Maternal arterial connections to the placental intervillous space during the first trimester of human pregnancy: The Boyd Collection revisited,☆☆,,★★

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Abstract

Objective: We sought to determine morphologically when the maternal uterine circulation to the human placenta is established. Study Design: We performed a histologic review of 12 early-pregnancy hysterectomy specimens contained within the Boyd Collection, ranging from 43 to 130 days’ gestation. Results: Before the eighth week of pregnancy, maternal arterial connections with the intervillous space are restricted to tortuous networks of intercellular spaces. Only after this period can direct channels be observed. Initially, these are of small caliber, but they become sizable and clearly delineated after 11 to 12 weeks. Conclusion: The maternal circulation to the placenta must be extremely sluggish before the eighth week of pregnancy but will be gradually established over the next few weeks. It is unlikely to be substantial until at least 12 weeks. The implication is that development of the human fetoplacental unit during most of the first trimester takes place in a low-oxygen environment. (Am J Obstet Gynecol 1999;181:718-24.)

Section snippets

Material and methods

The Boyd Collection is housed within the Department of Anatomy at the University of Cambridge and comprises embryonic, placental, and placenta-in-situ specimens. Only the latter were reviewed in this study to prevent any possible misinterpretations of artifacts introduced during separation at the maternofetal interface. In addition, only those with no recorded history of abnormality were reviewed. Twelve specimens met these criteria, and gestational age (from the last menstrual period) was

Results

In the earliest specimen available, a 43-day specimen identified as H710, multiple profiles of the endometrial arteries can be seen between the dilated uterine glands, indicating that the vessels follow convoluted paths. In all cases the diameter of the profiles reduces as the arteries approach the cytotrophoblastic shell, and in no instances can the vessels be followed beyond the endometrial stroma into the shell (Figs 1 and 2).

. Specimen H710, crown-rump length of 4 mm, approximately 43 days’

Comment

The findings presented here confirm that before the eighth week of pregnancy the maternal arterial connections with the intervillous space are restricted to a tortuous network of intercellular spaces. Only after this period can direct channels be observed. Initially, these are of small caliber, and it is not until 11 to 12 weeks that they become sizable and clearly delineated.

By restricting our study to placentas fixed in situ, we hope to have avoided artifacts induced during delivery. However,

Acknowledgements

The Boyd Collection is available for study purposes, and arrangements to view should be made with the Departmental Secretary (www.bio.cam.ac.uk/dept/anatomy ).

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    The other possibility is that the three lobes are only irrigated by spiral arteries from of one of the UtAs, the left UtA in our second example (Fig. 4B). The concept of obstruction of maternal blood flow to the IVS by trophoblastic plugs before 11–12 weeks' gestation has been widely accepted [30–33]. However, it still remains a controversial topic.

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From the Department of Anatomy, University of Cambridge,a and the Academic Department of Obstetrics and Gynaecology, University College London Medical School.b

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Supported by the Medical Research Council (G9701485). Financial support to the Department of Anatomy, University of Cambridge, was provided by the Anatomical Society of Great Britain and Ireland to assist in cataloging the Boyd Collection.

Reprint requests: Graham J. Burton, MD, Department of Anatomy, Downing St, Cambridge, United Kingdom CB2 3DY.

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