Dixon, John B. MBBS, PhD; Dixon, Maureen E. BSc; O'Brien, Paul E. MD
The increasing prevalence of obesity, especially severe obesity (body mass index [BMI] > 35 kg/m2),1 over recent decades has increased the likelihood of the obstetrician being confronted with problems of severe obesity. Pregnancy in severely obese women is associated with increased risks to both mother and infant. Maternal problems include an increased risk of induction of labor, primary cesarean or instrumental delivery, perioperative morbidity, pregnancy-induced hypertension and preeclampsia, gestational diabetes, and excessive weight gain throughout the pregnancy.2–8 The infants of these severely obese women are more likely to succumb in utero or in the neonatal period and are at greater risk of fetal growth abnormalities, macrosomia, and intrauterine growth restriction.8,9
Weight loss has been shown to lead to improved fertility and lower obstetric complications.4,10–12 Obesity or “bariatric” surgery provides the only reliable way to achieve and sustain significant weight loss in severely obese patients.13,14 Over the last decade, bariatric surgery has been expanding rapidly to meet the global epidemic of severe obesity, yet only 1% of severely obese patients are receiving this effective therapy.15 It is expected that the rapid growth of bariatric surgery will continue over the coming decade. Of those seeking surgery, 75–85% are women, and the mean age is approximately 40 years.16 Thus, many are in their childbearing years.
Reproduction for women who have had bariatric surgery confronts us with a new series of questions and concerns for both mothers and their offspring. Nutrition for the developing and growing fetus is important. Fetal nutritional deprivation may lead to maladaptive metabolic programming if contrasting nutritional circumstances are encountered later in life.17
Macronutrient status may be inferred from maternal weight gain during pregnancy and birth weight. This requires a balance between sufficient maternal weight gain to allow normal fetal growth, development, and metabolic programming and excessive weight gain leading to increased obstetric risk, macrosomia, and postpregnancy weight retention. The Institute of Medicine in 1990 issued total gestational weight gain recommendations based on prepregnancy BMI.18
Reports for pregnancy outcomes in women who have previously had bariatric surgery are very limited and usually involve a retrospective collection of data. Outcomes of surgery where there is significant malabsorption or gastrointestinal diversion have indicated problems related to both macronutrient and micronutrient inadequacy and resulted in lower mean birth weights (Matielli J, Garrido AB Jr, Oliveira MR, Berti LV, Elias AA. Pregnancy following silicone ring gastric bypass [abstract]. Obes Surg 2004;14:916).19–22
A laparoscopically placed adjustable gastric band (LAGB) provides an opportunity for achieving weight loss before the pregnancy and then, using the adjustability of the LAGB, modifying the degree of hunger and satiety during the pregnancy in an attempt to optimize outcomes for the mother and the baby. The gastric band is placed just below the gastroesophageal junction and functions by producing gentle restriction of the gastric cardia and a sense of early and prolonged satiety.23 Further description and outcomes have been published elsewhere,24 and we have previously described our approach to the adjustment of the band during pregnancy.12
The aim of this study was to collect prospective data regarding pregnancies and outcomes of consecutive births, of greater than 20 weeks gestation, to women who have undergone LAGB surgery, with a view to assessing for any particular problem or complication, compare outcomes with those seen in a severely obese population, and finally to compare outcomes with those of the general community. We, therefore, compare the outcomes of the 79 first consecutive post-LAGB pregnancies with those of the penultimate pre-LAGB pregnancies of these women (n= 40) and with obstetric histories of matched severely obese controls (n = 79) taken from a broader range of women presenting for LAGB surgery. In addition, outcomes are compared with community outcomes as reported in the most recent state statistics “Births in Victoria 2001–2002.”25 Also, we consider a number of secondary hypotheses regarding maternal nutrition and weight gain, band adjustability, and birth weight.
MATERIALS AND METHODS
Patients with a BMI greater than 35 kg/m2, who are suffering significant medical, physical, or psychosocial disabilities and have attempted multiple weight reduction attempts, were considered for entry into the LAGB program. Preoperative assessment included, as part of the medical assessment, a questionnaire that inquired about parity and obstetric history. The history was dependent on the mother's recall of weight change, birth weight, and obstetric events. All patients gave written informed consent to the LAGB procedure and the study received institutional review board exemption.
All patients were followed regularly at a central multidisciplinary bariatric clinic and urged to inform us of pregnancy or of any intention to become pregnant as soon as possible. Patients were advised to delay pregnancy for at least 1 year after Lap-Band (Inamed Health, Santa Barbara, CA) placement, but this recommendation was not always followed because obesity-related infertility often resolved with early weight loss. All LAGB patients are advised to take a single multivitamin supplement containing folate 400 μg and vitamins B1 and B12, and those planning pregnancies are advised to take an additional 500 μg of folate. In addition to routine follow up visits, patients have a regular annual review, which includes biochemical assessment of metabolic and nutritional status. The annual biochemical assessment includes fasting plasma glucose, lipid profile, insulin, liver function, thyroid function, total protein, albumin, iron studies, calcium, vitamin B12, folate studies, and homocysteine concentrations.
We performed prospective collection of data and attempted to follow each patient regularly during her pregnancies and with adjustment of the band when we felt it was clinically appropriate. The band has an internal balloon through which the stoma can be adjusted at any time by adding or removing saline via an access reservoir placed on the anterior rectus sheath. This can be felt through the skin allowing us to make adjustments as an office procedure, and we have not required radiological imaging to locate the access port site in any pregnant women to date. If significant vomiting, hyperemesis, or weight loss was experienced during the first trimester, the impact of the band was reduced by removing some saline. Weight gain was assessed at approximately 14 weeks of gestation, and if maternal weight gain or appetite appeared to be excessive, saline was added to the band. The maternal weight was monitored and volume adjustments made as indicated during the pregnancy. At 36 weeks of gestation some fluid was removed to reduce the impact and risks of gastric restriction during delivery. We reinstituted full band function as soon as breastfeeding has been established.
All LAGBs were placed between January 1, 1995, and August 31, 2003, and a total of 1,382 patients were treated during this time. Because 98% of all treated patients were traced during late 2004, the current series of pregnancy outcomes represents those of all patients, other than the 2% lost to follow-up. All adjustable gastric bands used were the Inamed Health Lap-Band.
Data on 100 consecutive births was collected from women who had previously undergone LAGB surgery. To minimize the oversampling problem of several pregnancies from a single subject, only the first pregnancy to each woman following band placement was included in the statistical analysis. There were 79 first pregnancies after band placement, and these were compared with 1) the obstetric history of any penultimate delivery before band placement (n = 40) and 2) the obstetric histories (n = 79) from a cohort of women presenting for surgery. These were selected from the obstetric histories of a larger group of 264 parous women and best matched for parity, maternal age, and BMI, without regard to the obstetric outcomes. Information from state-published birth outcomes, “Births in Victoria 2001–2002,” were used as community controls.
Pregnancy-induced hypertension included any history during pregnancy of hypertension of any type, preeclampsia, severe preeclampsia, or eclampsia, when there was no hypertension during the nonpregnant state before the pregnancy. Similarly, gestational diabetes included the development of diabetes during the pregnancy when it was absent immediately before pregnancy. Consideration was given to the high likelihood of remission of diabetes and hypertension with significant weight loss. Universal screening for gestational diabetes is performed in Victoria at 28 weeks of gestation. Maternal weight gain for the pregnancy was the maternal predelivery weight minus the maternal weight at the start of the pregnancy. Women were asked to obtain and record these weights as accurately as possible. Optimal weight gain for pregnancy was based on the Institute of Medicine recommendations for weight gain at varying BMI levels. In addition, we did not set a minimum weight gain for those with a BMI greater than 35 kg/m2 at the commencement of pregnancy.26–28 In addition to our primary analysis we consider the following secondary hypotheses: Infant birth weight, corrected for maternal age, parity, and gestation, will be positively related to maternal weight gain throughout pregnancy. Active management of the adjustable gastric band will enable maternal weight outcomes that more closely follow those recommended by the Institute of Medicine when compared with women who attended infrequently or have not been actively managed. The incidence of the more common complications of pregnancy related to obesity will be lower in those who have lost weight and more closely reflect those of the general community. Adequate maternal weight gain and multivitamin supplementation will prevent macro and micronutrient deficiencies and provide birth weights consistent with community normal values.
The inclusion of at least 75 cases and controls within the analysis allows an 80% likelihood of detecting 1) mean difference in birth weight between the 2 groups of 300 g and 2) a large two-thirds reduction in the incidence of pregnancy-induced hypertension, gestational diabetes, and preeclampsia, with P < .05 for both (1) and (2). Data were described using mean ± standard deviation for normally distributed variables (assessed visually and for skewness and kurtosis ≥ 2 and < 2 for both) and median ± interquartile range for other variables and percentages for some ordinal groups. Differences between groups were tested by using the Student t test, analysis of variance, and χ2 test, as appropriate. Pearson correlation coefficients and linear regression analysis, with forward and backward modeling to assess independence of predictors of birth weight, were used. All analysis was performed with SPSS 12 for Windows (SPSS Incorporated, Chicago, IL).
The characteristics of the 79 women for whom we report the results of their first pregnancy extending beyond 20 weeks of gestation following band placement are shown in Table 1. All women were white, of European origin, and all pregnancies singleton. The mean weight loss before pregnancy was 28.3 ± 14.0 (range 3–72) kg. Births were a median of 20 (interquartile range 26) months after band placement. Women were seen at least once during pregnancy in 86% of the births reported.
The mean maternal weight gain was 9.6 ± 9.0 kg, which was significantly lower than those of the penultimate pre-LAGB pregnancies (n = 40) and the severely obese matched controls (n = 79) (P < .001 for both). Mean maternal weight gains for the penultimate LAGB pregnancies and the severely obese control were both above recommended gestational weight gains (Table 1). For the 40 women with paired penultimate and first post-LAGB placement pregnancies, there was a significantly lower maternal weight gain during the post-LAGB pregnancy, but birth weights were not different (not shown).
The incidence of pregnancy-induced hypertension and gestational diabetes were lower in the first LAGB pregnancies than in the penultimate pre-LAGB pregnancies and those of the severely obese matched controls, and consistent with the community prevalence.12,29,30 The lower incidence of pregnancy-induced hypertension was statistically significant when compared with the penultimate pre-LAGB pregnancies (P < .001) and those of the matched severely obese women (P < .001). The incidence of gestational diabetes was consistent with the community incidence and lower than the severely obese controls (P = .02) but was not statistically significantly lower when compared with penultimate pre-LAGB pregnancies (P = .12) (Table 1). Preeclampsia was reported in 11 of the 40 (28%) penultimate pregnancies, 20 of the 79 (25%) matched severely obese controls, and 4 of 79 (5%) first post-LAGB pregnancies (P < .001, for both). Of 14 women with hypertension diagnosed before LAGB surgery, only 3 women had hypertension present any problem during pregnancy: 1 case of preeclampsia and 2 cases of mild hypertension late in pregnancy. Two of these women and only one other used antihypertensive medications during pregnancy. Thus, 10 (71%) women with a history of hypertension were normotensive without medication and did not redevelop problems with hypertension throughout the first post-LAGB pregnancy.
The outcomes of 79 consecutive first births after LAGB surgery are shown in Table 2. The mean birth weight was the same as the mean birth weight in the Australian community. The percentage of infants of low birth weight, high birth weight, and preterm births were consistent with current community values. There was one stillbirth of a 3,200 g infant delivered at 41 weeks and one congenital abnormality, a case of duodenal atresia.
There were 5 (6.3%) infants with a low birth weight (≤ 2500 g). Of these, 1 infant was born at 35 weeks of gestation, and 2 infants were from pregnancies complicated by preeclampsia. In one case the band may have contributed to low birth weight. This 41-year-old primigravid woman had episodic vomiting throughout pregnancy, despite having all the fluid removed at 8 weeks of gestation. She had a cesarean delivery at 39 weeks and delivered a baby with a birth weight of 1,920 g. She had lost 80% of excess weight before the pregnancy and lost 4 kg throughout the pregnancy.
There were 9 (13%) infants with a birth weight greater than 4,000 g. Two were to mothers with a history of type 2 diabetes, which had remitted with weight loss before pregnancy. These 2 women developed gestational diabetes during their pregnancies.
We hypothesized a relationship between maternal weight change and birth weight after correcting for confounders. There was no significant relationship between birth weight and maternal BMI at the start of pregnancy, age, parity, or gender of the infant. Using a linear regression model with birth weight the dependent variable, 2 independent factors influenced birth weight. Gestation length provided the most important contribution to variance (r = 0.4, P < .001), and after controlling for gestational age, maternal weight change was also significant (r = 0.22, P = .03). For 52 pregnancies, the maternal weight gain was 0–15 kg, whereas 11 had weight loss and 16 had a gain of greater than 15 kg. Mean birth weights were 3,410 g, 3,045 g, and 3,573 g, respectively. There was no relationship between the maternal weight loss before pregnancy and birth weight.
Women who were not seen early during the pregnancy (n = 16) were more likely to have less than the recommended maternal weight gain during pregnancy (P = .009; Fig. 1). Women seen throughout the pregnancy had the most favorable maternal weight outcomes. Those seen throughout had a mean weight gain of 9.2 ± 8.4 kg, whereas those not seen at all or not seen during the first trimester of the pregnancy had a weight gain of 4.8 ± 9.0 kg, and those seen in the first trimester, but not later during the pregnancy, had a weight gain of 13.0 ± 9.7 kg (analysis of variance, P = .027).
Five women who developed gestational diabetes during pregnancy had a mean weight gain of 13.4 kg and had infants with a significantly higher birth weight: 3,926 ± 436 g compared with 3,361 ± 535 g (P = .024) for the remainder. Two of these 5 women had previously had non–insulin-dependent diabetes mellitus but were in remission after surgically induced weight loss before pregnancy. Another 3 women with non–insulin-dependent diabetes mellitus before LAGB surgery went into remission with weight loss and did not develop gestational diabetes during the post-LAGB pregnancy.31
Compliance with multivitamin supplementation was good, with 84% of women reporting daily intake. One of the 79 women was anemic (hemoglobin < 110 g/L) at pre-LAGB placement and another one at the annual follow-up nearest to delivery. Six women had low iron levels presurgery and 7 women at closest annual follow-up to their child's birth. There were no pregnancies where anemia presented a clinical problem. There was no difference in mean folate, vitamin B12, and homocysteine concentrations between pre-LAGB and the annual visit closest to delivery, and there was a small, but significant, rise in mean iron concentration at the follow-up visit (data not shown). No patients reported any specific nutritional problems during pregnancy. There were no low folate or vitamin B12 concentrations at follow-up, but 8 women had high homocysteine (> 15 μmol/L) concentrations, compared with only 1 before surgery. Five of these 8 women were from 13 (16%) women who were not taking multivitamin supplements regularly and only 3 from the 66 (84%) women taking regular supplements (χ2, P = .012).
There was no change in plasma protein levels with weight loss. Mean total plasma protein and albumin concentrations were 71.5 ± 3.5 g/L and 42.9 ± 2.7 g/L before surgery, and 72.0 ± 4.2 g/L and 42.2 ± 2.7 g/L at annual review closest to delivery, respectively. There were no albumin concentrations below 35 g/L pre-LAGB or at follow-up, and we have not experienced any case of low plasma albumin levels following LAGB surgery.
There were 20 pregnancies where conception occurred within 1 year of band placement. Maternal weight gain for the pregnancy was significantly lower for these early post-LAGB pregnancies (2.3 ± 9.5 kg compared with 11.7 ± 8.4 kg, P < .001), but birth weights were similar (3,377 ± 735 g compared with 3,402 ± 469 g, P = .86). There were no statistical differences in any of the pregnancy complications, including gestational diabetes, gestational hypertension, and cesarean delivery rate, and no increase in preterm or low birth weight deliveries. One unexpected finding in the early postbanding group was a preponderance of male births. There were 17 male and 3 female infants born to those conceiving within 1 year of LAGB placement, whereas deliveries after 1 year were 26 male and 33 female (P = .001).
Laparoscopic adjustable gastric banding placement is known to be associated with late problems of prolapse (or slippage), erosion of the band into the stomach, and breaks in the tubing passing to the access port.24,32 None of these events occurred during the pregnancies followed. However, one woman developed symptomatic gallstones and had an episode of acute pancreatitis, and one woman had persistent vomiting despite removal of the fluid from the band. Two complained of tenderness over the reservoir site during late pregnancy. The majority of women commented very favorably regarding impact of weight loss before pregnancy and the LAGB management during pregnancy.
In this series of 79 first post-LAGB placement births, we have demonstrated results that are entirely consistent with community values for all measured outcomes. The incidence of the pregnancy complications, gestational hypertension, and gestational diabetes more closely reflected those of the general community than those seen in severely obese controls. In addition, we have demonstrated better control of maternal weight change during pregnancy if women were seen regularly during the pregnancy and had the band adjusted when necessary. Favorable maternal nutritional status was maintained if the advised supplementation was taken.
We have shown a significant positive relationship between maternal weight change and birth weight after controlling for gestational age. This may be important because fetal over- or undernutrition may adversely influence metabolic programming in individuals at considerable genetic risk of obesity and related disorders.33 Although we have found mean birth weights to be the same as those of the background population, this has not been the case for studies involving other forms of bariatric surgery.
Previous reports concerning pregnancy after bariatric surgery have been mixed, and the type of procedure may be important. Following the now-abandoned jejuno-ileal bypass, there were small series reports of fetal abnormalities, small for gestational age, and premature births.20,21 Two reports detailing pregnancy and childbirth after the currently used malabsorptive procedures, biliopancreatic diversion or the duodenal switch variant,19,22 have reported mean birth weights well below the mean expected for the respective populations, suggesting that after these malabsorptive procedures there is a state of general intrauterine nutritional deficiency that may increase the risk of adverse fetal programming.33 There is little published data regarding the birth weight outcomes of infants born to women following gastric bypass, but a report from Brazil suggests that nutritional deficiency and low birth weight are common (Matielli et al, 2004).10,34
Specific micronutrient deficiencies may also be of concern after bariatric surgery. Weight loss, however achieved, is associated with raised plasma homocysteine concentrations, and higher levels of vitamin B12 and folate are required to maintain favorably low levels.35 Fortunately, LAGB surgery does not predispose to deficiency if intake is adequate because there is no gastrointestinal diversion. However, we have demonstrated that, in women not adequately supplementing with multivitamins and folic acid, the risk of raised homocysteine levels, and therefore neural tube defects, is increased. The risk of specific nutritional deficiencies are greater after diversionary procedures such as Roux-en-Y gastric bypass, where impairment of iron, vitamin B12, and calcium absorption are predictable, and biliopancreatic diversion, where a broader range of deficiencies is likely. We urge all women to adequately supplement folate and vitamin B12 after all bariatric surgery, and additional supplements are necessary after diversionary procedures.36,37
The findings of the present study are consistent with 4 small observational reports of pregnancy after LAGB surgery, including an early report of our series, indicating that maternal weight gain and birth weights are normal with a reduction in pregnancy-induced hypertension and gestational diabetes.12,38–40 In the present study, we have demonstrated the nutritional safety and the benefits of adjustability provided by LAGB surgery.
There are several weaknesses in the present study. Although we report on 79 first LAGB births, there are insufficient numbers to be able to detect problems that are relatively uncommon. We have also limited our collection of data on births to the neonatal period so we may not be aware of concerns regarding growth and nutrition that present later. Our nutritional and metabolic assessments were carried out annually as close as possible to the anniversary of LAGB surgery. We have not surveyed at a particular time in relation to the pregnancy, and subtle abnormalities during the pregnancy itself may not have been detected.
The preponderance of male births in those conceiving within 12 months of surgery is potentially interesting because this would have been the time of maximal weight loss. Long-term studies from Finland have described an increase in male births during both World War I and II.41 It would be interesting to speculate that, at a time of maternal negative energy balance, male pregnancies may be more likely.
Relatively small series, such as the present study, can only provide general reassurance that birth outcomes are in line with community levels and expectations. Certainly it is reassuring that, in all areas measured, outcomes after LAGB follow this encouraging pattern. To further study the potential impact of bariatric surgery on a woman's subsequent pregnancies, larger numbers would be needed and the offspring should be studied prospectively throughout their years of growth and development.
In conclusion, pregnancy and birth outcomes for women who have undergone LAGB surgery are consistent with community normal values, rather than those of severely obese women, reflecting its safety and applicability for women of childbearing years. The adjustability of the band is an appealing feature because it provides an ability to adapt the surgery to the needs of the pregnancy. Active management of the band and advice regarding nutritional supplementation enhances outcomes. A multidisciplinary approach involving cooperation between the bariatric surgeon and the obstetrician is advised.
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