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Fetal heart rate observations in the brain-damaged infant
Fetal Heart Rate Observations in the Brain-Damaged Infant Jeffrey P. Phelan and Joo Oh Kim
The objective of this study was to describe the fetal heart rate patterns and underlying pathophysiologic changes in the brain-damaged fetus. Fetuses with brain damage from hypoxic ischemic encephalopathy do not manifest uniform fetal heart rate patterns. However, these fetuses do show distinct fetal heart rate patterns that permit categorization based on their admission heart rate, subsequent changes in their baseline rate; and neonatal findings. Based on the observations of infants brain damaged in utero because of hypoxic ischemic encephalopathy, the intrapartum fetal management will depend on the admission fetal heart rate pattern, and the subsequent changes in the baseline rate.
Copyright 9 2000 by W.B. Saunders Company lectronic Fetal Monitoring (EFM) has bein the assessm e n t of a n t e p a r t u m and i n t r a p a r t u m fetal wellbeing. 1 Since its inception, the goal of EFM has b e e n to continuously assess fetal health during labor and to theoretically p e r m i t the early detection of i n t r a p a r t u m fetal dis~tress in sufficient time to prevent fetal brain injury. AS such, the presence of contraction-mediated fetal h e a r t rate (FHR) decelerations such as repetitive late decelerations has served as the basis for intervention. If traditional maneuvers such as maternal position change, oxygen administration, intravenous fluid administration, a n d / o r discontinuation of oxytocin failed to ameliorate this F H R pattern within a reasonable period of time, expedited delivery was indicated. With the increasing use of continuous EF M, i n t r a p a r t u m fetal death rates but not cerebral palsy (CP) rates, have declined t h r o u g h o u t the United States. 2 This trend is in keeping with the prescient observations of Perkins 3 m o r e than a decade ago. T h e n , he Opined that "the n u m b e r of infants injured during labor is highly overestim a t e d and the n u m b e r injured prior to labor is highly underestimated. ''3 At that time, the prevailing thought was that changes in the F H R p r e c e d e d neurological i m p a i r m e n t of the fetus. However, as we have learned not all fetuses undergo brain injury in such a m a n n e r . 4-11 AS suggested by these investigators, 4-11 the F H R pattern appears to be a manifestation of underlying fetal neurological i m p a i r m e n t and may be m o r e useful in identifying those fetuses who have already
E c o m e an invaluable adjunct
sustained central nervous system (CNS) injury before labor. In m a n y ways, the low incidence of asphyxial induced CP, has in part, b e e n responsible for o u r limited u n d e r s t a n d i n g of Perkins' insights) In essence, asphyxial induced CP's relatively rarity requires a registry f o r m a t to study its pathophysiology. For example, the overall incidence of CP is a r o u n d 1% of all live births.12 T h e known causes for CP are n u m e r o u s and include but are not limited to c h r o m o s o m a l and structural abnormalities, infection, prematurity, and asph}-xia. Overall, asphyxial induced CP is one of the rarest forms o f CP with a r e p o r t e d incidence of 1 in 10,000 births. 13 Given the rarity of asphyxial induced CP, the only reliable way to investigate it's pathophysiology a n d prevention is through a National Registry f o r m a t similar to those patient registries established by Clark to study amniotic fluid embolus, TM Herbst to describe the link between diethylstilbesterol' and a d e n o c a r c i n o m a of the vagina, a5 and Busby to study a n o p h t h a l m i a / m i c r o p h t h a l m i a . 16 Following the lead of these world renown investigators, we at the Childbirth Injury Prevention FoundaFrom the Department of Obstetrics and Gynecology, Pomona Valley Hospital Medical Center, and Childbirth Injury Prevention Foundation, Pasadena, CA. Supported by the Childbirth Injury Prevention Foundation, Pasadena, CA. Address reprint requests to Jeffrey P. Phdan, MD, Suite 200, 959 East Walnut Street, Pasadena, CA 91106. Copyright 9 2000 by W.B. Saunders Company O146-0005/00/2403-000651 O.00/0 doi: 10.1053/spet:2000. 7079
Seminars in Perinatology, Vol 24, No 3 (June), 2000: pp 221-229
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tion 17 established a National Registry in 1991 to research the pathophysiology of asphyxial induced CP for the purpose of identifying clinical approaches that could, where possible, ultimately lead to its prevention. Therefore, the purpose of this article is 4-fold. First, we will review the FHR patterns associated with CNS injury in the term fetus. Second, we will review the neonatal observations associated with the FHR patterns in instances of fetal brain damage. Third, these FHR patterns will help to serve as a basis for providing intrapartum mana g e m e n t recommendations. Fourth, we must emphasize that these FHR patterns apply to term and postdate pregnancies and may not necessarily apply to preterm or twin pregnancies. Finally, the recommendations, contained herein, d o not imply n o r infer a standard of care for the management of intrapartum obstetrical patients. Rather, this article represents another piece of the cerebral palsy puzzle.
F H R Patterns in the Brain Damaged Infant
probability of intrapartum fetal distressf v,3~ Thus, a reactive FHR pattern obtained on admission to the hospital or anytime during labor serves as a reliable sign of fetal well-being. In contrast, a nonreactive fetal admission test is associated with a greater probability of an adverse fetal outcome. 29,3~For instance, there is an inverse relationship between the n u m b e r of FHR accelerations and oligohydramnios, s,~l FHR decelerations, 31 meconium-stained amniotic fluid, 2~ intrapar(um fetal distress, 1s,29~31 and long-term n e u r o l o g i c a l impairment. ~,4,7-a~ If, for example, fetal nonreactivity is present for more than 120 minutes from the time of admission to the hospital, higher rates of operative intervention, perinatal mortality, and long-term neurological impairment are observed. 1,4,7-11 In sum, the fetal admission test results enable the clinician and the labor and delivery nurse to categorize laboring patients for intrapartum m a n a g e m e n t and to reassign their risk status. At the same time, the FHR patterns associated with fetal brain damage can be used as guiding lights for intrapartum care and the potential prevention of fetal brain damage.
The First Step To understand fetal brain damage requires an assessment of fetal status with EFM on admission to the hospital. This has been referred to as the fetal or labor admission test. Is With the use of the fetal admission test, outpatient and inpatient fetal m o n i t o r i n g principles are applied to the laboring patient. Here, the principal goals of the labor admission test are to identify those fetuses at risk for intrapartum fetal distress and to reassign those patients alleged to be at high or low risk before labor to a different risk category soon after admission to labor and delivery. Thus, the initial admission test or fetal monitoring, period can be used to redefine the patient's risk status and to assist the clinician and nurse specialist with the intrapartum m a n a g e m e n t of a patient's labor. If, for example, the patient's FHR pattern on admission to the hospital is considered reactive, labor and delivery personnel know that the fetus is probably but not absolutely n o r m a l / 9 At the same time, a reactive fetal admission test is a sign of a healthy fetus and symbolizes fetal well-bei n g / 8,2~ normal fetal acid-base status, 2~27 normoxia, 2s an absence of asphyxia, 2~27 and a low
FHR Patterns in the Brain Damaged Infant Term infants f o u n d to be brain d a m a g e d do not manifest a uniform FHR pattern. 1,4,n However, these fetuses do manifest distinct FHR patterns intrapartum that can be easily categorized and identified based on the fetal admissions test and subsequent changes in the baseline rate. Figure 1 shows the three most c o m m o n FHR patterns
PERSISTENT NR-45 %
PATTERN-22% ~
~THER-13%
REACTIVE-PD-20 % Figure 1. The incidence of the 3 most common FHR patterns associated with fetal brain damage. (PD, prolonged FHR deceleration).
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FHR Patterns in the Brain-Damaged Infant
associated with fetal brain damage. The FHR patterns not included in Figure 1 that will n o t be discussed in this chapter are as follows: (1) the persistent reactive FHR pattern, 19 (2) FHR bradycardia on admission to the hospital, and (3) those that did not fit into any single category. AS n o t e d in Table 1, continuous EFM is useful in separating fetuses into distinct groups based on their admission and subsequent FHR patterns.
Reactive Admission Test and Subsequent Fetal Brain Damage Acute Asphyxia W h e n a pregnant woman is admitted to the hospital, the overwhelming n u m b e r of obstetrical patients will have a reactive FHR pattern. O f these, more than 98% will go t h r o u g h labor uneventfully and most will deliver vaginally. In the few patients (typically 1% to 2%) that develop intrapartum "fetal distress, ''29,3~ the characteristic "fetal distress" is usually, but not always, acute and manifested by a sudden p r o l o n g e d FHR deceleration that lasts until delivery. O f these, an even smaller n u m b e r of fetuses will ultimately experience CNS injury. As illustrated in Figure 1, fetal brain injury in the fetus with a reactive fetal admission test may arise, in the absence of trauma, as a result of a sudden prolonged FHR deceleration or a H o n pattern of intrapartum asphyxia. In the f o r m e r group, the FHR pattern is reactive; and, as a result of a sudden catastrophic event (Table 2),
a Sudden p r o l o n g e d FHR deceleration to approximately 60 beats per minute (bpm) occurs and lasts until the time of delivery. In this g r o u p (Table 1), the CNS injury is primarily located in the basal ganglia and thalami 32,~3 and is attributable to sudden and p r o l o n g e d reductions in fetal cardiac output. ~2,-~As shown in Table 2, the p r o l o n g e d FHR decelerations is associated with a wide array of patient groups such as uterine rupture, placental abruption, and cord prolapse. Given the acute nature of this FHR pattern, limited time is available to preserve normal CNS function. Based on our experience, the timing of neurological injury in this group depends on 5 factors (Table 3), First, the admission FHR pattern provides an indicator of fetal status before the catastrophic event. If, for example, the FHR pattern is reactive on admission and a sudden prolonged FHR deceleration occurs, the neurological insult is most likely acute. In contrast, a p r o l o n g e d FHR decelerations that follows a persistent nonreactive FHR pattern is most likely consistent with a postasphyxial insult-preterminal pattern/4,~5 Second, the fetal growth pattern at the time of presentation to the hospital also plays a role in the timing of fetal neurological injury. Fetal growth, to a large extent, is d e p e n d e n t on the functional placental surface area. 36 As such, infants who are small-, appropriate-, or large-forgestational-age usually have different functional placental surface areas available to them. To a
TaMe 1. FHR Patterns in the Normal and Brain-Damaged Infant and the Associated Perinatal Observations
Fetal movement on admission Admission FHR Meconium FHR baseline NRBC (#/100 WBC) NRBC clearance time (hrs) Platelet count Seizure onset time from birth (hrs) Organ dysfunction Cerebral edema Brain injury location cortical Basal ganglia thalami
Normal
NR
Normal Reactive 12% Fixed 2-3% <24 281 NA NA NA None None
Decreased absent NR 88% Fixed 52% 119 185 6 + 13 92% 66% Primary Uncommon
HON
Normal Reactive 50% ~ 35% 13% 66 251 10 -+ 14 64% 41% Primary Secondary if PD
RPD
Normal Reactive 23% ~ TO 60 BPM 12% 52 267 15 + 26 50% 51% Uncommon Primary
occurs
Abbreviations: NR, nonreactive; RPD, admission followed by a prolonged deceleration that lasts until delivery; NRBC, nucleated red blood cells. Data from r e f e r e n c e s 1,4,II,32,33,37,43~17,4%53,62,
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Table 2. Catastrophic Events That are Associated With a Reactive Fetal Admission Test and a Subsequent Prolonged FHR Deceleration to 60 bpm and Lasting Until Delivmy Umbilical cord prolapse Uterine rupture Placental abruption Maternal arrest Fetal exsanguination
large extent, the time interval to injury in an acute asphyxial event will d e p e n d o n the functional placental surface area to m a i n t a i n placental e x c h a n g e . For example, in infants with i n t r a u t e r i n e g r o w t h i m p a i r m e n t o r who are small-for-gestational-age, the time to CNS injury will be less t h a n that for an a p p r o p r i a t e - o r a large-for-gestational-age infant. In essence, fetal grbwth is a reflection o f either (1) the f u n c t i o n a l placental surface area available to each fetus or (2) the ability to withstand a catastrophic event for a l o n g e r p e r i o d o f time. T h e d e g r e e o f fetal vasoconstriction o r the level o f intrafetal s h u n t i n g at the time o f the catastrophic event is also a potential c o n t r i b u t o r to the timing a n d / o r the extent o f the fetal brain i n j u r y ) 7 Traditional obstetrical teachings r e g a r d i n g the p a t h o g e n e s i s o f fetal brain injury have described the centralization o f the fetal circulation d u r i n g i n t r a p a r t u m asphyxia to preserve fetal brain f u n c t i o n at the potential exp e n s e o f o t h e r o r g a n s such as the lungs o r kidneys (Figure 2). Intrafetal s h u n t i n g is b r o u g h t a b o u t by fetal vasoconstriction (Figure 3). T h e triggering m e c h a n i s m for the fetal vasoconstriction is u n k n o w n as o f this writing b u t m a y be i n d u c e d by the p r e s e n c e o f m e c o n i u m 38,39 or infection. 4~ T h e f i n d i n g o f o l i g o h y d r a m n i o s a n d / o r i n t r a u t e r i n e growth i m p a i r m e n t is illus-
Figure 2. The traditional view is that fetal blood flow is preferentially shunted away from organs such as the fetal kidneys in an effort to preserve fetal brain function. trative o f varying degrees o f fetal vasoconstriction o r shunting. If o n e assumes that intrafetal s h u n t i n g o r vasoconstriction has b e e n o n g o i n g f o r a p e r i o d o f time, the treating clinician o r nurse, in m o s t instances, will n o t k n o w the severity o f the vasoconstriction. Thus, h o w the table is set, with respect to the d e g r e e o f vasoconstriction, at the m o m e n t o f m a t e r n a l admission to l a b o r a n d delivery will d e t e r m i n e w h e t h e r fetal brain damage occurs, if at all, a n d its timing. T u r n i n g to Figure 3, assume that the vasoconstriction in fetuses I a n d II are at points A a n d C, respectively. O n admission to the hospital, b o t h fetuses have a reactive F H R pattern. D u r i n g the labor, a u t e r i n e r u p t u r e occurs resulting in a s u d d e n p r o l o n g e d F H R d e c e l e r a t i o n in b o t h p r e g n a n cies. D e p e n d i n g o n the d u r a t i o n o f the F H R d e c e l e r a t i o n a n d the o t h e r factors illustrated in Table 3, fetus II with vasoconstriction at p o i n t C is m o r e likely to sustain an injury t h a n is fetus I with vasoconstriction at p o i n t A. Moreover, the type o r location o f the brain injury will also p r o b a b l y be different (Table 1). T h e r e m a i n i n g 2 factors in Table 3, the duration o f the p r o l o n g e d F H R d e c e l e r a t i o n a n d the intactness o f the placenta, are also i m p o r t a n t factors. For example, in cases o f a c o m p l e t e placental separation, the o n s e t o f the p r o l o n g e d F H R d e c e l e r a t i o n to fetal injury interval will be s h o r t e r than if the p l a c e n t a were intact. Based o n the L e u n g study 42 in cases o f u t e r i n e r u p t u r e , the interval to CNS injury was less t h a n 18 min-
Table 3. Five Factors Useful in Determining the Timing of Fetal Brain Injury* Prior FHR pattern Fetal growth pattern Degree of fetal vasoconstriction Duration of the FHR deceleration Intactness of tile placenta * In the situation of a reactive admission test followed by a catastrophic event resulting in a sudden prolonged FHR deceleration to 60 bpm and lasting until delivery. Abbreviation: FHR, fetal heart rate.
~
NORMAL
A
B
~---'l~
C
ISCHEMIA
D
Figm'e 3. Persistent fetal vasoconstriction over time or intrafetal shunting leads to progressive narrowing of the fetal vascular tree leading nhimately to ischemia.
FHR Patterns in the Brain-Damaged Infant
utes. O u r experience 11 would suggest an even shorter time to neurological injury of 16 minutes whenever the placenta has completely separated. If the placenta remains intact, a longer period of time appears to be available before the onset of CNS injury.
Hon Pattern of Asphyxia The H o n pattern of intrapartum asphyxia (Figure 4) is uniquely different and evolves over a period o f time. 1,4,11 This FHR pattern begins with a reactive fetal admission test. Subsequently during labor, the fetus develops a nonreactive FHR pattern or loses its ability to accelerate its heart rate. 1,4a~ As the labor continues, a substantial rise in baseline heart rate from admission (135 _+ 10 bpm) to a mean m a x i m u m (186 + 15 bpm) baseline heart rate is seen. n The maxim u m FHR ranged from 155 b p m to 220 bpm. This constituted a 39 -+ 13% m e a n percent rise in baseline heart rate from admission and ranged from 17% to 82%. 11 This rise in baseline FHR is usually not a c c o m p a n i e d by maternal pyrexia. When a substantial rise in baseline fetal heart rate is encountered, the FHR pattern is also associated with repetitive FHR decelerations but not necessarily late decelerations and ultimately a loss of FHR variability (Figure 4).4,11 ,,As labor progresses and the fetus nears death, the slopes becomes progressively less steep until the
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FHR does not return to its baseline rate and ultimately terminates in a p r o f o u n d bradycardia "a5 or a stairsteps-to-death pattern. 1,4,11,34 Once a FHR tachycardia begins, the subsequent FHR pattern n does 1 of the following: (1) the FHR pattern remains tachycardic a n d / o r continues to rise until delivery (55%)37; (2) a prolonged FHR deceleration that lasts until delivery occurrs (27%)18; or (3) a stairsteps-to-death pattern or a progressive bradycardia are seen (18%). 12 O f particular clinical relevance is that all patients manifested a substantial rise in their baseline heart rates, lost their ability to accelerate their FHR, became nonreactive, and exhibited repetitive FHR decelerations. Of note, the repetitive FHR decelerations were not necessarily late decelerations and were frequently variable decelerations. 11 In this group, fetal heart rate variability does not appear to be a reliable indicator of fetal status. 1~ For example, many brain-damaged fetuses, upwards of 30% exhibited average FHR variability at the time of their deliveries. 11 In the neonatal period, fetuses with the H o n pattern of intrapartum asphyxia and average FHR variability had significantly less cerebral edema. 43 Kim's cerebral e d e m a findings suggest that the use o f diminished FHR variability is probably an imp r o p e r end-point to decide the timing of operative intervention. 43 This means that before a loss of FHR variability, the fetal brain has been
HON PATTERNINTRAPARTUMASPHYXIA [ FETALHYPOXIA
)
,)
160 FHR Figure 4. The characteristics of the Hon pattern of intrapartum asphyxia. From Phelan JP, Alan MO: The brain damaged baby: Fetal heart rate lessons from the data bank, in Maulik D (ed): Asphyxia and Fetal Brain Damage. New York, WileyLiss, pp 227-239. Copyright 9 1998 Wiley-Liss.Reprinted by Wiley-Liss, Inc., a subsidiary of John Wiley & Sons, Inc. 1
110
-INCREASINGBASELINERATE -REPETITIVEDECELS -LOSSOFVARIABILITY
"%
~.
~ . ~
-DECREASINGBASELINERATE -STAIR-STEPSTODEATH -FETALDEATH
UA
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and is unlikely to develop cerebral
t i m e s , 45-47 low initial platelet c o u n t s , 49 multior-
edema. T h e primary pathophysiologic m e c h a n i s m responsible for the H o n and the persistent nonreactive patterns appears to be progressive fetal vasoconstriction (Figure 3) a n d ultimately ischemia. As stated previously, the triggering mechanism may be m e c o n i u m zs,z9 or infection 4~ but is not uterine contractions. 4 T h e resultant vasoconstriction or intrafetal shunting probably results in i m p a i r e d renal perfusion and oligohydramnios. This is probably 1 explanation why amniotic fluid volume assessment in combination with a nonstress test (NST)20 or biophysical profile 2~ accounts for the r e p o r t e d reduction in cerebral palsy. 44 Nevertheless, once the fetus develops ischemia or is unable to perfuse its brain cells, cellular hypoxia or injury occurs. Thus, the hypoxia e n c o u n t e r e d in the fetus is cellular rather than systemic. By the time fetal systemic hypoxia develops, the fetus, in o u r opinion, has already b e e n brain injured and is probably n e a r death. Thus, cerebral perfusion deficits attributable to intrafetal and intracerebral shunting rather than fetal systemic hypoxia are most likely responsible for fetal brain injury. This means, for example, that a fetus who develops the H o n pattern of i n t r a p a r t u m asphyxia would a p p e a r to move f r o m point C to ischemia (Figure 3). During this transition, a progressive and substantial rise in FHR is observed in an effort to preserve cerebral perfusion and cellular oxygenation. At the same time, fetal systemic oxygenation and oxygen saturation is maintained. In o u r opinion, only after progressive a n d p r o l o n g e d ischemia and brain injury do fetal oxygen saturations begin to fall.
gan system dysfunction, s7,-~~ delayed onset of seizures f r o m birth 52,53 and cortical brain injuries. n T h e typical F H R pattern is nonreactive with a fixed baseline rate that normally does not change f r o m admission until delivery, 1,<7-11 in association with diminished to average variability. W h e n looking at the admission F H R pattern, the persistent nonreactive F H R pattern g r o u p can be divided into 3 phases (Table 4). These 3 phases, in our opinion, r e p r e s e n t a post-CNS insult c o m p e n s a t o r y response in the fetus. Moreover, this FHR pattern, in o u r opinion, does not r e p r e s e n t ongoing asphyxia or worsening of the CNS injury. 1,4,11 For a fetus to have o n g o i n g fetal asphyxia, a FHR pattern similar to that of H o n would have to be seen. There, (Figure 4) a progressive and substantial rise in baseline h e a r t rate in association with repetitive F H R decelerations is observed in response to o n g o i n g fetal asphyxia. In contrast, the F H R baseline in the nonreactive g r o u p remains fixed. Infrequently, a F H R tachycardia is seen; but, the rise in baseline rate is usually insubstantial. Thus, the phase of recovery appears to equate with the length of time f r o m the fetal CNS insult. This is similarly reflected in the neonatal findings described in Table 1. Thus, phase I would a p p e a r to be closer to the time of the insult, and phase III would a p p e a r to be m o r e distant in time f r o m the injury-producing event. 1' T h e persistent nonreactive F H R pattern is not, in o u r opinion, a sign of o n g o i n g fetal asphyxia but rather represents a static encephalopathy. 1,4,1t This means that earlier intervention in the f o r m of a cesarean on admission to
injured
The Persistent Nonreactive FHR Pattern The persistent nonreactive F H R pattern g r o u p accounted for 45% of the F H R patterns observed in a p o p u l a t i o n (Figure 1) of 300 braind a m a g e d babies/1 This population is typically but not always characterized by the presence of r e d u c e d fetal activity before admission to the hospital, male fetuses, old m e c o n i u m , mecon i u m sequelae such as m e c o n i u m aspiration synd r o m e and persistent p u l m o n a r y hypertension, and oligohydramnios. 4 Along with these observations, these fetuses (Table 1) have elevated N R B C , 45-48 p r o l o n g e d NRBC clearance
TaMe 4. Fetuses With Preadmission Central Nervous System Injury Exhibit a Persistent Nonreactive FHR Pattern Intrapartum 11 and Can be Divided Into 3 Phases Based on the Baseline FHR and the FHR Variability Phase
I II III
Baseline Rate (bpm)
Variability
Incidence (%)
> 160 110-160 110-160
Diminished Diminished Average
19 39 43
Reprinted with permission fi-om Phelan JP, Ahn MO: Fetal heart rate observations in 300 term brain damaged infants. J Mat Fetal Invest 8:1-5, 1998.11 9 Springer Verlag.
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the hospital would not, in our opinion, substantially alter fetal outcome.
FHR and Neonatal Associations In recent times, a split of opinion has arisen as to the reliability of EFM. The seminal manuscript on the subject by Nelson and associates 54 is quite limited in its scope. For example, n o n e of the fetal monitor strips were read by the investigators; and none of the investigators were an obstetrician. Although that is a major deficiency of the manuscript, the investigators did rely on the interpretations as r e c o r d e d in the medical records by the treating physicians and nurses. Using a case controlled approach, the investigators concluded there was no benefit to EFM. However, the question r e m a i n s - i s EFM valid? But first one must ask, did the investigators, like so many in the past 55-57 and, for that matter, the present 58,59 use i m p r o p e r end-points to arrive at their conclusions. All too often, fetal m o n i t o r i n g studies have been based on the final minutes of the m o n i t o r strips55-59; and, very few researchers have looked at fetal m o n i t o r strips in a prospective m a n n e r from admission to delivery. 4'11'29"60"61 At the same time, and until recently, few, if any articles, c o m p a r e d intraparturn FHR patterns with neonatal observations such as seizure onset, 52,5~ brain injury location, 11,32,33,43 organ dysfunction, 37,5~ NRBC, 45-48 and platelet counts. 49 W h e n the intrapartum fetal m o n i t o r patterns for brain damaged babies are contrasted with their neonatal findings, distinct patterns emerge (Table 1). For example, when fetuses with acute asphyxia are contrasted with preadmission asphyxia (the persistent nonreactive FHR pattern group), NRBC counts, NRBC clearance times, platelet counts, organ dysfunction, brain injury location, and seizure onset are distinctly different. These findings suggest that the reliance on the types of decelerations a n d / o r a loss of variability appears to be less reliable than changes in the baseline rate and the ability of the fetus to accelerate its own heart rate. W h e n these neonatal findings are taken in their entirety, fetal m o n i t o r i n g appears to be a reliable indicator of fetal status. W h e t h e r intrapartum fetal monitoring can lead to the prevention of intrapartum fetal brain damage is less certain. Nevertheless, fetal monitoring appears to provide sufficient
Table 5. What's Hot and What's Not Hot in Fetal Assessment in the New Millennium What's Hot
What's Not Hot
Fetal movement AFV assessment Baseline rate changes Reactivity NRBC Platelet counts
Variability Deceleration type
information to the physician and nurse to understand the fetal e n v i r o n m e n t and to make maternal and fetal health care decisions.
Fetal Monitoring Made Simple In light of the lessons learned from the children damaged in utero before and during labor, current fetal m o n i t o r i n g interpretation will need to change to reflect and include the significance of the initial fetal m o n i t o r i n g period (Table 5). When a patient presents to labor and delivery, the initial fetal assessment should include an initial fetal m o n i t o r i n g period to assess reactivity (the presence of FHR accelerations) and to ascertain from the patient the quality and quantity of fetal movement. In the patient with a reactive FHR pattern and normal fetal movement, the key to clinical m a n a g e m e n t is to follow the baseline rate. This means that the physician and nurse will need to watch for persistent elevations or falls of the baseline rate. To assist with the identification of the H o n pattern, medical and nursing personnel should try to compare the current tracing with the one obtained on admission. If the characteristics of the H o n pattern of intrapartum asphyxia develops, delivery should be considered. In the nonreactive group, clinical managem e n t is directed toward keeping the fetus on the EFM until fetal status is clarified with p r o l o n g e d fetal monitoring, a contraction stress test or a biophysical profile. O n c e fetal status is clarified in the nonreactive group, the subsequent mana g e m e n t with respect to the route of delivery will d e p e n d on the discussion with the family and the clinical findings.
References 1. Phelan JP, Ahn MO: The brain damaged baby: Fetal heart rate lessons from the data bank, in Maulik D (ed):
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Asphyxia and Fetal Brain Damage. New York, NY, WileyLiss, Inc, 1998, pp 227-239 2. Yeh SY, Diaz E, Paul RH: Ten year experience intraparturn fetal monitoring in Los Angeles County/University of Southern California Medical Center. Am J Obstet Gynecol 143:496-500, 1982 3. Perkins RP: Perspectives on perinatal brain damage. Obstet Gynecol 69:807-19, 1987 4, Phelan JP, Alan, MO: Perinatal observations in fortyeight neurologically impaired term infants. AnlJ Obstet Gynecol 171:424-31, 1994 5. Menticoglou SM, Manning FA, Harman CR, et al: Severe fetal brain injury without evident intrapartum trauma. Obstet Gynecol 74:457-61, 1989 6. Shields JR, Schifrin BS: Perinatal antecedents of cerebral palsy. Obstet Gynecol 71:899-905, 1988 7. Van der Moer P, Gerretsen G, Visser G: Fixed heart rate pattern after intrauterine accidental decerebration. Obstet Gynecol 65:125-7, 1985 8. Leveno KJ, Williams ML, DePalma RT, et al: Perinatal outcome in the absence of antepartum fetal heart rate acceleration. Obstet Gynecol 61:347-55, 1983 9. Devoe LD, McKenzieJ, Searle NS, et al: Clinical sequelae , of the extended nonstress test. Am J Obstet Gynecol 151:1074-8, 1985 10. Brown R, Patrick J: The nonstress test: How long is long enough? A m J Obstet Gynecol 141:646-51, 1981 11. PhelanJP, Alan MO: Fetal heart rate observations in 300 term brain-damaged infants. J Matern Fetal Invest 8:1-5, 1998 12. Toffs C, Van den Berg BJ, Oechsli FW, et al: Prenatal and Perinatal Factors in etiology of cerebral palsy. J Pediatr 116:615-9, 1990 13. Blair E, Stanley FJ: Intrapartum asphyxia: A rare cause of cerebral palsy. J Pediatr 112:515-19, 1988 14. Clark SL, Hankins GDV, Dudley DA, et al: Amniotic fluid embolism: Analysis of the national registry. A m J Obstet Gynecol 172:1158-1168, 1995 15. Herbst AL, Robboy SJ, Scully RE, et al: Clear cell adenocarcinoma of the vagina and cervix in girls: Analysis of 170 registry cases. AmJ Obstet Gynecol 119:713-24, 1974 16. Busby A, Dolk H, Collin R, et ah Compiling a national register of babies born with anophthalmia/microphthalmia in England 1988-94. Arch Dis Child Fetal Neonatal Ed 79:F168-F173, 1998 17. Ahn MO, PhelanJP: Amassing an arsenal of data for an assault of cerebral palsy. OBG Manag 9:111, 1997 18. Phelan JP: Labor admission test. Clin Perinatol 21:87985, 1994 19. Alan MO, Korst LM, Phelan ,JP: Normal fetal heart rate patterns in the brain-damaged infant: A failure of intrapartum fetal monitoring?J Mat Fetal Invest 8:58-60, 1998 20. Phelan JP: Antepartum fetal assessment: Newer techniques. Semin Perinatal 12:57-65, 1988 21. Phelan JP: The nonstress test: A review of 3000 tests. A m J Obstet Gynecol 139:7-10, 1981 22. Lee CY, DiLoreto PC, Logrand B: Fetal activity acceleration determination for the evaluation of fetal reserve. Obstet Gynecol 48:19-26, 1976 23. Smith CV, Phelan JP: Antepartum fetal assessment: The nonstress test, in Hill A, VolpeJ (eds): Fetal Neurology. New York, NY, Raven Press, 1989, pp 61-74
24. Clark SL, Gimovsky ML, Miller FC: The scalp stimulation test: A clinical alternative to fetal scalp blood sampling. A m J Obstet Gynecol 148:274-277, 1984 25. Smith CV, Nguygen HN, Phelan JP, et ah Intrapartum assessment of fetal well-being: A comparison of fetal acoustic stimulation with acid-base determinations. AmJ Obstet Gynecol 155:726-8, 1986 26. Shaw K, Clark SL: Reliability of intrapartum fetal heart rate monitoring in the post term fetus with meconium passage. Obstet Gynecol 72:886-889, 1988 27. Clark SL, Gimovsky ML, Miller FC: Fetal heart rate response to scalp blood sampling. Am J Obstet Gynecol 144:706-708, 1982 28. Carbonne B, Langer B, Goffinet F, et ah Multicenter study on the compared predictive values of pulse oximetry and blood analysis. A m J Obstet Gynecol 177:593-8, 1997 29. Krebs HB, Petres RE, Dunn LJ, et al: Intrapartum fetal heart rate monitoring: VI. Prognostic significance of accelerations. Am J Obstet Gynecol 142:297-305, 1982 30. Ingemarsson I, Arulkumaran S, Paul RH, et al: Admission test: A screening test for fetal distress in labor. Obstet Gynecol 68:800-6, 1986 31. Rutherford SE, Phelan JP, Smith CV, et al: The four quadrant assessment of amniotic fluid volume: An adjunct to antepartum fetal heart rate testing. Obstet Gynecol 70:353-6, 1987 32. Myers RE: Two pattern of perinatal brain damage and their conditions of occurance. Am J Obstet Gynecol 112:246-277, 1972 33. Roland EH, Poskitt K, Rodriguez E, et al: Perinatal hypoxic-ischemic thalamic injury: Clinical features and neuroimaging. Ann Neurol 44:161-66, 1998 34. Golditch BD, Ahn MO, Phelan JP: The fetal admission test and intrapartum fetal death. J Matern-Fet 15:273276, 1998 35. Hon EH, Lee ST: Electronic evaluation of the fetal heart rate: VIII. Patterns preceding fetal death, further observations. A m J Obstet Gynecol 87:814-26, 1963 36. Molteni RA, Stys SJ, Battaglia EC: Relationship of fetal and placental weight in human beings: Fetal/placental weight ratios at various gestational ages and birthweight distributions. J Reprod Med 21:327-332, 1978 37. Phelan JP, Ahn MO, Korst L, et al: Intrapartum fetal asphyxial brain injury with absent muhiorgan system dysfunction. J Matern-Fet Med 7:19-22, 1998 38. Altschuler G, Arizawa M, Molnar-Nadasy G: Meconiuminduced umbilical cord vascular necrosis and ulceration: A potential link between the placenta and poor pregnancy outcome. Obstet Gynecol 79:760-66, 1992 39. Alschuler G, Hyde S: Meconium induced vasoconstriction: A potential cause of cerebral and other fetal hypoperfusion and of poor pregnancy outcome.J Child Neurol 4:1337-42, 1989 40. Perlman JM, Risser R, Broyles RS: Bilateral Cystic leukomalacia in the premature infant: Associated risk factors. Pediatrics 97:822-27, 1996 41. Yoon BH, Kim cJ, JunJK: Amnitic fluid interleukin 6: A sensitive test for antenatal diagnosis of acute inflammatory lesions of preterm placenta and prediction of perinatal morbidity. Am J Obstet Gynecol 172:960-70, 1995 42. Leung A, Leung EK, Paul RH: Uterine rupture after
FHR Patterns in the Brain-Damaged Infant
43.
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previous cesarean delivery: Maternal and fetal consequences. Am J Obstet Gynecol 169:945-50, 1993 KimJO, Martin GI, Kirkendall C, et al: Intrapartum fetal hear rate variability and subsequent neonatal cerebral edema. Obstet Gynecol (in press) Manning FA, Bondaji N, Harman CR, et al: Fetal assessment based on fetal biophysical profile scoring VIII. The incidence of cerebral palsy in tested and untested perinates. A m J Obstet Gynecol 178:696-706, 1998 PhelanJP, Ahn MO, Korst L, et al: Nucleated red blood cells: A marker for fetal asphyxia? Am J Obstet Gynecol 173:1380-4, 1995 Korst LM, Phelan JP, Ahn MO, et al: Nucleated red blood cells: An update on the marker for fetal asphyxia? Am J Obstet Gynecol 175:843-6, 1996 Korst LM, Alan MO, Martin GI, et al: Dating fetal brain injury: The role of NRBCs. OBG Management. April:91101, 1997 Buonocore G, Perrone S, Gioia D, et al: Nucleated red blood cells at birth as an index of perinatal brain damage. Am J Obstet Gynecol 181:1500-5, 1999 Korst LM, Phelan JP, Wang YM, et al: Neonatal platelet counts in fetal brain injury. Am J Perinatol 16:79-83, 1999 Korst LM, PhelanJP, Alan MO, et al: Can persistent brain injury resulting fi-om intrapartum asphyxia be predicted by current criteria? Prenat Neonat Med 2:286-93, 1997 Korst L, PhelanJP, Wang YM, et al: Acute fetal asphyxia and permanent brain injury: A retrospective analysis of current indicators. J Mater Fet Med 8:101-106, 1999 Ahn MO, Korst LM, Phelan JP, et al: Does tile onset of neonatal seizures correlate with the timing of fetal neurologic injury. Clin Pediatr 37:673-676, 1998 Kirkendall C, Ahn MO, Martin G, et ah The brain in-
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jured baby, neonatal seizures, and the intrapartum fetal heart rate pattern: Is there a relationship? Am J Obstet Gynecol I82:S184, 2000 (abstr) Nelson KB, Dambrosia JM, Ting Ty, et al: Uncertain value of electronic fetal monitoring in predicting cerebral palsy. N EnglJ Med 334:613-18, 1996 Paul RH, Suidan AK, Yeh SY, et al: Clinical fetal monitoring VII: The evaluation and significance of intraparturn baseline FHR variability. Am J Obstet Gynecol 122: 206-10, 1975 Cibils L: Clinical significance of fetal heart rate patterns dm'ing labor V. Variable decelerations Am J Obstet Gynecol 132:791-805, 1978 Tejani NA, Mann LI, Sanghavi S e t al: The association of umbilical cord complications and variable decelerations with acid-base findings. Obstet Gynecol 49:159-62, 1977 National Institutes of Child Health and Human Development Research Planning Child Workshop: Electronic fetal heart rate monitoring: Research guidelines for interpretation. Am J Obstet Gynecol 177:1385-90, 1997 Spong CY, Rasul C, ColleaJV, et ah Characterization and prognostic significance of variable decelerations in the second stage of labor. A m J Perinatol 15:369-74, 1998 Samo AP, Phelan JP, Ahn MO: Relationship of early intrapartum fetal heart rate patterns to subsequent patterns and fetal outcome. J Reprod Med 35:239-42, 1990 Krebs HB, Petres RE, Dunn LJ, et al: Intrapartum fetal heart rate monitoring I. Classification and prognosis of fetal heart rate patterns. Am J Obstet Gynecol 133:762, 1979 Wiswell TE, Tuggle JM, Turner BS: Meconium aspiration syndrome: Have we made a difference? Pediatrics 85:715-18, 1990
The objective of this study was to describe the fetal heart rate patterns and underlying pathophysiologic changes in the brain-damaged fetus. Fetuses with brain damage from hypoxic ischemic encephalopathy do not manifest uniform fetal heart rate patterns. However, these fetuses do show distinct fetal heart rate patterns that permit categorization based on their admission heart rate, subsequent changes in their baseline rate; and neonatal findings. Based on the observations of infants brain damaged in utero because of hypoxic ischemic encephalopathy, the intrapartum fetal management will depend on the admission fetal heart rate pattern, and the subsequent changes in the baseline rate.
Copyright 9 2000 by W.B. Saunders Company lectronic Fetal Monitoring (EFM) has bein the assessm e n t of a n t e p a r t u m and i n t r a p a r t u m fetal wellbeing. 1 Since its inception, the goal of EFM has b e e n to continuously assess fetal health during labor and to theoretically p e r m i t the early detection of i n t r a p a r t u m fetal dis~tress in sufficient time to prevent fetal brain injury. AS such, the presence of contraction-mediated fetal h e a r t rate (FHR) decelerations such as repetitive late decelerations has served as the basis for intervention. If traditional maneuvers such as maternal position change, oxygen administration, intravenous fluid administration, a n d / o r discontinuation of oxytocin failed to ameliorate this F H R pattern within a reasonable period of time, expedited delivery was indicated. With the increasing use of continuous EF M, i n t r a p a r t u m fetal death rates but not cerebral palsy (CP) rates, have declined t h r o u g h o u t the United States. 2 This trend is in keeping with the prescient observations of Perkins 3 m o r e than a decade ago. T h e n , he Opined that "the n u m b e r of infants injured during labor is highly overestim a t e d and the n u m b e r injured prior to labor is highly underestimated. ''3 At that time, the prevailing thought was that changes in the F H R p r e c e d e d neurological i m p a i r m e n t of the fetus. However, as we have learned not all fetuses undergo brain injury in such a m a n n e r . 4-11 AS suggested by these investigators, 4-11 the F H R pattern appears to be a manifestation of underlying fetal neurological i m p a i r m e n t and may be m o r e useful in identifying those fetuses who have already
E c o m e an invaluable adjunct
sustained central nervous system (CNS) injury before labor. In m a n y ways, the low incidence of asphyxial induced CP, has in part, b e e n responsible for o u r limited u n d e r s t a n d i n g of Perkins' insights) In essence, asphyxial induced CP's relatively rarity requires a registry f o r m a t to study its pathophysiology. For example, the overall incidence of CP is a r o u n d 1% of all live births.12 T h e known causes for CP are n u m e r o u s and include but are not limited to c h r o m o s o m a l and structural abnormalities, infection, prematurity, and asph}-xia. Overall, asphyxial induced CP is one of the rarest forms o f CP with a r e p o r t e d incidence of 1 in 10,000 births. 13 Given the rarity of asphyxial induced CP, the only reliable way to investigate it's pathophysiology a n d prevention is through a National Registry f o r m a t similar to those patient registries established by Clark to study amniotic fluid embolus, TM Herbst to describe the link between diethylstilbesterol' and a d e n o c a r c i n o m a of the vagina, a5 and Busby to study a n o p h t h a l m i a / m i c r o p h t h a l m i a . 16 Following the lead of these world renown investigators, we at the Childbirth Injury Prevention FoundaFrom the Department of Obstetrics and Gynecology, Pomona Valley Hospital Medical Center, and Childbirth Injury Prevention Foundation, Pasadena, CA. Supported by the Childbirth Injury Prevention Foundation, Pasadena, CA. Address reprint requests to Jeffrey P. Phdan, MD, Suite 200, 959 East Walnut Street, Pasadena, CA 91106. Copyright 9 2000 by W.B. Saunders Company O146-0005/00/2403-000651 O.00/0 doi: 10.1053/spet:2000. 7079
Seminars in Perinatology, Vol 24, No 3 (June), 2000: pp 221-229
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tion 17 established a National Registry in 1991 to research the pathophysiology of asphyxial induced CP for the purpose of identifying clinical approaches that could, where possible, ultimately lead to its prevention. Therefore, the purpose of this article is 4-fold. First, we will review the FHR patterns associated with CNS injury in the term fetus. Second, we will review the neonatal observations associated with the FHR patterns in instances of fetal brain damage. Third, these FHR patterns will help to serve as a basis for providing intrapartum mana g e m e n t recommendations. Fourth, we must emphasize that these FHR patterns apply to term and postdate pregnancies and may not necessarily apply to preterm or twin pregnancies. Finally, the recommendations, contained herein, d o not imply n o r infer a standard of care for the management of intrapartum obstetrical patients. Rather, this article represents another piece of the cerebral palsy puzzle.
F H R Patterns in the Brain Damaged Infant
probability of intrapartum fetal distressf v,3~ Thus, a reactive FHR pattern obtained on admission to the hospital or anytime during labor serves as a reliable sign of fetal well-being. In contrast, a nonreactive fetal admission test is associated with a greater probability of an adverse fetal outcome. 29,3~For instance, there is an inverse relationship between the n u m b e r of FHR accelerations and oligohydramnios, s,~l FHR decelerations, 31 meconium-stained amniotic fluid, 2~ intrapar(um fetal distress, 1s,29~31 and long-term n e u r o l o g i c a l impairment. ~,4,7-a~ If, for example, fetal nonreactivity is present for more than 120 minutes from the time of admission to the hospital, higher rates of operative intervention, perinatal mortality, and long-term neurological impairment are observed. 1,4,7-11 In sum, the fetal admission test results enable the clinician and the labor and delivery nurse to categorize laboring patients for intrapartum m a n a g e m e n t and to reassign their risk status. At the same time, the FHR patterns associated with fetal brain damage can be used as guiding lights for intrapartum care and the potential prevention of fetal brain damage.
The First Step To understand fetal brain damage requires an assessment of fetal status with EFM on admission to the hospital. This has been referred to as the fetal or labor admission test. Is With the use of the fetal admission test, outpatient and inpatient fetal m o n i t o r i n g principles are applied to the laboring patient. Here, the principal goals of the labor admission test are to identify those fetuses at risk for intrapartum fetal distress and to reassign those patients alleged to be at high or low risk before labor to a different risk category soon after admission to labor and delivery. Thus, the initial admission test or fetal monitoring, period can be used to redefine the patient's risk status and to assist the clinician and nurse specialist with the intrapartum m a n a g e m e n t of a patient's labor. If, for example, the patient's FHR pattern on admission to the hospital is considered reactive, labor and delivery personnel know that the fetus is probably but not absolutely n o r m a l / 9 At the same time, a reactive fetal admission test is a sign of a healthy fetus and symbolizes fetal well-bei n g / 8,2~ normal fetal acid-base status, 2~27 normoxia, 2s an absence of asphyxia, 2~27 and a low
FHR Patterns in the Brain Damaged Infant Term infants f o u n d to be brain d a m a g e d do not manifest a uniform FHR pattern. 1,4,n However, these fetuses do manifest distinct FHR patterns intrapartum that can be easily categorized and identified based on the fetal admissions test and subsequent changes in the baseline rate. Figure 1 shows the three most c o m m o n FHR patterns
PERSISTENT NR-45 %
PATTERN-22% ~
~THER-13%
REACTIVE-PD-20 % Figure 1. The incidence of the 3 most common FHR patterns associated with fetal brain damage. (PD, prolonged FHR deceleration).
223
FHR Patterns in the Brain-Damaged Infant
associated with fetal brain damage. The FHR patterns not included in Figure 1 that will n o t be discussed in this chapter are as follows: (1) the persistent reactive FHR pattern, 19 (2) FHR bradycardia on admission to the hospital, and (3) those that did not fit into any single category. AS n o t e d in Table 1, continuous EFM is useful in separating fetuses into distinct groups based on their admission and subsequent FHR patterns.
Reactive Admission Test and Subsequent Fetal Brain Damage Acute Asphyxia W h e n a pregnant woman is admitted to the hospital, the overwhelming n u m b e r of obstetrical patients will have a reactive FHR pattern. O f these, more than 98% will go t h r o u g h labor uneventfully and most will deliver vaginally. In the few patients (typically 1% to 2%) that develop intrapartum "fetal distress, ''29,3~ the characteristic "fetal distress" is usually, but not always, acute and manifested by a sudden p r o l o n g e d FHR deceleration that lasts until delivery. O f these, an even smaller n u m b e r of fetuses will ultimately experience CNS injury. As illustrated in Figure 1, fetal brain injury in the fetus with a reactive fetal admission test may arise, in the absence of trauma, as a result of a sudden prolonged FHR deceleration or a H o n pattern of intrapartum asphyxia. In the f o r m e r group, the FHR pattern is reactive; and, as a result of a sudden catastrophic event (Table 2),
a Sudden p r o l o n g e d FHR deceleration to approximately 60 beats per minute (bpm) occurs and lasts until the time of delivery. In this g r o u p (Table 1), the CNS injury is primarily located in the basal ganglia and thalami 32,~3 and is attributable to sudden and p r o l o n g e d reductions in fetal cardiac output. ~2,-~As shown in Table 2, the p r o l o n g e d FHR decelerations is associated with a wide array of patient groups such as uterine rupture, placental abruption, and cord prolapse. Given the acute nature of this FHR pattern, limited time is available to preserve normal CNS function. Based on our experience, the timing of neurological injury in this group depends on 5 factors (Table 3), First, the admission FHR pattern provides an indicator of fetal status before the catastrophic event. If, for example, the FHR pattern is reactive on admission and a sudden prolonged FHR deceleration occurs, the neurological insult is most likely acute. In contrast, a p r o l o n g e d FHR decelerations that follows a persistent nonreactive FHR pattern is most likely consistent with a postasphyxial insult-preterminal pattern/4,~5 Second, the fetal growth pattern at the time of presentation to the hospital also plays a role in the timing of fetal neurological injury. Fetal growth, to a large extent, is d e p e n d e n t on the functional placental surface area. 36 As such, infants who are small-, appropriate-, or large-forgestational-age usually have different functional placental surface areas available to them. To a
TaMe 1. FHR Patterns in the Normal and Brain-Damaged Infant and the Associated Perinatal Observations
Fetal movement on admission Admission FHR Meconium FHR baseline NRBC (#/100 WBC) NRBC clearance time (hrs) Platelet count Seizure onset time from birth (hrs) Organ dysfunction Cerebral edema Brain injury location cortical Basal ganglia thalami
Normal
NR
Normal Reactive 12% Fixed 2-3% <24 281 NA NA NA None None
Decreased absent NR 88% Fixed 52% 119 185 6 + 13 92% 66% Primary Uncommon
HON
Normal Reactive 50% ~ 35% 13% 66 251 10 -+ 14 64% 41% Primary Secondary if PD
RPD
Normal Reactive 23% ~ TO 60 BPM 12% 52 267 15 + 26 50% 51% Uncommon Primary
occurs
Abbreviations: NR, nonreactive; RPD, admission followed by a prolonged deceleration that lasts until delivery; NRBC, nucleated red blood cells. Data from r e f e r e n c e s 1,4,II,32,33,37,43~17,4%53,62,
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Table 2. Catastrophic Events That are Associated With a Reactive Fetal Admission Test and a Subsequent Prolonged FHR Deceleration to 60 bpm and Lasting Until Delivmy Umbilical cord prolapse Uterine rupture Placental abruption Maternal arrest Fetal exsanguination
large extent, the time interval to injury in an acute asphyxial event will d e p e n d o n the functional placental surface area to m a i n t a i n placental e x c h a n g e . For example, in infants with i n t r a u t e r i n e g r o w t h i m p a i r m e n t o r who are small-for-gestational-age, the time to CNS injury will be less t h a n that for an a p p r o p r i a t e - o r a large-for-gestational-age infant. In essence, fetal grbwth is a reflection o f either (1) the f u n c t i o n a l placental surface area available to each fetus or (2) the ability to withstand a catastrophic event for a l o n g e r p e r i o d o f time. T h e d e g r e e o f fetal vasoconstriction o r the level o f intrafetal s h u n t i n g at the time o f the catastrophic event is also a potential c o n t r i b u t o r to the timing a n d / o r the extent o f the fetal brain i n j u r y ) 7 Traditional obstetrical teachings r e g a r d i n g the p a t h o g e n e s i s o f fetal brain injury have described the centralization o f the fetal circulation d u r i n g i n t r a p a r t u m asphyxia to preserve fetal brain f u n c t i o n at the potential exp e n s e o f o t h e r o r g a n s such as the lungs o r kidneys (Figure 2). Intrafetal s h u n t i n g is b r o u g h t a b o u t by fetal vasoconstriction (Figure 3). T h e triggering m e c h a n i s m for the fetal vasoconstriction is u n k n o w n as o f this writing b u t m a y be i n d u c e d by the p r e s e n c e o f m e c o n i u m 38,39 or infection. 4~ T h e f i n d i n g o f o l i g o h y d r a m n i o s a n d / o r i n t r a u t e r i n e growth i m p a i r m e n t is illus-
Figure 2. The traditional view is that fetal blood flow is preferentially shunted away from organs such as the fetal kidneys in an effort to preserve fetal brain function. trative o f varying degrees o f fetal vasoconstriction o r shunting. If o n e assumes that intrafetal s h u n t i n g o r vasoconstriction has b e e n o n g o i n g f o r a p e r i o d o f time, the treating clinician o r nurse, in m o s t instances, will n o t k n o w the severity o f the vasoconstriction. Thus, h o w the table is set, with respect to the d e g r e e o f vasoconstriction, at the m o m e n t o f m a t e r n a l admission to l a b o r a n d delivery will d e t e r m i n e w h e t h e r fetal brain damage occurs, if at all, a n d its timing. T u r n i n g to Figure 3, assume that the vasoconstriction in fetuses I a n d II are at points A a n d C, respectively. O n admission to the hospital, b o t h fetuses have a reactive F H R pattern. D u r i n g the labor, a u t e r i n e r u p t u r e occurs resulting in a s u d d e n p r o l o n g e d F H R d e c e l e r a t i o n in b o t h p r e g n a n cies. D e p e n d i n g o n the d u r a t i o n o f the F H R d e c e l e r a t i o n a n d the o t h e r factors illustrated in Table 3, fetus II with vasoconstriction at p o i n t C is m o r e likely to sustain an injury t h a n is fetus I with vasoconstriction at p o i n t A. Moreover, the type o r location o f the brain injury will also p r o b a b l y be different (Table 1). T h e r e m a i n i n g 2 factors in Table 3, the duration o f the p r o l o n g e d F H R d e c e l e r a t i o n a n d the intactness o f the placenta, are also i m p o r t a n t factors. For example, in cases o f a c o m p l e t e placental separation, the o n s e t o f the p r o l o n g e d F H R d e c e l e r a t i o n to fetal injury interval will be s h o r t e r than if the p l a c e n t a were intact. Based o n the L e u n g study 42 in cases o f u t e r i n e r u p t u r e , the interval to CNS injury was less t h a n 18 min-
Table 3. Five Factors Useful in Determining the Timing of Fetal Brain Injury* Prior FHR pattern Fetal growth pattern Degree of fetal vasoconstriction Duration of the FHR deceleration Intactness of tile placenta * In the situation of a reactive admission test followed by a catastrophic event resulting in a sudden prolonged FHR deceleration to 60 bpm and lasting until delivery. Abbreviation: FHR, fetal heart rate.
~
NORMAL
A
B
~---'l~
C
ISCHEMIA
D
Figm'e 3. Persistent fetal vasoconstriction over time or intrafetal shunting leads to progressive narrowing of the fetal vascular tree leading nhimately to ischemia.
FHR Patterns in the Brain-Damaged Infant
utes. O u r experience 11 would suggest an even shorter time to neurological injury of 16 minutes whenever the placenta has completely separated. If the placenta remains intact, a longer period of time appears to be available before the onset of CNS injury.
Hon Pattern of Asphyxia The H o n pattern of intrapartum asphyxia (Figure 4) is uniquely different and evolves over a period o f time. 1,4,11 This FHR pattern begins with a reactive fetal admission test. Subsequently during labor, the fetus develops a nonreactive FHR pattern or loses its ability to accelerate its heart rate. 1,4a~ As the labor continues, a substantial rise in baseline heart rate from admission (135 _+ 10 bpm) to a mean m a x i m u m (186 + 15 bpm) baseline heart rate is seen. n The maxim u m FHR ranged from 155 b p m to 220 bpm. This constituted a 39 -+ 13% m e a n percent rise in baseline heart rate from admission and ranged from 17% to 82%. 11 This rise in baseline FHR is usually not a c c o m p a n i e d by maternal pyrexia. When a substantial rise in baseline fetal heart rate is encountered, the FHR pattern is also associated with repetitive FHR decelerations but not necessarily late decelerations and ultimately a loss of FHR variability (Figure 4).4,11 ,,As labor progresses and the fetus nears death, the slopes becomes progressively less steep until the
225
FHR does not return to its baseline rate and ultimately terminates in a p r o f o u n d bradycardia "a5 or a stairsteps-to-death pattern. 1,4,11,34 Once a FHR tachycardia begins, the subsequent FHR pattern n does 1 of the following: (1) the FHR pattern remains tachycardic a n d / o r continues to rise until delivery (55%)37; (2) a prolonged FHR deceleration that lasts until delivery occurrs (27%)18; or (3) a stairsteps-to-death pattern or a progressive bradycardia are seen (18%). 12 O f particular clinical relevance is that all patients manifested a substantial rise in their baseline heart rates, lost their ability to accelerate their FHR, became nonreactive, and exhibited repetitive FHR decelerations. Of note, the repetitive FHR decelerations were not necessarily late decelerations and were frequently variable decelerations. 11 In this group, fetal heart rate variability does not appear to be a reliable indicator of fetal status. 1~ For example, many brain-damaged fetuses, upwards of 30% exhibited average FHR variability at the time of their deliveries. 11 In the neonatal period, fetuses with the H o n pattern of intrapartum asphyxia and average FHR variability had significantly less cerebral edema. 43 Kim's cerebral e d e m a findings suggest that the use o f diminished FHR variability is probably an imp r o p e r end-point to decide the timing of operative intervention. 43 This means that before a loss of FHR variability, the fetal brain has been
HON PATTERNINTRAPARTUMASPHYXIA [ FETALHYPOXIA
)
,)
160 FHR Figure 4. The characteristics of the Hon pattern of intrapartum asphyxia. From Phelan JP, Alan MO: The brain damaged baby: Fetal heart rate lessons from the data bank, in Maulik D (ed): Asphyxia and Fetal Brain Damage. New York, WileyLiss, pp 227-239. Copyright 9 1998 Wiley-Liss.Reprinted by Wiley-Liss, Inc., a subsidiary of John Wiley & Sons, Inc. 1
110
-INCREASINGBASELINERATE -REPETITIVEDECELS -LOSSOFVARIABILITY
"%
~.
~ . ~
-DECREASINGBASELINERATE -STAIR-STEPSTODEATH -FETALDEATH
UA
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and is unlikely to develop cerebral
t i m e s , 45-47 low initial platelet c o u n t s , 49 multior-
edema. T h e primary pathophysiologic m e c h a n i s m responsible for the H o n and the persistent nonreactive patterns appears to be progressive fetal vasoconstriction (Figure 3) a n d ultimately ischemia. As stated previously, the triggering mechanism may be m e c o n i u m zs,z9 or infection 4~ but is not uterine contractions. 4 T h e resultant vasoconstriction or intrafetal shunting probably results in i m p a i r e d renal perfusion and oligohydramnios. This is probably 1 explanation why amniotic fluid volume assessment in combination with a nonstress test (NST)20 or biophysical profile 2~ accounts for the r e p o r t e d reduction in cerebral palsy. 44 Nevertheless, once the fetus develops ischemia or is unable to perfuse its brain cells, cellular hypoxia or injury occurs. Thus, the hypoxia e n c o u n t e r e d in the fetus is cellular rather than systemic. By the time fetal systemic hypoxia develops, the fetus, in o u r opinion, has already b e e n brain injured and is probably n e a r death. Thus, cerebral perfusion deficits attributable to intrafetal and intracerebral shunting rather than fetal systemic hypoxia are most likely responsible for fetal brain injury. This means, for example, that a fetus who develops the H o n pattern of i n t r a p a r t u m asphyxia would a p p e a r to move f r o m point C to ischemia (Figure 3). During this transition, a progressive and substantial rise in FHR is observed in an effort to preserve cerebral perfusion and cellular oxygenation. At the same time, fetal systemic oxygenation and oxygen saturation is maintained. In o u r opinion, only after progressive a n d p r o l o n g e d ischemia and brain injury do fetal oxygen saturations begin to fall.
gan system dysfunction, s7,-~~ delayed onset of seizures f r o m birth 52,53 and cortical brain injuries. n T h e typical F H R pattern is nonreactive with a fixed baseline rate that normally does not change f r o m admission until delivery, 1,<7-11 in association with diminished to average variability. W h e n looking at the admission F H R pattern, the persistent nonreactive F H R pattern g r o u p can be divided into 3 phases (Table 4). These 3 phases, in our opinion, r e p r e s e n t a post-CNS insult c o m p e n s a t o r y response in the fetus. Moreover, this FHR pattern, in o u r opinion, does not r e p r e s e n t ongoing asphyxia or worsening of the CNS injury. 1,4,11 For a fetus to have o n g o i n g fetal asphyxia, a FHR pattern similar to that of H o n would have to be seen. There, (Figure 4) a progressive and substantial rise in baseline h e a r t rate in association with repetitive F H R decelerations is observed in response to o n g o i n g fetal asphyxia. In contrast, the F H R baseline in the nonreactive g r o u p remains fixed. Infrequently, a F H R tachycardia is seen; but, the rise in baseline rate is usually insubstantial. Thus, the phase of recovery appears to equate with the length of time f r o m the fetal CNS insult. This is similarly reflected in the neonatal findings described in Table 1. Thus, phase I would a p p e a r to be closer to the time of the insult, and phase III would a p p e a r to be m o r e distant in time f r o m the injury-producing event. 1' T h e persistent nonreactive F H R pattern is not, in o u r opinion, a sign of o n g o i n g fetal asphyxia but rather represents a static encephalopathy. 1,4,1t This means that earlier intervention in the f o r m of a cesarean on admission to
injured
The Persistent Nonreactive FHR Pattern The persistent nonreactive F H R pattern g r o u p accounted for 45% of the F H R patterns observed in a p o p u l a t i o n (Figure 1) of 300 braind a m a g e d babies/1 This population is typically but not always characterized by the presence of r e d u c e d fetal activity before admission to the hospital, male fetuses, old m e c o n i u m , mecon i u m sequelae such as m e c o n i u m aspiration synd r o m e and persistent p u l m o n a r y hypertension, and oligohydramnios. 4 Along with these observations, these fetuses (Table 1) have elevated N R B C , 45-48 p r o l o n g e d NRBC clearance
TaMe 4. Fetuses With Preadmission Central Nervous System Injury Exhibit a Persistent Nonreactive FHR Pattern Intrapartum 11 and Can be Divided Into 3 Phases Based on the Baseline FHR and the FHR Variability Phase
I II III
Baseline Rate (bpm)
Variability
Incidence (%)
> 160 110-160 110-160
Diminished Diminished Average
19 39 43
Reprinted with permission fi-om Phelan JP, Ahn MO: Fetal heart rate observations in 300 term brain damaged infants. J Mat Fetal Invest 8:1-5, 1998.11 9 Springer Verlag.
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the hospital would not, in our opinion, substantially alter fetal outcome.
FHR and Neonatal Associations In recent times, a split of opinion has arisen as to the reliability of EFM. The seminal manuscript on the subject by Nelson and associates 54 is quite limited in its scope. For example, n o n e of the fetal monitor strips were read by the investigators; and none of the investigators were an obstetrician. Although that is a major deficiency of the manuscript, the investigators did rely on the interpretations as r e c o r d e d in the medical records by the treating physicians and nurses. Using a case controlled approach, the investigators concluded there was no benefit to EFM. However, the question r e m a i n s - i s EFM valid? But first one must ask, did the investigators, like so many in the past 55-57 and, for that matter, the present 58,59 use i m p r o p e r end-points to arrive at their conclusions. All too often, fetal m o n i t o r i n g studies have been based on the final minutes of the m o n i t o r strips55-59; and, very few researchers have looked at fetal m o n i t o r strips in a prospective m a n n e r from admission to delivery. 4'11'29"60"61 At the same time, and until recently, few, if any articles, c o m p a r e d intraparturn FHR patterns with neonatal observations such as seizure onset, 52,5~ brain injury location, 11,32,33,43 organ dysfunction, 37,5~ NRBC, 45-48 and platelet counts. 49 W h e n the intrapartum fetal m o n i t o r patterns for brain damaged babies are contrasted with their neonatal findings, distinct patterns emerge (Table 1). For example, when fetuses with acute asphyxia are contrasted with preadmission asphyxia (the persistent nonreactive FHR pattern group), NRBC counts, NRBC clearance times, platelet counts, organ dysfunction, brain injury location, and seizure onset are distinctly different. These findings suggest that the reliance on the types of decelerations a n d / o r a loss of variability appears to be less reliable than changes in the baseline rate and the ability of the fetus to accelerate its own heart rate. W h e n these neonatal findings are taken in their entirety, fetal m o n i t o r i n g appears to be a reliable indicator of fetal status. W h e t h e r intrapartum fetal monitoring can lead to the prevention of intrapartum fetal brain damage is less certain. Nevertheless, fetal monitoring appears to provide sufficient
Table 5. What's Hot and What's Not Hot in Fetal Assessment in the New Millennium What's Hot
What's Not Hot
Fetal movement AFV assessment Baseline rate changes Reactivity NRBC Platelet counts
Variability Deceleration type
information to the physician and nurse to understand the fetal e n v i r o n m e n t and to make maternal and fetal health care decisions.
Fetal Monitoring Made Simple In light of the lessons learned from the children damaged in utero before and during labor, current fetal m o n i t o r i n g interpretation will need to change to reflect and include the significance of the initial fetal m o n i t o r i n g period (Table 5). When a patient presents to labor and delivery, the initial fetal assessment should include an initial fetal m o n i t o r i n g period to assess reactivity (the presence of FHR accelerations) and to ascertain from the patient the quality and quantity of fetal movement. In the patient with a reactive FHR pattern and normal fetal movement, the key to clinical m a n a g e m e n t is to follow the baseline rate. This means that the physician and nurse will need to watch for persistent elevations or falls of the baseline rate. To assist with the identification of the H o n pattern, medical and nursing personnel should try to compare the current tracing with the one obtained on admission. If the characteristics of the H o n pattern of intrapartum asphyxia develops, delivery should be considered. In the nonreactive group, clinical managem e n t is directed toward keeping the fetus on the EFM until fetal status is clarified with p r o l o n g e d fetal monitoring, a contraction stress test or a biophysical profile. O n c e fetal status is clarified in the nonreactive group, the subsequent mana g e m e n t with respect to the route of delivery will d e p e n d on the discussion with the family and the clinical findings.
References 1. Phelan JP, Ahn MO: The brain damaged baby: Fetal heart rate lessons from the data bank, in Maulik D (ed):
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