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Etiology of premature separation of the normally implanted placenta
Etiology of premature separation of the normally implanted placenta Preliminary
observations
R.
BURCHELL,
CLAY
WILLIAM Hartford,
F. Connecticut,
M.D.
MENGERT,
M.D.
and Chicago,
Illinois
Two mechanisms were discovered to impede venous flow from the uterus in late pregnancy: compression of deep veins by the lower uterine segment and obstruction of veins at the lateral pelvic walls by collapse of the flaccid uterus in an accordian-like fashion along its long axis. The implications of this observation discussed in relation to the etiology of premature separation of the placenta.
E V I D E N c E is increasing that interference with venous flow from the pregnant uterus is the primary etiologic factor in human abruptio placentae. Some of this evidence is recent and will be reported here for the first time. On the other hand, an association between venous obstruction and abruption was discovered in animals 50 years ago. Morsel produced abruption in one horn 01 the pregnant rabbit’s uterus by ligation of the ovarian, mesometric, and uterovaginal veins.. Barcroft, Herkel, and Hill2 were “much impressed with a tendency of even moderate pressure on the uterine veins to produce intrauterine hemorrhage.” In 1953 Howard, Goodson, and MengerP in the course of studies to ascertain the cause of the supine hypotensivc syndrome in late human pregnancy discovered that ligation or compres-, sion of the vena cava produced retroplacental bleeding in dogs. Later that year, on the basis of these animal experiments, Mengert and associates* produced human abruption
for the first time. This was accomplished in 2 women undergoing cesarean section by compressing the vena cava for 5 minutes just below the renal veins. This experiment demonstrated conclusively that interference with venous flow from the pelvis of the woman near term could produce placental separation. During the course of the present investigation, the vena cava was obstructed for 2 to 5 minutes in 5 patients, but uterine vein pressures were not elevated significantly. No abruption resulted. In light of this, it was fortuitous that caval compression did produce abruption in both patients in 1953. Collins and associates’* 6 have shown a rather wide variation in venous pressures after caval ligation. Despite these findings, on rare occasions, the supine hypotensive syndrome has been associated with spontaneous abruption.’ However, there is clear evidence that caval obstruction is a rare etiologic factor in the human. The pregnant woman does not voluntarily lie supine in late pregnancy. If she is made to do so, the supine hypotensive syndrome develops in about 5 minutes with a femoral venous pressure reaching 20 to 25 cm. of water. One in 10 of these women develops a classical picture of shock and hypotension.3 If a woman near term happens to lie supine on her back, she speedily becomes
From the Departments of Obstetrics and Gynecology, of Hartford Hospital and of the University of Illinois, Chicago. Presented at the Thirty-sixth Annual Meeting of the Central Association of Obstetricians and Gynecologists, Oklahoma
City,
Oklahoma,
Sept.
are
26-28,
1968. 795
796
Burchell
and
Mengert
uncomfortable and instinctively seeks another position. Thus, it is obvious that caval compression by the flaccid human uterus is neither a common nor an important etiologic factor in separation of the normally implanted placenta. Every obstetrician has noticed at cesarean section the plexus of distended and turgid broad ligament veins. Pressures of 20 to 40 cm. of water were measured in these veins while they were distended. They collapsed after removal of the products of conception with a drop in venous pressures to a range of 5 to 10 cm. of water. Since all patients \vere supine during operations, caval compression was thought likely to be the cause of distention. If this were the cause, uterine and femoral venous pressures should be approximately equal. Although caval compression by the pregnant uterus did produce elevated pressures in both these veins, it soon became apparent that additional factors were responsible for high pressures in uterine veins. Femoral vein pressures fell to normal when the uterus was lifted off the vena cava; uterine vein pressures remained clevated until after the birth of the baby or, in a few patients, the placenta. Observations
In order to investigate this seeming paradox, WC lifted the intact uterus out of the abdomen through an extended incision. The turgid uterine veins collapsed immediately. I (R. C. B.) saw an intact pregnant uterus without distended uterine veins for the first time. To prove this observation, the uterus was allowed to sink into the pelvis. The veins redistended. The uterus was lifted out of the pelvis again, The veins collapsed. Subsequently, two simple mechanisms were found to impede venous flow from the pregnant uterus. Both were demonstrated with the uterus out of the abdomen. First, the enlarging uterus in late pregnancy compressed veins deep in the pelvis. This was demonstrated by lifting, as noted above, or pushing the uterus out of the pelvis with pressure applied upward on the vaginal vault. Lifting produced complete collapse of
An.
July 15, 1969 J. Obst. & Gynec.
veins; pushing only partially relieved the congestion in the broad ligament veins. The second mechanism of impeding venous flow was elicited by compressing the uterus in an accordian-line fashion along its long axis. This was accomplished by lifting the uterus out of the pelvis with resulting collapse of broad ligament veins as before. The lower uterine segment was then compressed like an accordian by pushing upward on the vaginal vault and downward on the fundus. With this maneuver the broad ligament veins redistended and pressures rose to the higher levels. In other words, uterine vein pressures wcrc elevated when the lower uterus fitted snugly into the pelvis, or was compressed along its long axis. On the other hand, femoral pressures remained low (8 to 10 cm. of water) during thrse maneuvers. ‘I’hus, three mechanisms causing interference with venous outflow in late pregnancy were demonstrated: ( I) vena cava compression; (2) natural compression by gravity w:hcn the uterus sinks low in the pelvis; (3) accordianlike compression of the lower utcrinc segInerlt.
Comment
Obviously the first mechanism, caval compression, seldom occurs in the intact woman for any length of time. The second and third mechanisms may act together or independently. Obviously, they would be enhanced with the dccrrased uterine tone, increasing size of the uterus and in upright positions. ‘I’he following etiology of abruption seems plausible. These mechanisms impeding venous flow produce a pressure sufficient to rupture decidual veins leaving the intervillous space. Rupture of these veins must occur when the uterus is relaxed. Otherwise, veins arc splinted by surrounding tissues. This is the reason venous rupture does not occur with each uterine contraction. One of the strongest arguments in favor of this etiolog) is the paradoxical fact that these mechanisms tend to create the highest pressures when the uterus is most flaccid and has the least splinting effect. A number of secondary effects follow initial rupture. Hematoma de-
Volume
104
Etiology
Numbcr6
velops, separating the placenta from the uterus in the natural cleavage plane beneath the basal plate. Irritation increases uterine tonus. This alone may be adequate to stop further bleeding. If not, increased tonus will be sufficient to counteract these mechanisms impeding venous flow. Other factors such as collateral drainage through ovarian veins, and inherent strength of the vein wall may be important in preventing abruption. In fact, abruption probably occurs only under very specific circumstances; with a relaxed uterus, when ovarian veins cannot act as collaterals, and perhaps with inherent weakness of the vein wall. This work was interrupted before it could be completed. Additional information is necessary. We must ascertain the uterine venous pressure range which will usually result in
of premature
separation
of
placenta
797
abruption and be able to produce these pressures experimentally at will. Moreover, the potential of the ovarian veins as a route of collateral drainage must be investigated. We did so in 5 patients with high placental implantations. In four, the ovarian veins did not provide collateral pathways. In the fifth, uterine vein pressures were not elevated until after the ovarian veins were occluded. In all of these investigations no mother or infant was injured. Nevertheless, we plan in the near future to continue the investigation in pregnant rhesus monkeys. At the present time this theory seems plausible, is substantiated by much clinical and experimental evidence, provides an answer to the primary etiology of human abruption and seems to have no serious contradictions.
REFERENCES
1.
Morse, A. H.: Surg. Gynec. 1918.. 2. Barcroft, J., Herkel, W., Phvsiol. 77: 194, 1933. 3. Howard, B. K., &odson, J. W. F.: Obst. & Gynec. 1: 4. Mengert, W. F., Goodson, R. G., and Haynes, D. M.: GYNEC. 66: 1104, 1953.
Discussion DR. DOUGLAS M.
& Obst. and
Hill,
26:
133,
S.:
5.
J. 6.
H., and Mengert, 371, 1953. J. H., Campbell, AM, J. OBST. &
HAYNES, Louisville,
Ken-
tucky. It is a particular pleasure for me to discuss this intriguing paper by Drs. Burchell and Mengert because I have been interested in, and baflled by, the problem of the etiology of pIa-, cental abruption ever since my participation 15 years ago in Dr. Mengert’s original demonstra-, tion of the experimental production of placental separation by compression of the inferior vena cava. Despite numerous efforts by countless in-, vestigators throughout the years, the basic mechanism responsible for spontaneous separation of the placenta in the third trimester of pregnancy has eluded us to date. Such suggested etiologlc factors as toxemia, trauma, chronic hypertension: parity, and folic acid deficiency have proved difficult or impossible to substantiate as the definitive causes of the condition. Dr. Mengert’s work on the placental effects of vena caval compres-
7.
Collins, C. G., Weinstein, B. B., Norton, R. O., and Webster, H. D.: AM. J. OBST. & GYNEC. 63: 351, 1952. Collins, C. G.: ‘Discussion of Haynes, D. M.: AM. T. OBST. & GYNEC. 85: 626. 1963. Smite, K., and Fields, H.: Obst. & Gynec. 12: 369, 1958.
sion first focused venous congestion
serious attention on acute as the precipitating cause of premature separation, but by his own admission such venous compression is virtually always present in the supine position during late pregnancy and could scarcely account for more than an occasional instance of clinically significant abruptio placentae. Now Drs. BurcheIl and Mengert propose a provocative extension of the venous occlusion theory bolstered by the simple but dramatically graphic demonstration of the effect of uterine vein occlusion on the production of the often observed engorgement of the venous plexuses in the broad ligaments at the time of cesarean section. Should later experimental data establish a definite causal relationship between this venous turgidity and spontaneous placental separation, the authors will have laid the basis of a hypothesis based on a naturally occurring venous occlu-
798
Burchell
and
Mengert
sive mechanism rather than the improbable possibility inherent in the vena cava concept. The hypothesis is consistent with the observed limitation of clinical abruptio placentae to the third trimester and supports the contention of earlier workers that the underlying mechanism responsible for placental separation is dependent on acute passive hyperemia. It is also compatible with the local histologic findings in the vessels of the decidua which can be produced by vena cava compression, as described several years ago in the rabbit. I hope the authors will indeed extend their studies to the monkey, and that they test their hypothesis both by venous pressure measurements and by investigation of local changes in the placental site. It would also bc important to determine if the actual separation of the placenta from the decidua basalis reprcsents the resuIt of a purely mechanical rupture of overengorged venous channels, or if it is prrceded by recognizable alterations in decidual vessels which, in turn, create the local conditions responsible for the clinical abruption. Yet another possibility suggests itself for study. We know that the delivery of the fetus is followed by sudden collapse of the flaccid lowrr uterine segment, and that normal placental scpnration follows within minutrs; occasionally, hnwever, the placenta is cxtrudcd inltnrdiatcly and
is followed by a large amount of retroplacental blood. Could the venous congestion produced by the lower segment collapse be responsible fot either normal separation or so-called “terminal abruptio,” depending on the venous pressurr elevation created in a git,en uterine venous system? Perhaps, indeed, the authors’ future t’csearches may broaden our concepts of the mechanism of normal placental separation, hitherto assumed to he solely a function of uterine contractile activity. We all await with interest the publication of the authors’ studies to follow up this provocative preliminary report. DR. RURCHELL (Closing). I should like to thank Dr. Haynes very much for his kind retnarks. We had not considered the implirations of this venous obstruction on txttural placentai separation. This may be an important factot and should be studied in the future. His discussion also brings up one point that was probably not sufficiently clear in the paper. The venous congestion usually disappeared after the birth of the baby, hut sometimes not until the birth of the placenta. We found the deciding factor to 1~~ when the uterus was lifted out. Venous congestion persisted after the baby was born if the ~owcr uterine segment remained fitted into thr pelvis.
observations
R.
BURCHELL,
CLAY
WILLIAM Hartford,
F. Connecticut,
M.D.
MENGERT,
M.D.
and Chicago,
Illinois
Two mechanisms were discovered to impede venous flow from the uterus in late pregnancy: compression of deep veins by the lower uterine segment and obstruction of veins at the lateral pelvic walls by collapse of the flaccid uterus in an accordian-like fashion along its long axis. The implications of this observation discussed in relation to the etiology of premature separation of the placenta.
E V I D E N c E is increasing that interference with venous flow from the pregnant uterus is the primary etiologic factor in human abruptio placentae. Some of this evidence is recent and will be reported here for the first time. On the other hand, an association between venous obstruction and abruption was discovered in animals 50 years ago. Morsel produced abruption in one horn 01 the pregnant rabbit’s uterus by ligation of the ovarian, mesometric, and uterovaginal veins.. Barcroft, Herkel, and Hill2 were “much impressed with a tendency of even moderate pressure on the uterine veins to produce intrauterine hemorrhage.” In 1953 Howard, Goodson, and MengerP in the course of studies to ascertain the cause of the supine hypotensivc syndrome in late human pregnancy discovered that ligation or compres-, sion of the vena cava produced retroplacental bleeding in dogs. Later that year, on the basis of these animal experiments, Mengert and associates* produced human abruption
for the first time. This was accomplished in 2 women undergoing cesarean section by compressing the vena cava for 5 minutes just below the renal veins. This experiment demonstrated conclusively that interference with venous flow from the pelvis of the woman near term could produce placental separation. During the course of the present investigation, the vena cava was obstructed for 2 to 5 minutes in 5 patients, but uterine vein pressures were not elevated significantly. No abruption resulted. In light of this, it was fortuitous that caval compression did produce abruption in both patients in 1953. Collins and associates’* 6 have shown a rather wide variation in venous pressures after caval ligation. Despite these findings, on rare occasions, the supine hypotensive syndrome has been associated with spontaneous abruption.’ However, there is clear evidence that caval obstruction is a rare etiologic factor in the human. The pregnant woman does not voluntarily lie supine in late pregnancy. If she is made to do so, the supine hypotensive syndrome develops in about 5 minutes with a femoral venous pressure reaching 20 to 25 cm. of water. One in 10 of these women develops a classical picture of shock and hypotension.3 If a woman near term happens to lie supine on her back, she speedily becomes
From the Departments of Obstetrics and Gynecology, of Hartford Hospital and of the University of Illinois, Chicago. Presented at the Thirty-sixth Annual Meeting of the Central Association of Obstetricians and Gynecologists, Oklahoma
City,
Oklahoma,
Sept.
are
26-28,
1968. 795
796
Burchell
and
Mengert
uncomfortable and instinctively seeks another position. Thus, it is obvious that caval compression by the flaccid human uterus is neither a common nor an important etiologic factor in separation of the normally implanted placenta. Every obstetrician has noticed at cesarean section the plexus of distended and turgid broad ligament veins. Pressures of 20 to 40 cm. of water were measured in these veins while they were distended. They collapsed after removal of the products of conception with a drop in venous pressures to a range of 5 to 10 cm. of water. Since all patients \vere supine during operations, caval compression was thought likely to be the cause of distention. If this were the cause, uterine and femoral venous pressures should be approximately equal. Although caval compression by the pregnant uterus did produce elevated pressures in both these veins, it soon became apparent that additional factors were responsible for high pressures in uterine veins. Femoral vein pressures fell to normal when the uterus was lifted off the vena cava; uterine vein pressures remained clevated until after the birth of the baby or, in a few patients, the placenta. Observations
In order to investigate this seeming paradox, WC lifted the intact uterus out of the abdomen through an extended incision. The turgid uterine veins collapsed immediately. I (R. C. B.) saw an intact pregnant uterus without distended uterine veins for the first time. To prove this observation, the uterus was allowed to sink into the pelvis. The veins redistended. The uterus was lifted out of the pelvis again, The veins collapsed. Subsequently, two simple mechanisms were found to impede venous flow from the pregnant uterus. Both were demonstrated with the uterus out of the abdomen. First, the enlarging uterus in late pregnancy compressed veins deep in the pelvis. This was demonstrated by lifting, as noted above, or pushing the uterus out of the pelvis with pressure applied upward on the vaginal vault. Lifting produced complete collapse of
An.
July 15, 1969 J. Obst. & Gynec.
veins; pushing only partially relieved the congestion in the broad ligament veins. The second mechanism of impeding venous flow was elicited by compressing the uterus in an accordian-line fashion along its long axis. This was accomplished by lifting the uterus out of the pelvis with resulting collapse of broad ligament veins as before. The lower uterine segment was then compressed like an accordian by pushing upward on the vaginal vault and downward on the fundus. With this maneuver the broad ligament veins redistended and pressures rose to the higher levels. In other words, uterine vein pressures wcrc elevated when the lower uterus fitted snugly into the pelvis, or was compressed along its long axis. On the other hand, femoral pressures remained low (8 to 10 cm. of water) during thrse maneuvers. ‘I’hus, three mechanisms causing interference with venous outflow in late pregnancy were demonstrated: ( I) vena cava compression; (2) natural compression by gravity w:hcn the uterus sinks low in the pelvis; (3) accordianlike compression of the lower utcrinc segInerlt.
Comment
Obviously the first mechanism, caval compression, seldom occurs in the intact woman for any length of time. The second and third mechanisms may act together or independently. Obviously, they would be enhanced with the dccrrased uterine tone, increasing size of the uterus and in upright positions. ‘I’he following etiology of abruption seems plausible. These mechanisms impeding venous flow produce a pressure sufficient to rupture decidual veins leaving the intervillous space. Rupture of these veins must occur when the uterus is relaxed. Otherwise, veins arc splinted by surrounding tissues. This is the reason venous rupture does not occur with each uterine contraction. One of the strongest arguments in favor of this etiolog) is the paradoxical fact that these mechanisms tend to create the highest pressures when the uterus is most flaccid and has the least splinting effect. A number of secondary effects follow initial rupture. Hematoma de-
Volume
104
Etiology
Numbcr6
velops, separating the placenta from the uterus in the natural cleavage plane beneath the basal plate. Irritation increases uterine tonus. This alone may be adequate to stop further bleeding. If not, increased tonus will be sufficient to counteract these mechanisms impeding venous flow. Other factors such as collateral drainage through ovarian veins, and inherent strength of the vein wall may be important in preventing abruption. In fact, abruption probably occurs only under very specific circumstances; with a relaxed uterus, when ovarian veins cannot act as collaterals, and perhaps with inherent weakness of the vein wall. This work was interrupted before it could be completed. Additional information is necessary. We must ascertain the uterine venous pressure range which will usually result in
of premature
separation
of
placenta
797
abruption and be able to produce these pressures experimentally at will. Moreover, the potential of the ovarian veins as a route of collateral drainage must be investigated. We did so in 5 patients with high placental implantations. In four, the ovarian veins did not provide collateral pathways. In the fifth, uterine vein pressures were not elevated until after the ovarian veins were occluded. In all of these investigations no mother or infant was injured. Nevertheless, we plan in the near future to continue the investigation in pregnant rhesus monkeys. At the present time this theory seems plausible, is substantiated by much clinical and experimental evidence, provides an answer to the primary etiology of human abruption and seems to have no serious contradictions.
REFERENCES
1.
Morse, A. H.: Surg. Gynec. 1918.. 2. Barcroft, J., Herkel, W., Phvsiol. 77: 194, 1933. 3. Howard, B. K., &odson, J. W. F.: Obst. & Gynec. 1: 4. Mengert, W. F., Goodson, R. G., and Haynes, D. M.: GYNEC. 66: 1104, 1953.
Discussion DR. DOUGLAS M.
& Obst. and
Hill,
26:
133,
S.:
5.
J. 6.
H., and Mengert, 371, 1953. J. H., Campbell, AM, J. OBST. &
HAYNES, Louisville,
Ken-
tucky. It is a particular pleasure for me to discuss this intriguing paper by Drs. Burchell and Mengert because I have been interested in, and baflled by, the problem of the etiology of pIa-, cental abruption ever since my participation 15 years ago in Dr. Mengert’s original demonstra-, tion of the experimental production of placental separation by compression of the inferior vena cava. Despite numerous efforts by countless in-, vestigators throughout the years, the basic mechanism responsible for spontaneous separation of the placenta in the third trimester of pregnancy has eluded us to date. Such suggested etiologlc factors as toxemia, trauma, chronic hypertension: parity, and folic acid deficiency have proved difficult or impossible to substantiate as the definitive causes of the condition. Dr. Mengert’s work on the placental effects of vena caval compres-
7.
Collins, C. G., Weinstein, B. B., Norton, R. O., and Webster, H. D.: AM. J. OBST. & GYNEC. 63: 351, 1952. Collins, C. G.: ‘Discussion of Haynes, D. M.: AM. T. OBST. & GYNEC. 85: 626. 1963. Smite, K., and Fields, H.: Obst. & Gynec. 12: 369, 1958.
sion first focused venous congestion
serious attention on acute as the precipitating cause of premature separation, but by his own admission such venous compression is virtually always present in the supine position during late pregnancy and could scarcely account for more than an occasional instance of clinically significant abruptio placentae. Now Drs. BurcheIl and Mengert propose a provocative extension of the venous occlusion theory bolstered by the simple but dramatically graphic demonstration of the effect of uterine vein occlusion on the production of the often observed engorgement of the venous plexuses in the broad ligaments at the time of cesarean section. Should later experimental data establish a definite causal relationship between this venous turgidity and spontaneous placental separation, the authors will have laid the basis of a hypothesis based on a naturally occurring venous occlu-
798
Burchell
and
Mengert
sive mechanism rather than the improbable possibility inherent in the vena cava concept. The hypothesis is consistent with the observed limitation of clinical abruptio placentae to the third trimester and supports the contention of earlier workers that the underlying mechanism responsible for placental separation is dependent on acute passive hyperemia. It is also compatible with the local histologic findings in the vessels of the decidua which can be produced by vena cava compression, as described several years ago in the rabbit. I hope the authors will indeed extend their studies to the monkey, and that they test their hypothesis both by venous pressure measurements and by investigation of local changes in the placental site. It would also bc important to determine if the actual separation of the placenta from the decidua basalis reprcsents the resuIt of a purely mechanical rupture of overengorged venous channels, or if it is prrceded by recognizable alterations in decidual vessels which, in turn, create the local conditions responsible for the clinical abruption. Yet another possibility suggests itself for study. We know that the delivery of the fetus is followed by sudden collapse of the flaccid lowrr uterine segment, and that normal placental scpnration follows within minutrs; occasionally, hnwever, the placenta is cxtrudcd inltnrdiatcly and
is followed by a large amount of retroplacental blood. Could the venous congestion produced by the lower segment collapse be responsible fot either normal separation or so-called “terminal abruptio,” depending on the venous pressurr elevation created in a git,en uterine venous system? Perhaps, indeed, the authors’ future t’csearches may broaden our concepts of the mechanism of normal placental separation, hitherto assumed to he solely a function of uterine contractile activity. We all await with interest the publication of the authors’ studies to follow up this provocative preliminary report. DR. RURCHELL (Closing). I should like to thank Dr. Haynes very much for his kind retnarks. We had not considered the implirations of this venous obstruction on txttural placentai separation. This may be an important factot and should be studied in the future. His discussion also brings up one point that was probably not sufficiently clear in the paper. The venous congestion usually disappeared after the birth of the baby, hut sometimes not until the birth of the placenta. We found the deciding factor to 1~~ when the uterus was lifted out. Venous congestion persisted after the baby was born if the ~owcr uterine segment remained fitted into thr pelvis.