British Journal of Obstetrics and Gynaecology August 1992, Vol. 99, pp. 651-654 ~-
O B s TE T R I c s ~
Placental bed biopsies in placental abruption J . DOMMISSE Professor and Head of Department Departments of Obstetrics & Gynaecology University of Cape Town and Groote Schuur Hospital A. J. TILTMAN Associate Professor Departments of Anatomical Pathology University of Cape Town and Groote Schuur Hospital Cape, South Africa
ABSTRACT Objective To investigate structural changes in the uteroplacental blood vessels in association with placental abruption. Design Prospective descriptive study. Subjects 18 women with clinical evidence of severe placental abruption delivered by caesarean section. Interventions Placental bed biopsies were obtained at caesarean section and studied histologically. Results Six specimens did not include trophoblast in the myometrium and were therefore not representative of the placental bed. Of the 12 representative specimens, seven demonstrated absence of physiological transformation of the utero-placental arteries (four of these were from hypertensive patients). Four biopsies showed abnormal vascular structures deep in the myometrium. One of these abnormal vessels included a fresh plug and extensive surrounding intramyometrial haemorrhage. Conclusions Vascular malformations in association with placental abruption may be the result of trophoblastic invasion and could be the site of vessel rupture. Further descriptive and comparative studies are needed.
Placental abruption is an unpredictable, dramatic event with a 4 0 4 0 % fetal mortality and considerable maternal morbidity. While the cause is unknown, the premature separation of the placenta and the intramyometrial haemorrhage probably result from the rupture of a utero-placental artery with extravasation of blood under arterial pressure between myometrial bundles. Blood tracking to the decidual surface causes placental separation and fetal hypoxia while haemorrhage towards the serosal surface produces the typical ecchymosis of the Couvelaire uterus (Couvelaire 191 1). Whereas approximately 25% of women with placental abruption have hypertension (Brink et al. 1987; Abdella et al. 1984), most of them do not. The possibility of a primary defect in the utero-placental vessels needs to be considered. The microscopic features of the placental bed in placental abruption have been described among larger series of placental bed biopsies (Dixon et al. 1958; Hustin et al. 1983), but there are no published reports dealing specifically with this topic. The purpose of this study was to record the findings in placental bed biopsies in a series of women with clinical placental abruption.
Subjects and methods Design Placental bed biopsies were obtained at the time of caesarean section from 18 women with clinical evidence of placental abruption confirmed by the presence of retroplacental clot at Correspondence: Professor J. Dommisse, Department of Obstetrics and Gynaecology, University of Cape Town Medical School, Observatory, Cape, South Africa.
operation. The technique was that described by Robertson et al. (1986). The site of placental attachment was identified by the surgeon as soon as the fetus was born and marked by the assistant keeping a finger on the serosal surface opposite this area. After delivery of the placenta, this site was inspected for bleeding vessels, and a biopsy approximately 1 cm in diameter and 0.5 cm deep, including bleeding vessels where possible, was taken with a scalpel. A single haemostatic suture was inserted, No problems were encountered with this technique, except that it was more difficult to perform when the placenta was anteriorly situated. The specimen was formalin fixed and paraffin embedded. Sections were stained with haematoxylin and eosin, Victoria blue for elastic fibres, Martius scarlet blue for fibrin, Masson’s trichrome, van Gieson, periodic acid Schiff/alcian blue and combinations thereof. The presence of extra-villous trophoblast within the myometrium was required to confirm that the biopsy was from the placental site. Vessels within the decidua were labelled superficial. Those at the junction of the decidua and myometrium were called intermediate and those completely surrounded by myometrium were labelled deep. The study was approved by the ethics and review committee of the University of Cape Town and patient consent was obtained.
Results Of the 18 biopsies, six showed no trophoblast and were therefore regarded as not representative of the placental bed and excluded from further study. The main clinical and histological features of the remaining 12 women are summarized in Table 1.
65 I
652
J . DOMMISSE ET A L .
Table 1. Clinical and histological features in 12 women with placental abruption delivered by caesarean section Subject number Variable Age (years) Gravidity Gestation (weeks) PIH Outcome Trophoblast Endomet glands Myohaemorrhage UP artery int Phys change int UP artery deep Phys change deep Atherosis Sub int fibrosis Vasc malformation
1
2
3
4
5
6
7
8
9
10
11
12
19 1 31 No A
33 3 37 Yes A
24 2 32 No SB
34 3 36 No A
22 1 34 Yes A
25 2 40 Yes SB
19 1 34 No A
25 5 32 No A
17 1 35 No SB
19 1 32 No A
23 1 34 Yes SB
+/2
+
-
-
-
++
++
++
+ + 1
+ -
-
1
+ -
+ +
+/-
+/-
1 2 -
-
+
+ -
-
1 -
-
-
++
+
+/1 -
1
+/-
+/-
+
++ + +
1 -
+
-
1 -
I
1
-
++
+
1
1
-
1
+
-
-
-
-
+
+
-
-
-
++
+ +
-
-
-
-
1
++ 1
-
++ 1
+
++ 1
+ -
1
Symbols: -, absent: +/-, minimal; +, moderate; ++, marked; numerals 1 or 2 refer to the number of vessels present. Abbreviations: UP artery = Uterine placental artery; intermediate (int) or deep. Phys change = Physiological change. Sub int = Sub intimal fibrosis within arteries. PIH = Pregnancy-induced hypertension. Myo haemorrhage = Intramyometrial haemorrhage. Outcome A = livebirth; SB = still birth
Microscopic examination showed abundant extra villous trophoblast in seven of the 12 biopsies. This was largely composed of multinucleate cells but mononuclear cytotrophoblastic cells could also be found. The other five biopsies contained fewer trophoblastic giant cells and in one of these there were only isolated cells. In four of these latter five biopsies and in two of the first seven, there were endometrial glands on the surface. Haemorrhage was present in 10 of the 12 biopsies. In five there were only small focal collections of red blood cells lying between muscle fibres. In three biopsies haemorrhage was very heavy. In one of these the haemorrhage was predominantly superficial with only moderate haemorrhage in the myometriurn. In a second biopsy there was abundant haemorrhage on both the surface and between muscle bundles (Fig. 1) and in the third it was largely confined to the myometrium. In the remaining two specimens the haemorrhage was assessed as moderate. At least one uteroplacental artery was seen in the myometrium in each biopsy. In five biopsies these showed transformation with replacement of the media by trophoblast and fibrin (the so-called physiological changes). One of these transformed vessels had a layer of sub-intimal fibrin around 50% of its circumference and another showed a marked narrowing rather than dilatation of the lumen due to an accumulation of fibrin within the media. The uteroplacental arteries in the remaining seven biopsies showed no physiologic changes although trophoblast was present near the periphery of the vessels and in one instance a single trophoblastic cell was present within the wall. Four of these seven women were hypertensive. In three intermediate and two deep arteries there was an eccentric intimal fibrosis associated with an accumulation of acid mucopolysaccharide. Two of these arteries (one intermediate and the other deep) showed physiological changes; the other three did not. Four deep uteroplacental arteries showed
medial hypertrophy. Two of these four biopsies (nos. 6 and 7) were from women who were hypertensive. In another hypertensive women (no. 3) one deep vessel showed acute atherosis with lipophages and fibrin within the media. In five of the biopsies the veins showed trophoblast around the periphery, close to the media but not associated with any fibrin or other changes to the media (Fig. 2). In each of four biopsies there was an unusual vascular structure in the myometrium (Fig. 3). Although differing in size and detail they all showed similar features. There was a markedly dilated vessel which for the most part resembled a vein with a thin wall which contained no elastic lamina, trophoblast or fibrin (Fig. 4). In areas the wall was widened by sub-intimal fibrosis. In three of these vessels, fibrin and trophoblast were seen deep to the subintimal thickening. In the fourth vessel there were occasional trophoblastic cells but no fibrin. The dilated portion in all four contained a recent thrombus. These vessels differed from these usually seen in the placental bed and were interpreted as possible vascular malformations. Near
Fig. 1. Haemorrhage tracking between myometrial fibres. HLkEx7.5).
PLACENTAL BIOPSIES IN PLACENTAL ABRUPTION
Fig. 2. Intramyometrialvein showing trophoblast (arrows)in the wall but no fibrin and no transformation. (H&E x 75).
two of these malformations there was marked intramyometrial haemorrhage and in one this appeared to arise from the abnormal vessel (Fig. 5 ) .
Discussion This is essentially a descriptive study of the placental bed in women with placental abruption undertaken in an attempt to identify the origin of the intramyometrial bleeding and to examine the uteroplacental vessels with a view to identifying a possible causative anomaly. One of the problems with placental bed biopsies for such a study is sampling. Of the 18 biopsies, only 12 contained trophoblast and six of these showed some endometrial glands on the surface which might indicate that the biopsy came from near the periphery of the placental bed. Whereas abnormal vessels, if present, could as easily be near the edge as the centre, their presence or absence in the biopsy may be due to chance sampling. Moderate to severe intramyometrial haemorrhage, in keeping with the clinical diagnosis of placental abruption, was present in five biopsies. The vascular abnormalities included an absence of normal physiological changes in the myometrial portion of the utero-
Fig. 3. Vascular malformation. A large complex vessel with thin wall in places and intimal fibrosis (closed arrow) elsewhere. Numerous smaller channels are present at the periphery. Recent thrombus (open arrow) is present. (Trichrome x 20).
653
placental arteries in seven biopsies, intimal or sub-intimal thickenings in five and abnormal or malformed vessels in four. The absence of physiological transformation of the myometrial portion of uteroplacental arteries is associated with gestational hypertension (Khong et a/.1986). Five of the women in this study were hypertensive and four of them showed an absence of arterial transformation. The other three biopsies which showed a lack of transformation were from normotensive pregnancies. Intimal or sub-intimal thickenings were found in the uteroplacental arteries in five biopsies as well as in the four vessels regarded as malformed. In three instances the thickenings occurred in arteries not showing physiological transformation. These intimal thickenings are morphologically similar to the cushions described by Brosens et a/. (1967) who suggested that they may be the result of previous thrombosis. However, their presence in deeper non-transformed arteries in the myometrium suggests that they could also be jet lesions caused by increased or turbulent blood flow. That they are seen frequently in pregnancy indicates that they are not specifically related to placenta abruption. Brosens et al. (1967) also describe these thickenings in veins. Apart from their presence in the four lesions regarded as possible vascular malformations, which may be of venous origin, sub-intimal thickening was not observed in any of the other intramyometrial veins in this study. In four biopsies there were very dilated vessels lying within the myometrium. Brosens et a/.(1967) described superficial veins in the placental bed as being widely dilated with walls showing the presence of fibrin and a loss of normal architecture. The four abnormal vessels in our study might represent a partial extension of this superficial transformation of veins into the intramyometrial portion of the vessel. The precise nature of these vessels was not clear, but they resembled veins with a thin wall without much elastica and no internal elastic lamina. In these areas there was a normallooking media with no evidence of transformation, no trophoblast or intramural fibrin. In places, however, deep in the wall beneath focal intimal thickening, there was fibrin and trophoblast. Sub-intimal fibrosis and recent non-occlusive thrombi were present in all four biopsies. While these changes were not always in opposition, it is tempting to conclude that the intimal
Fig. 4. The wall of the vascular malformation (arrows) contains no elastic tissue. A basal artery in the centre acts ab positive control. (Victoria blue x 150).
654
J . D O M M I S S E ET A L .
cation; this may occur occasionally with the physiological invasion of blood vessels in normal pregnancy. Robertson (1987) suggested that the invading trophoblast sometimes may produce distorted or abnormal architecture. The significance of vascular malformations merits investigation. There is a need for comparable biopsies from the placental bed from pregnancies uncomplicated by placental abruption. If further studies can show that these vessels are the source of the original bleeding in placental abruption, additional factors will need to be identified to explain the higher frequency of placental abruption in women of lower socioeconomic status.
References Fig. 5. Haemorrhage apparently coming from a vascular malformation. Sub-intimal fibrosis is present on the right. A fibrin platelet thrombus (arrow) is present at the site of haemorrhage. (H&E x 75).
thickening is the result of organization of previous mural thrombosis. However, the intimal thickenings are morphologically similar to those seen in deeper radial arteries of the placental bed where they might be better interpreted as jet lesions which are due to increased or turbulent flow: this raises the possibility that these vascular abnormalities could be arteriovenous anastomoses. Heavy intramyometrial haemorrhage was present near two of these malformed vessels and in one instance the haemorrhage appeared to arise from the vessel. Burchell & Mengert have suggested that bleeding from veins might be responsible for the premature separation of the placenta but it would seem unlikely that venous pressure would be sufficient to cause the intramyometrial extravasation seen in placental abruption. Robertson (1 987) reports the occasional finding of arteriovenous malformations in hysterectomy specimens from patients with antepartum haemorrhage. His illustration does not show quite the same appearance as the lesions seen in the present study but it is possible that the structures seen in our study represent arteriovenous communications and the sub-intimal fibrosis could represent attempts at ‘arterialization’ of veins subject to arterial pressures. Haemorrhage from such a vessel may well be under sufficient pressure to track between muscle fibres. Arteriovenous malformations within the uterus are not common. They may be developmental and have also been described as a consequence of carcinoma, gestational trophoblastic disease and trauma following surgery (Fleming et al. 1989). It is tempting to speculate that if the malignant trophoblast of choriocarcinoma can produce arteriovenous communi-
Abdella T. N., Sibai B. M., Hayes J. M. & Anderson C. D. (1984) Relationship of hypertensive disease to abruptio placentae. Ohstet Gynecol63, 365-370. Brink A. L. & Odendaal H. J. (1987) Risk factors for abruptio placentae. S Afr Merd J 72,250-252. Brosens I., Robertson W. B. & Dixon H. G. (1967) The physiological response of the vessels of the placental bed to normal pregnancy. J Path B0c.t 93, 569-579. Burchell R. C. & Mengert W. F. (1969) Etiology of premature separation of the normally implanted placenta. Am .I Ohster Gynecol 104,795-798. Couvelaire A. (191 1 ) ‘Alexander Couvelaire and uteroplacental apoplexy’, Ann de Gynecol8,59 1, quoted in Ohstet Gynecol ( 1957)9, 740-743. Dixon H. G. & Robertson W. B. (1958) A study of the vessels of the placental bed in normotensive and hypertensive women. J Ohster Gynaecol Br Commonw 65,803-809. Fleming H., Ostor A. G., Pickel H. & Fortune D. W. ( 1989) Ateriovenous malformations of the uterus. Ohstet Gynecol73, 209-213. Hustin J., Foidart J. M. & Lambotte R. (1983) Maternal vascular lesions in pre-eclampsia and intrauterine growth retardation: light microscopy and immunofluoresence. Placenta 4,489-498. Khong T. Y., de Wolf F., Robertson W. B. & Brosens I. (1986) Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Ohstet Gynaecol93, 1049-1059. Robertson W. B., Khong T. Y., Brosens I., de Wolf F., Sheppard B. L. & Bonnar J. (1986) The placental bed biopsy: Review from three European centers. Am .I Ohstet Gynecol 155,401 -412. Robertson W. B. (1987) Pathology of the pregnancy uterus. In Huines and Taylor Obstetrical and Gynaecologicul Pathology (Fox H., ed), Churchill Livingstone, p. 1171.
Received 1 J d y 1991 Accepted 28 February 1992
O B s TE T R I c s ~
Placental bed biopsies in placental abruption J . DOMMISSE Professor and Head of Department Departments of Obstetrics & Gynaecology University of Cape Town and Groote Schuur Hospital A. J. TILTMAN Associate Professor Departments of Anatomical Pathology University of Cape Town and Groote Schuur Hospital Cape, South Africa
ABSTRACT Objective To investigate structural changes in the uteroplacental blood vessels in association with placental abruption. Design Prospective descriptive study. Subjects 18 women with clinical evidence of severe placental abruption delivered by caesarean section. Interventions Placental bed biopsies were obtained at caesarean section and studied histologically. Results Six specimens did not include trophoblast in the myometrium and were therefore not representative of the placental bed. Of the 12 representative specimens, seven demonstrated absence of physiological transformation of the utero-placental arteries (four of these were from hypertensive patients). Four biopsies showed abnormal vascular structures deep in the myometrium. One of these abnormal vessels included a fresh plug and extensive surrounding intramyometrial haemorrhage. Conclusions Vascular malformations in association with placental abruption may be the result of trophoblastic invasion and could be the site of vessel rupture. Further descriptive and comparative studies are needed.
Placental abruption is an unpredictable, dramatic event with a 4 0 4 0 % fetal mortality and considerable maternal morbidity. While the cause is unknown, the premature separation of the placenta and the intramyometrial haemorrhage probably result from the rupture of a utero-placental artery with extravasation of blood under arterial pressure between myometrial bundles. Blood tracking to the decidual surface causes placental separation and fetal hypoxia while haemorrhage towards the serosal surface produces the typical ecchymosis of the Couvelaire uterus (Couvelaire 191 1). Whereas approximately 25% of women with placental abruption have hypertension (Brink et al. 1987; Abdella et al. 1984), most of them do not. The possibility of a primary defect in the utero-placental vessels needs to be considered. The microscopic features of the placental bed in placental abruption have been described among larger series of placental bed biopsies (Dixon et al. 1958; Hustin et al. 1983), but there are no published reports dealing specifically with this topic. The purpose of this study was to record the findings in placental bed biopsies in a series of women with clinical placental abruption.
Subjects and methods Design Placental bed biopsies were obtained at the time of caesarean section from 18 women with clinical evidence of placental abruption confirmed by the presence of retroplacental clot at Correspondence: Professor J. Dommisse, Department of Obstetrics and Gynaecology, University of Cape Town Medical School, Observatory, Cape, South Africa.
operation. The technique was that described by Robertson et al. (1986). The site of placental attachment was identified by the surgeon as soon as the fetus was born and marked by the assistant keeping a finger on the serosal surface opposite this area. After delivery of the placenta, this site was inspected for bleeding vessels, and a biopsy approximately 1 cm in diameter and 0.5 cm deep, including bleeding vessels where possible, was taken with a scalpel. A single haemostatic suture was inserted, No problems were encountered with this technique, except that it was more difficult to perform when the placenta was anteriorly situated. The specimen was formalin fixed and paraffin embedded. Sections were stained with haematoxylin and eosin, Victoria blue for elastic fibres, Martius scarlet blue for fibrin, Masson’s trichrome, van Gieson, periodic acid Schiff/alcian blue and combinations thereof. The presence of extra-villous trophoblast within the myometrium was required to confirm that the biopsy was from the placental site. Vessels within the decidua were labelled superficial. Those at the junction of the decidua and myometrium were called intermediate and those completely surrounded by myometrium were labelled deep. The study was approved by the ethics and review committee of the University of Cape Town and patient consent was obtained.
Results Of the 18 biopsies, six showed no trophoblast and were therefore regarded as not representative of the placental bed and excluded from further study. The main clinical and histological features of the remaining 12 women are summarized in Table 1.
65 I
652
J . DOMMISSE ET A L .
Table 1. Clinical and histological features in 12 women with placental abruption delivered by caesarean section Subject number Variable Age (years) Gravidity Gestation (weeks) PIH Outcome Trophoblast Endomet glands Myohaemorrhage UP artery int Phys change int UP artery deep Phys change deep Atherosis Sub int fibrosis Vasc malformation
1
2
3
4
5
6
7
8
9
10
11
12
19 1 31 No A
33 3 37 Yes A
24 2 32 No SB
34 3 36 No A
22 1 34 Yes A
25 2 40 Yes SB
19 1 34 No A
25 5 32 No A
17 1 35 No SB
19 1 32 No A
23 1 34 Yes SB
+/2
+
-
-
-
++
++
++
+ + 1
+ -
-
1
+ -
+ +
+/-
+/-
1 2 -
-
+
+ -
-
1 -
-
-
++
+
+/1 -
1
+/-
+/-
+
++ + +
1 -
+
-
1 -
I
1
-
++
+
1
1
-
1
+
-
-
-
-
+
+
-
-
-
++
+ +
-
-
-
-
1
++ 1
-
++ 1
+
++ 1
+ -
1
Symbols: -, absent: +/-, minimal; +, moderate; ++, marked; numerals 1 or 2 refer to the number of vessels present. Abbreviations: UP artery = Uterine placental artery; intermediate (int) or deep. Phys change = Physiological change. Sub int = Sub intimal fibrosis within arteries. PIH = Pregnancy-induced hypertension. Myo haemorrhage = Intramyometrial haemorrhage. Outcome A = livebirth; SB = still birth
Microscopic examination showed abundant extra villous trophoblast in seven of the 12 biopsies. This was largely composed of multinucleate cells but mononuclear cytotrophoblastic cells could also be found. The other five biopsies contained fewer trophoblastic giant cells and in one of these there were only isolated cells. In four of these latter five biopsies and in two of the first seven, there were endometrial glands on the surface. Haemorrhage was present in 10 of the 12 biopsies. In five there were only small focal collections of red blood cells lying between muscle fibres. In three biopsies haemorrhage was very heavy. In one of these the haemorrhage was predominantly superficial with only moderate haemorrhage in the myometriurn. In a second biopsy there was abundant haemorrhage on both the surface and between muscle bundles (Fig. 1) and in the third it was largely confined to the myometrium. In the remaining two specimens the haemorrhage was assessed as moderate. At least one uteroplacental artery was seen in the myometrium in each biopsy. In five biopsies these showed transformation with replacement of the media by trophoblast and fibrin (the so-called physiological changes). One of these transformed vessels had a layer of sub-intimal fibrin around 50% of its circumference and another showed a marked narrowing rather than dilatation of the lumen due to an accumulation of fibrin within the media. The uteroplacental arteries in the remaining seven biopsies showed no physiologic changes although trophoblast was present near the periphery of the vessels and in one instance a single trophoblastic cell was present within the wall. Four of these seven women were hypertensive. In three intermediate and two deep arteries there was an eccentric intimal fibrosis associated with an accumulation of acid mucopolysaccharide. Two of these arteries (one intermediate and the other deep) showed physiological changes; the other three did not. Four deep uteroplacental arteries showed
medial hypertrophy. Two of these four biopsies (nos. 6 and 7) were from women who were hypertensive. In another hypertensive women (no. 3) one deep vessel showed acute atherosis with lipophages and fibrin within the media. In five of the biopsies the veins showed trophoblast around the periphery, close to the media but not associated with any fibrin or other changes to the media (Fig. 2). In each of four biopsies there was an unusual vascular structure in the myometrium (Fig. 3). Although differing in size and detail they all showed similar features. There was a markedly dilated vessel which for the most part resembled a vein with a thin wall which contained no elastic lamina, trophoblast or fibrin (Fig. 4). In areas the wall was widened by sub-intimal fibrosis. In three of these vessels, fibrin and trophoblast were seen deep to the subintimal thickening. In the fourth vessel there were occasional trophoblastic cells but no fibrin. The dilated portion in all four contained a recent thrombus. These vessels differed from these usually seen in the placental bed and were interpreted as possible vascular malformations. Near
Fig. 1. Haemorrhage tracking between myometrial fibres. HLkEx7.5).
PLACENTAL BIOPSIES IN PLACENTAL ABRUPTION
Fig. 2. Intramyometrialvein showing trophoblast (arrows)in the wall but no fibrin and no transformation. (H&E x 75).
two of these malformations there was marked intramyometrial haemorrhage and in one this appeared to arise from the abnormal vessel (Fig. 5 ) .
Discussion This is essentially a descriptive study of the placental bed in women with placental abruption undertaken in an attempt to identify the origin of the intramyometrial bleeding and to examine the uteroplacental vessels with a view to identifying a possible causative anomaly. One of the problems with placental bed biopsies for such a study is sampling. Of the 18 biopsies, only 12 contained trophoblast and six of these showed some endometrial glands on the surface which might indicate that the biopsy came from near the periphery of the placental bed. Whereas abnormal vessels, if present, could as easily be near the edge as the centre, their presence or absence in the biopsy may be due to chance sampling. Moderate to severe intramyometrial haemorrhage, in keeping with the clinical diagnosis of placental abruption, was present in five biopsies. The vascular abnormalities included an absence of normal physiological changes in the myometrial portion of the utero-
Fig. 3. Vascular malformation. A large complex vessel with thin wall in places and intimal fibrosis (closed arrow) elsewhere. Numerous smaller channels are present at the periphery. Recent thrombus (open arrow) is present. (Trichrome x 20).
653
placental arteries in seven biopsies, intimal or sub-intimal thickenings in five and abnormal or malformed vessels in four. The absence of physiological transformation of the myometrial portion of uteroplacental arteries is associated with gestational hypertension (Khong et a/.1986). Five of the women in this study were hypertensive and four of them showed an absence of arterial transformation. The other three biopsies which showed a lack of transformation were from normotensive pregnancies. Intimal or sub-intimal thickenings were found in the uteroplacental arteries in five biopsies as well as in the four vessels regarded as malformed. In three instances the thickenings occurred in arteries not showing physiological transformation. These intimal thickenings are morphologically similar to the cushions described by Brosens et a/. (1967) who suggested that they may be the result of previous thrombosis. However, their presence in deeper non-transformed arteries in the myometrium suggests that they could also be jet lesions caused by increased or turbulent blood flow. That they are seen frequently in pregnancy indicates that they are not specifically related to placenta abruption. Brosens et al. (1967) also describe these thickenings in veins. Apart from their presence in the four lesions regarded as possible vascular malformations, which may be of venous origin, sub-intimal thickening was not observed in any of the other intramyometrial veins in this study. In four biopsies there were very dilated vessels lying within the myometrium. Brosens et a/.(1967) described superficial veins in the placental bed as being widely dilated with walls showing the presence of fibrin and a loss of normal architecture. The four abnormal vessels in our study might represent a partial extension of this superficial transformation of veins into the intramyometrial portion of the vessel. The precise nature of these vessels was not clear, but they resembled veins with a thin wall without much elastica and no internal elastic lamina. In these areas there was a normallooking media with no evidence of transformation, no trophoblast or intramural fibrin. In places, however, deep in the wall beneath focal intimal thickening, there was fibrin and trophoblast. Sub-intimal fibrosis and recent non-occlusive thrombi were present in all four biopsies. While these changes were not always in opposition, it is tempting to conclude that the intimal
Fig. 4. The wall of the vascular malformation (arrows) contains no elastic tissue. A basal artery in the centre acts ab positive control. (Victoria blue x 150).
654
J . D O M M I S S E ET A L .
cation; this may occur occasionally with the physiological invasion of blood vessels in normal pregnancy. Robertson (1987) suggested that the invading trophoblast sometimes may produce distorted or abnormal architecture. The significance of vascular malformations merits investigation. There is a need for comparable biopsies from the placental bed from pregnancies uncomplicated by placental abruption. If further studies can show that these vessels are the source of the original bleeding in placental abruption, additional factors will need to be identified to explain the higher frequency of placental abruption in women of lower socioeconomic status.
References Fig. 5. Haemorrhage apparently coming from a vascular malformation. Sub-intimal fibrosis is present on the right. A fibrin platelet thrombus (arrow) is present at the site of haemorrhage. (H&E x 75).
thickening is the result of organization of previous mural thrombosis. However, the intimal thickenings are morphologically similar to those seen in deeper radial arteries of the placental bed where they might be better interpreted as jet lesions which are due to increased or turbulent flow: this raises the possibility that these vascular abnormalities could be arteriovenous anastomoses. Heavy intramyometrial haemorrhage was present near two of these malformed vessels and in one instance the haemorrhage appeared to arise from the vessel. Burchell & Mengert have suggested that bleeding from veins might be responsible for the premature separation of the placenta but it would seem unlikely that venous pressure would be sufficient to cause the intramyometrial extravasation seen in placental abruption. Robertson (1 987) reports the occasional finding of arteriovenous malformations in hysterectomy specimens from patients with antepartum haemorrhage. His illustration does not show quite the same appearance as the lesions seen in the present study but it is possible that the structures seen in our study represent arteriovenous communications and the sub-intimal fibrosis could represent attempts at ‘arterialization’ of veins subject to arterial pressures. Haemorrhage from such a vessel may well be under sufficient pressure to track between muscle fibres. Arteriovenous malformations within the uterus are not common. They may be developmental and have also been described as a consequence of carcinoma, gestational trophoblastic disease and trauma following surgery (Fleming et al. 1989). It is tempting to speculate that if the malignant trophoblast of choriocarcinoma can produce arteriovenous communi-
Abdella T. N., Sibai B. M., Hayes J. M. & Anderson C. D. (1984) Relationship of hypertensive disease to abruptio placentae. Ohstet Gynecol63, 365-370. Brink A. L. & Odendaal H. J. (1987) Risk factors for abruptio placentae. S Afr Merd J 72,250-252. Brosens I., Robertson W. B. & Dixon H. G. (1967) The physiological response of the vessels of the placental bed to normal pregnancy. J Path B0c.t 93, 569-579. Burchell R. C. & Mengert W. F. (1969) Etiology of premature separation of the normally implanted placenta. Am .I Ohster Gynecol 104,795-798. Couvelaire A. (191 1 ) ‘Alexander Couvelaire and uteroplacental apoplexy’, Ann de Gynecol8,59 1, quoted in Ohstet Gynecol ( 1957)9, 740-743. Dixon H. G. & Robertson W. B. (1958) A study of the vessels of the placental bed in normotensive and hypertensive women. J Ohster Gynaecol Br Commonw 65,803-809. Fleming H., Ostor A. G., Pickel H. & Fortune D. W. ( 1989) Ateriovenous malformations of the uterus. Ohstet Gynecol73, 209-213. Hustin J., Foidart J. M. & Lambotte R. (1983) Maternal vascular lesions in pre-eclampsia and intrauterine growth retardation: light microscopy and immunofluoresence. Placenta 4,489-498. Khong T. Y., de Wolf F., Robertson W. B. & Brosens I. (1986) Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Ohstet Gynaecol93, 1049-1059. Robertson W. B., Khong T. Y., Brosens I., de Wolf F., Sheppard B. L. & Bonnar J. (1986) The placental bed biopsy: Review from three European centers. Am .I Ohstet Gynecol 155,401 -412. Robertson W. B. (1987) Pathology of the pregnancy uterus. In Huines and Taylor Obstetrical and Gynaecologicul Pathology (Fox H., ed), Churchill Livingstone, p. 1171.
Received 1 J d y 1991 Accepted 28 February 1992
