Prenatal diagnosis of intracerebellar hemorrhage: Case report Raymond J. Jennett, MD," William J. R. Daily, MD," Theodore J. Tarby, MD: and Kim H. Manwaring, MDb Phoenix, Arizona Evidence continues to accumulate that neurologic damage can occur during the antenatal period, unrelated to intrapartum events. We report a case in which intracerebellar hemorrhage was diagnosed by antepartum ultrasonographic examination. Correlation of fetal heart rate patterns, Apgar scores with neonatal course, and neuropathologic findings are presented. Medicolegal implications are discussed. (AM J OSSTET GYNECOL 1990;162:1472-5.)
Key words: Intracranial hemorrhage, intracerebellar hemorrhage, medicolegal implications
The availability of increasingly sophisticated imaging techniques has made it possible to diagnose hemorrhage and other intracranial lesions in the live infant before birth. This not only helps to support clinical decisions but allows comparison of fetal heart rate patterns, blood gas values, Apgar scores, and neonatal course with documented incidents of perinatal asphyxia in otherwise normal infants before an asphyxial event.
Case report A 33-year-old woman was referred to the outpatient clinic at 35 weeks' gestation. The referring physician reported that the only unusual event before that time had been a hospital admission for suspected premature labor associated with a mild urinary tract infection. The From the Department of Reproductive Medicine" and Barrow Neurological Institute of St. joseph's Hospital and Medical Center.' Presented at the Fifty-sixth Annual Meeting of the Pacific Coast Obstetrical and Gynecological Society, Coronado, California, September 17-21,1989. Reprints not available. 6/6119931
patient had smoked more than a package of cigarettes a day throughout the pregnancy. No history of drug usage was obtained. Pertinent family history included her father and brother. Her father had incurred a stroke at age 32 followed by 7 years of coma before death. Her brother had a nonfatal myocardial infarction in his early 30s. Two days after her initial clinic visit she reported a decrease in fetal movement. A nonstress test performed later that day was deemed to be equivocal and a contraction stress test was ordered. An oxytocin infusion was begun at a rate of 0.5 mU Imin and gradually increased. Contractions began at a rate of 2.0 mU Imin and were associated with persistent late decelerations from the start (Fig. 1). The oxytocin infusion was stopped and an ultrasonographic examination was performed. Fetal measurements were consistent with the menstrual gestational age of 35 weeks. Amniotic fluid volume was within acceptable limits. Of particular note was a large region of abnormal echogenicity involving the posterior fossa (cerebellum) and thalamus (Fig. 2). Cesarean section was performed with the patient under epidural anesthesia. The amniotic fluid was clear
Fig. 1. Decelerations associated with oxytocin-induced contractions. 1472
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Intracerebellar hemorrhage
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and there was no evidence of cord entanglement. The male infant who weighed 2693 gm and had a head circumference of 34.8 em was described as pink with cyanotic extremities. He was limp and without reflex irritability or respiratory effort. Heart rate was less than 100 beats/min, resulting in a I-minute Apgar score of 2. Cord blood gases were reported as pH 7.33 and pH 7.37 for arterial and venous blood, respectively. He was immediately intubated and given supported ventilation. His condition at 5 minutes was unchanged, resulting in an Apgar score of 2. Gasping respirations began at 65 minutes of age. Neither reflex nor spontaneous activity was present until 75 minutes of age when gradual spasmodic movements of the right arm and leg began, progressing rapidly to tonic-clonic seizure activity. Cranial ultrasonographic scan showed massive hydrocephalus and a large echogenic structure in the right temporal lobe and atrium, spreading medially into the vicinity of the upper brain stem. Xenonenhanced computed tomography showed evidence of hemorrhage in the left cerebellar hemisphere and thalamus. There was also hemorrhage in both ventricles. A pulsed lumbar cysternostomy and right frontal external ventricular drain placement were done during the first day of life. Despite supportive treatment, the infant alternated between episodes of ventricular tachycardia and profound bradycardia. He had progressive acidosis, hyperchloremia and anuria, and died at age 46 hours. Pertinent autopsy findings were paraventricular leukomalacia with intraventricular, intracerebellar, and subarachnoid hemorrhage. No arteriovenous malformation was noted. Comment
Although the cause of the massive cerebellar hemorrhage must remain speculative, certain observations are pertinent. Hemorrhage occurred in a fetus with adequate placental support as evidenced by a birth weight that was concordant with his gestational age and cord blood gases within a normal range. The latter observation is also supported by his pink color at birth, which is inconsistent with hypoxia just before the birth. This underscores the ambiguities of the Apgar score, which is comprised of diverse elements. A low Apgar score is widely considered synonymous with perinatal asphyxia, a concept that is formalized by the ICD-9 coding scheme.' "Fetal distress" is a term with equally universal usage and similarly arbitrary definition. Certainly a fetus who has had a massive cerebellar hemorrhage is in "distress" in the most meaningful sense of the term. However, to rigidly equate fetal heart decelerations that occur in conjunction with contractions with placental insufficiency and fetal hypoxia is questionable because it ignores the possibility that an intracranial pathologic condition may result in increased sensitivity to repeated head compression manifested by similar decelerations.
Fig. 2. Antenatal ultrasonographic scan of fetal head shows large thalamic and posterior fossa echogenic mass.
The value of obtaining cord blood gas determinations in such instances is suggested, as well as the use of cranial ultrasonographic scan or other imaging techniques in selected cases. Finally, given the tremendous medicolegal problems arising from antenatal and perinatal brain damage, consideration should be given to the continued reporting of cases in which such damage is diagnosed prenatally. This is particularly the case for lesions commonly interpreted as occurring during birth and being traumatic in origin, as is cerebellar hemorrhage. 2 We recognize our deceased colleague, Charles M. Hohler, MD, who performed the prenatal examinations. REFERENCES 1. The International Classification of Diseases. 9th rev. Bethesda, Maryland: Department of Health and Human Services, United States Public Health Service, Health Care Financing Administration, 1980 vol 1:691. DHHS publication no. (PHS) 80-1260.
1474 Jennett et al.
2. Volpe JJ. Intracranial hemorrhage, subdural, primary subarachnoid, intracerebellar, miscellaneous. In: Volpe JJ, ed. Neurology of the newborn. Philadelphia: WB Saunders, 1981.
Editors' note: This manuscript was revised after these discussions were presented.
Discussion
T. PARER, San Francisco, California. The authors have presented a well-documented case of fetal intracranial hemorrhage that occurred at about 35 weeks' gestation, before the onset of labor, in an infant born subsequently by cesarean section. I would like to discuss this article from two points of view: first, the individual case, and second, the broader implications, such as incidence. The cause of this intracerebellar hemorrhage is not clearly evident. Possibilities include trauma, asphyxia, infection, and congenital defects, such as vascular anomaly or blood dyscrasia. There is not evidence for trauma but this may not rule it out. An intriguing report from New Zealand has suggested that trauma may not have to be particularly severe because there is a substantial increase in intracranial hemorrhages in Pacific Islanders among whom abdominal massage late in pregnancy is an established custom.' The site of the lesion does not support asphyxia as a cause. Conversely, there is evidence from the mother's assessment of decreased fetal movement for several days before intervention. This could conceivably have indicated an episode of severe asphyxia, which resulted in the hemorrhage, and then resolved sufficiently to result in normal umbilical cord pH at birth. The role of the late decelerations is puzzling. Although the presence of late decelerations at the time of a contraction stress test does not preclude the subsequent birth of an infant with normal blood gas levels, it does suggest that resting uterine blood flow (without uterine contractions) is just adequate to ensure fetal oxygenation. We are not given information regarding the ruling out of infection in this case, but perhaps Dr. Jennett can tell us if such data are available. The exact role of infection in such intracranial bleeding as presented here is not well established. However, in a series of 25 autopsy reports from near term stillbirths, all with intracranial hemorrhage or gliosis, Sims et al. 2 found evidence of infection in 36% of cases. Congenital conditions explaining this case are lacking. A tantalizing aspect of the patient'S family history is in her father's and sibling's early death and morbidity, respectively, in their 30s of cardiovascular causes. Another aspect of the case is the role of cigarette smoking. In summary, the cause of the intracerebellar hemorrhage in this case is unexplained. Some of the broader implications of this case have been outlined. The incidence of this condition can be approximated from the series reported by Sims et al. 2 They found prelabor intracranial hemorrhage and DR. JULIAN
Am
June 1990
J Obstet GynecoJ
gliosis in about 6% of stillbirths. Stillbirth occurs in less than I % of pregnancies, thus such a condition may occur in approximately 5 per 10,000 pregnancies. In contrast to this, legal suit is filed in such cases in close to 100% of cases, so it is critical that such cases be appropriately diagnosed, as was done in this case with fetal ultrasonography, to ensure than the health care providers are not inappropriately blamed for miscliagnosing intrapartum fetal asphyxia. We do not always have the luxury of such data, but we do have the possibility of ruling out intrapartum asphyxia in almost all cases. Intrapartum asphyxia can be ruled out if (1) the umbilical arterial acid-base state and blood gases are normal, (2) the Apgar score is normal (above 7 at 5 minutes), (3) there is normal fetal heart rate variability within several minutes of delivery, and (4) seizures do not occur in the first day or two of life. The authors ruled out intrapartum asphyxia with cord blood acid-base state studies.
REFERENCES 1. Becroft DM, Gunn TR. Prenatal intracranial hemorrhages in 47 Pacific Islander infants: is traditional massage the cause? Aust N Z MedJ 1989;102:207-10. 2. Sims ME, Turkel SB, Halterman G, Paul RH. Brain injury and intrauterine death. AM J OBSTET GYNECOL 1985; 151:721-3. DR. PETER WATSON, Portland, Oregon. I concur with Dr. Parer's remarks about the importance of obtaining cord blood gas levels whenever there is an abnormal fetal heart rate tracing and the possibility of an abnormal outcome. Obtaining cord blood gas levels helps much more than it hinders us in those medicolegal circumstances when it is very difficult to determine cause and effect. I would like to suggest maternal cocaine abuse as a possible cause for the neonatal outcome in this case. The incidence of maternal cocaine abuse is rising and its association with intracerebral bleeding is well documented.' I wonder if a drug screen was obtained in this case. A drug screen is obtained in our institution in the event of any unexplained fetal or neonatal bleeding. A maternal urine sample positive for cocaine in this particular situation would not only explain the circumstances but would also do much to avoid litigation.
REFERENCE I. Mercado A, Johnson (; Jr, Calver D, Sokol RJ. Cocaine, pregnancy, and postpartum intracerebral hemorrhage. Obstet Gynecol 1989;7:\:467-8. DR. RUSSELL LAROS, San Francisco, Calif()[)lia. Along the same line, Dr. Jennett, I assume laboratory studies were done on the infant to study the whole variety of coagulation abnormalities that could explain the bleeding. You did not mention platelet count, congenital hypofibrinogenemia, or congenital hypoprothrombinemia. Were all dotting factors evaluated and
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was the mother questioned about the use of anti platelet agents, such as aspirin or diuretics? DR. JENNETT (Closing). We have agonized over this case and greatly appreciate the suggestions that have been made concerning possible causes. Dr. Parer, I can measure the interval with a calipers and say that there is no question that these are late decelerations. They do not fit any other category. There was not a great length of time between discontinuation of oxytocin, reduction of contractions, and the cesarean section. I keep trying to think of an imaginative explanation that would prove the experts wrong and demonstrate late decelerations caused by head compression. This woman smoked heavily and her cigarette smoking was a source of a great deal of concern to us. Unfortunately, I cannot quote statistics on the incidence of intracerebellar hemorrhage. Dr. Watson asked about blood gas levels. I suppose
with our worry and consternation, the blood gas laboratory ran only the cord pHs. However, the umbilical cord was immediately catheterized and the blood samples obtained showed no deviation from accepted levels of carbon dioxide and oxygen. The infant was definitely not metabolically acidotic. Your question of maternal drug use, especially of cocaine, is certainly an intriguing and pertinent one. In this case, no drug screen was obtained. Our hospital has wrestled with the question of performing drug screenings without permission and it has unfortunately decided that such screenings will not be allowed. We have good reason to believe that in our affluent area, cocaine usage is greater than in many areas, such as Los Angeles, that get a "bad press." Dr. Laros, no history of the use of antiplatelet medications was sought and no coagulation studies were done.
Key words: Intracranial hemorrhage, intracerebellar hemorrhage, medicolegal implications
The availability of increasingly sophisticated imaging techniques has made it possible to diagnose hemorrhage and other intracranial lesions in the live infant before birth. This not only helps to support clinical decisions but allows comparison of fetal heart rate patterns, blood gas values, Apgar scores, and neonatal course with documented incidents of perinatal asphyxia in otherwise normal infants before an asphyxial event.
Case report A 33-year-old woman was referred to the outpatient clinic at 35 weeks' gestation. The referring physician reported that the only unusual event before that time had been a hospital admission for suspected premature labor associated with a mild urinary tract infection. The From the Department of Reproductive Medicine" and Barrow Neurological Institute of St. joseph's Hospital and Medical Center.' Presented at the Fifty-sixth Annual Meeting of the Pacific Coast Obstetrical and Gynecological Society, Coronado, California, September 17-21,1989. Reprints not available. 6/6119931
patient had smoked more than a package of cigarettes a day throughout the pregnancy. No history of drug usage was obtained. Pertinent family history included her father and brother. Her father had incurred a stroke at age 32 followed by 7 years of coma before death. Her brother had a nonfatal myocardial infarction in his early 30s. Two days after her initial clinic visit she reported a decrease in fetal movement. A nonstress test performed later that day was deemed to be equivocal and a contraction stress test was ordered. An oxytocin infusion was begun at a rate of 0.5 mU Imin and gradually increased. Contractions began at a rate of 2.0 mU Imin and were associated with persistent late decelerations from the start (Fig. 1). The oxytocin infusion was stopped and an ultrasonographic examination was performed. Fetal measurements were consistent with the menstrual gestational age of 35 weeks. Amniotic fluid volume was within acceptable limits. Of particular note was a large region of abnormal echogenicity involving the posterior fossa (cerebellum) and thalamus (Fig. 2). Cesarean section was performed with the patient under epidural anesthesia. The amniotic fluid was clear
Fig. 1. Decelerations associated with oxytocin-induced contractions. 1472
Volume 162 Number 6
Intracerebellar hemorrhage
1473
and there was no evidence of cord entanglement. The male infant who weighed 2693 gm and had a head circumference of 34.8 em was described as pink with cyanotic extremities. He was limp and without reflex irritability or respiratory effort. Heart rate was less than 100 beats/min, resulting in a I-minute Apgar score of 2. Cord blood gases were reported as pH 7.33 and pH 7.37 for arterial and venous blood, respectively. He was immediately intubated and given supported ventilation. His condition at 5 minutes was unchanged, resulting in an Apgar score of 2. Gasping respirations began at 65 minutes of age. Neither reflex nor spontaneous activity was present until 75 minutes of age when gradual spasmodic movements of the right arm and leg began, progressing rapidly to tonic-clonic seizure activity. Cranial ultrasonographic scan showed massive hydrocephalus and a large echogenic structure in the right temporal lobe and atrium, spreading medially into the vicinity of the upper brain stem. Xenonenhanced computed tomography showed evidence of hemorrhage in the left cerebellar hemisphere and thalamus. There was also hemorrhage in both ventricles. A pulsed lumbar cysternostomy and right frontal external ventricular drain placement were done during the first day of life. Despite supportive treatment, the infant alternated between episodes of ventricular tachycardia and profound bradycardia. He had progressive acidosis, hyperchloremia and anuria, and died at age 46 hours. Pertinent autopsy findings were paraventricular leukomalacia with intraventricular, intracerebellar, and subarachnoid hemorrhage. No arteriovenous malformation was noted. Comment
Although the cause of the massive cerebellar hemorrhage must remain speculative, certain observations are pertinent. Hemorrhage occurred in a fetus with adequate placental support as evidenced by a birth weight that was concordant with his gestational age and cord blood gases within a normal range. The latter observation is also supported by his pink color at birth, which is inconsistent with hypoxia just before the birth. This underscores the ambiguities of the Apgar score, which is comprised of diverse elements. A low Apgar score is widely considered synonymous with perinatal asphyxia, a concept that is formalized by the ICD-9 coding scheme.' "Fetal distress" is a term with equally universal usage and similarly arbitrary definition. Certainly a fetus who has had a massive cerebellar hemorrhage is in "distress" in the most meaningful sense of the term. However, to rigidly equate fetal heart decelerations that occur in conjunction with contractions with placental insufficiency and fetal hypoxia is questionable because it ignores the possibility that an intracranial pathologic condition may result in increased sensitivity to repeated head compression manifested by similar decelerations.
Fig. 2. Antenatal ultrasonographic scan of fetal head shows large thalamic and posterior fossa echogenic mass.
The value of obtaining cord blood gas determinations in such instances is suggested, as well as the use of cranial ultrasonographic scan or other imaging techniques in selected cases. Finally, given the tremendous medicolegal problems arising from antenatal and perinatal brain damage, consideration should be given to the continued reporting of cases in which such damage is diagnosed prenatally. This is particularly the case for lesions commonly interpreted as occurring during birth and being traumatic in origin, as is cerebellar hemorrhage. 2 We recognize our deceased colleague, Charles M. Hohler, MD, who performed the prenatal examinations. REFERENCES 1. The International Classification of Diseases. 9th rev. Bethesda, Maryland: Department of Health and Human Services, United States Public Health Service, Health Care Financing Administration, 1980 vol 1:691. DHHS publication no. (PHS) 80-1260.
1474 Jennett et al.
2. Volpe JJ. Intracranial hemorrhage, subdural, primary subarachnoid, intracerebellar, miscellaneous. In: Volpe JJ, ed. Neurology of the newborn. Philadelphia: WB Saunders, 1981.
Editors' note: This manuscript was revised after these discussions were presented.
Discussion
T. PARER, San Francisco, California. The authors have presented a well-documented case of fetal intracranial hemorrhage that occurred at about 35 weeks' gestation, before the onset of labor, in an infant born subsequently by cesarean section. I would like to discuss this article from two points of view: first, the individual case, and second, the broader implications, such as incidence. The cause of this intracerebellar hemorrhage is not clearly evident. Possibilities include trauma, asphyxia, infection, and congenital defects, such as vascular anomaly or blood dyscrasia. There is not evidence for trauma but this may not rule it out. An intriguing report from New Zealand has suggested that trauma may not have to be particularly severe because there is a substantial increase in intracranial hemorrhages in Pacific Islanders among whom abdominal massage late in pregnancy is an established custom.' The site of the lesion does not support asphyxia as a cause. Conversely, there is evidence from the mother's assessment of decreased fetal movement for several days before intervention. This could conceivably have indicated an episode of severe asphyxia, which resulted in the hemorrhage, and then resolved sufficiently to result in normal umbilical cord pH at birth. The role of the late decelerations is puzzling. Although the presence of late decelerations at the time of a contraction stress test does not preclude the subsequent birth of an infant with normal blood gas levels, it does suggest that resting uterine blood flow (without uterine contractions) is just adequate to ensure fetal oxygenation. We are not given information regarding the ruling out of infection in this case, but perhaps Dr. Jennett can tell us if such data are available. The exact role of infection in such intracranial bleeding as presented here is not well established. However, in a series of 25 autopsy reports from near term stillbirths, all with intracranial hemorrhage or gliosis, Sims et al. 2 found evidence of infection in 36% of cases. Congenital conditions explaining this case are lacking. A tantalizing aspect of the patient'S family history is in her father's and sibling's early death and morbidity, respectively, in their 30s of cardiovascular causes. Another aspect of the case is the role of cigarette smoking. In summary, the cause of the intracerebellar hemorrhage in this case is unexplained. Some of the broader implications of this case have been outlined. The incidence of this condition can be approximated from the series reported by Sims et al. 2 They found prelabor intracranial hemorrhage and DR. JULIAN
Am
June 1990
J Obstet GynecoJ
gliosis in about 6% of stillbirths. Stillbirth occurs in less than I % of pregnancies, thus such a condition may occur in approximately 5 per 10,000 pregnancies. In contrast to this, legal suit is filed in such cases in close to 100% of cases, so it is critical that such cases be appropriately diagnosed, as was done in this case with fetal ultrasonography, to ensure than the health care providers are not inappropriately blamed for miscliagnosing intrapartum fetal asphyxia. We do not always have the luxury of such data, but we do have the possibility of ruling out intrapartum asphyxia in almost all cases. Intrapartum asphyxia can be ruled out if (1) the umbilical arterial acid-base state and blood gases are normal, (2) the Apgar score is normal (above 7 at 5 minutes), (3) there is normal fetal heart rate variability within several minutes of delivery, and (4) seizures do not occur in the first day or two of life. The authors ruled out intrapartum asphyxia with cord blood acid-base state studies.
REFERENCES 1. Becroft DM, Gunn TR. Prenatal intracranial hemorrhages in 47 Pacific Islander infants: is traditional massage the cause? Aust N Z MedJ 1989;102:207-10. 2. Sims ME, Turkel SB, Halterman G, Paul RH. Brain injury and intrauterine death. AM J OBSTET GYNECOL 1985; 151:721-3. DR. PETER WATSON, Portland, Oregon. I concur with Dr. Parer's remarks about the importance of obtaining cord blood gas levels whenever there is an abnormal fetal heart rate tracing and the possibility of an abnormal outcome. Obtaining cord blood gas levels helps much more than it hinders us in those medicolegal circumstances when it is very difficult to determine cause and effect. I would like to suggest maternal cocaine abuse as a possible cause for the neonatal outcome in this case. The incidence of maternal cocaine abuse is rising and its association with intracerebral bleeding is well documented.' I wonder if a drug screen was obtained in this case. A drug screen is obtained in our institution in the event of any unexplained fetal or neonatal bleeding. A maternal urine sample positive for cocaine in this particular situation would not only explain the circumstances but would also do much to avoid litigation.
REFERENCE I. Mercado A, Johnson (; Jr, Calver D, Sokol RJ. Cocaine, pregnancy, and postpartum intracerebral hemorrhage. Obstet Gynecol 1989;7:\:467-8. DR. RUSSELL LAROS, San Francisco, Calif()[)lia. Along the same line, Dr. Jennett, I assume laboratory studies were done on the infant to study the whole variety of coagulation abnormalities that could explain the bleeding. You did not mention platelet count, congenital hypofibrinogenemia, or congenital hypoprothrombinemia. Were all dotting factors evaluated and
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Intracerebeliar hemorrhage
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Number ti
was the mother questioned about the use of anti platelet agents, such as aspirin or diuretics? DR. JENNETT (Closing). We have agonized over this case and greatly appreciate the suggestions that have been made concerning possible causes. Dr. Parer, I can measure the interval with a calipers and say that there is no question that these are late decelerations. They do not fit any other category. There was not a great length of time between discontinuation of oxytocin, reduction of contractions, and the cesarean section. I keep trying to think of an imaginative explanation that would prove the experts wrong and demonstrate late decelerations caused by head compression. This woman smoked heavily and her cigarette smoking was a source of a great deal of concern to us. Unfortunately, I cannot quote statistics on the incidence of intracerebellar hemorrhage. Dr. Watson asked about blood gas levels. I suppose
with our worry and consternation, the blood gas laboratory ran only the cord pHs. However, the umbilical cord was immediately catheterized and the blood samples obtained showed no deviation from accepted levels of carbon dioxide and oxygen. The infant was definitely not metabolically acidotic. Your question of maternal drug use, especially of cocaine, is certainly an intriguing and pertinent one. In this case, no drug screen was obtained. Our hospital has wrestled with the question of performing drug screenings without permission and it has unfortunately decided that such screenings will not be allowed. We have good reason to believe that in our affluent area, cocaine usage is greater than in many areas, such as Los Angeles, that get a "bad press." Dr. Laros, no history of the use of antiplatelet medications was sought and no coagulation studies were done.
