Abstract
Objective: Twin studies offer opportunities to investigate mechanisms underlying sex-associated differences in perinatal outcomes. The objective of the study was to investigate sex-related differences in perinatal complications.
Study design: A cohort of 16,045 twin pregnancies – 32,090 twins – was explored for obstetric complications, perinatal and infant mortality, and neonatal morbidities.
Results: Twin pregnancies with a female fetus had an increased risk for preeclampsia, but otherwise there were no pregnancy complications associated with fetal sex. After birth, female-female twins had lower early neonatal and infant mortality, and lower risk for respiratory morbidities than male-male twins at all gestational ages. In unlike-sexed twin pairs, very preterm males had higher respiratory morbidity than females and, females were at higher risk for being growth restricted.
Conclusion: Male-male twins have higher respiratory morbidity and neonatal mortality than female-female twins. In unliked-sexed twin pairs, the males seem to be protected by having a female co-twin.
Acknowledgments
The study was supported by grants from the Swedish Medical Research Council (Grant 0037), Lund University Hospital Funds and Uppsala University.
References
[1] Acromite MT, Mantzoros CS, Leach RE, Hurwitz J, Dorey LG. Androgens in preeclampsia. Am J Obstet Gynecol. 1999;180:60–3.10.1016/S0002-9378(99)70150-XSearch in Google Scholar
[2] Altman M, Vanpee M, Cnattingius S, Norman M. Risk factors for acute respiratory morbidity in moderately preterm infants. Paediatr Perinat Epidemiol. 2013;27:172–81.10.1111/ppe.12035Search in Google Scholar
[3] Benterud T, Sandvik L, Lindemann R. Cesarean section is associated with more frequent pneumothorax and respiratory problems in the neonate. Acta Obstet Gynecol Scand. 2009;88:359–61.10.1080/00016340802668899Search in Google Scholar
[4] Blickstein I, Weissman A. Birth weight discordancy in male-first and female-first pairs of unlike-sexed twins. Am J Obstet Gynecol. 1990;162:661–3.10.1016/0002-9378(90)90977-FSearch in Google Scholar
[5] Chen SJ, Vohr BR, Oh W. Effects of birth order, gender, and intrauterine growth retardation on the outcome of very low birth weight in twins. J Pediatr. 1993;123:132–6.10.1016/S0022-3476(05)81556-2Search in Google Scholar
[6] Chervenak FA, Youcha S, Johnson RE, Berkowitz RL, Hobbins JC. Twin gestation. Antenatal diagnosis and perinatal outcome in 385 consecutive pregnancies. J Reprod Med. 1984;29:727–30.Search in Google Scholar
[7] Dammann CE, Ramadurai SM, McCants DD, Pham LD, Nielsen HC. Androgen regulation of signaling pathways in late fetal mouse lung development. Endocrinology. 2000;141:2923–9.10.1210/endo.141.8.7615Search in Google Scholar PubMed
[8] Derom R, Derom C, Loos RJ, Thiery E, Vlietinck R, Fryns JP. Gender mix:does it modify birthweight--outcome association? Paediatr Perinat Epidemiol. 2005;19(Suppl 1):37–40.10.1111/j.1365-3016.2005.00613.xSearch in Google Scholar PubMed
[9] Drevenstedt GL, Crimmins EM, Vasunilashorn S, Finch CE. The rise and fall of excess male infant mortality. Proc Natl Acad Sci USA. 2008;105:5016–21.10.1073/pnas.0800221105Search in Google Scholar PubMed PubMed Central
[10] Elsmen E, Hansen Pupp I, Hellstrom-Westas L. Preterm male infants need more initial respiratory and circulatory support than female infants. Acta Paediatr. 2004;93:529–33.10.1080/08035250410024998Search in Google Scholar PubMed
[11] Elsmen E, Kallen K, Marsal K, Hellstrom-Westas L. Fetal gender and gestational-age-related incidence of pre-eclampsia. Acta Obstet Gynecol Scand. 2006;85:1285–91.10.1080/00016340600578274Search in Google Scholar PubMed
[12] Fellman V, Hellstrom-Westas L, Norman M, Westgren M, Kallen K, Lagercrantz H, et al. One-year survival of extremely preterm infants after active perinatal care in Sweden. J Am Med Assoc. 2009;301:2225–33.10.1001/jama.2009.771Search in Google Scholar
[13] Ghai V, Vidyasagar D. Morbidity and mortality factors in twins. An epidemiologic approach. Clin Perinatol. 1988;15:123–40.10.1016/S0095-5108(18)30730-9Search in Google Scholar
[14] Glinianaia SV, Magnus P, Harris JR, Tambs K. Is there a consequence for fetal growth of having an unlike-sexed cohabitant in utero? Int J Epidemiol. 1998;27:657–9.10.1093/ije/27.4.657Search in Google Scholar
[15] Hack KE, Koopman-Esseboom C, Derks JB, Elias SG, de Kleine MJ, Baerts W, et al. Long-term neurodevelopmental outcome of monochorionic and matched dichorionic twins. PLoS ONE. 2009;4:e6815.10.1371/journal.pone.0006815Search in Google Scholar
[16] Halvorsen CP, Ek S, Dellgren A, Grunewald C, Kublickas M, Westgren M, et al. Survival and neonatal outcome after fetoscopic guided laser occlusion (FLOC) of twin-to-twin transfusion syndrome in Sweden. J Perinat Med. 2012;40:533–8.10.1515/jpm-2011-0265Search in Google Scholar
[17] Hindmarsh GJ, O’Callaghan MJ, Mohay HA, Rogers YM. Gender differences in cognitive abilities at 2 years in ELBW infants. Extremely low birth weight. Early Hum Dev. 2000;60:115–22.10.1016/S0378-3782(00)00105-5Search in Google Scholar
[18] Hoffman EL, Bennett FC. Birth weight less than 800 grams:changing outcomes and influences of gender and gestation number. Pediatrics. 1990;86:27–34.10.1542/peds.86.1.27Search in Google Scholar
[19] Hsu CD, Johnson TR, Witter FR. Fetal gender effect on pre-eclampsia:a retrospective study of Baltimore area in the United States of America. Int J Gynaecol Obstet. 1994;45:160–1.10.1016/0020-7292(94)90125-2Search in Google Scholar
[20] Marsal K, Persson PH, Larsen T, Lilja H, Selbing A, Sultan B. Intrauterine growth curves based on ultrasonically estimated foetal weights. Acta Paediatr. 1996;85:843–8.10.1111/j.1651-2227.1996.tb14164.xSearch in Google Scholar PubMed
[21] Massaro D, Massaro GD. Estrogen receptor regulation of pulmonary alveolar dimensions:alveolar sexual dimorphism in mice. Am J Physiol Lung Cell Mol Physiol. 2006;290:L866–70.10.1152/ajplung.00396.2005Search in Google Scholar PubMed
[22] McMillen MM. Differential mortality by sex in fetal and neonatal deaths. Science. 1979;204:89–91.10.1126/science.571144Search in Google Scholar
[23] Melamed N, Yogev Y, Glezerman M. Effect of fetal sex on pregnancy outcome in twin pregnancies. Obstet Gynecol. 2009;114:1085–92.10.1097/AOG.0b013e3181bd8874Search in Google Scholar
[24] Papile LA, Burstein J, Burstein R, Koffler H. Incidence and evolution of subependymal and intraventricular hemorrhage:a study of infants with birth weights <1500 gm. J Pediatr. 1978;92:529–34.10.1016/S0022-3476(78)80282-0Search in Google Scholar
[25] Perelman RH, Palta M, Kirby R, Farrell PM. Discordance between male and female deaths due to the respiratory distress syndrome. Pediatrics. 1986;78:238–44.10.1542/peds.78.2.238Search in Google Scholar
[26] Powers WF, Wampler NS. Further defining the risks confronting twins. Am J Obstet Gynecol. 1996;175:1522–8.10.1016/S0002-9378(96)70101-1Search in Google Scholar
[27] Rydhstrom H. Discordant birthweight and late fetal death in like-sexed and unlike-sexed twin pairs:a population-based study. Br J Obstet Gynaecol. 1994;101:765–9.10.1111/j.1471-0528.1994.tb11943.xSearch in Google Scholar
[28] Sarkar P, Bergman K, Fisk NM, O’Connor TG, Glover V. Amniotic fluid testosterone:relationship with cortisol and gestational age. Clin Endocrinol (Oxf). 2007;67:743–7.10.1111/j.1365-2265.2007.02955.xSearch in Google Scholar PubMed
[29] Shinwell ES, Reichman B, Lerner-Geva L, Boyko V, Blickstein I. “Masculinizing” effect on respiratory morbidity in girls from unlike-sex preterm twins:a possible transchorionic paracrine effect. Pediatrics. 2007;120:e447–53.10.1542/peds.2006-3574Search in Google Scholar PubMed
[30] Stevenson DK, Verter J, Fanaroff AA, Oh W, Ehrenkranz RA, Shankaran S, et al. Sex differences in outcomes of very low birthweight infants: the newborn male disadvantage. Arch Dis Child Fetal Neonatal Ed. 2000;83:F182–185.10.1136/fn.83.3.F182Search in Google Scholar
[31] Van Marter LJ, Leviton A, Kuban KC, Pagano M, Allred EN. Maternal glucocorticoid therapy and reduced risk of bronchopulmonary dysplasia. Pediatrics 1990;86:331–6.10.1542/peds.86.3.331Search in Google Scholar
[32] Vatten LJ, Skjaerven R. Offspring sex and pregnancy outcome by length of gestation. Early Hum Dev. 2004;76:47–54.10.1016/j.earlhumdev.2003.10.006Search in Google Scholar PubMed
[33] Wood NS, Marlow N, Costeloe K, Gibson AT, Wilkinson AR. Neurologic and developmental disability after extremely preterm birth. EPICure Study Group. N Engl J Med. 2000;343:378–84.10.1056/NEJM200008103430601Search in Google Scholar PubMed
The authors stated that there are no conflicts of interest regarding the publication of this article.
©2014 by Walter de Gruyter Berlin Boston
Articles in the same Issue
- frontmatter
- Review articles
- Evaluation of the role of first-trimester obstetric ultrasound in the detection of major anomalies: a systematic review
- Austrian Newborn Screening Program: a perspective of five decades
- Original articles – Obstetrics
- Cervical strain determined by ultrasound elastography and its association with spontaneous preterm delivery
- Risk factors for unfavorable pregnancy outcome in women with adverse childhood experiences
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- Premature rupture of membranes at term in low risk women: how long should we wait in the “latent phase”?
- Ferrous bisglycinate 25 mg iron is as effective as ferrous sulfate 50 mg iron in the prophylaxis of iron deficiency and anemia during pregnancy in a randomized trial
- Neonatal serum magnesium concentrations are determined by total maternal dose of magnesium sulfate administered for neuroprotection
- Labor induction in nulliparous women with an unfavorable cervix: double balloon catheter versus dinoprostone
- Peripartum thromboprophylaxis before and after implementation of a uniform heparin protocol
- Original articles – Fetus
- Impact of sex on perinatal mortality and morbidity in twins
- Opinion paper
- Preeclampsia is caused by continuous sympathetic center excitation due to an enlarged pregnant uterus
- Original articles – Newborn
- Practical application of kangaroo mother care in preterm infants: clinical characteristics and safety of kangaroo mother care
- Survival and neonatal morbidity among extremely preterm born infants in relation to gestational age based on the last menstrual period or ultrasonographic examination
- Short communication
- Reference values of nuchal translucency thickness in a Brazilian population sample: experience from a single center
- Letters to the Editor
- Hepatic rupture: a rare but serious complication of HELLP syndrome
- Reply
- Reply to: hepatic rupture – a rare but serious complication of HELLP syndrome
- Congress Calendar
- Congress Calendar
Articles in the same Issue
- frontmatter
- Review articles
- Evaluation of the role of first-trimester obstetric ultrasound in the detection of major anomalies: a systematic review
- Austrian Newborn Screening Program: a perspective of five decades
- Original articles – Obstetrics
- Cervical strain determined by ultrasound elastography and its association with spontaneous preterm delivery
- Risk factors for unfavorable pregnancy outcome in women with adverse childhood experiences
- Peroxisome proliferator-activated receptor-gamma (PPARγ) is down regulated in trophoblast cells of gestational diabetes mellitus (GDM) and in trophoblast tumour cells BeWo in vitro after stimulation with PPARγ agonists
- Premature rupture of membranes at term in low risk women: how long should we wait in the “latent phase”?
- Ferrous bisglycinate 25 mg iron is as effective as ferrous sulfate 50 mg iron in the prophylaxis of iron deficiency and anemia during pregnancy in a randomized trial
- Neonatal serum magnesium concentrations are determined by total maternal dose of magnesium sulfate administered for neuroprotection
- Labor induction in nulliparous women with an unfavorable cervix: double balloon catheter versus dinoprostone
- Peripartum thromboprophylaxis before and after implementation of a uniform heparin protocol
- Original articles – Fetus
- Impact of sex on perinatal mortality and morbidity in twins
- Opinion paper
- Preeclampsia is caused by continuous sympathetic center excitation due to an enlarged pregnant uterus
- Original articles – Newborn
- Practical application of kangaroo mother care in preterm infants: clinical characteristics and safety of kangaroo mother care
- Survival and neonatal morbidity among extremely preterm born infants in relation to gestational age based on the last menstrual period or ultrasonographic examination
- Short communication
- Reference values of nuchal translucency thickness in a Brazilian population sample: experience from a single center
- Letters to the Editor
- Hepatic rupture: a rare but serious complication of HELLP syndrome
- Reply
- Reply to: hepatic rupture – a rare but serious complication of HELLP syndrome
- Congress Calendar
- Congress Calendar