Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

The cardiopulmonary haemodynamic transition at birth is not different between male and female preterm lambs

Graeme R. Polglase A B F , Stuart B. Hooper A B , Martin Kluckow C , Andrew W. Gill D , Richard Harding E and Timothy J. M. Moss A B

A The Ritchie Centre, Monash Institute of Medical Research, Monash University, Clayton, Vic. 3168, Australia.

B Department of Obstetrics and Gynaecology, Monash University, Clayton, Vic. 3168, Australia.

C Department of Neonatal Medicine, Royal North Shore Hospital and University of Sydney, Sydney, NSW 2065, Australia.

D School of Women’s and Infants’ Health, The University of Western Australia, Crawley, WA 6009, Australia.

E Department of Anatomy and Developmental Biology, Monash University, Clayton, Vic. 3800, Australia.

F Corresponding author. Email: graeme.polglase@monash.edu

Reproduction, Fertility and Development 24(3) 510-516 http://dx.doi.org/10.1071/RD11121
Submitted: 3 May 2011  Accepted: 30 September 2011   Published: 16 November 2011

Abstract

Males born preterm are at greater risk of illness and death than females, principally due to respiratory disease. Much of the excess morbidity occurs within the first few hours of life. Therefore, the aim of the present study was to investigate whether or not differences in the cardiopulmonary transition soon after birth underlie the increased morbidity in males after preterm birth. Nine female and thirteen male lambs (128 ± 2 days gestation) underwent surgery immediately before delivery for implantation of a pulmonary arterial flow-probe and catheters into the main pulmonary artery and a carotid artery. After birth lambs were ventilated for 30 min (tidal volume 7 mL kg–1) while anaesthetised. Arterial pressures and flows were recorded in real time and left-ventricular output measured using Doppler echocardiography. Before birth, fetal cardiopulmonary haemodynamics, arterial blood gases, pH, glucose and lactate did not differ between sexes. Similarly, in the neonatal period there were no significant differences in arterial blood gas status, ventilation parameters, respiratory indices or cardiopulmonary haemodynamics between the sexes. Our data show that the cardiopulmonary transition at birth in ventilated, anaesthetised preterm lambs is not influenced by sex. Thus, the neonatal ‘male disadvantage’ is not explained by an impaired cardiovascular transition at birth.

Additional keywords: Doppler echocardiography, preterm birth, pulmonary blood flow, respiratory distress syndrome, sex difference, sheep.


References

Abeywardana, S. (2006) ‘The Report of the Australian and New Zealand Neonatal Network, 2004’. (ANZNN: Sydney.)

Churg, A. M., Myers, J. L., Tazelaar, H. D., and Wright, J. L. (2005) ‘Thurlbeck’s Pathology of the Lung’. 3rd edn. (Thieme Medical Publishers, Inc.: New York.)

Crossley, K. J., Allison, B. J., Polglase, G. R., Morley, C. J., Davis, P. G., and Hooper, S. B. (2009). Dynamic changes in the direction of blood flow through the ductus arteriosus at birth. J. Physiol. 587, 4695–4704.
Dynamic changes in the direction of blood flow through the ductus arteriosus at birth.CrossRef | 1:CAS:528:DC%2BD1MXhtlSitrvI&md5=e61c99f1b2cbb297c18dde4203c11c0cCAS | 19675069PubMed | open url image1

De Matteo, R., Stacy, V., Probyn, M., Desai, M., Ross, M., and Harding, R. (2008). The perinatal development of arterial pressure in sheep: effects of low birth weight due to twinning. Reprod. Sci. 15, 66–74.
The perinatal development of arterial pressure in sheep: effects of low birth weight due to twinning.CrossRef | 18212356PubMed | open url image1

De Matteo, R., Blasch, N., Stokes, V., Davis, P., and Harding, R. (2010). Induced preterm birth in sheep: a suitable model for studying the developmental effects of moderately preterm birth. Reprod. Sci. 17, 724–733.
Induced preterm birth in sheep: a suitable model for studying the developmental effects of moderately preterm birth.CrossRef | 20445008PubMed | open url image1

Drevenstedt, G. L., Crimmins, E. M., Vasunilashorn, S., and Finch, C. E. (2008). The rise and fall of excess male infant mortality. Proc. Natl. Acad. Sci. USA 105, 5016–5021.
The rise and fall of excess male infant mortality.CrossRef | 1:CAS:528:DC%2BD1cXksVOmurs%3D&md5=9c01dbcc1b088c27e655051a503b014cCAS | 18362357PubMed | open url image1

Ingemarsson, I. (2003a). Gender aspects of preterm birth. BJOG: An International Journal of Obstetrics and Gynaecology 110, 34–38. open url image1

Ingemarsson, I. (2003b). Gender aspects of preterm birth. BJOG: An International Journal of Obstetrics and Gynaecology 110, 34–38. open url image1

Khoury, M. J., Marks, J. S., McCarthy, B. J., and Zaro, S. M. (1985). Factors affecting the sex differential in neonatal mortality: the role of respiratory distress syndrome. Am. J. Obstet. Gynecol. 151, 777–782.
| 1:STN:280:DyaL2M7ks1Sqsg%3D%3D&md5=05f5f2a4a58922eb5b3fae032602e27bCAS | 3976790PubMed | open url image1

Lemons, J. A., Bauer, C. R., Oh, W., Korones, S. B., Papile, L.-A., Stoll, B. J., Verter, J., Temprosa, M., Wright, L. L., Ehrenkranz, R. A., Fanaroff, A. A., Stark, A., Carlo, W., Tyson, J. E., Donovan, E. F., Shankaran, S., Stevenson, D. K., NICHD Neonatal Research Network (2001). Very low birth weight outcomes of the National Institute of Child Health and Human Development Neonatal Research Network, January 1995 through December 1996. Pediatrics 107, e1.
Very low birth weight outcomes of the National Institute of Child Health and Human Development Neonatal Research Network, January 1995 through December 1996.CrossRef | 1:STN:280:DC%2BD3M%2FpsVajuw%3D%3D&md5=27c7b42fc284d614ec1908859abbb481CAS | 11134465PubMed | open url image1

Mitanchez, D. (2007). Glucose regulation in preterm newborn infants. Horm. Res. 68, 265–271.
Glucose regulation in preterm newborn infants.CrossRef | 1:CAS:528:DC%2BD2sXht1Gqu73N&md5=4d498f3c33a3424c19165e4da2190bb3CAS | 17587854PubMed | open url image1

Mittwoch, U. (1993). Blastocysts prepare for the race to be male. Hum. Reprod. 8, 1550–1555.
| 1:STN:280:DyaK2c7jt1amtQ%3D%3D&md5=b877a3d929d2ecd67b659fa0d7910767CAS | 8300805PubMed | open url image1

Ogilvy-Stuart, A. L., and Beardsall, K. (2010). Management of hyperglycaemia in the preterm infant. Arch. Dis. Child. Fetal Neonatal Ed. 95, F126–F131.
Management of hyperglycaemia in the preterm infant.CrossRef | 1:STN:280:DC%2BC3c7osFGqtw%3D%3D&md5=ac5fd6e548e6cdceeb74de09f95c5f90CAS | 20231218PubMed | open url image1

Packer, C. S., Johnson, T. C., Vijay, P., Sharp, T. G., Jha, D., Tighe, S. M., and Chukwu, H. V. (2003). Gender differences in pulmonary arterial reactivity to dilatory agonists in pulmonary hypertension. J. Gend. Specif. Med. 6, 30–38.
| 14513574PubMed | open url image1

Perelman, R. H., Engle, M. J., Palta, M., Kemnitz, J. W., and Farrell, P. M. (1986a). Fetal lung development in male and female nonhuman primates. Pediatr. Res. 20, 987–991.
Fetal lung development in male and female nonhuman primates.CrossRef | 1:STN:280:DyaL2s%2FktVGmsw%3D%3D&md5=1cddc7ac45c5e82fda8f26ce9e311047CAS | 3774413PubMed | open url image1

Perelman, R. H., Palta, M., Kirby, R., and Farrell, P. M. (1986b). Discordance between male and female deaths due to the respiratory distress syndrome. Pediatrics 78, 238–244.
| 1:STN:280:DyaL283os1eqtA%3D%3D&md5=7eb0d6fc69fdcaaa295c1e946781a77eCAS | 3737300PubMed | open url image1

Polglase, G. R., and Hooper, S. B. (2006). Role of intra-luminal pressure in regulating PBF in the fetus and after birth. Curr. Pediatr. Rev. 2, 287–299.
Role of intra-luminal pressure in regulating PBF in the fetus and after birth.CrossRef | open url image1

Polglase, G. R., Moss, T. J., Nitsos, I., Allison, B. J., Pillow, J. J., and Hooper, S. B. (2008). Differential effect of recruitment manoeuvres on pulmonary blood flow and oxygenation during HFOV in preterm lambs. J. Appl. Physiol. 105, 603–610.
Differential effect of recruitment manoeuvres on pulmonary blood flow and oxygenation during HFOV in preterm lambs.CrossRef | 18535129PubMed | open url image1

Polglase, G. R., Hooper, S. B., Gill, A. W., Allison, B. J., McLean, C. J., Nitsos, I., Pillow, J. J., and Kluckow, M. (2009). Cardiovascular and pulmonary consequences of airway recruitment in preterm lambs. J. Appl. Physiol. 106, 1347–1355.
Cardiovascular and pulmonary consequences of airway recruitment in preterm lambs.CrossRef | 19213936PubMed | open url image1

Polglase, G. R., Hooper, S. B., Gill, A. W., Allison, B. J., Crossley, K. J., Moss, T. J., Nitsos, I., Pillow, J. J., and Kluckow, M. (2010). Intrauterine inflammation causes pulmonary hypertension and cardiovascular sequelae in preterm lambs. J. Appl. Physiol. 108, 1757–1765.
Intrauterine inflammation causes pulmonary hypertension and cardiovascular sequelae in preterm lambs.CrossRef | 20339013PubMed | open url image1

Polglase, G. R., Kluckow, M., Gill, A. W., Allison, B. J., Moss, T. J., Dalton, R. G., Pillow, J. J., Andersen, C. C., Nitsos, I., and Hooper, S. B. (2011). Cardiopulmonary haemodynamics in lambs during induced capillary leakage immediately after preterm birth. Clin. Exp. Pharmacol. Physiol. 38, 222–228.
Cardiopulmonary haemodynamics in lambs during induced capillary leakage immediately after preterm birth.CrossRef | 1:CAS:528:DC%2BC3MXkvVait7c%3D&md5=607ab0661d0ba4e4555480c638b99b00CAS | 21281333PubMed | open url image1

Pollak, A., and Birnbacher, R. (2004). Preterm male infants need more initial respiratory support than female infants. Acta Paediatr. 93, 447–448.
Preterm male infants need more initial respiratory support than female infants.CrossRef | 1:STN:280:DC%2BD2c3ovVCgtQ%3D%3D&md5=34fd0496c1e711651549554d379a5e99CAS | 15188966PubMed | open url image1

Provost, P. R., Boucher, E., and Tremblay, Y. (2009). Apolipoprotein A-I, A-II, C-II and H expression in the developing lung and sex difference in surfactant lipids. J. Endocrinol. 200, 321–330.
Apolipoprotein A-I, A-II, C-II and H expression in the developing lung and sex difference in surfactant lipids.CrossRef | 1:CAS:528:DC%2BD1MXjs1Wksrk%3D&md5=59fe799412de4278a8b05e25e8001877CAS | 19106236PubMed | open url image1

Sozo, F., Ishak, N., De Matteo, R., Hooper, S. B., and Harding, R. (2009). Structural and biochemical development of the ovine fetal lung: are there gender differences? J. Paediatr. Child Health 45, A114.. open url image1

Stark, M. J., Clifton, V. L., and Wright, I. M. (2008). Sex-specific differences in peripheral microvascular blood flow in preterm infants. Pediatr. Res. 63, 415–419.
Sex-specific differences in peripheral microvascular blood flow in preterm infants.CrossRef | 18356749PubMed | open url image1

Stark, M. J., Wright, I. M., and Clifton, V. L. (2009). Sex-specific alterations in placental 11beta-hydroxysteroid dehydrogenase 2 activity and early postnatal clinical course following antenatal betamethasone. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R510–R514.
Sex-specific alterations in placental 11beta-hydroxysteroid dehydrogenase 2 activity and early postnatal clinical course following antenatal betamethasone.CrossRef | 1:CAS:528:DC%2BD1MXhtVaht7zK&md5=32c68794b5b139872ee35c4cf84a37baCAS | 19535674PubMed | open url image1

Stevenson, D. K., Verter, J., Fanaroff, A. A., Oh, W., Ehrenkranz, R. A., Shankaran, S., Donovan, E. F., Wright, L. L., Lemons, J. A., Tyson, J. E., Korones, S. B., Bauer, C. R., Stoll, B. J., and Papile, L. A. (2000). Sex differences in outcomes of very low birthweight infants: the newborn male disadvantage. Arch. Dis. Child. Fetal Neonatal Ed. 83, F182–F185.
Sex differences in outcomes of very low birthweight infants: the newborn male disadvantage.CrossRef | 1:STN:280:DC%2BD3M%2FksVOlug%3D%3D&md5=c06486c9695bc886ca7b31efffaa0406CAS | 11040165PubMed | open url image1

Torday, J. S. (1984). The sex difference in type II cell surfactant synthesis originates in the fibroblast in vitro. Exp. Lung Res. 7, 187–194.
The sex difference in type II cell surfactant synthesis originates in the fibroblast in vitro.CrossRef | 1:CAS:528:DyaL2MXhsVensr8%3D&md5=9cb1638eca7d2daf5c276880b09c6093CAS | 6549292PubMed | open url image1

Torday, J. S., and Nielsen, H. C. (1987). The sex difference in fetal lung surfactant production. Exp. Lung Res. 12, 1–19.
The sex difference in fetal lung surfactant production.CrossRef | 1:CAS:528:DyaL2sXhtlGksbk%3D&md5=d5cfb67461c0e4d68082708ec205930dCAS | 3545796PubMed | open url image1

Willet, K. E., Jobe, A. H., Ikegami, M., Polk, D., Newnham, J., Kohan, R., Gurrin, L., and Sly, P. D. (1997). Postnatal lung function after prenatal steroid treatment in sheep: effect of gender. Pediatr. Res. 42, 885–892.
Postnatal lung function after prenatal steroid treatment in sheep: effect of gender.CrossRef | 1:CAS:528:DyaK2sXnvFags7Y%3D&md5=1d3ab8aeaaacd4655e4864174a6eb4f4CAS | 9396574PubMed | open url image1



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