Placental
Emboli From a Fetus Papyraceous
By Douglas S. Wagner,
Robert L. Klein, Haynes B. Robinson,
Akron, l A syndrome in monozygotic twins that consists of a macerated twin fetus (fetus papyraceous) and a live-born twin with various anatomical defects has been described. The etiology is thought to be placental transfer of emboli or thromboplastic material through vascular shunts. Thromboplastic material precipitates disseminated intravascular coagulation {DIG) in the fetus, with a resultant hypercoagulable state due to relative fetal antithrombin Ill deficiency. Two cases of this syndrome will be discussed. The case of a live-born twin with intestinal atresia, who developed in utero with a fetus papyraceous, is reported. Emboli were demonstrated in vascular shunts of the diamnioticmonochorionic placenta. The hypothesis of intestinal atresia as a result of a vascular accident is reviewed. Another case involving a live-born twin with congenital skin defects, who developed in utero with a fetus papyraceous, is also reported. The skin defects were a congenital disruption from fetal DIC with resultant hypercoagulable state. Several other manifestations of the placental emboli syndrome will be discussed and the vascular etiology of the disruptions explained. 0 1955 by W.5. Saunders Company. INDEX WORDS:
Fetus papyraceous;
placental
emboli.
A
SYNDROME occurring in monozygotic twins that consists of a macerated twin fetus (fetus papyraceous) and a live-born twin with various structural defects has been described. Possible etiologies are thought to be placental transfer of thromboplastic material or emboli through vascular shunts. Two cases involving a live-born twin with a congenital defect who developed in utero with a macerated twin are presented. Thrombi were demonstrated in placental vascular shunts. This syndrome, its various manifestations, its anatomic placental basis, and the causes of some specific congenital defects are described. CASE
Case l-Intestinal
REPORTS
Atresia
A healthy 2%year-old (gravida 3, para 1, abortus 1) white woman’s twin pregnancy was complicated by the death of one twin at approximately 18 to 20 weeks’ gestation. This was documented by ultrasound. Hydramnios became evident as the pregnancy progressed, and was treated on four occasions by therapeutic amniocen-
and Robert W. Novak
Ohio
tesis. Because of a decreasing maternal fibrinogen level, the twins were delivered by cesarean section at 28 weeks’ gestation. The live twin was a boy, weighed 1,600 g, and had Apgars of 4 and 6. He had respiratory distress, was intubated, and transferred to the neonatal intensive care unit. The physical examination showed abdominal distention, ascites, and hepatomegaly. Abdominal films demonstrated small-bowel distention, and a barium enema outlined an unused colon. Ultrasound showed a normal urinary tract and ascites. Bile-stained ascitic fluid was obtained by paracentesis. A diagnosis of intestinal atresia with perforation was made, and a laparotomy was performed. An ileal atresia with perforation was found; resection and end-to-end anastamosis restored intestinal continuity. The postoperative course was uneventful. There was no evidence of central nervous system damage, renal dysfunction, or any other defects. Pathologic examination of the atretic specimen confirmed an KS-cm segment of atretic ileum with perforation and evidence of remote ischemia. The mesentery adjacent to the perforation was necrotic and rendering the demonstration of emboli impossible. The dead twin fetus was severely macerated (Fig 1). The placenta was diamniotic and monochorionic. Careful physical examination and injection of water soluble contrast material showed a large vein-tovein anastamosis connecting the two halves of the placenta. Multiple intravascular thrombi were seen on the live twin side of the placenta (Fig 2).
Case 2-Congenital
Skin Defects
A 26-year-old woman (gravida 1, para O-2) went into spontaneous premature labor and delivered twins. One twin was normal. The other infant, a boy, weighed 1,800 g and had transient respiratory distress in the delivery room. He also had multiple cutaneous defects, the largest measuring 4 cm by 3 cm on the vertex of the scalp in the midline (Fig 3). There was a bony defect under the lesion, and the dura was covered by a thin layer of tissue that resembled parchment. He also had skin defects over both knees that measured 1 cm by 1 cm. Skull films showed an ossification defect underneath the skin lesion, and a computed axial tomography scan showed an anatomically normal brain. The remainder of the physical examination yielded normal results. A careful examination of the placenta showed the pregnancy to have actually been a triplet pregnancy. There were two placental discs. The normal baby had its own placenta, and the patient shared a diamniotic-monochorionic placenta with a fetus papyraceous that was 8 cm in length (Fig 4). Vascular injection studies of the placenta were impossible to perform because the referring institution fixed the specimen in formalin before transferring the patient with the placenta. Two days after birth, the baby was taken to the operating room, the lesions on the knees were excised, and the skin defects closed primarily. The parchment-like tissue covering the dura was excised, and a split-thickness skin graft obtained from the back was placed on the scalp wound. The graft and donor site were dressed with Biobrane (Winthrop Pharmaceuticals, Kalamazoo, MI). The recovery was uneventful.
From the Department of Surgery, Akron City Hospital; the Departments of Surgery and Pathology, Children’s Hospital Medical Center of Akron; and the Departments of Surgery and Pathology, Northeastern Ohio Universities College of Medicine, Rootstown, OH. Date accepted: October 1.1988. Address reprint requests to Dr Robert L. Klein, 300 Locust St. Akron. OH 44302. o 1990 by W.B. Saunders Company. 0022-3468/90/2505-0017$03.00/0
In order to understand the pathophysiology of these conditions, it is necessary to understand the different variations in placental anatomy in twinning. The placenta is composed of the maternai decidua basalis,
538
Journalof Pediafric
DISCUSSION
Surge-y, Vol
25, No 5 (May). 1990: pp 538-542
PLACENTAL EMBDLI
Fig 1. Cane 1-Macerated twin on left and placental diu: on right. Diamniotic-monochorionic placenta.
the fetal chorion, and the amniotic sac. The amnion, the innermost membrane, forms a sac surrounding the embryo, covers the umbilical cord, and joins the embryo at the umbilicus. The chorion is the outermost membrane and is composed of chorion laeve and chorion frondosum. Fraternal (dizygous) twins usually have diamniotic-dichorionic membranes, with separate placental masses, and occasionally have a diamnioticdichorionic arrangement with fused choria and fused placental masses. The type of placental arrangement associated with monozygotic twins depends on the time from conception that twinning occurs. If twinning
occurs from 1 to 3 days after conception, before the blastocyst stage, the twins will have a diamnioticdichorionic separate or diamniotic-dichorionic fused arrangement. If twinning occurs from 3 to 8 days after conception, which is the usual case, a diamnioticmonochorionic single placenta will develop. In those instances when twinning occurs after 8 days, by which time the amniotic cavity has already begun to form, a monoamniotic-monochorionic single placenta develops (Fig 5).’ This arrangement occurs in 4% of cases of monozygotic twins, and is often fatal due to tangling of the umbilical cords with circulatory impairment.*
Fii 2. CaH 1--Macerated twin on the keft, thrombi in vasoular ahunt+ (arrow) demonstratod by w&ersoluable contrast.
WAGNER ET AL
Fig 3. fect.
Benirschke and Driscol13 performed injection studies on twin placentas and found vascular shunts between the two halves of the placenta in almost all monochorial twin placentas. They could demonstrate no shunts in dichorial twin placentas. These shunts may be artery-to-artery (A-A) occurring in 65% of diamnioticmonochorionic placentas, artery-to-vein (A-V) in 43% or vein-to-vein (V-V) in 10’K3 Depending on the number and type of anastamoses in the placenta, the shunts may be innocuous or give rise to the placental transfusion syndromes. It has also been postulated, originally by Benirschke,4 that particulate matter or thromboplastic material from a dead twin fetus can traverse vascular shunts. This may promote disseminated intravascular coagulation or localized ischemic infarcts, with resultant tissue loss in the surviving twin. Apparently, A-A shunts are usually harmless and the concomitant occurrence of A-A and A-V shunts (28%) is also not associated with problems. However, if A-V shunts exist alone (12%), the classic transfusion syndrome often develops. The existence of V-V shunts alone (5%) is also associated with a higher incidence of congenital problems in the twin pregnancy. Disseminated intravascular coagulation (DIC) in the surviving twin with a macerated twin fetus has been recognized as a syndrome.‘-’ The mechanism for production of this syndrome seems to be release of thromboplastic material from the dead twin into the placental circulation of the surviving twin via vascular shunts. In the maternal circulation, a consumptive coagulopathy occurs with resultant hypofibrinogen-
Case
2-Scalp
de-
emia and bleeding tendency. In contrast, the viable fetus has an immature fibrinolytic system with a relative antithrombin III deficiency and in this situation, the presence of thromboplastic material will lead to a hypercoagulable state with resultant infarction (Fig 6). Benirschke4 and Hoyme et al9 documented fibrin thrombi-occluding vessels of a live-born twin at the time of autopsy. Fibrin thrombi found in vessels of the brain, kidney, spleen, and liver resulted in necrosis of these organs. Another possible mechanism of production of congenital defects in the surviving twin, in a monozygous twin pair with single fetal death, is embolization of clot or necrotic fetal tissue across placental shunts4 that may give rise to localized ischemic infarcts with resultant tissue loss in the live-born twin. By either mechanism, DIC or embolus, there are certain sites of predilection where occlusion of a particular fetal artery will produce recognizable end organ damage. Depending on the magnitude and site of intravascular catastrophe, a range of clinical manifestations is found. Renal artery involvement causes renal cortical necrosis. % Internal carotid artery occlusion causes a variety of central nervous system defectsse9 Stapedial artery involvement may cause hemifacial microstomia.’ Mesenteric vascular occlusion may cause small bowel atresias8”09” or colonic atresia.’ Other end organ damage includes congenital skin defects” and possible terminal limb defects (Fig 7).12 The most highly regarded hypothesis on the causes of intestinal atresia is in utero disruption of the
PLACENTAL EMBOLI
Fig 4. Case Z-_(A) Fetus papyraceous in diamniotic-monochorionic placenta (arrow) next to placenta of normal baby. IB) Macerated triplet (isolated).
vascular supply to a segment of the developed intestine with resultant necrosis. The hypothesis has been supported by Louw and Barnard’si work with fetal puppies. By ligation of various mesenteric vessels, they were able to produce all the varieties of intestinal atresia including webs, stenosis, fibrous connections, and discontinuous gaps. Intestinal atresias are rarely associated with other malformations, thus the interruption of blood supply to an intestinal segment is usually a local event such as herniation, volvulus, kinking, or intussusception.i4 Therefore, we assume that DIC from placental emboli would be a rare cause of intestinal atresia, rather than a common mechanism. The patient born with ileal atresia and a macerated twin fetus shared a diamniotic-monochorionic placenta, in which vascular shunts from one side of the
placenta to the other were demonstrated, Furthermore, thrombi were identified in these V-V shunts by taking placental x-rays after injecting the placental vessels with contrast material. We hypothesize that thrombi and/or throboplastic material from the macerated twin fetus passed through vascular shunts to the live-born twin, resulting in DIC with thrombosis of a portion of the mesenteric circulation and resultant infarction of distal ileum. An embolus, traversing the vascular shunt and lodging in a portion of the mesenteric circulation, is also a plausible explanation for the findings. The patient born with congenital skin defects shared a diamniotic-monochorionic placenta with the fetus papyraceous. We theorize that thromboplastic material from the macerated fetus entered the live-born
542
WAGNER ET AL
Mi! TWIN
CUT6 APLASIA
NECROTIC TISSUE
Fig 7. Various anatomically disruptive defects caused by death of one twin and the release of emboli or thromboplastic material into shared placental vascular communications. Fig 6.
Placental variations
in twinning.
triplet’s circulation via placental shunts and precipitated a fetal hypercoagulable state. Pressure points secondary to fetal position, scalp, and knees, in the amniotic sac were susceptible to infarction secondary to intravascular coagulation. In other cases of congenital skin defects with associated fetus papyraceous, the lesions are usually symmetrical and most often affect the flanks and knees.” It is estimated that 32S3 of twin pregnancies at 10 weeks result in singleton deliveries, so fetus papyraceous is probably more common than is recognized. Therefore, all placentas should be examined in the delivery room for evidence of twinning and a macerated fetus. If evidence of fetus papyraceous is discovMONOZYGOUS
TWIN DEATH
MACERATION J THRDMBOPLASTIN
CONSUMPTION
MATERNAL
HYPOFRIBRINOGENEMIA & BLEEDING
TENDENCY
J COAGULOPATHY
- DIC
TWIN
IMMATURE FIBRINOLYTIC SYSTEM AT III 4
( HYPER 1COAGULABILITY 4 ORGAN INFARCTION
Pathophysiologioal events precipitated by in utero death Fig 6. of a monosygous twin and release of thromboplastin.
ered, the baby at risk for congenital malformations due to placental emboli phenomenon must be thoroughly evaluated. Likewise, children born with disruptive congenital defects should have their placentas evaluated for a fetus papyraceous. In this way, further knowledge of this interesting problem may be gained. REFERENCES 1. Benirschke K, Kim CK: Multiple pregnancy. N Engl J Med 288:1276-1284and 1329-1336,1973 2. Moore KL: The Developing Human. Philadelphia, PA, Saunders, 1982, pp 113-139 3. Benirschke K, Driscoll SG: The Pathology of the Human Placenta. New York, NY, Springer-Verlag, 1967, pp 91-179 4. Benirschke K: Twin placenta in perinatal mortality. NY State J Med 61:1499-1508,196l 5. Moore CM, McAdams AJ, Sutherland J: Interuterine disseminated intravascular coagulation: A syndrome of multiple pregnancy with a dead twin fetus. J Pediatr 74:523-528, 1981 6. VanAllen MI: Fetal vascular disruptions: mechanisms and some resulting birth defects. Ped Ann 10:219-233, 1981 7. Yoshioka H, Kadamoto Y, Mino M, et al: Multicystic encephalomalacia in live born twin with a stillborn macerated co-twin. J Pediatr 95:798-800,1979 8. Schinzel AAGL, Smith DW, Miller JR: Monozygotic twinning and structural defects. J Pediatr 95:921-930, 1979 9. Hoyme HE, Higginbottom MC, Jones KL: Vascular etiology of disruptive structural defects in monozygotic twins. Pediatrics 67:288-290,198l 10. Confalonieri C: Gravidanza gemellare monochoriale biamniotica con feto papiraceo ed atresia intestinale congenita nell altro feto. RivOst Ginec Prat 33:199-201, 1951 11. Saier F, Burden L, Cavanagh D: Fetus papyraceous, an unusual case with congenital anomaly of the surviving fetus. Obstet Gynecol45:217-220,1975 12. Mannino FL, Jones KL, Benirschke K: Congenital skin defects and fetus papyraceous. J Pediatr 91:559-564, 1977 13. Louw JH, Barnard CN: Congenital intestinal atresia observations on its origin. Lancet 2:1065-1067, 1955 14. Louw JH: Jejunoileal atresia and stenosis. J Pediatr Surg 1:8-23, 1966