2Josué de Castro Nutrition’s Institute, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil.Edifício do Centro de Ciências da Saúde, Bloco J - Av. Carlos Chagas Filho, 373 - Cidade Universitária, Rio de Janeiro - RJ, CODE: 21941-902
3Maternity School of Hospital Federal University of Rio de Janeiro, Rio de Janeiro, Brazil.R. Das Laranjeiras, 180 - Laranjeiras, Rio de Janeiro - RJ, CODE: 22240-000
Methods: A retrospective cross-sectional study of records of newborn twins from adult and adolescent pregnancies. Twins were divided into two groups, Twin 1, the first one delivered, and Twin 2, the second. The association between gestational age at birth and neonatal characteristics were analysed using Chi Square and Fisher’s exact tests and associations were considered significant when p-values were ≤ 0.05.
Results: We evaluated 218 infants with a mean gestational age of 35.7 weeks at birth. The groups twin 1 and 2 showed, respectively, average weight at birth of 2343.9 grams (SD = 627.3) and 2267.6 grams (SD = 608.2). Most twins of group 1 presented appropriate birth weight (n = 53; 48.6%) and were classified as appropriate for gestational age (n = 88; 80.7%). The group twin 2 had, mostly, low birth weight (n = 55; 50.5%), and were classified as appropriate for gestational age (n = 93; 85.3%). Prematurity was relevant to the development of postnatal complications (twin 1 - p = 0.002; twin 2 - p = 0.001) and low birth weight (twins 1 - p = 0.000; twins 2 - p = 0.000) for both groups.
Conclusion: Prematurity was an important risk factor for the development of postnatal metabolic and respiratory complications and low birth weight for both groups.
Keywords: Twin pregnancy; Nutritional Epidemiology; Prenatal care; prenatal nutrition; Prematurity
The twins have changes of different magnitudes in childhood, compared to single newborns, with a strong tendency to be born with low weight and gestational age [6]. According to the survey “Nasser no Brazil” the rate of neonatal mortality in twin pregnancies corresponds to 52.2 per 1,000 live births which represents a 5 times greater risk for neonatal mortality multiple foetuses compared to single [7].
The fatal development of twins is virtually identical to the single foetuses up to 32 weeks of pregnancy and then there is a slowdown in growth and may result in high rates of intrauterine growth restriction (IUGR) in term pregnancies [8-9]. About 10% of monozygotic twins (derived from individuals of a fertilized egg) have a weight of disagreement at birth more than 10% and higher expectation of being classified as small for gestational age (SGA) [9, 10].
The low weight at birth in twin research, complication capable of raising birth rates Caesarean, prematurity and disabling accommodation postpartum whole is rarely described in the literature. In Porto Alegre, Brazil, a rate of 24.7% of low birth weight in twin pregnancies in 11 years of research has demonstrated [11].
Some of multiple pregnancy associated changes represent high maternal and fatal risk highlighting the fatal anomaly, intrauterine death, premature rupture of membranes and discordant preterm delivery, conjoined twins, twin to twin transfusion syndrome and TRAP sequence (Twin Reversed Arterial Perfusion Sequence) or twin acardiac [1].
Preterm birth in twin pregnancy has an average occurrence rate of 30% to 50% being more prevalent in monochorionic pregnancies (present only one placenta) than dichorionic (two different placentas) [12]. The mean gestational age at birth to the twins is three weeks shorter than for single gestation and birth weight will depend on the time of pregnancy is significantly lower for twins [13]. In addition to prematurity, monochorionicity is one of the most important factors responsible for morbidity and mortality in twin pregnancies [14].
The reduction in preterm birth rates is one of the main goals of prenatal care in twin pregnancies [15]. However, when considering the reduction of fatal mortality considering birth weight and gestational age, are as ideal references 2500g to 2800g and 36 to 37 weeks. Population studies show that perinatal mortality increased from 38 weeks gestation, being prudent to anticipate the interruption of delivery in these pregnancies [16- 17].
Knowing the neonatal anthropometric and clinical conditions of the twin structure will enable the pre care and post-natal and promote fatal development. This study aims to evaluate the characteristics of newborn twin pregnant women assisted in a public hospital in Rio de Janeiro, analysing gestational age and birth weight.
The survey was conducted at a maternity hospital located in the south of the city of Rio de Janeiro, health unit has multiservice, specializes in services to multiple pregnancies.
Inclusion criteria were twin neonates born to adolescent and adult pregnant women, double pregnancy (two foetuses), mono or dizygotic, mono or dichorionic, mono or dianoetic accompanied prenatal and delivery in the study hospital. They excluded pregnant women who have undergone abortion process or intrauterine fatal death during prenatal care and conjoined twins.
In the period studied were met in 6442 maternity mothers with single or twin pregnancies, being selected 151 medical records of twin pregnant women and their newborns, which were analyzed 109 who met the inclusion criteria for the study. They were excluded from the study, 42 records, for pregnant women did not undergo prenatal and / or delivery in maternity studied, because they are triplet pregnancies and due to the occurrence of discordant intrauterine death or Vanish Twin in different gestational ages. They selected 218 twins divided into two groups, called T1 as the first born and the last T2.
The collection of medical record data was performed by trained staff and recording information of pregnant women occurred in standardized protocol containing maternal information and newborns (sociodemographic, clinical, obstetrical and gynaecological, prenatal care, childbirth and postpartum , anthropometric and nutritional).
The dependent variables were: gestational age at birth according to ultrasonography (premature, if < 37 weeks; term, if > 37 weeks) and weight rating birth measured continuously and categorically (normal weight, if > 2500g; low weight is < 2500 g, very low birth weight if < 1500 g, extremely low weight if < 1000g).
Independent variables related to foetuses were studied, such as: classification of newborns according to gestational age at birth (extreme immaturity if < 28 weeks; preterm if < 37 weeks, the term is between 37 to 42 weeks), weight (grams), length (cm) and head circumference at birth (cm); Apgar 1 and 5 minutes (< 7, low vitality at birth,> 7, adequate vitality at birth) [18-20]; somatic Capurro (weeks); classification of weight according to gestational age [21] (small for gestational age - SGA if weight < 10th percentile; appropriate for gestational age - AGA, if weight is between 10 and 90 percentiles, large for gestational age - LGA if weight> 90th percentile) [22]; presence of congenital anomalies; site postpartum hospital stay (rooming or Neonatal Intensive Care Unit - NICU); reason for hospitalization in the NICU; type of food during hospitalization (zero diet, breast milk exclusively, only infant formula, breast milk associated with infant formula, total parenteral nutrition or exclusively associated with infant formula); fatal complications in the first seven days of life (neither, metabolic, respiratory, malformations, infectious, early neonatal death - when this occurs within 7 days after delivery); length of stay; weight, length and head circumference at discharge.
Exploratory data analysis was performed with a description of the sample with estimates of mean and standard deviation (SD) for continuous variables and proportions for categorical variables. The association between gestational age at birth and neonatal characteristics were analyzed using Chi Square and Fisher’s Exact tests were considered significant p values less than 0.05. Statistical analysis was performed with SPSS (Statistical Package for Social Sciences) software for Windows version 21.0.
The T1 and T2 presented, respectively, average weight at birth of 2343.9g (SD = 627.3) and 2267.6g (SD = 608.2), length of 44.6 cm (SD = 4, 1) and 44.6cm (SD = 4.0), head circumference of 32.4cm (SD = 2.7) and 32.1cm (SD = 2.6) and mean gestational age by method Capurro of 36.0 weeks (SD = 3.0) and 36.1 weeks (SD = 2.7).
The average length of hospital stay for the T1 was 13 days (SD = 21.8) ranging from 1-105 days and the average high weight was higher than the birth weight, corresponding to 2429.5g (SD = 452.3). T2 remained on average 12.7 days (SD = 22.1) admitted, ranging from 2-117 days and mean weight at discharge equal to 2336.8g (SD = 420.3). Information about the head circumference and length at discharge were underreported or were not available in the medical records of all twins. Information regarding the T1 showed that they had an average head circumference of 33,2cm (n = 10, SD = 2.7) and the G2 was 32,1cm (n = 10, SD = 2.7) at the time of hospital.
The early neonatal death was similar in T1 (n = 2; 1.8%) and T2 (n = 2, 1.8%) as described in Table 1. Most T1 was male (n = 56; 51.9%) had adequate birth weight (n = 53; 48.6%) showed good vitality at birth according to the Apgar at 1 (n = 94; 86.2%) and 5 minutes (n = 106; 97.2%) were classified as AGA (n = 88; 80.7%) were in accommodation postpartum set (n = 58; 53.2%) and were fed composed of infant formula and breast milk (n = 73; 67.0%).
Most T2 was woman (n = 56; 51.4%) had low birth weight (n = 55; 50.5%), good vitality at birth according to the Apgar score at 1 (n = 106; 97.2%) and 5 minutes (n = 106; 97.2%) were classified as AGA (n = 93; 85.3%) remained in the accommodation postpartum set (n = 61, 56, 0%) and were fed a combination of breast milk and infant formula (n = 76; 69.7%) (Table 1).
Characteristics of twins |
T1 |
T2 |
||
n |
% |
n |
% |
|
Condition at birth |
||||
Born alive |
107 |
98,2 |
107 |
98,2 |
Stillbirth |
2 |
1,8 |
2 |
1,8 |
Total |
109 |
100 |
109 |
100 |
Classification according to gestational age at birth |
||||
Term |
52 |
47,7 |
52 |
47,7 |
Preterm |
52 |
47,7 |
52 |
47,7 |
Immaturity extreme |
5 |
4,6 |
5 |
4,6 |
Total |
109 |
100 |
109 |
100 |
Gender |
||||
Male |
56 |
51,9 |
53 |
48,6 |
Female |
52 |
48,1 |
56 |
51,4 |
Total |
108 |
100 |
109 |
100 |
Birth weight classification |
||||
Extremely low birth weight |
6 |
5,5 |
6 |
5,5 |
Very low birth weight |
4 |
3,7 |
7 |
6,4 |
Low birth weight |
46 |
42,2 |
55 |
50,5 |
Normal weight |
53 |
48,6 |
41 |
37,6 |
Total |
109 |
100 |
109 |
100 |
Apgar 1º minute |
||||
< 7 |
15 |
13,8 |
3 |
2,8 |
> 7 |
94 |
86,2 |
106 |
97,2 |
Total |
109 |
100 |
109 |
100 |
Apgar 5º minute |
||||
< 7 |
3 |
2,8 |
3 |
2,8 |
> 7 |
106 |
97,2 |
106 |
97,2 |
Total |
109 |
100 |
109 |
100 |
Relationship weight / gestational age |
||||
<p10 |
17 |
15,6 |
16 |
14,7 |
p10-p90 |
88 |
80,7 |
93 |
85,3 |
>p90 |
4 |
3,7 |
0 |
0,0 |
Total |
109 |
100 |
109 |
100 |
Place of postpartum hospitalization |
||||
Rooming-in |
58 |
53,2 |
61 |
56,0 |
NICU |
51 |
46,8 |
48 |
44,0 |
Total |
109 |
100 |
109 |
100 |
Given the high prevalence of prematurely born foetuses (47.7%), neonatal characteristics were described as gestational age at birth of T1 and T2 (Tables 2 and 3).
Neonatal characteristics of T1 |
Gestational age at birth |
Total |
p |
|
< 37 weeks |
> 37 weeks |
|||
Birth weight classification |
||||
Extremely low birth weight |
6 |
0 |
6 |
0,000 |
Very low birth weight |
4 |
0 |
4 |
|
Low birth weight |
31 |
15 |
46 |
|
Normal weight |
16 |
37 |
53 |
|
Total |
57 |
52 |
109 |
|
Apgar 1º minute |
||||
< 7 |
11 |
2 |
13 |
0,017 |
> 7 |
46 |
50 |
96 |
|
Total |
57 |
52 |
109 |
|
Apgar 5º minute |
||||
< 7 |
3 |
0 |
3 |
0,245 |
> 7 |
54 |
52 |
106 |
|
Total |
57 |
52 |
109 |
|
Relationship weight / gestational age |
||||
<p10 |
11 |
6 |
17 |
0,387 |
p10 - p90 |
45 |
43 |
88 |
|
> p90 |
1 |
3 |
4 |
|
Total |
57 |
52 |
109 |
|
Place of postpartum hospitalization |
||||
Rooming-in |
14 |
44 |
58 |
0,000 |
NICU |
43 |
8 |
51 |
|
Total |
57 |
52 |
109 |
|
Tipo de alimentação na internação |
||||
Neither |
2 |
0 |
2 |
0,029 |
Breastmilk |
6 |
13 |
19 |
|
Infant formula |
4 |
2 |
6 |
|
TNP |
1 |
0 |
1 |
|
Breast Milk + Infant formula |
36 |
37 |
73 |
|
Infant formula + TPN |
3 |
0 |
3 |
|
Breast Milk + Infant formula + TPN |
5 |
0 |
5 |
|
Total |
57 |
52 |
109 |
|
Presence of neonatal complications |
||||
No |
8 |
21 |
29 |
0,002 |
Yes |
49 |
31 |
80 |
|
Total |
57 |
52 |
109 |
|
Neonatal characteristics of T2 |
Gestational age at birth |
Total |
p |
|
< 37 semanas |
> 37 semanas |
|||
Birth weight classification |
||||
Extremely low birth weight |
6 |
0 |
6 |
0,000* |
Very low birth weight |
7 |
0 |
7 |
|
Low birth weight |
39 |
16 |
55 |
|
Normal weight |
5 |
36 |
41 |
|
Total |
57 |
52 |
109 |
|
Apgar 1º minute |
||||
< 7 |
14 |
1 |
15 |
0,001* |
> 7 |
43 |
51 |
94 |
|
Total |
57 |
52 |
109 |
|
Apgar 5º minute |
||||
< 7 |
3 |
0 |
3 |
0,245 |
> 7 |
54 |
52 |
106 |
|
Total |
57 |
52 |
109 |
|
Relationship weight / gestational age |
||||
<p10 |
10 |
6 |
16 |
0,086 |
p10 - p90 |
47 |
46 |
93 |
|
Total |
57 |
52 |
109 |
|
Place of postpartum hospitalization |
||||
Rooming-in |
13 |
48 |
61 |
0,000 |
NICU |
44 |
4 |
48 |
|
Total |
57 |
52 |
109 |
|
Feed type in hospital |
||||
Nenhuma |
2 |
0 |
0 |
0,001 |
Breastmilk |
3 |
13 |
16 |
|
Infant formula |
5 |
1 |
6 |
|
Breast Milk + Infant formula |
38 |
38 |
76 |
|
Infant formula + TPN |
2 |
0 |
0 |
|
Breast Milk + Infant formula + TPN |
7 |
0 |
7 |
|
Total |
57 |
52 |
109 |
|
Presence of neonatal complications |
||||
No |
8 |
30 |
38 |
0,000 |
Yes |
49 |
22 |
71 |
|
Total |
57 |
52 |
109 |
|
The first minute Apgar score was satisfactory to both, however, observed a higher number of premature twins with index less than 7, showing a low fatal birth for T1 (p = 0.017) and T2 (p = 0.001). The Apgar 5 minutes no difference to T1 (p = 0.245) T2 (p = 0.245) were born prematurely or not.
The analysis of the gestational age at birth and weight rating for gestational age showed no significant difference with respect to T1 (p = 0.387) and T2 (p = 0.086).
According to the site postpartum hospital stay, it is observed that more premature infants were allocated in the neonatal NICU after delivery compared to those who were born with adequate gestational age, both the T1 (p = 0.000) , as for T2 (p = 0.000).
During the hospital stay, it is observed that only premature neonates receiving TPN isolated (T1) or associated with infant formula and / or breast milk (T1 and T2), and it was identified that two premature neonates were zero diet during admission evolving to death. The breast milk supply alone was higher for the group of infants with adequate gestational age T1 (p = 0.029) and T2 (p = 0.001).
Neonatal complications were identified in greater numbers in T1 (p = 0.002) and T2 (p = 0.000) with gestational age at birth less than 37 weeks, unlike those with adequate gestational age.
Prematurity and the average maternal age were relevant factors in this study and may represent adverse perinatal outcomes. Research in Mexico [24], which analyzed the determinants of birth weight in 244 double pregnancies, found average maternal age in adult of 28 years (SD = 7.0) and gestational age at birth 35 weeks , similar to those found in this study. Doss et al. [25] , showed that the optimal gestational age associated with lower Perinatal mortality is more than 38 weeks pregnancy and births less than 36 weeks gestation, the risk of infectious complications, respiratory and admission to NICU rise by 4 to 6 times. Garner and Oliveira de Barros [26], in a study with women from multiple pregnancies by assisted reproduction techniques found mean maternal age of 33.9 years and 64.9% of births before 36 weeks.
Most deliveries were caesarean (92.7%) in the sample, far superior results to those found in national and international studies. American survey of 377 twin pregnancies found 52.5% of spontaneous births and 47.5% caesarean [25], different from that found in this study. However, in Rio de Janeiro, Brazil, study of 104 twin pregnancies [27] showed 69% of surgical deliveries. In São Paulo, Brazil, study of 249 twin pregnancies revealed that 84.8% were caesarean [29], approaching the results found in this study. Caesarean section is recommended in monoamniotic pregnancies when the fetes are not in cephalic presentation and if there is high risk for the combination of abdominal and vaginal delivery [29] may represent maternal and fatal protection factor [30].
Much of the concepts were classified as low birth weight, being more frequent for G2 than for G1. In Maringa, Paraná, Brazil, Cardim and colleagues [31] found low birth weight in 64% of the sample. Maximiano [27] showed a higher frequency of low birth weight in group 2 (60.6%), a result similar to that found in this study. The low birth weight may be related to prematurity, maternal complications and gestational weight gain and should be a relevant factor in neonatal care.
Twins are at greater risk of developing intrauterine growth deviations compared to single, very often characterized as IUGR [32]. Understanding this dynamic depends on weight ratings considering the gestational age according to the recommendations for the twin foetuses. In the present study, the majority of the twin 1 and 2 was classified as AGA and approximately 15% were SGA. We also observed that 3.7% were classified as T1 LGA, while no T2 reached this classification.
The vitality at birth can determine the neonatal development and is related to the hospital stay and institutional costs. Most twin 1 and 2 showed good fatal according to Apgar first and fifth minutes. A similar result was found by Maximiano [27] also noted that among the twin 1 and 2, the first present with higher Apgar scores than the others. Neonatal depression, represented by Apgar score < 7, was seen in only 2.7% of a sample of 1429 multiple Argentine newborns [33], lower than that found in this study.
Metabolic complications were proportionally higher than the other (respiratory, infectious, malformations and neonatal death), both for the T1 as for the T2 and, among them, stood out hypoglycaemia and jaundice and death in the early neonatal period occurred similarly for both twins. A study conducted in São Paulo, Brazil, from 131 medical records of multiple pregnancies resulting from assisted reproduction techniques showed that 37.5% of newborns had jaundice and early neonatal death rate reached 2.7% [26].
Lateral and colleagues [33] demonstrated that early neonatal mortality rate reached 2.9% (n = 42) in a sample of 10-year study of multiple pregnancies in Buenos Aires, Argentina. Early neonatal death was lower than that found in other studies may reflect the proper development of the fetes and possibly indicating an effective prenatal care. The care offered to pregnant women in the twin study of motherhood can be extremely important factor to contribute to the findings of this study, as there are specific institutional protocols that guide the perinatal care, in addition to the infrastructure available for quality care.
Postnatal stay in the NICU was lower than in rooming-ing for both twins, which may represent a good postnatal prognosis. Doss and colleagues [25] demonstrated that premature birth is responsible for high admission rates in intensive care units and the risk six times higher for those with 36 gestational weeks compared to 38 weeks and that the risk decreases with increasing age gestational at birth. Recommendations for the prenatal care of twin pregnancies [34-35] consider that dichorionic pregnancies should be discontinued, electively, at 37 weeks, while for monochorionic is considered 36 weeks and to prolong gestation to 38 weeks increases the risk of fatal death.
Preterm birth caused by premature labour, premature rupture of membranes or iatrogenic factors, is the most important fatal complications in multiple pregnancies and increases the adverse neonatal outcomes [34, 36]. It is usual for the multiple pregnancies that labour occurs spontaneously before 37 weeks and the mean gestational age is inversely related to the number of foetuses: 35-36 weeks for twins, 32 to 34 for triplets and less than 30 for other categories of multiple pregnancy [37].
Low birth weight was significantly related to preterm birth for both the T1 and T2. In 2006, the United States, 60% of twin births were premature, classified as low birth weight and that 1 to 10 twins (n = 13,983) was born less than 1500g [38].
The Apgar score in the first minute below 7 was rated among the twin 1 and 2 and it was observed that in premature infants, the prevalence of this change was higher. The same finding was not repeated for the Apgar score in the fifth minute. Study in Caxias do Sulk, Rio Grande do Sulk, Brazil, with multiple pregnancies (n = 193) showed similar results and associated low Apgar score with a reduction in umbilical artery pH, which can be caused by prolonged labour (more than 60 minutes) which can increase the risk of neonatal acidosis[39].
Preterm newborns may require intensive care during the neonatal period and in relation to premature twins, this assumption is confirmed. It was observed a significant relationship between the NICU - Neonatal and preterm delivery for T1 and T2. The admission to intensive care unit was 10% higher for twins at 36 weeks gestation than for newborns only in an American sample with 260 twins and the main causes for this high admission would be transient tachypnea, suspected sepsis and infants small for gestational age [25].
Brazil recommends that breastfeeding is encouraged for all newborns [40]. In the present study breast milk supply often associated with infant formula for T1 and T2 was similar, regardless of gestational age at birth. Qualitative study [41] that investigated breastfeeding in twin, identified that problems like long-time duration of breastfeeding, exhaustion, lack of help in the care of children and information with respect to power multiple, can be factors for the failure of this practice and, in addition, many women find that their milk is not strong enough for twins, asking thus the supply of infant formula. Damato and colleagues [42] show that the main unfavourable conditions related to multiple breastfeeding would prematurity, lack or weak sucking reflex, neurological immaturity and the permanence of the concepts for long periods in intensive care. Important to note that the supply of infant formula and parenteral nutrition can significantly increase hospital costs and family after discharge, should be minimized and better conducted in health facilities.
The particularities involving multiple pregnancies and care for twin newborns are important objects of study, especially the growing number of cases arising from technological development to enable safe assisted reproduction techniques and advanced maternal age [40,43].
The limitations of this study was the fact that present data in a single maternity in Rio de Janeiro, Brazil, which prevents generalized conclusions about the population of twin pregnancy; the lack of comparison of data from twin newborns studied with a group of unique newborns, which could demonstrate features differential between these population groups.
- MOREIRA DE SÁ RA, RIBEIRO DA SILVA N, FILGUEIRAS DE REZENDE KR, Gestação Gemelar: problemas em dobro? Femina. 2008;365(12):749-755.
- SPELLACY WN, HANDLER A, FERRE CD. A case-control study of 1253 twin pregnancies from a 1982-1987 perinatal data base. Obstetrics and Gynaecology, 1990;75(2):168-171.
- LUKE B & BROWN MB. Contemporary risks of maternal morbidity and adverse outcomes with increasing maternal age and plurality. Fertility and Sterility 2007;88(2):283-293.
- BEIGUELMAN B, FRANCHI-PINTO C. Perinatal mortality among twins and singletons in a city in southeastern Brazil, 1984-1996. Genetics and Molecular Biology, 2000;23(1):15-23. Doi:10.1590/S1415-47572000000100003
- COLLETO D, G M & ROSÁRIO H. Gestações múltiplas em amostras de uma população da cidade de São Paulo. Einstein, 2004;2(1):9-13.
- JAYA DS, KUMAR NS & BAI LS. A study on the health status of twin babies. The Indian Journal of Paediatrics, 1995;62(3):357-361.
- LANSKY S, FRICHE AA L, CAMPOS D, BITTENCOURT, SDA, LAZARO DE CARVALHO M, CAVALCANTE RS & ALVES DA CUNHA A.J.L. Pesquisa Nascer no Brasil: perfil da mortalidade neonatal e avaliação da assistência à gestante e ao recém-nascido. Caderno de Saúde Pública, 2014;30(Suppl 1):S192-S207.
- DUBOIS S, DOUGHERTY C, DUQUETTE M, HANLEY J & MOUTQUIN, J. Twin pregnancy:The impact of the Higgins Nutrition Intervention Program on maternal and neonatal outcomes. American Society for Clinical Nutrition, 1991;53(6):1397–1403. Doi:10.1093/ajcn/53.6.1397
- HALL JG. Twinning. The Lancet. 2003;362(9385):735-743. Doi: 10.1016/S0140-6736(03)14237-7
- KEET MP, JAROSZEWICZ AM & LOMBARD CJ. Follow-up study of physical growth of monozygous twins with discordant with-pair birth weights. Paediatrics. 1986;77(3):336-344.
- HOMRICH DA SILVA C, GOLDANI MZ., SILVA AA, M AGRANONIK, H BARBIERI MA & RONA R. The rise of multiple births in Brazil. Acta Paediatric, 2008;97(8):1019-1023. Doi:10.1111/j.1651-2227.2008.00791
- MARTINS WP, BARRA DA & MAUAD-FILHO F. Gestação múltipla – aspectos clínicos. Femina, 2006;34(6):423-431.
- BEIGUELMAN BO, ESTUDO DE GÊMEOS. Bernardo Beiguelman - Ribeirão Preto: SBG; 2008.
- RYDHSTROEM H & HERAIB F. Gestational durantion, and fetal and infanto mortality for twins vs singletons. Twin Research, 2001;4(4):227-231. Doi: 10.1375/twin.4.4.227
- VALENZUELA MP, BECKER V J & CARVAJAL CJ. Pautas de manejo clínico de embarazos gemelares. Revista Chilena de Obstetricia y Ginecologia, 2009;74(1):52-68. Doi:10.4067/S0717-75262009000100010
- LUKE B. Reducing fetal death in multiple births:optimal birthweights and gestacional age for infants for twin and triplet births. Acta Geneticae Medicae et Gemellologiae,1996;45(3):333-348.Doi:10.1017/S0001566000000933
- CHANG EY. Timing of delivery in multiple gestation.Clinical Obstetrics and Gynecology, 2004;47(1)237-247.
- AMERICAN ACADEMY OF PEDIATRICS. The Apgar score. Pediatrics,2006;117(4):1445-1447.
- APGAR V. A proposal for a new method of evaluation.of the newborn infant.current researches in anesthesia and analgesia. Current Researches in Anesthesia and Analgesia,1953;260-267.
- BRASIL MINISTÉRIO DA SAÚDE. Secretaria de Atenção à Saúde. Departamento de Ações Programáticas e Estratégicas. Atenção à saúde do recém-nascido: guia para os profissionais de saúde [Newborn health care: a guide for health professional]2011;Brasília:Ministério da Saúde.
- ALEXANDER GR, KOGAN M, MARTIN J & PAPIERNIK E. What are the Fetal Growth Patterns of Singletons, Twins, and Triplets in the United States? Clinical Obstetrics and Gynecology,1998;41(1):115-125.
- SBP-SOCIEDADE BRASILEIRA DE PEDIATRIA. Avaliação nutricional da criança e do adolescente – Manual de Orientação [Nutritional assessment of children and adolescents - Guidance Manual ].2009;São Paulo, Brazil: Sociedade Brasileira de Pediatria.
- CLEARY-GOLDMAN J, MORGAN MA, ROBINSON JN, D’ALTON, M.E & SCHULKIN J. Multiple pregnancy: knowledge and practice patterns of obstetricians and gynecologists. American College of Obstetricians and Gynecologists,2004;104:232-237.Doi:10.1097/01.AOG.0000132805.79318.99
- MARES M, CASANUEVA E. Embarazo gemelar.Determinantes maternas del peso al nascer.Perinatologia y Reproducción Humana, 2001;15(4):238-244.
- DOSS AE, MANCUSO MS, CLIVER SP, JAUK VC & JENKIMS SM. Gestational age at delivery and perinatal outcomes of twin gestations. American Journal of Obstetrics and Gynecology, 2012;207:410e1–410e8.Doi: 10.1016/j.ajog.2012.08.012
- GRANER VR & OLIVEIRA DE BARROS SM. Complicações maternas e ocorrências neonatais associadas às gestações múltiplas resultantes de técnicas de reprodução assistida. Revista da Escola de Enfermagem da USP, 2009;43(1):103-109.Doi:10.1590/S0080-62342009000100013
- MAXIMIANO N. Perfil materno-infantil de nascimentos por parto duplo em uma amostra de puérperas do município do Rio de Janeiro, 1999-2001. [Maternal-infant profile of births by double birth in a sample of puerperal women from the city of Rio de Janeiro, 1999-2001]. (Master’s Thesis). Instituto Oswaldo Cruz, Escola Nacional de Saúde Pública, Rio de Janeiro. 2002
- ASSUNÇÃO RA.Perfil clinico-epidemiológico das gestações gemelares com parto no Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo no período de 2003 a 2006. [Clinical and epidemiological profile of twin pregnancies with parturition at Hospital das Clínicas, Faculty of Medicine, University of São Paulo, from 2003 to 2006.].(Master’s Thesis) –Faculdade de Medicina, Universidade de São Paulo, São Paulo. 2008
- LEE YM. Delivery Twins. Seminars in Perinatology, 2012;36:195-200.Doi:10.1053/j.semperi.2012.02.004
- VOGEL JP, TORLONI MR, SEUC A, BETRÁN AP, WIDMER M, SOUZA JP & MERIALDI M. Maternal and Perinatal Outcomes of Twin Pregnancy in 23 Low- and Middle-Income Countries. PLoS ONE, 2013;8(8):e70549,7p.Doi: 10.1371/journal.pone.0070549
- CARDIM HJP, MACHADO CF, BORNIA JA, HIGA LT & UCHIMURA NS. Análise retrospectiva das gestações múltiplas no Hospital Universitário Regional de Maringá no período de janeiro de 2000 a julho de 2003. Acta Scientiarum Health Sciences, 2005;27(1):57-61. Doi:10.4025/actascihealthsci.v27i1.1444
- MIN SJ, LUKE B, GILLESPIE B, MIN L, NEWMAN RB, MAUDIN JG, SALMAN FA, O’SULLIVAN, MJ. Birth weight references for twins. American Journal of Obstetrics and Gynecology,2000;182(5):1250-1257.Doi: 10.1067/mob.2000.104923
- LATERRA C, SUSACASA S, FRAILUNA MA, FLORES L, SECONDI V. Embarazo doble: diez años de resultados perinatales em el Hospital Materno Infantil Ramón Sadrá. Revista del Hospital Materno Infantil Ramón Sadrá, 2006; 25(1):32-37.
- BRICKER L.Optimal antenatal care for twin and triplet pregnancy:The evidence base. Best Practice & Research Clinical Obstetrics and Gynaecology, 2014;28:305-317.Doi:10.1016/j.bpobgyn.2013.12.006
- NATIONAL COLLABORATING CENTER FOR WOMEN’S AND CHILDREN’S HEALTH.Multiple pregnancy: the management of twin and triplet pregnancies in the antenatal period. London: RCOG Press 2011.
- HASBÚN J. El riesgo perinatal y materno del embarazo gemelar. Revista Chilena Salud As Pública,2006;10(1):27-34.Doi:10.5354/0719-5281.2010.5487
- RAMSEY PS & REPKE JT. Intrapartum Management of Multifetal Pregnancies. Seminars in Perinatology, 2003;27(1):54-72.Doi:10.1053/sper.2003.50009
- CHAUHAN SP, SCARDO JA, HAYES E, ABUHAMAD AZ & BERGHELLA V. Twins: prevalence, problems, and preterm births. American Journal of Obstetrics & Gynecology,2010;203(4):305-315.Doi:10.1016/j.ajog.2010.04.031
- HEINECK DE SOUZA L, MADI JM, ARAUJO BF, ZATTI H, MADI SRCM, LORENCETTI J & MARCON NO. Características e resultados perinatais das gestações gemelares (1998-2007).Revista da AMRIGS,2009;53(2):50-155.
- BRASIL MINISTÉRIO DA SAÚDE. Secretaria de Atenção à Saúde. Departamento de Atenção Básica. Atenção ao pré-natal de baixo risco [Attention to low-risk prenatal care], 2012;Brasília:Ministério da Saúde.
- CINAR ND, ALVUR TM & NEMUT T. Breastfeeding Twins:A Qualitative Study. Journal of Health, Population, and Nutrition, 2013;31(4):504-509.
- DAMATO EG, DOWLING DA, MADIGAN EA & THANATTHERAKUL C. Duration of breastfeeding for mothers of twins. Journal of Obstetric,Gynecology and Neonatal Nursing, 2005;34:201-209. Doi:10.1177/0884217504273671
- CDC - CENTER FOR DISEASE CONTROL. MARTIN JA, HAMILTON BE & OSTERMAN MJK. Three Decades Twin Births in the United States,1980–2009. NCHS Data Brief, 2012;80:8.


