OBSTETRICĂ

Prognosticul neonatal şi matern în naşterea întârziată intenţionat a celui de-al doilea făt din sarcina dizigotică. Caz clinic şi revizuirea literaturii

 Neonatal and maternal outcomes after intentional delayed delivery for the second twin in dyzigotic pregnancy. Case report and literature review

First published: 15 aprilie 2016

Editorial Group: MEDICHUB MEDIA

Abstract

Intentional delayed delivery of second twin in dizygotic pregnancy is rare. There are analyzed the peculiarities regarding maternal, short-term neonatal outcomes in a 41-year-old mother, admitted in a tertiary university maternity, diagnosed with: IVG IIP 24 weeks + 3 days dizygotic pregnancy, alive fetuses (A. breech presentation, 690 g, palpable amniotic sac; B. cephalic presentation, intact membranes, EFWs of 690/700 g - ultrasound). At 26 weeks of gestation, after PROM, short positive trial of labor for planned vaginal delivery, under continuous CTG, Bracht maneuver for breech presentation which records the birth of female fetus A, 920 g, Apgar score 5/6. Sectioned umbilical cord is introduced in the vagina. At 50 days of close monitoring and treatment for both mother and fetus B, it is done caesarean section for female fetus B, 1870 g (34 weeks of gestation), Apgar score 8, placentae A/B: 200/450g. Maternal postoperative evolution is normal. Baby A is admitted at Neonatal Intensive Care Unit (NICU) for moderate hypoxia at birth, repeated apnea crisis, without functional respiratory syndrome, anemia being corrected with blood derivates, 70 days, with gastric-tube nutrition, antibiotics, stage I retinopathy, bilateral hip risk; the weight of fetus B was 1550 g at the cesarean section and 2250 when discharged. Baby B had a favorable evolution (breastfeeding plus formula milk). Conclusions. Vaginal delivery at a multipara can be assumed in breech presentation, after a precise protocol, followed by experienced obstetrical/neonatological teams, and an intentional delayed CS delivery is feasible. Fetus B is larger at delivery than fetua A at the same moment (1870 g vs. 1550 g), and at discharge (2250 g vs. 2975 g), with a very short admission in NICU/preterm wards. No maternal complication appeared.
 

Keywords
intentional delayed delivery, dizygotic pregnancy, preterm delivery, outcome

Rezumat

Sarcina gemelară dizigotică - cu riscurile şi costurile crescute ale mortalităţii şi morbidităţii perinatale, induse de prematuritate, complicaţiile fetale/materne intrapartum - impune decizii dificile pentru terminarea naşterii, dictate de vârsta gestaţională, calităţile colului, starea membranelor, prezentaţiile şi starea feţilor. Operaţia cezariană planificată pentru prezentaţia pelviană şi monitorizarea CTG intrapartum nu au fost urmate de succesul scontat, ci de discordanţa dintre morbiditatea perinatală pe termen scurt şi prognosticul neurologic pe termen lung. MG, de 41 de ani, UM 15 mai 2014, internată în 2.11.2014 pentru CUD sistematizate, suspiciune de membrane fisurate, diagnosticată cu: IVG II P, sarcină gemelară dizigotică de 24 săptămâni + 3 zile, feţi vii (A. prezentaţie pelviană, 690 g, pungă amniotică palpabilă; B. prezentaţie craniană, 700 g, membrane intacte ecografic). În 17.11.2014 se rup membranele la fătul A, iar după un travaliu de 4 ore se expulzează cu ajutor manual Bracht un făt feminin de 920 g, scor Apgar 5/6, se pensează cordonul, gravida este menţinută sub supraveghere/tratament continuu, cu evoluţie favorabilă, fără decolarea placentei fătului A, spitalizat la NICU (hipoxie moderată la naştere, adaptare cu crize de apnee, fără sindrom funcţional respirator, anemie plurifactorială, antibioterapie complexă cu spectru larg, gavaj 70 de zile, retinopatie stadiul I, risc bilateral de şold). La 50 de zile de la naştere, la 33 de săptămâni şi 4 zile (cronologic, sonografic), se decide extragerea fătului B prin operaţie cezariană: sex feminin, 1870 g, scor Apgar =8; placenta A de 200 g, placenta B de 450 g. Evoluţia post-partum este normală, cu prelungirea spitalizării cu alte 23 de zile, din cauza prematurităţii fetale. La data operaţiei cezariene fătul A cântărea 1550 g şi apoi 2250 g la externare. Fătul B are evoluţie favorabilă, cu 2975 g la externare, alimentat mixt (la sân şi biberon). Concluzii. Monitorizarea extrem de atentă a sarcinii dizigotice, la secundipară, poate permite alegerea naşterii pe cale vaginală a primului făt în prezentaţie pelviană după un protocol precis, urmat de o echipă obstetricală experimentată, iar operaţia cezariană intenţionat amânată este folositoare; fătul B este cu greutate mai mare la naştere (1820 g vs. 1550 g) şi la externare (2975 g vs. 2250 g) comparativ cu fratele şi cu o durată redusă de spitalizare la NICU/neonatologie în prima perioadă postnatală; nu a existat nici o complicaţie maternă.
 

Introduction 

The incidence of twin pregnancies has increased in the last 10 years, and the delivery of the fetuses, especially of the second one, is a great challenge, regarding actual opportunities of intrapartum fetal monitoring, and advantages/disadvantages of planned caesarean section, in the presence of prematurity(1). The costs of antenatal and postnatal care (for the antenatal 27 weeks and postnatal 30 days) are very high for both mother and fetuses, from the first neonatal day, being appreciated to be 20 fold higher than for a single fetus pregnancy(2).
The high risks for perinatal mortality and morbidity induced by prematurity, and intraoperative maternal, and fetal complications had induced a special care for the decision of birth in dizygotic twin (biamniotic - bichorionic/fraternal), which is established by gestational age, uterine cervix qualities, membrane, presentations, and fetal status. Planned caesarean section for breech presentation, and electronic fetal heart monitoring were not followed by the expected/wanted results, and have shown an unexpected discordance between short-term perinatal morbidity and long-term neurological outcome(3), the rate of cerebral palsy being increased in comparison to single fetus pregnancies(4), and the trend (though not statistically significant) was in the opposite direction.
The intentional delayed delivery of the second twin in dizygotic pregnancy is rarely reported, and this paper is focusing on such a case, which is discussed in relation to the main issues of twinning.

Case presentation

MG, 41-years-old, from the Romanian town of Piteşti, worker, married, with a medium education, with one spontaneous birth (2800 g, healthy), two abortions, with LMP in May 15,  2014, was monitored precocious for pregnancy, and diagnosed at 16 weeks with dizygotic twins, treated with folic acid, vitamins, progesterone 200 mg/day. The patient is admitted in “Dr. I. Cantacuzino” Clinic of Obstetrics in 2.11.2014 for uterine contractions, and suspicion of rupture of membranes, being diagnosed with: IVG II P 24 weeks + 3 days dizygotic pregnancy, alive both fetuses, breech presentation fetus A, cranial presentation fetus B, intact membranes at ultrasound assessment, and ultrasound estimated fetal weights (EFW) of 690 g (A), and 700 g (B).

Case evolution 

It is initiated the treatment with corticosteroids, progesterone 200 mg/day, tocolysis (nifedipine 30 mg x 2/day), magnesium sulphate, 5% dextrose 1000 ml/day, and antibiotics.
In 17.11.2014 it is recorded the spontaneous rupture of membranes of the leading twin, and it was decided the vaginal delivery of fetus A, because we appreciated a Friedman curve delivery in  normal parameters, good ripening of uterine orifice, under continuous electronic fetal heart monitoring,  mother being informed about the benefits and risks.
After a short trial of labor, and a labor of 4 hours, on intravenous perfusion with 5% dextrose, vitamins, magnesium sulphate, in breech presentation with Bracht maneuver, it is delivered a girl of 920 g, Apgar score =5/6, and pH =7.00 in the umbilical cord. The umbilical cord is sectioned, introduced in the vagina, and the mother is very carefully monitored clinically, hematologically, and bacteriologically (WBC, CRP), under treatment with antibiotics, progesterone, tocolytics, intravenous perfusions. The remaining twin is monitored twice a day with NST and once a week with ultrasound scan. Maternal, and remaining twin evolutions are normal, the placental masses are not separated. It is decided caesarean section (CS) at 33 weeks + 4 days (chronological and sonographical) for the risks of blood redistribution to fetus A placenta, and an umbilical cord procubitus loop of the remaining fetus, with high position of the head, and chorioamniotic infection (increasing WBC, CRP). 
It is delivered the twin B, female 1870 g, Apgar score =8, pH =7.15 of umbilical cord blood, and a 200 g corporeal inserted placenta of fetus A, with calcium impregnations, reduced consistency, and a 450 g fundus and posterior placenta of fetus B, calcium impregnations of membranes. Uterine retraction is normal, and maternal intra- and postoperative evolution is normal, the mother being maintained in hospital for another 23 days, for her preterm babies. Baby A was admitted at NICU with moderate hypoxia at birth, repeated apnea crisis, without functional respiratory syndrome, plurifactorial anemia corrected with blood derivates, 70 days of gastric-tube nutrition, fourth generation cephalosporines (positive procalcitonin test), stade I retinopathy, bilateral hip risk. At the date of CS, baby A had 1550 g, and at discharge she had 2250 g. Baby B had favourable evolution, 2975 g at discharge, being breastfed plus milk formula.

Discussion

The twinning rates across the world, and especially for the developing world, have changed, and in India, USA, and Europe it is an intermediate rate of 9-16 pairs /1000 births among the very high 18-30 pairs/1000 births (Central Africa) and the lowest of 6-9 pairs/1000 births (Latin America, South Asia, and South-East Asia) as it is provided in the most complete and comparable overview of twinning rates across the 76 low- and middle-income countries, as Romania(5). In USA, the rate had increased from 18.9 in 1989 to 33.3 per 1000 births in 2009(6). 

Eighty years ago, Greunlich WW(7), cited by Hochstra C et al.(8), discussed the factors involved in variable incidence of dizygotic pregnancy: times, geographic areas, seasons(9), populations, familial, and genetics: X fragile syndrome determined by the deficiency of FMR1 protein located on chromosome Xp27.3, followed by ovarian insufficiency and premature menopause(8), and the GDF9 and BMP15 mutations(11,12). Dizygotic (fraternal) pregnancies were 70% from natural twins in USA(13), but the incidence is more variable in time in comparison to monozygotic pregnancy, with a constant incidence, and this situation is connected to familial history of fraternal twins - from genetic risk of hyperovulation, diet with high content of growth factors as insulin-like growth factor, from high intake of cattle meat(14), and mothers’ advanced age because of pregnancy postponing, and necessity of medication/technologies for ovulation induction(14,15). The Romanian patient reported pregnancy was naturally conceived, with no family history of twins, with no preconceptional folic acid administration, as it was considered to be an explanation of twinning(16,17).
Recently, it is not known why elder women have a higher natural rate of dizygotic twins, one explanation being the higher FSH level, which makes ovaries to be more responsive(18,19).

The presentations in the studied case are breech/cephalic, and the literature reports in the dizygotic twins are cephalic/cephalic (40%), cephalic/non-cephalic (35%), and 25% with the leading fetus in non-cephalic (vertex) presentation, like the Romanian one(20,21). The assigned risk associated to fetal presentations is increasing in discordance to frequencies of fetal presentations, as it is reported in “The Netherlands Perinatal Registry” for cases with a gestational age (GA) of 32+0 - 41+0 weeks(22): cephalic-non-cephalic - OR 2.27; non-cephalic- cephalic - OR 13.63; non-cephalic - non-cephalic: OR 21.92. It was described that after the delivery of the leading fetus the presentation of the second can be changed (20% of cases(23)), to breech, converted to transverse lie, or it can be registered a cord prolapse
The most frequent dizygotic twins’ gender is male/female (50%), then female/female (sororal), and male/male.

The dizygotic twins have a lower risk in comparison to monozygotic twins, but the risks of twin-infants, and of their mothers are still very high in contemporary societies. It has long been known that perinatal morbidity and mortality are in conjunction to prematurity, alone or associated to intrauterine fetal growth restriction in comparison to singletons of the same GA and/or same birthweight(24,25), and in conjunction to the quality of hospital/maternity, qualification of medical staff, and to the timing, and route of birth. Cochrane Database Systematic Reviews(26) and Hofimeyr GJ et al.(3) revealed that the absolute rates of perinatal mortality and morbidity vary by population, country, and the moment of parturition complication (antepartum/intrapartum/postpartum). Another discussion is in relation to the higher risk of the second twin, independent to presentation, chorionicity or fetal sex(27).

In this case, the optimal delivery timing discussed to be at 37 to 38 weeks of gestation(28-30) or near term(26), or according to the French College of Obstetricians-Gynecologists(31) from 38 to 40 weeks, was not possible to be achieved, because maternal incompetent internal os of the uterine cervix (as we suppose to be in the Romanian case), and/or of low efficacy of tocolysis (nifedipine), and due to the premature rupture of membranes associated to the first two, as it is appreciated by literature to be the most frequent reasons for delivery before 32 weeks of gestation(32). In the Cochrane Database Systematic Review, 2014(33), it is compaired the optimal elective delivery timming for twins from 37 weeks in uncomplicated dizygotic twin pregnancies versus an expectant management, and it was concluded that early birth at 37 weeks of gestation does not appear to be associated with an increased risk of harms, and the authors considered that there are not sufficient clinical equipoise to allow for the randomization of women to a later gestational age at birth.
When complications regarding the babies are depicted or suspected, it is proved by the last Cochrane Database Systematic Review (November 2015) that a planned early delivery with less than 10 days to full term versus expectant management is improving primary maternal outcomes, and primary neonatal outcomes (perinatal mortality and morbidity, and neurodevelopment/ disability/ impairment at two years of age(34)). It was considered that planned caesarean section may reduce with 75% the risk of perinatal death in term twins, especially for the twin B, versus a vaginal delivery(35-38), mainly by reducing the risk of death of the second twin due to intrapartum anoxia(39) or versus a trial of labour.
At term when the leading fetus is in breech presentation, the caesarean section was the rule at the beginning of this century(40,41), but during time, there had been some controversies, which are discussed by some of the same authors of the previous paper(42,43), regarding fetal morbidity and mortality. For babies under 1500 g, there was no difference in mortality and morbidity based on a 5-minute Apgar Score under 5, in multigravidas, after vaginal route vs. caesarean section, as it is revealed by the largest multi-centre study in terms of numbers by Blickstein I et al.(44), but when the second twin is in breech presentation the cord pH is lower than for the second twin in cephalic presentation after the vaginal delivery, and more cases are admitted to NICU. According to authors, multiparity and elective caesarean seemed to have little influence on outcome measures, extremely preterm twins may have a higher risk of neonatal mortality(44,45).

The Romanian obstetricians involved in the reported case considered that vaginal route for the leading fetus in breech presentation is safe, and the trial of labour was positive, in the favorable conditions of the case, on continuous electronic monitoring. After a retrospective study of 10 years(46), it was concluded that the attempting vaginal route versus planned caesarean delivery for the first twin in dizygotic pregnancy is possible based on correct, and attentively intrapartum criteria, after a precise protocol, which must be followed by a experienced obstetrician comfortable in the performance of vaginal breech delivery, and well trained, skilled midwives, in the presence of an anesthesiologist, with the existence of an adequate operative room for an emergency cesarean section. All these criteria were present in the Romanian case.
The choice of CS for the second twin after the vaginal delivery of the leading twins is more frequent in term fetuses than in preterm pregnancies(47), the indications are maternal reasons, or complications of labor/delivery, or second twin in a non-cephalic presentation (breech presentation, or malpresentations) which sometimes are emergency indications(48,49). Most recent retrospective studies(50,51), and a population based study from Denmark(52) state that there is no advantage in elective C-section over vaginal delivery in the case of twin births in which the first twin is in cephalic presentation and the second is not in cephalic presentation; and even an increase of two-fold(48) or four-fold(52) for the second twin risk delivered by CS after the vaginal route of the leading twin. In the Danish study(52) the Apgar Score less than 8, and pH umbilical cord under 7.1 were significantly higher compared to the vaginal delivery route of the second twin in non-cephalic position (OR 6.2; 95% CI 2.1-18).

The interval between the deliveries of the twins is a very much discussed and analyzed issue. After the delivery of the fetus A, it appears an interval free of uterine contractions of 15-30 minutes, which can be longer than 60 minutes, during which uterine bleeding and the remaining fetus must be very well assessed. Studies on the influence of the birth interval on neonatal morbidity have contradictory results. 
In the literature of the last 10 years, there are considered different intervals between the two deliveries: 15 minutes in France(53), 30 minutes in USA(54), and in Germany(55) the second twin delivery was recorded at different intervals (15 minutes: 75.8%; 16-30 minutes: 16.4%; 31-45 minutes: 4.3%; 46-60 minutes: 1.7%; >60 minutes: 1.8%; 72 instances).
In the “Twin Birth Study”, held for 15 years, from the German Region Hesse, the birth interval between twins was on average 3.6 ± 1.5 minutes in the group with planned caesarean sections, and with longer duration (56.2%) in the group with planned vaginal delivery (of 10±16.7 minutes), and the conclusions were that no significance of the birth interval on child morbidity can be drawn from the “Twin Birth Study”, and that the obstetrician who monitors the pregnancy/labor/birth may accelerate or not the procedures/maneuvers for the second twin delivery(56).

There is a historical recommendation that the delivery of the second twin must not be later than 60 minutes(57), but the German obstetrician was citing cases with a delayed delivery of the second twin from 35 to 169 days, and actually in different countries the possibility of increasing the interval between the births of dizygotic twins is much discussed: The Netherlands(58), Spain(59), Italy(60), with analysis of maternal and infants outcome (short and long time follow-up), some of the offspring being considered miscarriages (the Spanish cases). In Romania (2005), it was presented by BBC a case with an interval of 59 days between the deliveries of fraternals.
Table 1. Short term neonatal outcomes of twins
Table 1. Short term neonatal outcomes of twins

Initial Neonatal Outcomes

Neonatal outcome is dominated by prematurity, low Apgar Score and low pH of blood cord, duration of admission in NICU especially for respiratory distress syndrome, neonatal seizures(61), which is more severe for the second twin, and is associated to birth trauma - cervical and brachial plexus, facial nerv, fractures of skull, and clavicles, soft tissue lacerations(62). There are to be added the intrinsic abnormalities connected to twins genetics, especially for male fetuses from mothers with X fragile syndrome/GDF9 and BMP15 mutations, which are prone for mental retardation or neurodegenerative disorders in adult life(8,10). 
The short-term neonatal outcomes of the twins are listed in Table 1.
The Romanian obstetricians involved in the management of the reported case are wondering about the explanations/determinants/factors which may explain the evolution. One explanation is represented by the recommended drugs (progesterone, tocolytics, antibiotics), but we consider the placentae of the twins to be more important. The placenta of the leading fetus did not separate after the first birth, and the placenta of the fetus B permitted a future normal evolution. The placenta of fetus B was 450 g, larger than that of fetus A, of 200 g, with calcium stores. This hypothesis is discussed by the most recent Cochrane Database Systematic Review(63), with the conclusion that the biochemical tests (estrogens, human placental lactogen) for placental functions are not sufficient markers, or are of low or very low evidence.

Conclusions

Planned vaginal delivery at a multipara can be assumed in breech presentation, in a case with cervical incompetence, short labor, and a fetus below 1000 g, after a precise protocol, followed by experienced obstetrical/neonatological teams. An intentional delayed CS delivery is feasible with very few risks. Fetus B is larger at delivery than fetus A at the moment of CS (1870 g vs. 1550 g), and at  discharge (2250 g vs. 2975 g), and fetus B has a very short admission in NICU/preterm wards in comparison to leading fetus. No maternal complication appeared.

Bibliografie

1. Barrett JF - Twin delivery: method, timing and conduct. Best Pract Res Clin Obstetr Gynecol: 2014; 28 (2): 327-8. 
2. Lemos VE., Zhang D, Van Voorhis JB, Hu XH. Healthcare Expenses Associated with Multiple Pregnancies versus Singletons in the United States. Am Jf Obstet Gynecol, 2013;  209(6):586.e1–586.e11.
3. Hofimeyr GJ, Barrett FJ, Crowther AC. Planned caesarean section for women with a twin pregnancy. Cochrane Database Syst Rev, 2011(12). CD006553.
4. Pharoah PO, Cooke T. Cerebral palsy and multiple births. Arch Dis Child Fetal Neonatal Ed, 1996; 75(3):F174 – F177.
5. Smits J, Monden C. Twinning across the Developing World. PLoS ONE: 2011; 6(9):e25239. 
6. Martin AJ, Hamilton EB, Osterman JKM. Three Decades of Twin Births in the United States, 1980–2009, National Center for Health Statistics Data Brief, 2012, 80.
7. Greunlich WW. Heredity in human twinning. Am J Phys Anthrop, 1934;19:391-443, cited by Hochstra C, Zhao ZZ, et al. (1997).
8. Hochstra C, Zhao ZZ, Lambalk CB, Willemsen G, Martin NG, Boomsma DI, Healey SC, Duffy DL, Martin NG, Turner G. Is fragile X syndrome a risk factor for dizygotic twinning? Am J Med Genet, 1997; 72:245-6.
9. Krieger H, Colletto GM, Franchi-Pinto C, Beiguelman B. Investigation on seasonality of twin births in Brazil. Acta Genet Med Gemellol, 1996; 45:397-403.
10. Montgomery GW, Zhao ZZ, Marsh AJ, Mayne R, Treloar SA, James M, Martin NG, Boomsma DI, Duffy DL. A deletion mutation in GDF9 in sisters with spontaneous DZ twins. Twin Res, 2004; 7:548-55.
11. Montgomery GW. Dizygotic twinning. Hum Reprod Update: 2008; 14(1):37-47. Epub 2007.
12. MacGillivray I. Epidemiology of twin pregnancy. Semin Perinatol., 1986; 10:4-8.
13. Steinman Gary. Mechanism of twinning. Effect of diet and heredity on the human twinning rate. Reprod Med, 2006; 51(5):405–10. 
14. Anonymous. Health Canada. Canadian perinatal health report. Minister of Public Health Works and Government Services Canada; Ottawa: 2000.
15. Laws PJ, Li Z, Sullivan EA. Australia’s mothers and babies 2008. AIHW Perinatal Statistic Unit; 2010. Perinatal Statistic Series no. 24. Cat. no. PER 50.
16. Levy T, Blickstein I. Does the use of folic acid increase the risk of twinning? Int J Fertil Womens Med, 2006; 51:130-5.
17. Muggli EE, Halliday JL. Folic acid and risk of twinning: a systematic review of the recent literature, July 1994 to July 2006. Med J Aust, 2007; 186:243-8.
18. Lambalk CB, Boomsma DI, De Boer L, De Koning CH, Schoute E, Popp-Snijders C, Schoemaker J.  Increased levels and pulsatility of follicle-stimulating hormone in mothers of hereditary dizygotic twins. J Clin Endo Metab 1998; a83:481-6.
19. Beemsterboer SN, Homburg R, Gorter NA, Schats R, Hompes PG, Lambalk CB. The paradox of declining fertility but increasing twinning rates with advancing maternal age. Hum. Reprod, 2006; 21(6):1531–2 
20. Blickstein I, Schwartz-Shoham, Lancet M, Borenstein R. Vaginal delivery of the second twin in breech presentation. Obstet Gynecol, 1987; 69:774–6.
21. Grisaru D, Fuchs S, Kupferminc MJ, Har-Toov J, Niv J, Lessing JB. Outcome of 306 twin deliveries according to first twin presentation and method of delivery. Am J Perinatol, 2000; 17:303–7.
22. Goossens S, Hukkelhoven C, de Vries L, Mol B, Nijhuis J, Roumens F. Clinical characteristics associated with the planned and actual mode of delivery of twins: an analysis of 22,864 twin pairs from 32-41 weeks. Book of Abstracts for the 15th International Congress on Twin Studies and the 3rd World Congress on Twin Pregnancy, 2015
23. Houlihan C, Knuppel RA. Intrapartum management of multiple gestations. Complicated labor and delivery II. Clinics in Perinatology, 1996; 23:91–116.
24. Glinianaia SV, Rankin J, Renwick M. Northern Region Perinatal Mortality Survey Steering Group. Time trends in twin perinatal mortality in northern England, 1982-94. Twin Res, 1998; 1:189–95.
25. Wenckus JD, Gao W, Kominiarek AM, Wilkins I (2014). The effects of labor and delivery on maternal and neonatal outcomes in term twins: a retrospective cohort study. BJOG, 121(9):1137- 44.
26. Dodd  JM, Crowther CA. Elective delivery of women with a twin pregnancy from 37 weeks’ gestation. Cochrane Database of Systematic Reviews, 2003; (1) DOI: 10.1002/14651858. CD003582.
27. Armson BA, O’Connel C, Persad V, Joseph KS, Young DC, Baskett TF. Determinants of perinatal mortality and serious neonatal morbidity in the second twin. Obstet Gynecol, 2006; 108 (3 Pt 1):556-64.
28. Hartley SR, Emanuel I, Hitti J.  Perinatal mortality and neonatal morbidity rates among twin pairs at different gestational ages: Optimal delivery timing at 37 to 38 weeks’ gestation AJOG, 2001:184, (3):451–8.
29. Barrett JF. Delivery of the term twin. Best Practice & Research. Clinical Obstet Gynaecol, 2004; 18(4): 625–30.
30. Dias T, Akolekar R. Timing of birth in multiple pregnancy. Best Pract Res Clin Obstet Gynaecol, 2014; 28:319–26.
31. Vayssière C, Benoist G, Blondel B, Deruelle P, Favre R, Gallot D, Jabert P, Lemery D, Picone O, Pons JC, Puech F, Quarello E, Salomon L, Schmitz T, Senat MV, Sentilhes, Simon A, Stirneman J, Vendittelli F, Winer N, Ville Y. French College of Gynecologists and Obstetricians - Twin pregnancies: guidelines for clinical practice from the French College of Gynaecologists and Obstetricians (CNGOF). Eur J Obstet Gynecol Reprod Biol, 2011; 156 (1):12-7.
32. Lee CM, Yang HS, Lee SP, Hwang BC, Kim SY. Clinical factors affecting the timing of delivery in twin pregnancies. Obstet Gynecol Sci, 2014; 57(6):436–41. 
33. Dodd JM, Deussen AR, Grivell RM, Crowther CA. Elective birth at 37 weeks’ gestation for women with an uncomplicated twin pregnancy. Cochrane Database Syst Rev, 2014; 2:CD003582. doi.
34. Bond DM, Gordon A, Hyett J, de Vries B, Carberry AE, Morris J. Planned early delivery versus expectant management of the term suspected compromised baby for improving outcomes. Cochrane Database Syst Rev, 2015; 11:CD009433. 
35. Hogle K, Hutton E, McBrien KA, Barrett J, Hannah ME. Cesarean delivery for twins: a systematic review and meta-analysis. Am J Obstet Gynecol, 2002; 188:220–7.
36. Nassar AH, Maarouf HH, Hobeika EM et al. Breech presenting twin A: is vaginal delivery safe? J Perinat Med, 2004; 129:470-4. 
37. Lee HC, Gould JB, Boscardin WJ, El-Sayed YY, Blumenfeld YJ. Trends in Cesarean Delivery for Twin Births in the United States. Obstet Gynecol, 2011; 118 (5): 1095–101. 
38. Barrett JF, Hannah ME, Hutton EK, Willan AR, Allen AC, Armson BA, Gafni A, Joseph KS, Mason D, Ohlsson A, Ross S, Sanchez JJ, Asztalos EV. A Randomized Trial of Planned Cesarean or Vaginal Delivery for Twin Pregnancy. New Engl J Med,  2013; 369(14):1295–305.
39. Smith GC, Shah I, White IR, Pell JP, Dobbie R. Mode of delivery and the risk of delivery-related perinatal death among twins at term: a retrospective cohort study of 8073 births. BJOG, 2005; 112(8):1139-44.
40. Hannah ME, Hannah WJ, Hewson S, Hodnett E, Saigal S, Willan A. Planned caesarean section versus planned vaginal birth for breech presentation at term: a randomised multicentre trial. Lancet, 2000;356:1375–83.
41. Hofmeyr GJ, Hannah ME. Planned caesarean section for term breech delivery. Cochrane Database of Systematic Reviews, 2003; (2) DOI: 10.1002/14651858.CD000166. 
42. Hofimeyr GJ, Barrett FJ, Crowther AC. Planned caesarean section for women with a twin pregnancy. Cochrane Ddatabase Syst Rev, 2011, (12);CD006553.
43. Ganchimeg T, Morisaki N, Vogel JP, Cecatti JG, Barret J, Jayaratne K, Mittal S, Panozo-Ortiz E, Souza JP, Crowther CA, Ota E, Mori R, for the WHO MultiCountry Survery Maternal Network - Mode and timing of twin delivery and perinatal outcomes in low- and middle-income countries: a secondary analysis of the WHO Multicountry Survey on Maternal and Newborn Health. Bjog-Int J Obstet Gy, 2014; 121:89-100. 
44. Blickstein I, Goldman RD, Kupferminc M. Delivery of breech first twins: a multicenter retrospective study. Obstet Gynecol 2000; 95:37-42.
45. Blickstein I. Is cesarean section for all twins? J Perinatal Med: 2000; 28:169.  
46. Sentilhes L, Goffinet F, Talbot A, Diguet A, Verspyck E, Cabrol D, Marpeau L. Attempted vaginal versus planned cesarean delivery in 195 breech first twin pregnancies Acta Obstet Gynecol Scan, 2007; 86(1):55-60.
47. Wen SW, Fung KF, Oppenheimer L, Demissie K, Yang Q, Walker M. Occurrence and predictors of cesarean delivery for the second twin after vaginal delivery of the first twin. Obstet Gynecol, 2004; 103(3):413-9.
48. Persad V, Baskett T, O’Connell CM, Scott HM. Combined vaginal-cesarean delivery of twin pregnancies. Obstet Gynecol, 2001; 98:1032–7.
49. Suzuki S.  Risk factors for emergency cesarean delivery of the second twin after vaginal delivery of the first twin. J Obstet Gynaecol Res, 2009; 35(3):467–71.
50. Atis A, Aydin Y, Donmez M, Sermet H. Apgar Scores in assessing morbidity of the second neonate of cephalic/non-cephalic twins in different delivery modes. J Obstet Gynaecol, 2011; 31:43-7. 
51. Steins Bisschop CN, Vogelvang TE, May AM, Schuitemaker WEN. Mode of delivery in non-cephalic presenting twins: a systematic review. Arch Gynecol Obstet, 2012; 286:237-47. 
52. Engelbrechtsen L, Nielsen EH, Perin T, Oldenburg A, Tabor A, Skibsted L, Danish Fetal Medicine Study Group. Cesarean section for the second twin: a population - based study of occurence and outcome. Birth, 2013; 40: 10-6. 
53. Gourteux N, Deruelle P, Houffin- Debarge V, Dubois JP, Subtil D. Twin-to-twin delivery interval: is a time limit justified? Gynecol Obstetr Fertil, 2007; 35(10):982-9.
54. McGrail CD, Bryant DR. Intertwin time interval. How it affects the immediate neonatal outcome of the second twin. Am J Obstet Gynecol, 2005; 192:1420-2. 
55. Stein W, Misselwitz B, Schmidt S. Twin to twin delivery time interval influencing factors and effect on short term outcome of the second twin. Acta Obstet Gynecol Scand, 2008; 87:346-53.
56. Seelbach-Goebel B. Twin Birth Considering the Current Results of the “Twin Birth Study”. Geburtshilfe Frauenheilkd, 2014; 74(9):838-44.
57. Martius H. Manual de Obstetrică, Ed Medicală, Bucureşti, România, 1956.
58. Arabin B, Van Eyck J. Delayed-interval delivery in twin and triplet pregnancies: 17 years of experience in 1 perinatal center. Am J Obstet Gynecol, 2009; 200(2):154.el.
59. Iserte PP, Vila-Vives JM, Ferri B, Gomez-Portero R, Diago V,Perales-Marin A. Delayed Interval Delivery of the Second Twin: Obstetric Management, Neonatal Outcomes, and 2-Year Follow-Up. J Obstet Gynaecol India, 2014; 64(5):344–8.
60. Cozzolino M, Seralli V, Masini G, Pasquini  L, Di Tommaso M. Delayed-Interval Delivery in Dichorionic Twin Pregnancies: A Single-Center Experience. Ochsner J, 2015;15(3):248-50.
61. Ghai V, Vidyasagar D. Morbidity and mortality factors in twins, an epidemiologic approach. Clinics in Perinatology, 1988; 15:123–40.
62. Bjelic-Radisic V, Pristauz G, Haas J, Giuliani A, Tamussino K. Bader A, Lang U, Sclembach D. Neonatal outcome of second twins depending on presentation and mode of delivery. Twin Res Hum Genet, 2007; 10(3):521-7.
63. Heazell AE, Whitworth M, Duley L, Thornton JG. Use of biochemical tests of placental function for improving pregnancy outcome. Cochrane Database Syst Rev, 2015; 11:CD011202.

Articole din ediţiile anterioare

GINECOLOGIE | Ediţia 3 21 / 2018

Corelaţii clinicopatologice în leiomiosarcoamele uterine – prezentare de cazuri şi review de literatură

Octavian Munteanu, Diana Voicu, Luciana Arsene, Ana Uzunov, Maria Sajin, Tiberiu A. Georgescu, Adrian Dumitru, Andreea Ruxandra Albu, Monica Mihaela Cîrstoiu

Sarcoamele uterine sunt un grup de tumori morfologic etergene extrem de agresive, cu o evoluţie clinică im­pre­vi­zibilă şi cu prognostic slab. Con...

28 septembrie 2018
INTERDISCIPLINARY | Ediţia 2 24 / 2019

Rolul infecţiilor orale în naşterea prematură

Alexandru A Iliescu, Paula Perlea, Kamel Earar, Irina-Maria Gheorghiu

Prematuritatea şi greutatea scăzută la naştere sunt unele din complicaţiile frecvente ale sarcinilor. Infecţiile orale, în special bolile parodonta...

21 mai 2019
OBSTETRICS | Ediţia 2 24 / 2019

Infecţia cu Mycoplasma în determinismul naşterii premature – review din literatură

Anca Rîcu, Cristina Moisei, Romina-Marina Sima, Cristian Balalau, Liana Pleș

Naşterea prematură este responsabilă pentru majoritatea cazurilor de deces neonatal. În cele mai multe dintre aceste cazuri, cauzele nu au fost sta...

21 mai 2019
OBSTETRICS | Ediţia 2 24 / 2019

Impactul bolii renale cronice în sarcină asupra mamei şi fătului. Prezentare de două cazuri şi review al literaturii

Luciana Grozavu-Arsene, Sorin Vasilescu, Octavian Munteanu, Monica Mihaela Cîrstoiu

Incidenţa sarcinii la pacientele cu boală renală cronică (BRC) este în continuă creştere, în ciuda faptului că patologia renală se asociază cu o cr...

21 mai 2019