Skip to main content
Log in

Alterations in the Maternal Peripheral Microvascular Response in Pregnancies Complicated by Preeclampsia and the Impact of Fetal Sex

  • Original Articles
  • Published:
The Journal of the Society for Gynecologic Investigation: JSGI Aims and scope Submit manuscript

Abstract

Objective

Peripheral microvascular function is altered in preeclampsia (PE). Recent studies suggest that maternal physiology varies with fetal sex. We wanted to examine if there were sex-specific differences in maternal peripheral microvascular function in normal pregnancy and pregnancy complicated by PE.

Methods

Peripheral microvascular responses were examined using the noninvasive technique of laser Doppler flowmetry in normotensive healthy pregnant women and in women diagnosed with PE. We measured baseline perfusion, response to thermal hyperemia, post-occlusive reperfusion, and vasodilatation in response to corticotropin-releasing hormone (CRH), a potent vasodilator in human skin.

Results

At 31 to 40 weeks’ gestation those women with a male fetus exhibited increased vasodilatation in response to CRH (P <0.5) and greater baseline perfusion (P <.05) than those pregnant with a female fetus. PE women pregnant with a male fetus demonstrated a significantly reduced vasodilatation in response to CRH (P <.05), reduced baseline perfusion (P <.05), and reduced response to thermal hyperemia (P <.05) compared to normotensive women pregnant with a male fetus. Microvascular function was not significantly different between preeclamptic and normotensive women with a female fetus.

Conclusion

These data show that there are differences in maternal peripheral microvascular function in relation to fetal sex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Abraham WT, Schrier RW. Body fluid volume regulation in health and disease. Adv Intern Med 1994;39:23–47.

    CAS  PubMed  Google Scholar 

  2. Bosio PM, McKenna PJ, Controy R, O’Herlihy C. Matrnal central hemodynamics in hypertensive disorders of pregnancy. Obstet Gynecol 1999;94:978–984.

    CAS  PubMed  Google Scholar 

  3. Alexander BT, Reckelhoff JF, Kassab S, Granger JP. Differential expression of renal nitric oxide synthase isoforms during pregnancy in rats. Hypertension 1999;33:435–439.

    Article  CAS  PubMed  Google Scholar 

  4. Cox BE, Williams CE, Rosenfeld CR. Angiotensin II indirectly vasoconstricts the ovine uterine circulation. Am J Physiol Regul Integr Comp Physiol 2000;278:R337–R344.

    Article  CAS  PubMed  Google Scholar 

  5. Brooks VL, Clow KA, Welch LS, Giraud GD. Does nitric oxide contribute to the basal vasodilation of pregnancy in conscious rabbits? Am J Physiol Regul Integr Comp Physiol 2001;281:R1624–R1632.

    Article  CAS  PubMed  Google Scholar 

  6. Hibbard J, Shroff SG, Lang RM. Cardiovascular changes in pre-eclampsia. Semin Nephrol 2004;24:580–587.

    Article  PubMed  Google Scholar 

  7. Eguchi K, Oguni N, Sawai T, Yonezawa M. Comparison of plasma concentrations or arginine vasopressin (AVP) and atrial natriuretic petide (ANP) in normal and pre-eclamptic pregnancies. J Perinat Med 1996;24:437–443.

    Article  CAS  PubMed  Google Scholar 

  8. Salas SP, Rosso P, Espinoza R, Robert JA, Valdes G, Donoso E. Maternal plasma volume expanison and hormonal changes in women with idiopathic fetal growth retardation. Obstet Gynecol 1993;81:1029–1033.

    CAS  PubMed  Google Scholar 

  9. Nadar SK, Karalis I, Yemini E Al, Blann AD, Lip GY. Plasma markers of angiogenesis in pregnancy induced hypertension. Thromb Haemost 2005;94:1071–1076.

    Article  CAS  PubMed  Google Scholar 

  10. Rinehart BK, Terrone DA, Lagoo-Deenadayalan S, et al. Expression of the placental cytokines tumour necrosis factor alpha, interleukin-1 beta, and interleukin-10 is increased in pre-eclampsia. Am J Obstet Gynecol 1999;181:915–920.

    Article  CAS  PubMed  Google Scholar 

  11. Roberts JM, Taylor RN, Goldfien A. Clinical and biochemical evidence of endothelial cell dysfunction in the pregnancy syndrome pre-eclampsia. Am J Hypertens 1991;4:700–708.

    Article  CAS  PubMed  Google Scholar 

  12. Curtis NE, Gude NM, King RG. Nitric oxide metabolites in normal human pregnancy and pre-eclampsia. Hypertens Pregnancy 1995;14:339–349.

    Article  CAS  Google Scholar 

  13. Crompton R, Clifton VL, Bisits AT, Read MA, Smith R, Wright IMR. Corticotropin releasing hormone causes vasodilatation in human skin via mast cell dependant pathways. J Clin Endocrinol Metab 2003;88:5427–5432.

    Article  CAS  PubMed  Google Scholar 

  14. Chrousos GP, Gold PW. The concepts of stress and stress system disorders. Overview of phsical and behavioural homeostasis. JAMA 1992;267:1244–1252.

    Article  CAS  PubMed  Google Scholar 

  15. Singh LK, Boucher W, Pang X, et al. Potent mast cell degranulation and vascular permeability triggered by urocortin through activation of corticotropin-releasing hormone receptors. J Pharmacol Exp Ther 1999;288:1349–1356.

    CAS  PubMed  Google Scholar 

  16. McLean M, Smith R. Corticotropin-releasing hormone and human parturition. Reproduction 2001;121:493–501.

    Article  CAS  PubMed  Google Scholar 

  17. Clifton VL, Read MA, Leitch IM, et al. corticotropin-releasing hormone-induced vasodilatation in the human fetal-placental circulation: Involvement of the nitric oxide-cyclic guanosine 3′,5′-monophosphate-mediated pathway. J Clin Endocrinol Metab 1995;80:2888–2893.

    CAS  PubMed  Google Scholar 

  18. Ingemarsson I. Gender aspects of preterm birth. Br J Obstet Gynaecol 2003;110:34–38.

    Article  Google Scholar 

  19. Cooperstock M, Campbell J. Excess males in preterm birth: Interaction with gestational age, race, and mutiple birth. Obstet Gynaecol 1996;88:189–193.

    Article  CAS  Google Scholar 

  20. Stevenson DK, Verter J, Fanaroff AA et al. Sex differences in outcomes of very low birthweight infants: The newborn male disadvantage. Arch Dis Child Fetal Neonat Ed 2000;83:F182–F185.

    Article  CAS  Google Scholar 

  21. Clifton VL, Murphy VE. Maternal asthma as a model for examining fetal sex specific effects on maternal physiology and placental mechanisms that regulate human fetal growth. Placenta 2003;168:S45–S42.

    Google Scholar 

  22. Brown MA, Hague WM, Higgins J, et al. Australasian Society of the Study of Hypertension in pregnancy. The detection, investigation, and management of hypertension in pregnancy: Full consensus statement. Aust N Z J Obstet Gynaecol 2000;40:139–155.

    Article  CAS  PubMed  Google Scholar 

  23. Kubli S, Waeber B, Dalle-Ave A, Feihl F. Reproducibility of laser doppler imaging of skin blood flow as a tool to assess endothelial function. J cardiovasc Pharmacol 2000;36:640–648.

    Article  CAS  PubMed  Google Scholar 

  24. Hu J, Norman M, Wallensteen M, Gennser G. Increased large arterial stiffiness and impaired acetlycholine induced skin vasodilatation in women with previous gestational diabetes. Br J Obstet Gynaecol 1998;105:1279–1287.

    Article  CAS  PubMed  Google Scholar 

  25. Tur E, Tamir A, Guy RH. Cutaneous blood flow in gestational hypertension and normal pregnancy. J Invest Dermatol 1992;99:310–314.

    Article  CAS  PubMed  Google Scholar 

  26. Anim-Nyame N, Sooranna SR, Johnson MR, Gamble J, Steer PJ. A longitudenal study of resting periphral blood fow in normal pregnancy and pregnancies complicated by chronic hypertension and pre-eclampsia. Cardiovasc Res 2001;50:603–609.

    Article  CAS  PubMed  Google Scholar 

  27. Beinder E, Schlemabach D. Skin during reactive hyperemia and local hyperthermia in patients with pre-eclampsia. Obstet Gynecol 2001;98:313–318.

    CAS  PubMed  Google Scholar 

  28. Bowyer L, Brown MA, Jones M. Forearm blood flow in preeclampsia. Br J Obstet Gynaecol 2003;110:383–391.

    Article  Google Scholar 

  29. Kisin I, Yuzhakov S. Effects of reserpine, guanethidine, and methyldopa on cardiac output and its distribution. Eur J Pharmacol 1976;35:253–260.

    Article  CAS  PubMed  Google Scholar 

  30. Carbillon L, Uzan M, Uzan S. Pregnancy, vascular tone, and maternal hemodynamics. A crucial adaptation. Obstet Gynecol Sury 2000;55:574–581.

    Article  CAS  Google Scholar 

  31. Anumba DO, Robson SC, Boys RJ, Ford GA. Nitric oxide activity in the peripheral vasculature during normotensive and pre-eclamptic pregnancy. Am J Physiol 1999;277:H848–H854.

    CAS  PubMed  Google Scholar 

  32. Parisi VM, Walsh SW. Arachidonic acid metabolites and regulation of placental and other vascular tone during pregnancy. Semin Perinatol 1986;10:288–298.

    CAS  PubMed  Google Scholar 

  33. Kinzler WL, Smulian JC, Ananth CV, Vintzileos AM. Noninvasive ultrasound assessment of maternal vascular reactivity during pregnancy: A longitudinal study. Obstet Gynaecol 2004;104:362–369.

    Article  Google Scholar 

  34. Clifton VL, Crompton R, Smith R, Wright IM. Microvascular effects of CRH in human skin vary in relation to gender. J Clin Endocrinol Metab 2002;87:267–270.

    Article  CAS  PubMed  Google Scholar 

  35. Clifton VL, Read MA, Leitch IM, et al. Corticotropin releasing hormone induced vasodilatation in the human fetal placental circulation. J Clin Endocrinol Metab 1994;79:666–669.

    CAS  PubMed  Google Scholar 

  36. Clifton VL, Crompton R, Read MA, Gibson PG, Smith R, Wright IM. Microvascular effects of CRH in human skin vary in relation to oestrogen concentration during the menstrual cycle. J Endocrinology 2005;186:69–76.

    Article  CAS  Google Scholar 

  37. Eneroth-Grimfors E, Linblad LE, Westgren M, Ihrman-Sandahl C, Bevegard S. Non-invasive test of microvascular endothelial function in normal and hypertensive pregnancies. Br J Obstet Gynaecol 1993;100:469–471.

    Article  CAS  PubMed  Google Scholar 

  38. Davis KR, Ponnampalam J, Hayman R, Baker PN, Arulkumaran S, Donnelly R. Microvascular vasodilator response to acetlycholine is increased in women with preeclampsia. Br J Obstet Gynaecol 2001;108:610–614.

    CAS  Google Scholar 

  39. Kellogg DL, Liu Y, Kosiba IF, O’Donnell D. Role of nitric oxide in the vascular effects of local warming of the skin in humans. J Appl Physiol 1999;86:1185–1190.

    Article  CAS  PubMed  Google Scholar 

  40. Beecroft N, Cochrane GM, Milburn HJ. Effect of sex of fetus on asthma during pregnancy: A blind prospective study. BMJ 1998;317:856–857.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Murphy VE, Gibson P, Giles WB, et al. Maternal asthma is associated with reduced female fetal growth. Am J Respir Crit Care Med 2003;168:1317–1323.

    Article  PubMed  Google Scholar 

  42. Tamimi RM, Mucci LA. Average energy intake among pregnant women carrying a boy compared with a girl. BMJ 2003;326:1245–1246.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Steier JA, Ulstein M, Myking OL. Human chorionic gonadotropin and testosterone in normal and pre-eclamptic pregnancies in relation to fetal sex. Obstet Gynecol 2002;100:552–556.

    CAS  PubMed  Google Scholar 

  44. Al Atawi F, Warsy A, Babay Z, Addar M. Fetal sex and leptin concentration in pregnant females. Ann Saudi Med 2005;25:124–128.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Nelson JL. Microchimerism and human autoimmune diseases. Lupus 2002;11:651–654.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ian M. R. Wright MBBS, FRACP.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stark, M.J., Dierkx, L., Clifton, V.L. et al. Alterations in the Maternal Peripheral Microvascular Response in Pregnancies Complicated by Preeclampsia and the Impact of Fetal Sex. Reprod. Sci. 13, 573–578 (2006). https://doi.org/10.1016/j.jsgi.2006.06.006

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.jsgi.2006.06.006

Key words

Navigation