Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Circulation to Female Reproductive Organs

Giacomo Meschia

10.1002/cphy.cp020308

Source: Supplement 8: Handbook of Physiology, The Cardiovascular System, Peripheral Circulation and Organ Blood Flow

Originally published: 1983

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Utero‐Ovarian Arteries and Veins
2 Blood Flow to the Nonpregnant Uterus
2.1 Effect of Estrogens
2.2 Effect of Vasoactive Compounds
3 Placental Circulation
3.1 Vascular Anatomy
3.2 Theoretical Models
3.3 Flow‐Limited Placental Clearance
3.4 Growth of Uteroplacental Blood Flow
3.5 Relation of Blood Flow to O2 Consumption in the Gravid Uterus
3.6 Comparative Aspects
3.7 Pressure‐Flow Relationship
4 Short‐Term Regulation of Uteroplacental Blood Flow
4.1 Respiratory Gases
4.2 Estrogens
4.3 Catecholamines
4.4 Prostaglandins
4.5 Renin‐Angiotensin System
4.6 Neural Control
4.7 Concepts of Placental Blood Flow Regulation
5 Ovarian Blood Flow
6 Mammary Blood Flow
Figure 1. Figure 1.

Branching of uterine arteries within the human uterus.

From Ramsey and Donner 139
Figure 2. Figure 2.

Semilogarithmic plot of variation of uterine blood flow in nonpregnant sheep during estrous cycle.

From Greiss and Anderson 80
Figure 3. Figure 3.

Preparation used to study the local effect of hormones and drugs on the uterine blood flow in sheep. Substance under investigation is injected intra‐arterially via infusion catheter, and blood flow through uterine artery is measured continually by means of an electromagnetic flow probe.

From Resnik, Meschia, et al. 153
Figure 4. Figure 4.

Blood flow response to 1‐min injection of 1 μg estradiol‐17β (E2) or estriol (E3) into uterine artery of nonpregnant ovariectomized ewe. Preinjection flow was approximately 10 ml/min.

From Clewell, Carson, and Meschia 50
Figure 5. Figure 5.

Cycloheximide blocks uterine blood flow response to estrogen. This protein‐synthesis inhibitor was infused into right uterine artery from time 0 to 2.5 h. The sheep received an intravenous injection of estrogen 30 min after time 0. Note the normal blood flow response to estrogen on left side of uterus and reversible inhibition of response on right side. Under cycloheximide blockade, uterine vasculature had a normal vasodilatory response to bradykinin.

From Killam, Meschia, et al. 96
Figure 6. Figure 6.

Countercurrent arrangement of maternal and fetal microcirculatory channels in placenta of a small rodent. Lightly stippled area, course of maternal blood; densely stippled area, course of fetal blood. In exchange area (labyrinth) maternal and fetal blood run in opposite directions.

From Mossman 126. Organogenesis, edited by Robert L. DeHaan and Heinrich Ursprung. Copyright © 1965 by Holt, Rinehart and Winston, Inc. Reprinted by permission of Holt, Rinehart and Winston
Figure 7. Figure 7.

Circulation of maternal and fetal blood in human placenta.

From Ramsey 138
Figure 8. Figure 8.

Three elementary models of placental transfer.
Figure 9. Figure 9.

Ratio of clearance to blood flow (i.e., effectiveness, transfer index) plotted against ratio of permeability to blood flow with maternal and fetal placental blood flows equal. Same models as in Fig. 8.
Figure 10. Figure 10.

Hypothetical double countercurrent exchange formed by a maternal and a fetal capillary loop. Maternal blood enters at A carrying a highly diffusible substance with concentration 100 and runs in opposite direction to fetal blood entering at a with concentration 0. At end of arterial branches of the 2 loops, fetal concentration is 100 and maternal concentration is 0. The 2 streams run countercurrent again in the venous branches of the loops (V, v) and consequently maternal concentration increases to 100 and fetal concentration returns to 0. Result is no net transfer of highly diffusible substance from mother to fetus.
Figure 11. Figure 11.

Difference between arterial and venous oxygen content across the uterine circulation, expressed as percent of arterial oxygen content, plotted against gestational age for chronic sheep preparations. End of gestation is approximately day 145.
Figure 12. Figure 12.

Blood flow to the uterus of pregnant sows in early gestation. Note initial decline of blood flow in first 11 days of pregnancy.

From Ford and Christenson 67
Figure 13. Figure 13.

Inverse relation of placental blood flow to intrauterine pressure in the rhesus monkey.

From Novy et al. 130
Figure 14. Figure 14.

Effect of epinephrine on uterine blood flow of pregnant sheep at 130 days gestation. Progressively larger doses of epinephrine infused into left uterine artery in periods marked A, B, C, and D. Right uterine artery served as control.

From Barton, Killam, and Meschia 15


Figure 1.

Branching of uterine arteries within the human uterus.

From Ramsey and Donner 139


Figure 2.

Semilogarithmic plot of variation of uterine blood flow in nonpregnant sheep during estrous cycle.

From Greiss and Anderson 80


Figure 3.

Preparation used to study the local effect of hormones and drugs on the uterine blood flow in sheep. Substance under investigation is injected intra‐arterially via infusion catheter, and blood flow through uterine artery is measured continually by means of an electromagnetic flow probe.

From Resnik, Meschia, et al. 153


Figure 4.

Blood flow response to 1‐min injection of 1 μg estradiol‐17β (E2) or estriol (E3) into uterine artery of nonpregnant ovariectomized ewe. Preinjection flow was approximately 10 ml/min.

From Clewell, Carson, and Meschia 50


Figure 5.

Cycloheximide blocks uterine blood flow response to estrogen. This protein‐synthesis inhibitor was infused into right uterine artery from time 0 to 2.5 h. The sheep received an intravenous injection of estrogen 30 min after time 0. Note the normal blood flow response to estrogen on left side of uterus and reversible inhibition of response on right side. Under cycloheximide blockade, uterine vasculature had a normal vasodilatory response to bradykinin.

From Killam, Meschia, et al. 96


Figure 6.

Countercurrent arrangement of maternal and fetal microcirculatory channels in placenta of a small rodent. Lightly stippled area, course of maternal blood; densely stippled area, course of fetal blood. In exchange area (labyrinth) maternal and fetal blood run in opposite directions.

From Mossman 126. Organogenesis, edited by Robert L. DeHaan and Heinrich Ursprung. Copyright © 1965 by Holt, Rinehart and Winston, Inc. Reprinted by permission of Holt, Rinehart and Winston


Figure 7.

Circulation of maternal and fetal blood in human placenta.

From Ramsey 138


Figure 8.

Three elementary models of placental transfer.



Figure 9.

Ratio of clearance to blood flow (i.e., effectiveness, transfer index) plotted against ratio of permeability to blood flow with maternal and fetal placental blood flows equal. Same models as in Fig. 8.



Figure 10.

Hypothetical double countercurrent exchange formed by a maternal and a fetal capillary loop. Maternal blood enters at A carrying a highly diffusible substance with concentration 100 and runs in opposite direction to fetal blood entering at a with concentration 0. At end of arterial branches of the 2 loops, fetal concentration is 100 and maternal concentration is 0. The 2 streams run countercurrent again in the venous branches of the loops (V, v) and consequently maternal concentration increases to 100 and fetal concentration returns to 0. Result is no net transfer of highly diffusible substance from mother to fetus.



Figure 11.

Difference between arterial and venous oxygen content across the uterine circulation, expressed as percent of arterial oxygen content, plotted against gestational age for chronic sheep preparations. End of gestation is approximately day 145.



Figure 12.

Blood flow to the uterus of pregnant sows in early gestation. Note initial decline of blood flow in first 11 days of pregnancy.

From Ford and Christenson 67


Figure 13.

Inverse relation of placental blood flow to intrauterine pressure in the rhesus monkey.

From Novy et al. 130


Figure 14.

Effect of epinephrine on uterine blood flow of pregnant sheep at 130 days gestation. Progressively larger doses of epinephrine infused into left uterine artery in periods marked A, B, C, and D. Right uterine artery served as control.

From Barton, Killam, and Meschia 15
References
 1. Abdul‐Karim, R. W., and N. Bruce. Blood flow to the ovary and corpus luteum at different stages of gestation in the rabbit. Fertil. Steril. 24: 44–47, 1973.
 2. Abrams, R. M., D. Caton, J. R. Cotter, and D. H. Barron. The oxygen consumption of the uterus and its tissue contents in late gestation: a comparison of simultaneous measurements using two different techniques. Q. J. Exp. Physiol. 57: 24–29, 1972.
 3. Adham, N., and E. Schenk. Autonomic innervation of the rat vagina, cervix, and uterus and its cyclic variations. Am. J. Obstet. Gynecol. 104: 508–516, 1969.
 4. Anderson, D., A. Berssenbrugge, T. Phernetton, and J. H. G. Rankin. Effect of angiotensin II on ovine placental blood How. Proc. Soc. Exp. Biol. Med. 158: 54–58, 1978.
 5. Anderson, J. N., E. J. Peck, Jr., and J. H. Clark. Estrogen–induced uterine responses and growth: relationship to receptor estrogen binding by uterine nuclei. Endocrinology 96: 160–167, 1975.
 6. Anderson, S. G., J. G. Still, and F. C. Greiss. Differential reactivity of the gravid uterine vasculatures: effects of norepinephrine. Am. J. Obstet. Gynecol. 129: 293–298, 1977.
 7. Barcroft, J. Researches on Pre‐Natal Life. Springfield, IL: Thomas, 1947.
 8. Barcroft, J., and D. H. Barron. Observations upon the form and relations of the maternal and fetal vessels in the placenta of the sheep. Anat. Rec. 94: 569–595, 1946.
 9. Barcroft, J., W. Herkel, and S. Hill. Rate of blood flow and gaseous metabolism of uterus during pregnancy. J. Physiol. London 77: 184–206, 1933.
 10. Barron, D. H., and F. C. Battaglia. Oxygen concentration gradient between the plasmas in the maternal and fetal capillaries of the placenta of the rabbit. Yale J. Biol. Med. 28: 197–207, 1955.
 11. Barron, D. H., J. Metcalfe, G. Meschia, W. Huckabee, A. Hellegers, and H. Prystowsky. Adaptations of pregnant ewes and their fetuses to high altitude. In: The Symposium on the Physiological Effects of High Altitude. New York: Pergamon, 1962, p. 115–129.
 12. Bartelmez, G. W., G. W. Corner, and C. G. Hartman. Cyclic changes in the endometrium of the rhesus monkey (Macaca mulatta). Contrib. Embriol. Carnegie Inst. 34: 99–144, 1951.
 13. Bartels, H., D. El Yassin, and W. Reinhardt. Comparative studies of placental gas exchange in guinea pigs, rabbits, and goats. Respir. Physiol. 2: 149–162, 1967.
 14. Bartels, H., and W. Moll. Passage of inert substances and oxygen in the human placenta. Pfluegers Arch. Gesamte Physiol. Menschen Tiere 280: 165–177, 1964.
 15. Barton, M. D., A. P. Killam, and G. Meschia. Response of ovine uterine blood flow to epinephrine and norepinephrine. Proc. Soc. Exp. Biol. Med. 145: 996–1003, 1974.
 16. Battaglia, F. C., R. E. Behrman, G. Meschia, A. E. Seeds, and P. B. Bruns. Clearance of inert molecules, Na and Cl ions across the primate placenta. Am. J. Obstet. Gynecol. 102: 1135–1143, 1968.
 17. Battaglia, F. C., E. L. Makowski, and G. Meschia. Physiologic study of the uterine venous drainage of the pregnant rhesus monkey. Yale J. Biol. Med. 42: 218–228, 1970.
 18. Battaglia, F. C., and G. Meschia. Principal substrates of fetal metabolism. Physiol. Rev. 58: 499–527, 1978.
 19. Battaglia, F. C., G. Meschia, E. L. Makowski, and W. Bowes. The effect of maternal oxygen inhalation upon fetal oxygenation. J. Clin. Invest. 47: 548–555, 1968.
 20. Behrman, R. E., E. N. Peterson, and C. W. Delannoy. The supply of O2 to the primate fetus with two different O2 tensions and anesthetics. Respir. Physiol. 6: 271–283, 1969.
 21. Beischer, N. A., R. Sivasamboo, S. Vohra, S. Silpisornkosal, and S. Reid. Placental hypertrophy in severe pregnancy anaemia. J. Obstet. Gynaecol. Br. Commonw. 77: 398–409, 1970.
 22. Bell, C. Dual vasoconstrictor and vasodilator innervation of the uterine arterial supply in the guinea pig. Circ. Res. 23: 279–289, 1968.
 23. Bell, C. Distribution of cholinergic vasomotor nerves to the parametrial arteries of some laboratory and domestic animals. J. Reprod. Fertil. 27: 53–58, 1971.
 24. Bell, C., and S. J. Malcolm. Observations on the loss of catecholamine fluorescence from intrauterine adrenergic nerves during pregnancy in the guinea pig. J. Reprod. Fertil. 53: 51–58, 1978.
 25. Bieniarz, J. Venous drainage from the uterus. In: Trans. 5th Conf. on Gestation, edited by C. Villee. New York: Josiah Macy, Jr. Found., 1959, p. 109–130.
 26. Bissonnette, J. M., and G. H. Gurtner. Transfer of inert gases and tritiated water across the sheep placenta. J. Appl. Physiol. 32: 64–69, 1972.
 27. Bissonnette, J. M., L. D. Longo, M. J. Novy, Y. Murata, and C. B. Martin. Placental diffusing capacity and its relation to fetal growth. J. Dev. Physiol. 1: 351–359, 1979.
 28. Blechner, J. N., V. G. Stenger, and H. Prystowsky. Uterine blood flow in women at term. Am. J. Obstet. Gynecol. 120: 633–640, 1974.
 29. Bonds, D. R., S. Anderson, and G. Meschia. Transplacental diffusion of ethanol under steady‐state conditions. J. Dev. Physiol. 2: 409–416, 1980.
 30. Borell, U., I. Fernstrom, L. Ohlson, and N. Wiqvist. Effect of uterine contractions on the human uteroplacental blood circulation: an arteriographic study. Am. J. Obstet. Gynecol. 89: 881–890, 1964.
 31. Brosens, I. A., W. B. Robertson, and H. G. Dixon. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet. Gynecol. Annu. 1: 177–191, 1972.
 32. Brown, B. W., M. J. Emery, and P. E. Mattner. Ovarian arterial blood velocity measured with Doppler ultrasonic transducer in conscious ewes. J. Reprod. Fertil. 58: 295–300, 1980.
 33. Browne, J. C. M., and N. Veall. The maternal placental blood flow in normotensive and hypertensive women. J. Obstet. Gynaecol. Br. Emp. 60: 141–147, 1953.
 34. Bruce, N. W., and R. W. Abdul‐Karim. Relationship between fetal weight, placental weight, and maternal placental circulation in the rabbit at different gestational ages. J. Reprod. Fertil. 32: 15–24, 1973.
 35. Bruce, N. W., and S. B. Dimmitt. Ovarian venous blood flow in non‐pregnant and pregnant rats. J. Endocrinol. 72: 127–133, 1977.
 36. Bruce, N. W., and K. Hillier. The effect of prostaglandin F2α on ovarian blood flow and corpora lutea regression in the rabbit. Nature London 249: 176–177, 1974.
 37. Burd, L. I., J. A. Lemons, E. L. Makowski, F. C. Battaglia, and G. Meschia. Relationship of mammary blood flow to parturition in the ewe. Am. J. Physiol. 229: 797–800, 1975.
 38. Burd, L. I., J. A. Lemons, E. L. Makowski, G. Meschia, and G. Niswender. Mammary blood flow and endocrine changes during parturition in the ewe. Endocrinology 98: 748–754, 1976.
 39. Buss, D. D., G. E. Bisgard, C. A. Rawlings, and J. H. G. Rankin. Uteroplacental blood flow during alkalosis in the sheep. Am. J. Physiol. 228: 1497–1500, 1975.
 40. Carter, A. M., and T. Olin. Effect of adrenergic stimulation and blockade on the uteroplacental circulation and uterine activity in the rabbit. J. Reprod. Fertil. 29: 251–260, 1972.
 41. Chaichareon, D. P., J. H. Rankin, and O. J. Ginther. Factors which affect the relative contributions of ovarian and uterine arteries to the blood supply of reproductive organs in guinea pigs. Biol. Reprod. 15: 281–290, 1976.
 42. Chamley, W. A., J. C. Cerini, M. E. Cerini, I. A. Cumming, J. R. Goding, and J. D. O'Shea. Luteal function following the infusion of prostaglandin F2α into the uterine vein of the ewe. Biol. Reprod. 11: 191–197, 1974.
 43. Clapp, J. F. Cardiac output and uterine blood flow in the pregnant ewe. Am. J. Obstet. Gynecol. 130: 419–423, 1978.
 44. Clark, J. H., Z. Paszko, and E. J. Peck, Jr. Nuclear binding and retention of the receptor estrogen complex: relation to the agonistic properties of estriol. Endocrinology 100: 91–96, 1977.
 45. Clark, K. E. Antagonism by PGF2α vasodilation induced by PGE1, PGE2, and PGA1 in the canine uterus. Blood Vessels 14: 204–211, 1977.
 46. Clark, K. E., D. B. Farley, D. E. Van Orden, and M. J. Brody. Role of endogenous prostaglandins in regulation of uterine blood flow and adrenergic neurotransmission. Am. J. Obstet. Gynecol. 127: 455–461, 1977.
 47. Clark, K. E., S. J. Stys, and J. E. Austin. Vasoactive properties of prostaglandins during pregnancy (Abstract). Soc. Gynecol. Invest., 27th Annu. Meet., Denver, Colorado, 1980, p. 175.
 48. Clark, K. E., S. J. Stys, J. E. Austin, and M. Golter. Post surgical effects of indomethacin on uterine blood flow (Abstract). Soc. Gynecol. Invest., 27th Annu. Meet., Denver, Colorado, 1980, p. 37.
 49. Clark, K. E., S. J. Stys, J. E. Austin, and M. Golter. Prostaglandins: mediator of estrogen induced increases in uterine blood flow? (Abstract). Soc. Gynecol., Invest., 27th Annu. Meet, Denver, Colorado, 1980, p. 176.
 50. Clewell, W. H., B. A. Carson, and G. Meschia. Comparison of uterotrophic and vascular effects of estradiol‐17β and estriol in the mature organism. Am. J. Obstet. Gynecol. 129: 384–388, 1977.
 51. Clewell, W. H., S. Stys, and G. Meschia. Stimulus summation and tachyphylaxis in estrogen response. Am. J. Obstet. Gynecol. 138: 485–493, 1980.
 52. Cohen, D. M., S. J. Steinberger, J. F. Swan, and J. Disalvo. Angiotensin II increases uterine vascular resistance in pregnant and nonpregnant rabbits. Proc. Soc. Exp. Biol. Med. 154: 597–601, 1977.
 53. Coudert, S. P., G. D. Phillips, C. Faiman, W. Chernecki, and M. Palmer. Infusion of tritiated prostaglandin F2α into the anterior uterine vein of the ewe: absence of local venous‐arterial transfer. J. Reprod. Fertil. 36: 333–343, 1974.
 54. Del Campo, C. H., and O. J. Ginther. Vascular anatomy of the uterus and ovaries and the unilateral luteolytic effect of the uterus: guinea pigs, rats, hamsters, and rabbits. Am. J. Vet. Res. 33: 2561–2578, 1972.
 55. Del Campo, C. H., and O. J. Ginther. Vascular anatomy of the uterus and ovaries and the unilateral luteolytic effect of the uterus: horses, sheep, and swine. Am. J. Vet. Res. 34: 305–316, 1973.
 56. Del Campo, C. H., and O. J. Ginther. Vascular anatomy of the uterus and ovaries and the unilateral luteolytic effect of the uterus: angioarchitecture in sheep. Am. J. Vet. Res. 34: 1377–1385, 1973.
 57. DelCampo, C. H., and O. J. Ginther. Arteries and veins of uterus and ovaries in dogs and cats. Am. J. Vet. Res. 35: 409–415, 1974.
 58. Dilts, P. V., Jr., C. R. Brinkman III, T. H. Kirschbaum, and N. S. Assali. Uterine and systemic hemodynamic interrelationships and their response to hypoxia. Am. J. Obstet. Gynecol. 103: 138–157, 1969.
 59. Duncan, S. L. The partition of uterine blood flow in the pregnant rabbit. J. Physiol. London 204: 421–433, 1969.
 60. Edelstone, D. I., J. J. Botti, E. Mueller‐Heubach, and S. N. Caritis. Response of the circulation of pregnant sheep to angiotensin and norepinephrine before and after dexamethasone. Am. J. Obstet. Gynecol. 130: 689–192, 1978.
 61. Elsner, R., D. D. Hammond, and H. R. Parker. Circulatory responses to asphyxia in pregnant and fetal animals: a comparative study of Weddell seals and sheep. Yale J. Biol. Med. 42: 202–217, 1970.
 62. Faber, J. J. Steady‐state methods for the study of placental exchange. Federation Proc. 36: 2640–2646, 1977.
 63. Faber, J. J., and F. M. Hart. The rabbit placenta as an organ of diffusional exchange. Circ. Res. 19: 816–833, 1966.
 64. Falck, B., C. Owman, E. Rosengren, and N.‐O. Sjöberg. Reduction by progesterone of the estrogen‐induced increase in transmitter level of the short adrenergic neurons innervating the uterus. Endocrinology 84: 958–959, 1969.
 65. Ferris, T. F., J. H. Stein, and J. Kauffman. Uterine blood flow and uterine renin secretion. J. Clin. Invest. 51: 2827–2833, 1972.
 66. Ford, S. P., J. R. Chenault, and S. E. Echternkamp. Uterine blood flow of cows during the oestrous cycle and early pregnancy: effect of the conceptus on the uterine blood supply. J. Reprod. Fertil. 56: 53–62, 1979.
 67. Ford, S. P., and R. K. Christenson. Blood flow to uteri of sows during estrous cycle and early pregnancy: local effect of the conceptus on the uterine blood supply. Biol. Reprod. 21: 617–624, 1979.
 68. Freese, V. E. Vascular relations of placental exchange areas in primates and man. In: Respiratory Gas Exchange and Blood Flow in the Placenta, edited by L. D. Longo and H. Bartels. Washington, DC: DHEW Publ. (NIH) 73–361, 1972, p. 31–54.
 69. Friess, A. E., F. Sinowatz, R. Skolek‐Winnisch, and W. Traütner. The placenta of the pig—1. Fine structural changes of the placental barrier during pregnancy. Anat. Embryol. 158: 179–191, 1980.
 70. Fuller, E. O., P. M. Galletti, J. W. Manning, and T. F. Fitzgerald. Responses of the uterine circulation to sympathetic nerve stimulation. J. Dev. Physiol. 1: 209–218, 1979.
 71. Fuller, E. O., P. M. Galletti, and T. Takeuchi. Major and collateral components of blood flow to pregnant sheep uterus. Am. J. Physiol. 229: 279–285, 1975.
 72. Gant, N. F., G. L. Daley, S. Chand, P. J. Whalley, and P. C. MacDonald. A study of angiotensin II pressor response throughout primigravid pregnancy. J. Clin. Invest. 52: 2682–2689, 1973.
 73. Gerber, J. G., R. A. Branch, W. C. Hubbard, and A. S. Nies. Indomethacin is a placental vasodilator in the dog. The effect of prostaglandin inhibition. J. Clin. Invest. 62: 14–19, 1978.
 74. Ginther, O. J. Internal regulation of physiological processes through local venoarterial pathways: a review. J. Anim. Sci. 39: 550–564, 1974.
 75. Ginther, O. J., and C. H. Del Campo. Vascular anatomy of the uterus and ovaries and the unilateral luteolytic effect of the uterus: cattle. Am. J. Vet. Res. 35: 193–203, 1974.
 76. Ginther, O. J., D. J. Dierschke, S. W. Walsh, and C. H. Del Campo. Anatomy of arteries and veins of uterus and ovaries in rhesus monkeys. Biol. Reprod. 11: 205–219, 1974.
 77. Gorski, J., and F. Gannon. Current models of steroid hormone action: a critique. Annu. Rev. Physiol. 38: 425–450, 1976.
 78. Greiss, F. C., Jr. Pressure‐flow relationship in the gravid uterine vascular bed. Am. J. Obstet. Gynecol. 96: 41–46, 1966.
 79. Greiss, F. C., Jr. Differential reactivity of the myoendometrial and placental vasculatures: adrenergic responses. Am. J. Obstet. Gynecol. 112: 20–30, 1972.
 80. Greiss, F. C., Jr., and S. G. Anderson. Uterine vascular changes during the ovarian cycle. Am. J. Obstet. Gynecol. 103: 629–640, 1969.
 81. Greiss, F. C., Jr., and S. G. Anderson. Uterine blood flow during early ovine pregnancy. Am. J. Obstet. Gynecol. 106: 30–38, 1970.
 82. Greiss, F. C., Jr., and S. G. Anderson. Effect of ovarian hormones on the uterine vascular bed. Am. J. Obstet. Gynecol. 107: 829–836, 1970.
 83. Greiss, F. C., Jr., S. G. Anderson, and L. C. King. Uterine vascular bed: effects of acute hypoxia. Am. J. Obstet. Gynecol. 113: 1057–1064, 1972.
 84. Greiss, F. C., Jr., S. G. Anderson, and L. C. King. Uterine vascular bed: effects of acute hyperoxia. Am. J. Obstet. Gynecol. 118: 542–547, 1974.
 85. Greiss, F. C., Jr., S. G. Anderson, and J. G. Still. Uterine pressure‐flow relationships during early gestation. Am. J. Obstet. Gynecol. 126: 799–808, 1976.
 86. Grosser, O. Vergleichende Anatomie und Entwicklungsgeschichte der Eihäute und der Placenta. Vienna: Braumuller, 1909.
 87. Hanka, R., L. Lawn, I. H. Mills, D. C. Prior, and P. M. Tweeddale. The effects of maternal hypercapnia on foetal oxygenation and uterine blood flow in the pig. J. Physiol. London 247: 447–460, 1975.
 88. Hanwell, A., and J. L. Linzell. The effects of engorgement with milk and of suckling on mammary blood flow in the rat. J. Physiol. London 233: 111–125, 1973.
 89. Harbert, G. M., Jr. Biorhythms of the pregnant uterus (Macaca mulatta). Am. J. Obstet. Gynecol. 129: 401–408, 1977.
 90. Harvey, C. A., and D. A. Owen. Changes in uterine and ovarian blood flow during the oestrous cycle in rats. J. Endocrinol. 71: 367–369, 1976.
 91. Hendricks, C. H., E. J. Quilligan, C. W. Tyler, and G. J. Tucker. Pressure relationships between the intervillous space and the amniotic fluid in human term pregnancy. Am. J. Obstet. Gynecol. 77: 1028–1307, 1959.
 92. Hohimer, A. R., M. J. Morton, and J. Metcalfe. Maternal hemodynamics during guinea pig pregnancy (Abstract). Physiologist 23 (4): 148, 1980.
 93. Hoversland, A. S., J. T. Parer, and J. Metcalfe. Hemodynamic adjustments in the pygmy goat during pregnancy and early postpartum. Biol. Reprod. 10: 578–588, 1974.
 94. Huckabee, W. E., C. Crenshaw, L. B. Curet, L. Mann, and D. H. Barron. The effect of exogenous oestrogen on the blood flow and oxygen consumption of the uterus of the non‐pregnant ewe. Q. J. Exp. Physiol. 55: 16–24, 1970.
 95. Karlsson, K. The influence of hypoxia on uterine and maternal placental blood flow and the effect of α‐adrenergic blockade. J. Perinat. Med. 2: 176–184, 1974.
 96. Killam, A. P., C. R. Rosenfeld, F. C. Battaglia, E. L. Makowski, and G. Meschia. Effect of estrogens on the uterine blood flow of oophorectomized ewes. Am. J. Obstet. Gynecol. 115: 1045–1052, 1973.
 97. Ladner, C., C. R. Brinkman III, P. Weston, and N. S. Assali. Dynamics of uterine circulation in pregnant and nonpregnant sheep. Am. J. Physiol. 218: 257–263, 1970.
 98. Lee, W., and M. J. Novy. Effects of luteinizing hormone and indomethacin on blood flow and steroidogenesis in the rabbit ovary. Biol. Reprod. 18: 799–807, 1978.
 99. Lees, M. H., J. D. Hill, A. J. Ochsner III, C. L. Thomas, and M. J. Novy. Maternal placental and myometrial blood flow of the rhesus monkey during uterine contractions. Am. J. Obstet. Gynecol. 110: 68–81, 1971.
 100. Lees, M. M., S. H. Taylor, D. B. Scott, and M. G. Kerr. A study of cardiac output at rest throughout pregnancy. J. Obstet. Gynaecol. Br. Commonw. 74: 319–328, 1967.
 101. Leitch, I., F. E. Hytten, and W. Z. Billewicz. The maternal and neonatal weights of some mammalia. Proc. Zool. Soc. London 133: 11–29, 1959.
 102. Levinson, G., S. M. Shnider, A. A. DeLorimier, and J. L. Steffenson. Effects of maternal hyperventilation on uterine blood flow and fetal oxygenation and acid‐base status. Anesthesiology 40: 340–347, 1974.
 103. Liggins, G. C., S. A. Grieves, J. Z. Kendall, and B. S. Knox. The physiological roles of progesterone, oestradiol‐17β and prostaglandin F2α in the control of ovine parturition. J. Reprod. Fertil. Suppl. 16: 85–103, 1972.
 104. Linzell, J. L. Mammary blood flow and methods of identifying and measuring precursors of milk. In: Lactation, A Comprehensive Treatise, edited by B. L. Larson and V. R. Smith. New York: Academic, 1974, vol. I, pt. 2, p. 143–220.
 105. Longo, L. D., M. Delivoria‐Papadopoulos, G. G. Power, E. P. Hill, and R. E. Forster II. Diffusion equilibration of inert gases between maternal and fetal placental capillaries. Am. J. Physiol. 219: 561–569, 1970.
 106. Lyon, C. K., J. B. Scott, and C. Y. Wang. Flow through collapsible tubes at low Reynolds numbers. Circ. Res. 47: 68–73, 1980.
 107. Makowski, E. L. Maternal and fetal vascular nets in placentas of sheep and goats. Am. J. Obstet. Gynecol. 100: 283–288, 1968.
 108. Makowski, E. L., R. H. Hertz, and G. Meschia. Effects of acute maternal hypoxia and hyperoxia on the blood flow to the pregnant uterus. Am. J. Obstet. Gynecol. 115: 624–631, 1973.
 109. Markee, J. E. Rhythmic vascular uterine changes. Am. J. Physiol. 100: 32–39, 1932.
 110. Markee, J. E. An analysis of the rhythmic vascular changes in the uterus of the rabbit. Am. J. Physiol. 100: 374–382, 1932.
 111. Markee, J. E. Menstruation in intraocular endometrial transplants in the rhesus monkey. Contrib. Embryol. Carnegie Inst. 28: 219–308, 1940.
 112. McCracken, J. Prostaglandin F2α and corpus luteum regression. Ann. NY Acad. Sci. 180: 456–472, 1971.
 113. McLaughlin, M. K., S. C. Brennan, and R. A. Chez. Vasoconstrictive effects of prostaglandins in sheep placental circulations. Am. J. Obstet. Gynecol. 130: 408–413, 1978.
 114. McLaughlin, M. K., S. C. Brennan, and R. A. Chez. Effects of indomethacin on sheep uteroplacental circulations and sensitivity to angiotensin II. Am. J. Obstet. Gynecol. 132: 430–435, 1978.
 115. Meschia, G. Physiology of transplacental diffusion. Obstet. Gynecol. Annu. 5: 21–38, 1976.
 116. Meschia, G., F. C. Battaglia, and P. D. Bruns. Theoretical and experimental study of transplacental diffusion. J. Appl. Physiol. 22: 1171–1178, 1967.
 117. Meschia, G., E. L. Makowski, and F. C. Battaglia. The use of indwelling catheters in the uterine and umbilical veins of sheep for a description of fetal acid‐base balance and oxygenation. Yale J. Biol. Med. 42: 154–165, 1970.
 118. Meschia, G., A. S. Wolkoff, and D. H. Barron. The oxygen, carbon dioxide, and hydrogen ion concentrations in the arterial and uterine venous bloods of pregnant sheep. Q. J. Exp. Physiol. 44: 333–341, 1959.
 119. Metcalfe, J., W. Moll, H. Bartels, P. Hilpert, and J. T. Parer. Transfer of carbon monoxide and nitrous oxide in the artificially perfused sheep placenta. Circ. Res. 16: 95–101, 1965.
 120. Metcalfe, J., S. L. Romney, L. H. Ramsey, D. E. Reid, and C. S. Burwell. Estimation of uterine blood flow in normal pregnancy at term. J. Clin. Invest. 34: 1632–1638, 1955.
 121. Moll, W., and E. Kastendieck. Transfer of N2O, CO and HTO in the artificially perfused guinea pig placenta. Respir. Physiol. 29 (3): 283–302, 1977.
 122. Moll, W., and W. Künzel. The blood pressure in arteries entering the placentae of guinea pigs, rats, rabbits, and sheep. Pfluegers Arch. 338: 125–131, 1973.
 123. Moll, W., W. Künzel, and H. G. Ross. Gas exchange of the pregnant uterus of anesthetized and unanesthetized guinea pigs. Respir. Physiol. 8: 303–310, 1970.
 124. Moll, W., W. Künzel, L. A. M. Stolte, J. Kleinhout, P. A. Dejong, and A. F. L. Veth. The blood pressure in the decidual part of the uteroplacental arteries (spiral arteries) of the rhesus monkey. Pfluegers Arch. 346: 291–297, 1974.
 125. Mossman, H. W. The rabbit placenta and the problem of placental transmission. Am. J. Anat. 37: 417–432, 1926.
 126. Mossman, H. W. The principal interchange vessels of the chorioallantoic placenta of mammals. In: Organogenesis, edited by R. L. DeHaan and H. Ursprung. New York: Holt, Rinehart, & Winston, 1965, p. 771–786.
 127. Mueller, D., B. Stoehr, Jr., T. Phernetton, and J. H. G. Rankin. The effect of indomethacin and meclofenamate on estrogen induced vasodilation in the rabbit uterus. Proc. Soc. Exp. Biol. Med. 159: 25–29, 1978.
 128. Niswender, G. D., T. J. Reimers, M. A. Diekman, and T. M. Nett. Blood flow: a mediator of ovarian function. Biol. Reprod. 14: 64–81, 1976.
 129. Novy, M. J., and M. J. Cook. Redistribution of blood flow by prostaglandin F2α in the rabbit ovary. Am. J. Obstet. Gynecol. 117: 381–385, 1973.
 130. Novy, M. J., C. L. Thomas, and M. H. Lees. Uterine contractility and regional blood flow responses to oxytocin and prostaglandin E2 in pregnant rhesus monkeys. Am. J. Obstet. Gynecol. 122: 419–433, 1975.
 131. Oakes, G. K., A. M. Walker, R. A. Ehrenkranz, R. C. Cefalo, and R. A. Chez. Uteroplacental blood flow during hyperthermia with and without respiratory alkalosis. J. Appl. Physiol. 41: 197–201, 1976.
 132. Peeters, L. L., G. Grutters, and C. B. Martin. Distribution of cardiac output in the unstressed pregnant guinea pig (Abstract). Soc. Gynecol. Invest, 27th Annu. Meet., Denver, Colorado, 1980, p. 38.
 133. Pharriss, B. B., J. C. Cornette, and G. D. Gutknecht. Vascular control of luteal steroidogenesis. J. Reprod. Fertil. 10: 97–103, 1970.
 134. Piacsek, B. E., and J. F. Huth. Changes in ovarian venous blood flow following cannulation: effects of luteinizing hormone (LH) and antihistamine. Proc. Soc. Exp. Biol. Med. 138: 1022–1024, 1971.
 135. Piiper, J., and P. Scheid. Gas transport efficacy of gills, lungs and skin: theory and experimental data. Respir. Physiol. 23: 209–221, 1975.
 136. Prill, H. J., and F. Göxtz. Blood flow in the myometrium and endometrium of the uterus. Am. J. Obstet. Gynecol. 82: 102–108, 1961.
 137. Ralston, D. H., S. M. Shnider, and A. A. DeLorimier. Uterine blood flow and fetal acid‐base changes after bicarbonate administration to the pregnant ewe. Anesthesiology 40: 348–353, 1974.
 138. Ramsey, E. M. Placental vasculature and circulation. In: Handbook of Physiology. Endocrinology, edited by R. O. Greep and E. B. Astwood. Bethesda, MD: Am. Physiol. Soc., 1973, sect. 7, vol. II, pt. 2, chapt. 47, p. 323–337.
 139. Ramsey, E. M., and M. W. Donner. Placental Vasculature and Circulation. Philadelphia, PA: Saunders, 1980.
 140. Rankin, J. H. G. The effects of shunted and unevenly distributed blood flows on crosscurrent exchange in the sheep placenta. In: Respiratory Gas Exchange and Blood Flow in the Placenta, edited by L. D. Longo and H. Bartels. Washington, DC: DHEW Publ. (NIH) 73–361, 1972, p. 207–226.
 141. Rankin, J. H. G. Role of prostaglandins in the maintenance of the placental circulation. Adv. Prostaglandin Thromboxane Res. 4: 261–269, 1978.
 142. Rankin, J. H. G., A. Berssenbrugge, D. Anderson, and T. Phernetton. Ovine placental vascular responses to indomethacin. Am. J. Physiol. 236 (Heart Circ. Physiol. 5): H61–H64, 1979.
 143. Rankin, J. H. G., G. Meschia, E. L. Makowski, and F. C. Battaglia. Relationship between uterine and umbilical venous Po2 in sheep. Am. J. Physiol. 220: 1688–1692, 1971.
 144. Rankin, J. H. G., and T. M. Phernetton. Effect of prostaglandin E2 on ovine maternal placental blood flow. Am. J. Physiol. 231: 754–759, 1976.
 145. Rankin, J. H. G., T. M. Phernetton, D. F. Anderson, and A. D. Berssenbrugge. Effect of prostaglandin I2 on ovine placental vasculature. J. Dev. Physiol. 1: 151–160, 1979.
 146. Raye, J. R., A. P. Killam, F. C. Battaglia, E. L. Makowski, and G. Meschia. Uterine blood flow and O2 consumption following fetal death in sheep. Am. J. Obstet. Gynecol. 111: 917–924, 1971.
 147. Rekonen, A., H. Lutola, M. Pitkänen, J. Kuikka, and T. Pyörälä. Measurement of intervillous and myometrial blood flow by an intravenous 133Xe method. Br. J. Obstet. Gynaecol. 83: 723–728, 1976.
 148. Resnik, R., F. C. Battaglia, E. L. Makowski, and G. Meschia. The effect of actinomycin D on estrogen‐induced uterine blood flow. Am. J. Obstet. Gynecol. 122: 273–277, 1975.
 149. Resnik, R., and G. W. Brink. Effects of prostaglandins E1, E2, and F2α on uterine blood flow in nonpregnant sheep. Am. J. Physiol. 234 (Heart Circ. Physiol. 3): H557–561, 1978.
 150. Resnik, R., and G. W. Brink. Uterine vascular response to prostacyclin in nonpregnant sheep. Am. J. Obstet. Gynecol. 137: 267–270, 1980.
 151. Resnik, R., G. W. Brink, and M. H. Plumer. The effect of progesterone on estrogen‐induced uterine blood flow. Am. J. Obstet. Gynecol. 128: 251–254, 1977.
 152. Resnik, R., A. P. Killam, M. D. Barton, F. C. Battaglia, E. L. Makowski, and G. Meschia. The effect of various vasoactive compounds upon the uterine vascular bed. Am. J. Obstet. Gynecol. 125: 201–206, 1976.
 153. Resnik, R., A. P. Killam, F. C. Battaglia, E. L. Makowski, and G. Meschia. The stimulation of uterine blood flow by various estrogens. Endocrinology 94: 1192–1196, 1974.
 154. Reynolds, M. L., and M. Young. The transfer of free alpha‐amino nitrogen across the placental membrane in the guinea pig. J. Physiol. London 214: 583–597, 1971.
 155. Reynolds, S. R. M. Maternal blood flow in the uterus and placenta. In: Handbook of Physiology. Circulation, edited by W. F. Hamilton. Bethesda, MD: Am. Physiol. Soc., 1963, sect. 2, vol. II, chapt. 45, p. 1585–1618.
 156. Rosenfeld, C. R. Distribution of cardiac output in ovine pregnancy. Am. J. Physiol. 232 (Heart Circ. Physiol. 1): H231–H235, 1977.
 157. Rosenfeld, C. R., M. D. Barton, and G. Meschia. Effects of epinephrine on distribution of blood flow in the pregnant ewe. Am. J. Obstet. Gynecol. 124: 156–163, 1976.
 158. Rosenfeld, C. R., A. P. Killam, F. C. Battaglia, E. L. Makowski, and G. Meschia. Effect of estradiol‐17β on the magnitude and distribution of uterine blood flow in nonpregnant, oophorectomized ewes. Pediatr. Res. 7: 139–148, 1973.
 159. Rosenfeld, C. R., F. H. Morriss, Jr., F. C. Battaglia, E. L. Makowski, and G. Meschia. Effect of estradiol‐17β on blood flow to reproductive and nonreproductive tissues in pregnant ewes. Am. J. Obstet. Gynecol. 124: 618–629, 1976.
 160. Rosenfeld, C. R., F. H. Morriss, Jr., E. L. Makowski, G. Meschia, and F. C. Battaglia. Circulatory changes in the reproductive tissues of ewes during pregnancy. Gynecol. Invest. 5: 252–268, 1974.
 161. Rosenfeld, C. R., and J. West. Circulatory response to systemic infusion of norepinephrine in the pregnant ewe. Am. J. Obstet. Gynecol. 127: 376–383, 1977.
 162. Ryan, M. J., K. E. Clark, and M. J. Brody. Neurogenic and mechanical control of canine uterine vascular resistance. Am. J. Physiol. 227: 547–555, 1974.
 163. Schröder, H., and H.‐P. Leichtweiss. Perfusion rates and the transfer of water across isolated guinea pig placenta. Am. J. Physiol. 232 (Heart Circ. Physiol. 1): H666–H670, 1977.
 164. Silver, M., and R. S. Comline. Transfer of gases and metabolites in the equine placenta: a comparison with other species. J. Reprod. Fertil. Suppl. 23: 589–594, 1975.
 165. Silver, M., and D. Steven. Placental exchange of blood gases. In: Comparative Placentation, edited by D. H. Steven. New York: Academic, 1975, p. 161–186.
 166. Silver, M., D. H. Steven, and R. S. Comline. Placental exchange and morphology in ruminants and the mare. In: Foetal and Neonatal Physiology, edited by K. S. Comline, K. W. Cross, G. S. Dames, and P. W. Nathaniels. Cambridge, UK: Cambridge Univ. Press, 1973, p. 245–271. (Proc. Sir Joseph Barcroft Centenary Symp. 1973.)
 167. Simmons, M. A., F. C. Battaglia, and G. Meschia. Placental transfer of glucose. J. Dev. Physiol. 1: 227–239, 1979.
 168. Sjöberg, N.‐O. New considerations on the adrenergic innervation of the cervix and the uterus. Acta Obstet. Gynecol. Scand. Suppl. 3: 28–32, 1969.
 169. Speroff, L. J. An autoregulatory role for prostaglandins in placental hemodynamics and their possible influence on blood pressure in pregnancy. J. Reprod. Med. 15: 181–188, 1975.
 170. Steven, D. H. Anatomy of the placental barrier. In: Comparative Placentation, edited by D. H. Steven. New York: Academic, 1975, p. 25–56.
 171. Still, J. D., and F. C. Greiss. The effects of prostaglandins and other vasoactive substances on uterine blood flow and myometrial activity. Am. J. Obstet. Gynecol. 130: 1–8, 1978.
 172. Sullivan, F. M., and J. F. Tucker. Uterine blood flow in the pregnant rabbit. J. Reprod. Fertil. 42: 239–250, 1975.
 173. Symonds, E. M., M. A. Stanley, and S. L. Skinner. Production of renin by in vitro cultures of human chorion and uterine muscle. Nature London 217: 1152–1153, 1968.
 174. Teasdale, F. Numerical density of nuclei in the sheep placenta. Anat. Rec. 185: 187–196, 1976.
 175. Terragno, N. A., D. A. Terragno, D. Pacholczyk, and J. C. McGiff. Prostaglandins and the regulation of uterine blood flow in pregnancy. Nature London 249: 57–58, 1974.
 176. Thorbert, G., P. Alm, C. Owman, and N.‐O. Sjöberg. Regional distribution of autonomic nerves in guinea pig uterus. Am. J. Physiol. 233 (Cell Physiol. 2): C25–C34, 1977.
 177. Thorbert, G., P. Alm, C. Owman, N.‐O. Sjöberg, and B. Sporrong. Regional changes in structural and functional integrity of myometrial adrenergic nerves in pregnant guinea‐pig, and their relationship to the localization of the conceptus. Acta Physiol. Scand. 103: 120–131, 1978.
 178. Venuto, R. C., J. W. Cox, J. H. Stein, and T. F. Ferris. The effect of changes in perfusion pressure on uteroplacental blood flow in the pregnant rabbit. J. Clin. Invest. 57: 938–944, 1976.
 179. Venuto, R. C., T. O'Dorisio, J. H. Stein, and T. F. Ferris. Uterine prostaglandin E secretion and uterine blood flow in the pregnant rabbit. J. Clin. Invest. 55: 193–197, 1975.
 180. Walker, A. M., G. K. Oakes, R. Ehrenkranz, M. McLaughlin, and R. A. Chez. Effects of hypercapnia on uterine and umbilical circulations in conscious pregnant sheep. J. Appl. Physiol. 41: 727–733, 1976.
 181. Walker, A. M., G. K. Oakes, M. K. McLaughlin, R. A. Ehrenkranz, D. W. Alling, and R. C. Chez. 24‐Hour rhythms in uterine and umbilical blood flows of conscious pregnant sheep. Gynecol. Invest. 8: 288–298, 1977.
 182. Wallenburg, H. C., J. Mazer, and D. L. Hutchinson. Effects of a beta‐adrenergic agent (metaproterenol) on uteroplacental circulation. An angiographic study in the pregnant rhesus monkey. Am. J. Obstet. Gynecol. 117: 1067–1075, 1973.
 183. Wehrenberg, W. B., D. P. Chaichareon, D. J. Dierschke, J. H. Rankin, and O. J. Ginther. Vascular dynamics of the reproductive tract in the female rhesus monkey: relative contributions of ovarian and uterine arteries. Biol. Reprod. 17: 148–153, 1977.
 184. Wehrenberg, W. B., D. J. Dierschke, J. H. G. Rankin, and R. C. Wolf. Variations in “functional” blood flow as related to corpus luteum activity in cyclic guinea pigs. Biol. Reprod. 19: 380–384, 1978.
 185. Wigglesworth, J. S. Vascular organization of the human placenta. Nature London 216: 1120–1121, 1967.
 186. Wilkin, P. Les theories explicatives du mecanisme des echanges transplacentaires. In: Le placenta humain, edited by J. Snoeck. Paris: Masson, 1958, p. 248–279.
 187. Wulf, K. H., W. Künzel, and V. Lehmann. Clinical aspects of placental gas exchange. In: Respiratory Gas Exchange and Blood Flow in the Placenta, edited by L. D. Longo and H. Bartels. Washington, DC: DHEW Publ. (NIH) 73–361, 1972.
 188. Wurtman, R. J. An effect of luteinizing hormone on the fractional perfusion of the rat ovary. Endocrinology 75: 927–933, 1964.
 189. Yamaguchi, R., M. Shintani, S. Ishibashi, E. Ushioda, and Y. Nishikawa. Uteroplacental blood flow and uteroplacental shunt rates in normal and prolonged pregnancies in rats. Tohoku J. Exp. Med. 127: 389–396, 1979.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Circulation to Female Reproductive Organs
 

How to Cite

Giacomo Meschia. Circulation to Female Reproductive Organs. Compr Physiol 2011, Supplement 8: Handbook of Physiology, The Cardiovascular System, Peripheral Circulation and Organ Blood Flow: 241-269. First published in print 1983. doi: 10.1002/cphy.cp020308