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. 1967 May;46(5):812–828. doi: 10.1172/JCI105581

Respiratory Function of the Placenta as Determined with Carbon Monoxide in Sheep and Dogs*

Lawrence D Longo 1,2,, Gordon G Power 1,2,, Robert E Forster II 1,2
PMCID: PMC297083  PMID: 6067334

Abstract

A technique is described for studying the respiratory function of the placenta using carbon monoxide, a gas whose exchange across the placenta between the maternal and fetal circulations is limited by diffusion rather than blood flow.

During the steady state before the introduction of CO, the normal concentration of carboxyhemoglobin in the ewe, [COHb]M, is approximately 0.90%, and that in the fetus is 2.9%, the ratio [COHb]F/[COHb]M being 3.2. In dogs the corresponding values are 1.9%, 4.8%, and 2.4%.

After the introduction of CO into the mother animal, CO diffused across the placenta slowly with an equilibration half-time of approximately 2 hours.

The average carbon monoxide diffusing capacity (DPco) of the placenta during maternal to fetal exchange was 0.54 ml per (minute × mm Hg × kg fetal weight) (SD ± 0.13) in sheep and 0.57 ml per (minute × mm Hg × kg) (SD ± 0.18) in dogs.

The fetal to maternal placental diffusing capacity in two sheep was 0.54 ml per (minute × mm Hg × kg).

Calculations considering the relative rates of reaction of O2 and CO with red cell hemoglobin and the relative rates of diffusion of the two gases suggest that the true DPo2 should be about 1.2 to 2 times greater than the DPco or 0.65 to 1.1 per (minute × mm Hg × kg). This is about 5 times greater than the reported value of DPo2 calculated from measurements of PO2 in the mixed uterine and umbilical venous blood. With a diffusing capacity of this magnitude the maternal and fetal placental end capillary PO2 would approach equilibrium, becoming too small to measure, and the calculation of DPo2 would be unreliable. We suggest that the apparent end capillary Po2 gradients of 15 to 20 mm Hg, obtained from sampling uterine and umbilical venous blood, result from a combination of uneven distribution of maternal and fetal placental blood flow and from placental oxygen consumption.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ALLEN T. A., ROOT W. S. Partition of carbon monoxide and oxygen between air and whole blood of rats, dogs and men as affected by plasma pH. J Appl Physiol. 1957 Mar;10(2):186–190. doi: 10.1152/jappl.1957.10.2.186. [DOI] [PubMed] [Google Scholar]
  2. BARRON D. H., ALEXANDER G. Supplementary observations on the oxygen pressure gradient between the maternal and fetal bloods of sheep. Yale J Biol Med. 1952 Sep;25(1):61–66. [PMC free article] [PubMed] [Google Scholar]
  3. BARRON D. H., MESCHIA G. A comparative study of the exchange of the respiratory gases across the placenta. Cold Spring Harb Symp Quant Biol. 1954;19:93–101. doi: 10.1101/sqb.1954.019.01.013. [DOI] [PubMed] [Google Scholar]
  4. BARTELS H., MOLL W., METCALFE J. Physiology of gas exchange in the human placenta. Am J Obstet Gynecol. 1962 Dec 1;84:1714–1730. doi: 10.1016/0002-9378(62)90012-1. [DOI] [PubMed] [Google Scholar]
  5. BARTELS H., MOLL W. PASSAGE OF INERT SUBSTANCES AND OXYGEN IN THE HUMAN PLACENTA. Pflugers Arch Gesamte Physiol Menschen Tiere. 1964 Jul 1;280:165–177. doi: 10.1007/BF00363755. [DOI] [PubMed] [Google Scholar]
  6. Barcroft J., Kennedy J. A., Mason M. F. The direct determination of the oxygen consumption of the foetal sheep. J Physiol. 1939 Mar 14;95(2):269–275. doi: 10.1113/jphysiol.1939.sp003725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. COBURN R. F., BLAKEMORE W. S., FORSTER R. E. Endogenous carbon monoxide production in man. J Clin Invest. 1963 Jul;42:1172–1178. doi: 10.1172/JCI104802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. COBURN R. F., DANIELSON G. K., BLAKEMORE W. S., FORSTER R. E., 2nd CARBON MONOXIDE IN BLOOD: ANALYTICAL METHOD AND SOURCES OF ERROR. J Appl Physiol. 1964 May;19:510–515. doi: 10.1152/jappl.1964.19.3.510. [DOI] [PubMed] [Google Scholar]
  9. CURTIS G. W., ALGERI E. J., McBAY A. J., FORD R. The transplacental diffusion of carbon monoxide; a review and experimental study. AMA Arch Pathol. 1955 Jun;59(6):677–690. [PubMed] [Google Scholar]
  10. Campbell A. G., Dawes G. S., Fishman A. P., Hyman A. I., James G. B. The oxygen consumption of the placenta and foetal membranes in the sheep. J Physiol. 1966 Jan;182(2):439–464. doi: 10.1113/jphysiol.1966.sp007831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Coburn R. F., Williams W. J., White P., Kahn S. B. The production of carbon monoxide from hemoglobin in vivo. J Clin Invest. 1967 Mar;46(3):346–356. doi: 10.1172/JCI105536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. DANESINO V. Dispositivi di blocco ed anastomosi artero-venose nei vasi fetali della placenta umana. Arch Ostet Ginecol. 1950 May-Jun;55(3):251–272. [PubMed] [Google Scholar]
  13. FRIBERG L., NYSTROM A., SWANBERG H. Transplacental diffusion of carbon monoxide in human subjects. Acta Physiol Scand. 1959 Apr 22;45(4):363–368. doi: 10.1111/j.1748-1716.1959.tb01708.x. [DOI] [PubMed] [Google Scholar]
  14. FRIEDMAN E. A., LITTLE W. A., SACHTLEBEN M. R. Placental oxygen consumption in vitro. II. Total uptake as an index of placental function. Am J Obstet Gynecol. 1962 Sep 1;84:561–569. [PubMed] [Google Scholar]
  15. GEMZELL C. A., ROBBE H., STROM G. On the equilibration of carbon monoxide between human maternal and fetal circulation in vivo. Scand J Clin Lab Invest. 1958;10(4):372–378. doi: 10.3109/00365515809051239. [DOI] [PubMed] [Google Scholar]
  16. HADDON W., Jr, NESBITT R. E., GARCIA R. Smoking and pregnancy: carbon monoxide in blood during gestation and at term. Obstet Gynecol. 1961 Sep;18:262–267. [PubMed] [Google Scholar]
  17. HOLLINGSWORTH J. W. Lifespan of fetal erythrocytes. J Lab Clin Med. 1955 Mar;45(3):469–473. [PubMed] [Google Scholar]
  18. Haldane J., Smith J. L. The Absorption of Oxygen by the Lungs. J Physiol. 1897 Nov 20;22(3):231–258. doi: 10.1113/jphysiol.1897.sp000689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. JONES R. H., ELLICOTT M. F., CADIGAN J. B., GAENSLER E. A. The relationship between alveolar and blood carbon monoxide concentrations during breathholding; simple estimation of COHb saturation. J Lab Clin Med. 1958 Apr;51(4):553–564. [PubMed] [Google Scholar]
  20. LUDWIG K. S. [On the fine structure of the maternal-fetal connection in the placentoma of the sheep (Ovis aries L.)]. Experientia. 1962 May 15;18:212–213. doi: 10.1007/BF02148304. [DOI] [PubMed] [Google Scholar]
  21. Lawson W. H., Jr, Holland R. A., Forster R. E. Effect of temperature on deoxygenation rate of human red cells. J Appl Physiol. 1965 Sep;20(5):912–918. doi: 10.1152/jappl.1965.20.5.912. [DOI] [PubMed] [Google Scholar]
  22. MESCHIA G., COTTER J. R., BREATHNACH C. S., BARRON D. H. THE HEMOGLOBIN, OXYGEN, CARBON DIOXIDE AND HYDROGEN ION CONCENTRATIONS IN THE UMBILICAL BLOODS OF SHEEP AND GOATS AS SAMPLED VIA INDWELLING PLASTIC CATHETERS. Q J Exp Physiol Cogn Med Sci. 1965 Apr;50:185–195. doi: 10.1113/expphysiol.1965.sp001780. [DOI] [PubMed] [Google Scholar]
  23. MESCHIA G., HELLEGERS A., BLECHNER J. N., WOLKOFF A. S., BARRON D. H. A comparison of the oxygen dissociation curves of the bloods of maternal, fetal and newborn sheep at various pHs. Q J Exp Physiol Cogn Med Sci. 1961 Jan;46:95–100. doi: 10.1113/expphysiol.1961.sp001520. [DOI] [PubMed] [Google Scholar]
  24. METCALFE J., MOLL W., BARTELS H., HILPERT P., PARER J. T. TRANSFER OF CARBON MONOXIDE AND NITROUS OXIDE IN THE ARTIFICIALLY PERFUSED SHEEP PLACENTA. Circ Res. 1965 Feb;16:95–101. doi: 10.1161/01.res.16.2.95. [DOI] [PubMed] [Google Scholar]
  25. PAUL W., ROUGHTON F. J. W. The equilibrium between oxygen and sheep haemoglobin at very low percentage saturations. J Physiol. 1951 Mar;113(1):23–35. doi: 10.1113/jphysiol.1951.sp004553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. ROUGHTON F. J., FORSTER R. E. Relative importance of diffusion and chemical reaction rates in determining rate of exchange of gases in the human lung, with special reference to true diffusing capacity of pulmonary membrane and volume of blood in the lung capillaries. J Appl Physiol. 1957 Sep;11(2):290–302. doi: 10.1152/jappl.1957.11.2.290. [DOI] [PubMed] [Google Scholar]
  27. ROUGHTON F. J. The equilibrium between carbon monoxide and sheep haemoglobin at very high percentage saturations. J Physiol. 1954 Nov 29;126(2):359–383. doi: 10.1113/jphysiol.1954.sp005215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. STAUB N. C., BISHOP J. M., FORSTER R. E. Importance of diffusion and chemical reaction rates in O2 uptake in the lung. J Appl Physiol. 1962 Jan;17:21–27. doi: 10.1152/jappl.1962.17.1.21. [DOI] [PubMed] [Google Scholar]
  29. WIMSATT W. A. Some aspects of the comparative anatomy of the mammalian placenta. Am J Obstet Gynecol. 1962 Dec 1;84:1568–1594. doi: 10.1016/0002-9378(62)90004-2. [DOI] [PubMed] [Google Scholar]
  30. YOUNG I. M., PUGH L. G. THE CARBON MONOXIDE CONTENT OF FOETAL AND MATERNAL BLOOD. J Obstet Gynaecol Br Commonw. 1963 Aug;70:681–684. doi: 10.1111/j.1471-0528.1963.tb04967.x. [DOI] [PubMed] [Google Scholar]

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