The effect of gestational weight gain on perinatal outcomes among Chinese twin gestations based on Institute of Medicine guidelines

Twin gestations, different from singleton gestations, are associated with significant adverse perinatal outcomes, such as fetal growth restriction, intrauterine fetal death, preterm birth and perinatal mortality [1, 2]. To date, many efforts have been developed in identifying factors which may jeopardize maternal and fetal health.

As reported in previous studies, gestational weight gain (GWG) has implications for the health of mother and child. Women with insufficient weight gain during gestation were observed to be associated with lower birth weight whereas those with excessive weight gain were associated with macrosomia, postpartum weight retention and offspring obesity [3‐6]. The demand for nutrition supply, theoretically, should be higher for twin pregnancies than singletons [7]. Guidelines of GWG for singleton pregnancies were well established, whereas those for twin pregnancies were undeveloped. In 2009, the US institute of Medicine (IOM) released revised recommendations on maternal GWG for twin gestations [8]. These recommendations represented the interquartile range of weight gain among women who deliver twins with a mean weight of ≥2500 g at term (37–42 weeks of gestation) and were referred as provisional.

One of the most important questions comes to their validity since there are a significant proportion of twins born before 37 weeks of gestation and other perinatal outcomes to be assessed. Multiple researches from western countries had attempted to examine these guidelines on various perinatal outcomes among twin pregnancies, however, these studies yielded inconsistent results possibly due to several limitations, such as small sample size, exclusion of monochorionic or pre-term pregnancies [9‐13]. Besides, as the Chinese adult body mass index (BMI) category standards for normal weight, overweight and obesity were lower than WHO standards, it is not clear whether these guidelines could apply to Chinese women with twin gestations.

In the view of the ever-increasing incidence of twin births in China [14], it is imperative to provide more evidence regarding this issue, in order to optimize maternal and fetal outcomes. Therefore, this study aimed to elucidate the association between maternal GWG and a series of perinatal outcomes, based on 2009 IOM recommendations.

There were 1308 women with twin pregnancy admitted to maternal and child health hospital in Foshan, China, during the study period. Six-hundred and forty-five women with 1290 infants were finally included for analysis after excluding records of pregnancies which did not meet our inclusion criteria (n = 552), and underweight women (n = 111) (Fig. 1).

This study sought to evaluate the associations between gestational weight gain and perinatal outcomes among Chinese twin gestations, according to 2009 IOM guidelines. We found that, on one hand, weight gain below the IOM guidelines was associated with significant increases in spontaneous preterm birth < 37 and < 35 weeks as well as anemia; on the other hand, weight gain above the guidelines was associated with higher rates of gestational hypertensive disorder, pre-eclampsia and fetal macrosomia and lower rates of birth weight < 2500 g and < 1500 g.

Preterm birth, the primary outcomes in the current study, predominates in adverse outcomes among twin pregnancies. Identifying indicators of PTB would be beneficial for optimization of neonatal outcomes. We found none of the association between maternal weight gain and PTB < 37, < 35 or < 32 weeks. The increased risks of spontaneous PTB < 37 and < 35 weeks, nevertheless, were found among women with weight gain below the recommended level, compared to those with weight gain within the recommended range. These results were similar with the previous findings of González-Quintero et al. They reported women with twin gestations who had weight gain at or above guidelines, could had a significantly lower rate of spontaneous preterm birth than those who had weight gain below the guidelines [21]. Rather than combining women with weight gain at or above the guidelines as a reference, we did only use normal weight gain as the reference, compared to previous studies [21, 22]. Thus, our results may provide more detailed information on the association between maternal weight gain and spontaneous preterm birth. Algeri et al. [11] reported that excessive GWG is associated with higher risk of spontaneous preterm delivery < 37 weeks as well. This finding is less valid due to the limited number of women with inadequate weight gain. The mechanism how maternal weight gain influence the spontaneous preterm birth is uncertain. Similar incidence of PPROM was observed between three GWG categories in our results, which was supported by a former study [9]. In addition, an increased risk of gestational anemia was observed among women with inadequate weight gain. Recently Pécheux et al. [26] speculated that strengthening uterine contractions may occur by a surge of stress hormones, induced by placenta dysfunction in the anemia status. Based on our results, we stressed the necessity of sufficient weight gain among women with twin gestations.

The association between weight gain above recommended GWG and gestational hypertensive disorder reported in our study was endorsed by those of previous studies [10, 11, 27]. Interestingly, when gestational hypertension and pre-eclampsia were analyzed separately, we found an association between excessive weight gain and pre-eclampsia but not gestational hypertension. Existing evidence was controversial on the correlation between maternal weight gain and these vascular complications during twin pregnancy. Some studies reported nonsignificant difference of pre-eclampsia among different GWG categories [9, 12, 28]. The study of Lal et al. [20] showed that the association between preeclampsia and excessive GWG only found in the normal-weight/underweight group but not in overweight and obese groups. The conflicting results, which could be due to the heterogeneity of the study population and sample size, made it difficult to draw a conclusion on whether these weight gain thresholds may be beneficial in decreasing the risk of these complications. Kosinska-Kaczynska et al. [9] suggested that IOM guidelines could be unsuitable for analyzing pre-eclampsia among twin pregnancies, as they found no overlaps between the GWG ratio range associated with pre-eclampsia and specific IOM-recommended GWG value. Our results may imply the reverse causality between excessive weight gain and pre-eclampsia, since women who have pre-eclampsia develop edema more frequently than those who solely have gestational hypertension. Further prospective studies considering edema as a covariate are warranted to elucidate the causality between weight gain and pregnancy-related hypertensive disorder.

A few of previous studies evaluated the association between maternal weight gain and birth weight without including the length of gestation or chorionicity as confounders [20, 21, 27‐29]. We thought that these variables play significant roles in fetal growth among twins thus we adjusted these confounders for neonatal outcomes. We found no associations between weight gain below IOM guidelines and neonatal outcomes although higher rates of birth weight < 2500 g and SGA were observed in the inadequate weight gain group. In this study, maternal BMI was categorized based on Chinese adult standard, different from those in previous studies conducted in western countries [9, 13, 21, 22]. These results raised a question whether the lower limit of IOM recommended weight gain has enough sensitivity to detect the SGA twins among Chinese pregnant women, which deserves further study. Alternatively, the lack of significant association could be partly attributed to the smaller number of women gaining weight inadequately than other groups. Large studies suggested that GWG below the IOM recommendations was associated with an increased risk of SGA twins [27, 29]. On the opposite, we found that weight gain above the recommended GWG was associated with a higher risk of LGA, which is consistent with the previous finding of Ozcan et al. [27]. In addition, this GWG category also decreased the risk of birth weight < 2500 g and < 1500 g.

As gestational weight gain is a satisfying index for evaluating maternal nutrition and a modifiable factor during pregnancy, our results are of clinical significance for patients and clinicians to achieve improved pregnancy outcomes among twin gestations. IOM recommendations could provide a good reference in managing weight gain for Chinese women with twin pregnancies, despite of difference in BMI category between Chinese standard and WHO standard. Furthermore, an intervention on maternal nutrition and weight gain could help to reduce the risk of the above-mentioned adverse outcomes.

Since the 2009 IOM recommendations are for the general twins, we included both monochorionic diamniotic and dichorionic diamniotic twins. Therefore, our study possesses more profound significance than those which only included dichorionic twins [30, 31] or did not have information on chorionicity [27, 29]. In addition, different from majority of prior studies [10, 16, 20, 28], one merit of this study was to apply GEE models to assess neonatal outcomes, which could yield more robust and valid effect estimates and confidence intervals with the correlation in a twin set being controlled. Nevertheless, we also acknowledged some limitations in our study. Firstly, the inherent potential for bias unable to be avoided in the retrospective design may impede the interpretation of the causal relationship between maternal weight gain and pregnancy outcomes. Secondly, due to the limited number in twin pregnancies with weight gain below recommended GWG group, some outcomes need more assessment in further studies. Thirdly, since pre-pregnancy weight was not available in the medical charts, we used the measured weight at the first prenatal visit before 14 weeks to calculate the maternal BMI and maternal weight gain. This value has some limitations, despite its satisfying correlation with pre-pregnancy weight [32].

Weight gain below the provisional guidelines for twins is associated twin spontaneous preterm birth while weight gain above the guidelines is associated with gestational hypertensive disorder, pre-eclampsia and LGA. Further prospective research is warranted to confirm the causality of these associations.