks of gestation or later and those diagnosed as having GDM were included in the study group (GDM group). Those who did not have diabetes were included in the control group (non-GDM group). Mothers who had pregestational diabetes, plastic surgery of the breast, major systemic disease, or chronic metabolic disease, and those who did not consent to participate in the study were excluded. Gestational age at delivery was determined according to the mother's last menstrual period and/or early ultrasound findings. Maternal weight was measured after birth and used to calculate body mass index (BMI). Neonates whose birth weight was above the 90th percentile according to age and sex were classified as large for gestational age.¹⁶

Maternal age and weight, parity, weight gain during pregnancy, type of diabetes treatment (diet alone or diet and insulin), treatment adherence, expression time, mastitis status at the time of sampling, and the gestational age and birth weight of the infant were recorded.

Sample size

In a study investigating macronutrient content in the colostrum of GDM mothers using the same analysis method as in our study, the carbohydrate content of colostrum was reported as 5.8 ± 0.8 g/100 mL.³ To detect a significant difference of 10% in colostrum carbohydrate content with 80% power and an alpha error level of 0.05, the minimum sample size was calculated as 30 in each group (stat.ubc.ca). We decided to make the control group twice the size of the study group. Considering possible insufficient colostrum sampling or withdrawal of consent to participate, we included 35 mothers in the study group and 65 mothers in the control group.

Diagnosis and management of diabetes in pregnancy

Oral glucose tolerance test was performed at the first prenatal visit for pregnant women with risk factors for GDM and at 24–28 weeks of gestation for those with no risk factors.¹⁷ Women diagnosed with GDM were referred to the internal medicine department for dietary modifications and insulin therapy if necessary. GDM patients who received insulin therapy and demonstrated good metabolic control and normal fetal biometric measurements were followed at 2-week intervals. Those with poor metabolic control were followed on a weekly basis and their insulin therapy was adjusted.

Good metabolic control was defined as maintaining a glycated hemoglobin level <6.5% in the third trimester.

Breast milk sampling and analysis

A 3 mL sample of colostrum was collected once between postpartum day 2 and 5 by manual expression either from the right or left breast of each lactating mother. The calorie, fat, crude protein, and carbohydrate content of the unfrozen samples were measured immediately after milk collection using a Miris AB human milk analyzer (HMA) (Uppsala, Sweden) according to the manufacturer's protocol. The Miris HMA makes measurements using a spectroscopic method and is approved by the International Standardization Organization ([ISO] 9622: 1999).

Statistical analyses

The variables were investigated using visual (histograms, probability plots) and analytical methods (Kolmogorov–Smirnov/Shapiro–Wilk tests) to determine whether the data were normally distributed. Descriptive analyses were presented as mean and standard deviation for normally distributed variables and median and interquartile range for non-normally distributed variables. For intergroup comparisons, the independent samples t-test was used for normally distributed variables and the Mann–Whitney U-test was used for non-normally distributed variables. Chi-square tests were used to compare categorical variables between the groups.

Multiple linear regression analysis was used to control for other factors that may affect the colostrum carbohydrate level. Maternal age, BMI, expression time (postnatal hour), and having GDM were analyzed as independent variables in regression analysis. An overall 0.05 type-I error level was used to infer statistical significance.

Results

The study included 35 mothers in the GDM group and 65 mothers in the non-GDM group. Eight samples were of insufficient volume for analysis. Therefore, a total of 92 colostrum samples were analyzed, 31 in the GDM group and 61 in the non-GDM group.

In the GDM group, 7 mothers were treated with diabetic diet and insulin, whereas 24 were followed-up with diabetic diet only. Twenty-eight (90.3%) of the GDM mothers had good metabolic control during follow-up. None of the mothers had mastitis at the time of sampling.

Comparison of the characteristics of the groups showed that maternal age was higher in the GDM group than in the non-GDM group (32.0 ± 6.3 years versus 27.5 ± 5.3 years; p = 0.001). BMI was also higher in the GDM group (31.3 ± 6.4 versus 27.0 ± 4.1; p = 0.005). There was no difference in parity or the infants' gestational age, birth weight, or sex between the groups (Table 1).

Table 1.

Demographic Characteristics of the Groups

	Non-GDM (n = 31)	GDM (n = 61)	p
Maternal age, years	27.5 ± 5.3	32.0 ± 6.3	0.001
Maternal weight, kg	72.5 ± 11.3	77.8 ± 15.5	0.11
Parity	2 (1–3)	2 (2–3)	0.59
BMI	27.0 ± 4.1	31.3 ± 6.4	0.005
Weight gained during pregnancy, kg	11.9 ± 4.2	9.8 ± 5.7	0.07
Gestational age, weeks	39.0 (38.0–39.0) (37.0–41.0)	38.0 (37.0–39.0) (37.0–41.0)	0.14
Cesarean delivery	14 (23.0)	21 (67.7)	0.001
Birth weight, g	3126.1 ± 531.0	3289 ± 649.8	0.20
LGA	4 (12.9)	3 (4.9)	0.15
Female	28 (45.9)	16 (51.6)	0.60

Data are expressed as mean ± SD, median and (IQR), (minimum-maximum) or n (%).

BMI, body mass index; GDM, gestational diabetes mellitus; LGA, large for gestational age; SD, standard deviation.

Colostrum lipid, protein, and calorie content were similar in both groups. The colostrum carbohydrate content was higher in the GDM group than in the non-GDM group (p = 0.004) (Table 2).

Table 2.

Colostrum Macronutrient and Calorie Content in the Groups

	Non-GDM (n = 31)	GDM (n = 61)	p
Expression time
Postnatal hour	37.0 (30.0–60.0)	42.0 (33.5–50.5)	0.78
Postnatal day	2 (2–3)	2 (2–3)	0.59
Calorie, kcal/dL	61.0 (48.5–72.5)	54.0 (47.0–70.0)	0.39
Carbohydrate, g/dL	4.6 ± 1.5	5.7 ± 1.6	0.004
Fat, g/dL	2.6 (1.7–3.9)	2.1 (1.3–3.6)	0.17
Protein, g/dl	2.2 (1.6–3.4)	2.1 (1.5–2.7)	0.41

Data are expressed as mean ± SD or median and (IQR).

GDM, gestational diabetes mellitus.

In the regression analysis, GDM was the only factor associated with colostrum carbohydrate content, whereas maternal age, BMI, and expression time were not related (R² = 0.134) (Table 3).

Table 3.

Factors Affecting of Colostrum Carbohydrates Content (n = 92)

Factors	B	SE	T	P	95% lower	CI upper
Maternal age	−0.012	0.043	−0.277	0.783	−0.099	0.075
BMI	−0.025	0.044	−0.570	0.571	−0.113	0.063
GDM	1.344	0.463	2.900	0.005	0.416	2.271
Expression time	0.004	0.008	0.488	0.628	−0.013	0.021

B, β coefficient; BMI, body mass index; CI, confidence interval; GDM, gestational diabetes mellitus; SE, standard error; T, t-score of the regression model.

Discussion

In this study, it was found that carbohydrate content of the colostrum was higher in mothers diagnosed with GDM compared with mothers without GDM, whereas the calorie, protein, and lipid contents were similar.

In the lactating mammary gland, glucose is used to produce lactose and most intracellular glucose is obtained from blood glucose.¹ Studies have shown that milk glucose concentrations in diabetic women are proportional to their blood glucose concentrations.^10,18 Contrary to our results, Shapira et al. reported that the carbohydrate content of colostrum did not change in GDM mothers. In their study, about half of GDM mothers required insulin therapy, and the prepregnancy metabolic control status was uncertain.¹⁴ To clarify the effect of GDM on colostrum carbohydrate content, studies investigating the effect of metabolic control and treatment modality are required.

There was no difference in the total fat content of colostrum produced by mothers with and without GDM in this study. This is consistent with a previous report that the total fat content of maternal colostrum did not change in GDM.¹⁴ In contrast, in another study it was observed that the total fat content of GDM maternal colostrum was lower compared with the control group.¹³ The authors attributed this to lipid metabolism abnormalities in the mammary gland cells owing to poor metabolic control, leading to impaired esterification of free fatty acids and increased lipolysis. However, the metabolic control status of the GDM mothers in that study was not clear.

In previous studies, no difference in colostrum protein content and amino acid concentrations were observed between mothers with and without GDM.^14,15,19 Our results also demonstrated that protein content did not change in the colostrum of GDM mothers. In a study by Dritsakou et al. investigating energy content in the milk of GDM mothers, it was reported that their colostrum was higher in calories, but not knowing whether the groups had the same rate of preterm delivery makes it difficult to interpret these results.³ In another study, it was reported that the mature milk of GDM mothers had fewer calories.¹⁴ Our results indicate that the colostrum of GDM mothers with term delivery did not differ in calorie content.

It has been reported that maternal factors such as age, parity, diet, and obesity affect breast milk content.^3,20–23 In this study, regression analysis performed to control for maternal age, BMI, and expression time on carbohydrate content also showed that having GDM was associated with carbohydrate content.

Our study has several limitations. We could not measure the blood glucose levels of mothers simultaneously with colostrum sampling, and therefore were not able to determine whether colostrum macronutrients were correlated with blood glucose. Another limitation is that we calculated the sample size based on carbohydrate content. Therefore, the lack of statistically significant differences in the calorie and fat content of colostrum between the groups in our study might be owing to our sample size. In addition, the study did not include any data on maternal diet, which is one of the factors that could affect breast milk content.

In conclusion, carbohydrate content is higher in the colostrum of GDM mothers with good metabolic control. High carbohydrate levels in colostrum might be one of the factors that can explain the relationship between diabetic breast milk and infantile obesity. Whether this difference might be a protective modification for newborns of GDM mothers who are at risk of hypoglycemia in the first postpartum days may be the subject of future research. Larger studies that are well controlled for factors affecting breast milk composition are needed to clarify the composition of diabetic breast milk.

Footnotes

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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