Abstract
BACKGROUND:
Information on exclusive breastfeeding (BF) and BF initiation following bariatric surgery (BS) among obese women with diabetes mellitus (DM) and without DM (non-DM) is limited.
METHODS:
Retrospective cohort study. Obesity was defined by BMI (kg/m2) as grade 1 (30–34.9), grade 2 (35–39.9) or grade 3 (≥40). The 65 women in the DM group (40 women with gestational, 19 with Type 2 and 6 with Type 1) was similar to 84 with non-DM in BS type: Roux-en-Y (51 vs 55%), sleeve gastrectomy (32 vs 35%), laparoscopic gastric banding (17 vs 7%) and gastro-duodenal anastomosis (0 vs 4%).
RESULTS:
Women with DM were older (35 vs 33y), of advanced age (54 vs 27%), with higher prevalence of grade 3 obesity (66 vs 46%), chronic hypertension (31 vs 10%), delivery of late-preterm infants (23 vs 10%) and neonatal hypoglycemia (25 vs 12%). Although infant feeding intention was similar: BF (66 vs 79%), partial BF (9 vs 7%) or formula (25 vs 14%), at discharge women with DM had lower exclusive BF (29 vs 41%) and BF initiation rates (68 vs 76%) than those with non-DM. Women with grade 3 obesity (52% were DM) differed from those with grades 1-2 (34% were DM) in exclusive BF (27 vs 52%), and BF initiation rates (66 vs 86%).
CONCLUSION:
After BS, women with DM, especially those with grade 3 obesity, had higher rates of chronic hypertension and preeclampsia and lower rates of exclusive BF and BF initiation than those who had DM but had less severe obesity.
Background
Obesity is the most common medical condition in women of reproductive age and is increasing worldwide [1–3]. Concurrently, the incidence of Type 1 and Type 2 diabetes mellitus (DM) in women has risen in parallel to the obesity epidemic [1, 3]. Bariatric surgery (BS) is considered one of the most effective methods for substantial and sustained weight loss [4, 5]. Thus, it is not surprising that eighty percent of patients undergoing BS are women of reproductive age, and that this type of surgery has a significant impact on maternal and neonatal outcomes including the frequency of gestational diabetes mellitus (GDM), Type 2 DM, intrauterine growth, prematurity and admission to the NICU in subsequent pregnancies [4–9]. The benefits of lactation on short- and long-term maternal and infant health are well accepted [10–14]. More specifically, exclusive BF during birth hospitalization and during the first postpartum year are clearly desirable goals [13, 14].
Comorbidities such as GDM, Type 1 DM, Type 2 DM and maternal obesity have been independently recognized as significant obstacles to BF initiation and duration [1, 15–17]. Consequently, the effects of BS on GDM and the nutritional status of their infants following surgery attracted the attention of investigators [6–9]. Unfortunately, information on BF among obese women with DM and other comorbidities following BS remains limited [17, 18].
Objective
The primary objective was to evaluate exclusive BF and BF initiation among 65 obese women with a history of DM and 84 obese women without DM following pregnancies preceded by BS. A secondary objective was to ascertain if the severity of obesity (grade 1-2 vs grade 3) and DM affects BF rates.
Subjects and methods
This retrospective cohort investigation was approved by the Institutional Review Board at The Ohio State University Wexner Medical Center (IRB 2010H0198). Electronic maternal and neonatal records (2013-21) were reviewed. Some data obtained from women who delivered between 2013-18 was presented in previous investigations [19, 20]. GDM, Type 1 and Type 2 DM, chronic hypertension (CHTN) and preeclampsia were diagnosed and treated following established guidelines [21–23]. Women were categorized by prepregnancy BMI as normal (18.5–24.9 kg/m2), overweight (25–29.9 kg/m2), obese grade 1 (30–34.9 kg/m2), obese grade 2 (35–39.9 kg/m2) or obese grade 3 (≥40 kg/m2) [1]. According to recently published guidelines, gestational weight gain (GWG) was categorized as adequate, inadequate or excessive [24].
In this study, BS procedures included Roux-en-Y gastric bypass (RYGB), sleeve gastrectomy (SG), laparoscopic gastric band (LGB) and gastro-duodenal anastomosis (GDA). Indications for BS were in line with the American Association of Clinical Endocrinologists/American College of Endocrinology, The Obesity Society, American Society for Metabolic and Bariatric Surgery, Obesity Medicine Association and The American Society of Anesthesiologists [4, 5] as well as the American College of Obstetrics and Gynecology [23]. The interval from BS to conception was calculated as the time in months that elapsed between the surgical date and the start of the following pregnancy which was estimated by subtracting the gestational age in weeks from the date of birth [25]. Following BS and at different conception intervals, 96 women delivered one infant, 25 women delivered two infants and one woman delivered three infants. These 149 mother-infant dyads comprised the study population. Multiple births, infants born before 34 weeks or those affected by major malformations were not included in the analysis. Upon arrival to Labor and Delivery, each woman described her infant feeding preference. In our institution, maternity practices include BF within 1 hour of delivery, no formula supplementation unless indicated, rooming in, on demand BF, full-time lactation consultants and post discharge BF support [16, 20]. Furthermore, our institution reports BF data to the Joint Commission as required for hospital accreditation [13].
Per our hospital practice, any symptomatic infants were directly transferred from the delivery room to the NICU for further care. If the condition of the mother and her infant allowed interactions such as holding, skin-to-skin contact, and BF were encouraged [16, 20]. Asymptomatic infants able to feed were transferred to the Newborn Nursery with their mothers for routine care and glucose monitoring [19, 20]. According to standard intrauterine growth charts, infants were categorized as appropriate for gestational age (AGA), small for gestational age (SGA), large for gestational age (LGA) or macrosomic (birthweight ≥4000 g) [26].
Screening for hypoglycemia (blood glucose <40 mg/dl) was done via serial point of care testing (Accu-Chek®) or by plasma glucose measurement in the laboratory (Beckman Coulter AU5800, Beckman Coulter Inc., Brea, CA, U.S.A.) starting within the first hour of life after the first feeding and every 2–4 hours thereafter as clinically indicated [19]. Infants in the Newborn Nursery with hypoglycemia were promptly BF, formula fed (FF) or given dextrose gel and those with recurrent hypoglycemia were transferred to the NICU for further care. On admission to the NICU, most infants were administered intravenous dextrose and those who were able to feed were BF or FF [19, 20].
Exclusive BF was defined as direct feedings from the breast or by expressed breast milk alone or in combination with direct BF [16, 20]. Partial BF was defined as formula supplementation with direct BF or with expressed breast milk. BF was considered initiated if, during the 24 hours preceding hospital discharge, infants were exclusively BF or partially BF [16, 20]. Due to the retrospective study design, no information was available on infant feeding practices following hospital discharge.
Statistical analysis
Comparisons between DM and non-DM groups were made with Wilcoxon Two Sample test for continuous and Chi-square tests for categorical variables. Multivariate logistic regressions were used to determine the influence of DM and non-DM in predicting exclusive BF and BF initiation at discharge. Variables included CHTN, age, race, BMI, obesity grade, BS to conception interval, parity, mode of delivery, prior BF, late prematurity, AGA, SGA, LGA, hypoglycemia, admission to NICU and length of stay. Significance was established at a p value <0.05.
Results
Demographic and clinical features of obese diabetic and non-diabetic women
The DM group was composed of 28 women (43%) with history of GDM, 12 (19%) with current GDM, 19 (29%) with Type 2 and 6 (9%) with Type 1 DM. BS procedures were similar among 65 DM and 84 non-DM dyads: RYGB (51 vs 55%), SG (32 vs 35%), LGB (17 vs 7%) and GDA (0 vs 4%) (Table 1). Gestational weight gain (GWG) was inadequate (5 vs 6%), adequate (25 vs 25%) or excessive (71 vs 69%). CHTN was more common in the DM group (31 vs 10%) which also differed in age (35 vs 33y), advanced maternal age (54 vs 27%) and median pregestational BMI (42 vs 38 kg/m2) at the onset of the current pregnancy. Racial distribution was comparable among both groups with higher prevalence of white (72 vs 73%) than African American women (20 vs 24%). Public assistance (46 vs 52%), rate of vaginal (60 vs 55%) and cesarean deliveries (40 vs 45%) were all similar. Additionally, at the time of delivery, women in the DM group were more often classified as obese grade 3 (66 vs 46%). History of smoking (22 vs 32%) or smoking during the current pregnancy (5 vs 7%) affected both groups equally.
Demographic and clinical features of obese diabetic and non-diabetic women
Demographic and clinical features of obese diabetic and non-diabetic women
Analysis: †Fisher’s Exact Test, ∧Chi-Square, *T-Test, ‡Wilcoxon Two Sample Test.
Infants born to women from the DM group were often late-preterm (23 vs 10%) but had similar birthweight (3142 vs 3046 g) compared to those in the non-DM group (Table 2). Intrauterine fetal growth was comparable across groups: AGA (85 vs 80%), LGA (5 vs 2%) and SGA infants (11 vs 18%). Neonatal hypoglycemia was more common in the DM group (25 vs 12%) while admission to the NICU remained similar among groups (20 vs 21%).
Neonatal outcomes of infants born following maternal bariatric surgery
Neonatal outcomes of infants born following maternal bariatric surgery
Analysis: †Fisher’s Exact Test, ∧Chi-Square, *T-Test, ‡Wilcoxon Two Sample Test.
Considering the similarities in NICU admission diagnoses, 13 infants from the DM and 18 from the non-DM group were combined for analysis. Twenty-one of the 31 (68%) infants were admitted to the NICU directly from the delivery room. The remaining ten infants stayed with their mothers in the nursery prior to NICU transfer. Primary admission diagnoses were respiratory distress (42%), hypoglycemia (20%), apnea-bradycardia-cyanosis (23%) and miscellaneous (15%). Thirteen of 31 (42%) were late preterm while 10 (32%) were SGA. Forty-eight percent stayed in the NICU less than three days, 29% between 3–7 days and 23% greater than 7 days. All mothers and their infants were discharged home in good health.
Mothers infant feeding preferences were comparable for the DM and non-DM groups: BF exclusively (66 vs 79%), BF partially (9 vs 7%) and FF only (25 vs 14%) (Table 2). Of note, none of the women from either group who intended FF changed their choice during their hospitalization.
Infant feeding at discharge for all DM and non-DM women showed exclusive BF (29 vs 41%), partial BF (39 vs 35%) and FF (32 vs 24%). Regression analysis showed that prior BF (OR 2.401 95% CI 1.13,5.09 p 0.02) was the strongest predictor of exclusive BF. Conversely, women who delivered late premature infants (OR 0.18 95% CI 0.04,0.70 p 0.01) and women who received public assistance (OR 0.39 95% CI 0.18,0.86 p 0.01) were less likely to BF exclusively. Furthermore, despite the use of expressed breast milk or donor human milk, direct BF was less common among women in the DM group (53 vs 80%), p 0.01. However, BF initiation at discharge (68 vs 76%) was not different between the groups.
Perinatal outcomes according to mother’s obesity grade at conception
The study population following BS was categorized by BMI at the time of conception: 9 normal/overweight, 29 obesity grade 1, 29 obesity grade 2 and 82 obesity grade 3. For analysis purposes, data from 29 grade 1 and 29 grade 2 women were combined. (Table 3). Comparison of grade 1-2 with grade 3 obese women showed that maternal age was similar (33 vs 35 years), while the incidence of DM (34 vs 52%), CHTN (7 vs 28%), preeclampsia (0 vs 15%) and pregestational BMI (35 vs 45 kg/m2) were different. There were also dissimilarities in BS type: RYGB (64 vs 46%), SG (28 vs 38%), LGB (7 vs 16%) and GDA (2 vs 0%). Otherwise, median surgery to conception interval (42 vs 41 months) and gestational weight gain (GWG): inadequate (3 vs 7%), adequate (14 vs 24%) and excessive (83 vs 69%) were not different. Infants gestational age (39 vs 38 weeks), birthweight (3133 vs 3103 g), AGA (89 vs 77%), SGA (9 vs 18%), LGA (2 vs 5%) and rate of neonatal hypoglycemia (14 vs 18%) were similar among groups, while admission to NICU was more frequent in the grade 3 group (29 vs 9%). Prior BF experience was more common among grades 1-2 (43 vs 28%). Intention to BF exclusively (78 vs 72%) and BF partially (10 vs 5%) were similar. Intention to formula feed only, although more common among grade 3 (23 vs 12%), did not reach statistical significance.
Perinatal outcomes according to mothers obesity grade at conception
Perinatal outcomes according to mothers obesity grade at conception
Analysis: †Fisher’s Exact Test, ∧Chi-Square, *T-Test, ‡Wilcoxon Two Sample Test.
The rate of exclusive BF was higher among grade 1-2 (52 vs 27%), partial BF was similar (34 vs 39%) while formula feeding only was more common among grade 3 (34 vs 14%). As a result, infants in the grade 1-2 group initiated BF more often (86 vs 66%) than those in the grade 3 group.
During the 2013–2021 study period there were 79 RYGB, 50 SG and 17 LGB and 3 GDA. After the exclusion of the 3 GDA cases (due to small sample size), a comparison of maternal and neonatal outcomes according to the most frequently used procedures, 79 RYGB and 50 SG and 17 LGB combined is presented in Table 4. Neither maternal nor neonatal outcomes were different except that among women in the RYGB group, the prevalence of grade 3 obesity (48 vs 66%) was lower, the women at delivery were older (35 vs 32 y) and their infants hospital stay was longer (4 vs 3d).
Perinatal Outcomes according to type of bariatric procedure
Perinatal Outcomes according to type of bariatric procedure
RYGB - Roux-en-Y Gastric Bypass, SG - Sleeve Gastrectomy, LGB - Laparoscopic Gastric Band. Analysis: †Fisher’s Exact Test, ∧Chi-Square, *T-Test, ‡Wilcoxon Two Sample Test.
The National Institute of Health indications for BS include grade 3 obesity (BMI ≥40 kg/m2) or grade 2 (BMI 35–39 kg/m2) with one or more associated co-morbidities including DM, cardiovascular disease, obstructive sleep apnea and previous weight loss attempts [4–6]. The higher prevalence of CHTN or preeclampsia among obese women with DM has been previously reported [27–30]. Until recently, most of the literature on BS primarily focused on obesity and prevention of GDM in subsequent pregnancies [6, 32]. Despite the difficulties diagnosing GDM after BS (i.e., inability to perform glucose tolerance testing, dumping syndrome, etc.), investigators have reported a decrease in GDM recurrences [6, 33]. As the incidence of Type 2 DM rises globally, BS is increasingly being considered a safe alternative for long term weight control [4, 32]. Recent data showed that BS also reduces post-operative insulin requirements in obese and severely obese Type 1 DM patients, however, these authors cautioned that high volume, randomized prospective trials are still necessary to elucidate benefits versus risks in this group of patients [34]. Recently, we reported that of 185 Type 1 severely obese pregnant women, 43 (23%) could have been candidates for BS, but only one had this procedure [16]. Similarly, of 212 Type 2 women 92 (43%) also could have been candidates for BS but only two had this procedure [16]. Considering the above, it is possible that soon more obese women with history of DM would benefit from BS [4, 34].
Earlier studies of perinatal outcomes following BS showed increased rates of SGA or LGA infants, which were associated with the type of surgery or with short intervals between BS and conception [31–35]. The data presented here showed no changes in prevalence of SGA or LGA in either the DM or the non-DM groups which is consistent with that reported by others [6–9, 32].
The American Academy of Pediatrics and the Academy of Breastfeeding Medicine recommend exclusive BF for all healthy infants during birth hospitalization because of its predictive value for BF 6 months or longer [13, 20]. In a recent study of maternity care practices and policies in 1,305 hospitals in the United States, the mean in-hospital exclusive BF rate for infants in the general population was 51.4% and for those in the most BF supportive hospitals was 64.7% [14]. Additionally, we have reported lower exclusive BF in women with severe preeclampsia (37%) [27], and preeclampsia superimposed on pregestational diabetes (18%) [28], with mild (47%) and severe CHTN (50%) [29] and with CHTN superimposed on pregestational diabetes (19%) [30]. Thus, the lower exclusive BF rates associated with DM compared with non-DM women (29 vs 41%) reported here are not unexpected. The association of obesity with DM is strengthened by the fact that 34% of women with grade 1-2 obesity and 52% of those with grade 3 had DM. Furthermore, at discharge, the exclusive BF rate in the grade 3 group was lower (27 vs 52%).
BF initiation rate (any BF at discharge) is also a predictor of BF duration, albeit not as strong as exclusive BF rates [36]. In the present study we observed BF initiation rates to be 68% for women with DM, 76% for non-DM; 86% for obese grade 1-2 (34% were DM) and 66% for grade 3 (52% were DM). Consequently, BF initiation rates post-BS observed here among women with grade 1-2 were similar to the 84.1% rate of those in the general U.S. population [36]. Factors known to be associated with low exclusive BF and low BF initiation affecting our study population included: intention to feed formula, no prior BF experience, preeclampsia, CHTN, pregestational diabetes, obesity, cesarean delivery, premature birth, excessive GWG, neonatal hypoglycemia, admission to the NICU, formula supplementation, delayed lactogenesis II, type of insurance and maternal-infant separation [16, 37–40].
The high rate of partial BF at the time of discharge for DM and non-DM groups deserves further comment. Women who intended exclusive BF, but partially BF their infants could with support and encouragement potentially achieve exclusive BF. Women who prenatally intended partial BF and accomplished their goal, like women who prenatally intended to feed formula, seldom change their infant feeding preference [16, 27–30].
Based on our experience, we speculate that the high incidence of hypoglycemia and NICU admissions unique to infants born to obese women with DM could explain their lower rate of exclusive BF [16, 30]. Also concerning is that women who BF by expressed breast milk only without any direct BF tend to have short duration of any form of BF [39]. Excessive GWG and low rates of exclusive BF observed here among obese women with DM and non-DM is in line with that reported by others [40].
A limitation of this investigation is that the definition of exclusive BF and BF initiation at discharge used here may be applicable only to women with high-risk obstetrical conditions whose early mother-infant interactions may be delayed. Another limitation is the small sample size of the DM group and the lack of follow-up information regarding BF after discharge from the hospital. The strength of this investigation is the inclusion of not only women with GDM, but also women with Type 1 and Type 2 DM and that the obstetrical and neonatal data was obtained directly from medical records, and not via post-delivery maternal questionnaires.
In conclusion, after BS, women with DM and women with grade 3 obesity with and without DM had lower rates of exclusive BF and BF initiation than those reported for the general population. On the other hand, following BS, some women with severe post-bariatric obesity, DM and other comorbidities can initiate BF. Further investigation of obstacles to BF following BS among women with severe obesity with and without DM would be helpful to design specific strategies for future successful lactation.
