Background With improved survival of preterm infants, questionshave been raised about the limit of viability. To provide betterinformation and counseling for parents of infants about to bedelivered after 22 to 25 weeks' gestation, we evaluated themortality and neonatal morbidity of preterm infants born atthese gestational ages.
Methods We studied retrospectively all 142 infants born at 22to 25 weeks' gestation (as judged by best obstetrical estimate)from May 1988 through September 1991 in a single hospital. Mortalityin the first six months, including stillbirths, and neonatalmorbidity (i.e., the presence of intracranial pathologic conditions,chronic lung disease, and retinopathy of prematurity) were analyzed.
Results Fifty-six infants (39 percent) survived for six months.Survival improved with increasing gestational age; none of 29infants born at 22 weeks' gestation survived, as compared with6 of 40 (15 percent) born at 23 weeks, 19 of 34 (56 percent)born at 24 weeks, and 31 of 39 (79 percent) born at 25 weeks.There were seven stillbirths at 22 weeks' gestation and fourstillbirths at 23 weeks. The more immature the infant, the higherthe incidence of neonatal complications as determined by thenumber of days of mechanical ventilation, the length of thehospital stay, and the presence of retinopathy of prematurity,periventricular or intraventricular hemorrhage, or periventricularleukomalacia. Only 2 percent of infants born at 23 weeks' gestationsurvived without severe abnormalities on cranial ultrasonography,as compared with 21 percent of those born at 24 weeks and 69percent of those born at 25 weeks.
Conclusions We believe that aggressive resuscitation of infantsborn at 25 weeks' gestation is indicated, but not of those bornat 22 weeks. Whether the occasional child who is born at 23or 24 weeks' gestation and does well justifies the considerablemortality and morbidity of the majority is a question that shouldbe discussed by parents, health care providers, and society.
Improved obstetric and neonatal interventions and aggressivetechniques of resuscitation have gradually improved the survivalof preterm infants and lowered the limit of viability1,2,3,4,5,6,7,8,9,10.Although the prophylactic administration of surfactant has furtherimproved the survival of extremely-low-birth-weight infants,its effect on morbidity is unclear,11,12,13,14 and the qualityof life of the survivors remains a concern.
These developments have created a new difficulty in counselingobstetricians and the parents of infants about to be born atthe limit of viability. Options for delivery and resuscitationneed to be weighed against the infant's chance of survival andnormal life. Current efforts to resuscitate extremely preterminfants aggressively and administer surfactant to them in thedelivery room raise the question, What is the limit of viability?
Most studies of mortality and outcome in preterm infants arebased on birth weight,1,2,3,4,7,8,9,10 an objective, reliablecriterion. Data based on birth weight are very useful in discussingthe treatment and follow-up care of preterm infants with parentsand colleagues in a neonatal intensive care unit. Clinical andultrasonographic estimates of fetal weight are often inaccurate,however, making it difficult to translate data based on birthweight into information that will be helpful in prenatal counselingwith parents.
In this study we sought to obtain more accurate informationon both survival and neonatal morbidity in preterm infants bornat the limit of viability who routinely received surfactantin our institution. We chose infants born at 22 to 25 weeks'gestation in order to include those born 1 week before and 1week after the limit of viability suggested in the current literature(23 or 24 weeks)1,2,3,4,5,6,7,8,9,10. We evaluated all infantsborn at each week of gestational age, including those stillborn,determining gestational age on the basis of the best obstetricalestimate. Because the incidence of major handicap (cerebralpalsy or mental retardation) is 50 to 100 percent in preterminfants with severe grade 3 or 4 intraventricular hemorrhageor periventricular leukomalacia,15,16,17,18,19,20,21 we focusedon the combination of these neonatal morbid conditions as aprimary outcome measure, referring to it as severe abnormalityon cranial ultrasonography.
Methods
We retrospectively studied all 142 infants born at 22 or 25weeks' gestation between May 26, 1988, when routine prophylacticadministration of calf-lung surfactant extract (Infasurf) wasbegun, and September 3, 1991, when a new surfactant protocolwas instituted at our hospital. Gestational age at deliverywas estimated on the basis of the date of the most recent menstrualperiod, ultrasonography of the fetus, and physical examinationof the neonate, because at this age there are no good postnatalmeasures of gestational age22,23.
During this period, there were no specific protocols in ourhospital for the care of fetuses or infants born at the limitof viability. In general, the obstetricians and neonatologistsconsulted with each other and with the families about the timingand mode of delivery and the care of the infant in the deliveryroom. Because of the risk to the mother and concern about theinfant's survival, the obstetricians tried to avoid performingcesarean section at 22 to 24 weeks' gestation.
A neonatologist attended each delivery whenever possible anddetermined whether the neonate was viable and how aggressiveresuscitation should be. No resuscitation was given if the infantwas stillborn. In general, if the infant was initially vigorous,he or she underwent intubation, was given surfactant, and wastaken immediately to the neonatal intensive care unit. If theinfant had poor respiratory effort or a low heart rate at birth,our general practice was to attempt resuscitation with bag-and-maskventilation; if there was a response, the infant underwent intubationand was given surfactant. There was no prolonged resuscitationof infants who did not respond.
The mortality rate we used differs from traditional calculationsof mortality in that we included stillbirths, so that the resultswould be applicable to the labor and delivery room as well asto the neonatal intensive care unit. Because we sought the mostrealistic assessment of mortality, we included deaths occurringup to six months after birth. The survival rate was definedas the number of infants born at a given gestational age whosurvived six months from birth, divided by the number of infantsborn at that gestational age, including stillborn infants.
Mortality was determined from a computerized data base in theneonatal intensive care unit, the obstetrical logbook, the pathologylogbook, and the follow-up clinic records. Age at death wasalso recorded. The time of fetal death in utero was generallynot discernible, however, because most parents and obstetricianschose not to monitor a fetus if no intervention was planned.Because no infant born at 22 weeks of gestation survived, thesedata are included only in the mortality data.
Cranial ultrasonography was performed in surviving infants atleast three times: 3 to 7 days after birth, at 10 to 14 days,and again at 6 weeks or at the time a term delivery would haveoccurred. The images were analyzed by ultrasonographers whowere unaware, for the most part, of the infants' clinical status.The Papile grading system was used to grade periventricularor intraventricular hemorrhages on a scale from 1 to 424. Periventricularleukomalacia was defined as any cyst formation observed at anytime (excluding periventricular echodensities that subsequentlydisappeared). We defined poor outcome on the basis of the percentageof all infants born at a given gestational age, including thosestillborn, who died or in whom severe abnormalities developedthat were detected on cranial ultrasonography, either grade3 or 4 intraventricular hemorrhage or periventricular leukomalacia.
Other indicators of neonatal morbidity included measures ofchronic lung disease (i.e., the duration of mechanical ventilationor supplemental oxygen therapy), postmenstrual age (calculatedas the infant's gestational age at birth plus the chronologicage) at the discontinuation of oxygen therapy, the length ofthe hospital stay, and the presence of retinopathy of prematurity.All the surviving infants were examined in the neonatal intensivecare unit by an ophthalmologist skilled at diagnosing retinopathyof prematurity. This condition was scored as present if therewas active disease (stage 2, 3, or 3+). The administration ofcryotherapy treatment to either eye was also recorded.
Mortality, including the incidence of stillbirths, was analyzedin the overall group and according to gestational age. Morbiditywas analyzed in surviving infants according to gestational age.The effect of various maternal and perinatal factors and ofsex and race on mortality and perinatal outcomes (poor vs. good)was evaluated by logistic-regression analysis. Differences inmorbidity between gestational-age groups were investigated witha one-way analysis of variance using the Student-Newman-Keulscomparison.
Results
Mortality Including Stillbirths
Among the 142 infants born at 22 to 25 weeks' gestation accordingto the best obstetrical estimate, 80 (56 percent) survived longenough (at least 30 minutes) to be admitted to the neonatalintensive care unit, and 56 (39 percent) survived for at least6 months. Both mortality and the proportion of infants who diedin the delivery room decreased with increasing gestational age(Figure 1). Of 29 infants born at 22 weeks, including 7 stillborn,none survived for 6 months. Survival improved to 15 percent(6 of 40 infants, including 4 stillborn) at 23 weeks' gestation,to 56 percent (19 of 34 infants) at 24 weeks, and to 80 percent(31 of 39 infants) at 25 weeks. There were no stillbirths at24 or 25 weeks of gestation.
Figure 1. Survival of Infants Born at 22 to 25 Weeks' Gestation, According to Gestational Age.
Survival was studied from the time of infants' admission into the neonatal intensive care unit to six months after birth. Gestational ages were based on the best obstetrical estimate.
Demographic Characteristics
The mean (±SD) birth weight of the stillborn infantswas 459 ±81 g (range, 405 to 690). The mean birth weightof the 80 infants admitted to the neonatal intensive care unitwas 703 ±121 g. The mean birth weight of the 56 infantswho lived six months was 724 ±112 g. More girls livedat least six months (32 of 39, or 82 percent) than did boys(24 of 41, or 59 percent; P = 0.02). Table 1 shows the birthweight, sex, race, and maternal socioeconomic status of the80 infants who were admitted to the neonatal intensive careunit. When the best obstetrical estimates were used, with anextension of the standard curve for intrauterine growth, onlythree infants were small for their gestational ages; all threewere born at 25 weeks' gestation, and two survived for 6 months.
Table 1. Demographic Characteristics of Infants Admitted to the Neonatal Intensive Care Unit.
Only 23 to 28 percent of the infants admitted to the neonatalintensive care unit in a given gestational-age group were white.Two infants were Hispanic, and one was Asian. For purposes ofanalysis, these three infants were grouped with the black infants.All three infants born at 22 weeks' gestation who underwentsuccessful resuscitation in the delivery room were black.
Morbidity and Length of Stay
The infants born at each gestational age who survived for sixmonths were compared by an analysis of variance in which thevariables were the number of days of mechanical ventilation,the number of days of supplemental oxygen administration, theinfant's postmenstrual age at the discontinuation of oxygen,and the length of the hospital stay (Table 2). The only significantdifferences were those between the infants born at 23 to 24weeks of gestation and the infants born at 25 weeks.
Table 2. Outcomes in Infants Born at 23 to 25 Weeks' Gestation Who Survived for 6 Months.
Active retinopathy of prematurity (stage 2, 3, or 3+) occurredin five of the six surviving infants born at 23 weeks' gestation(83 percent), 53 percent of those born at 24 weeks, and 32 percentof those born at 25 weeks (Table 2).
The incidence of periventricular or intraventricular hemorrhageand periventricular leukomalacia decreased with increasing gestationalage (Table 2). One of 6 survivors born at 23 weeks of gestation,5 of 19 infants born at 24 weeks (26 percent), and 20 of 31infants born at 25 weeks (65 percent) had normal cranial ultrasonograms.
The proportion of infants who died or had severe abnormalitieson cranial ultrasonography at each gestational age is shownin Figure 2. The majority of infants born at 23 or 24 weeks'gestation (98 percent and 79 percent, respectively) had pooroutcomes (they either died or had severe intracranial abnormalities).In contrast, less than one third (31 percent) of those bornat 25 weeks' gestation had poor outcomes.
Figure 2. Six-Month Outcomes in Infants Born at 22 to 25 Weeks' Gestation.
"Good outcomes" denotes survival without severe abnormalities on cranial ultrasonography, "abnormalities" denotes the presence of severe abnormalities on cranial ultrasonography, and "infant deaths" denotes all perinatal, neonatal, and infant mortality.
Relation between Perinatal Variables and Outcome
In a logistic-regression analysis in which mortality was usedas the dependent variable, the following perinatal variableswere evaluated: birth weight ( 600 vs. >600 g), gestationalage ( 24 weeks vs. >24 weeks), sex, race, mode of delivery(vaginal vs. cesarean), and the presence or absence of antepartumhemorrhage, fetal distress, illicit drug use by the mother,and chorioamnionitis. Only birth weight of 600 g or less (P<0.001)and male sex (P = 0.02) were significantly related to increasedmortality. When poor outcome was used as the dependent variablein a similar analysis with the same perinatal variables, onlygestational age of 24 weeks or less (P = 0.03) and male sex(P = 0.005) were significantly related to poor outcome.
Discussion
Our results suggest that the limit of viability in the era ofroutine use of surfactants is 23 to 24 weeks of gestation. Thesurvival rate reported here is slightly better than the ratebefore surfactant was routinely used: 15 percent as comparedwith 3 to 8 percent in infants born at 23 weeks, and 56 percentas compared with 4 to 31 percent in those born at 24 weeks7.Since few studies have included stillbirths in their analysis,this improvement in survival is a conservative estimate. Datafrom our hospital suggest that survival at the limit of viabilityhas improved since the introduction of surfactant, as comparedwith historical controls25. However, other changes in obstetricaland neonatal management may have contributed to the improvedsurvival.
Occasional survivors born at 22 weeks' gestation have been reported7.Despite our initial resuscitation of three infants born at 22weeks' gestation who appeared to be viable (i.e., there wasa heart rate and respiratory effort at birth), all died by 4months of age. The frequency of late deaths was similar to thatpreviously reported. Hack and Fanaroff7 found that aggressivetreatment (such as delivery by cesarean section or the use ofintubation) of infants with birth weights below 750 g did notchange neonatal mortality but only increased the mean age atdeath from 73 to 880 hours. Although an argument can be madein favor of keeping an infant alive long enough for the parentsto say goodbye, deliberately prolonging death beyond a few hoursis difficult to justify. Prolonging death means prolonging suffering,not only for the infant, but also for the family and the membersof the staff.
In defining a poor outcome as death or the presence of a severeabnormality on cranial ultrasonography, we attempted to provideparents and obstetricians with more informative data than wouldbe gained merely from studying mortality rates for each gestationalage. Because the long-term developmental outcome of these infantsis not known, we evaluated predictors of outcome (i.e., measuresof chronic lung disease, retinopathy of prematurity, and intracranialpathology). As expected, these neonatal conditions were frequent,especially in the most immature infants. The mean duration ofmechanical ventilation and the mean length of the hospital staycompared favorably with the data reported by Nwaesei et al.5in infants born before 27 weeks' gestation, who received 50days of mechanical ventilation and who stayed 135 days in thehospital.
Because the incidence of major handicapping conditions is high(50 to 100 percent) in infants with severe abnormalities oncranial ultrasonography,15,16,17,18,19,20,21 we think our measureof poor outcome was appropriate. If we assume instead that disabilitywould develop in 60 percent of infants with severe ultrasonographicabnormalities, the results would still be discouraging: 93 percentof infants born at 23 weeks of gestation, 67 percent of thoseborn at 24 weeks, and 26 percent of those born at 25 weeks wouldhave poor outcomes.
In decisions about aggressive resuscitation for infants bornat 23 or 24 weeks of gestation, how much weight should the possibilityof a good outcome carry? During prenatal discussions of cesareansection, resuscitation, and surfactant administration, parentsdeeply committed to having children frequently hold onto evena small possibility of a good outcome. Parents are importantpartners in the decision-making process, but these discussionsare difficult in the delivery room.
These and other data suggest that we should define a limit ofviability, but is it enough to use criteria based on gestationalage, birth weight, or both? Should other factors, such as theparents' desires and history of fertility, the method of payment,the infant's sex, the response to resuscitation, and the findingson cranial ultrasonography, also be considered? Concern aboutlimited health care resources necessitates opening discussionsabout who should receive intensive care and how these decisionsshould be made.
Supported by the Thomas Wilson Sanitarium for the Children ofBaltimore City.
We are indebted to M. Douglas Jones, Jr., M.D., for his support.
Source Information
From the Department of Pediatrics, Johns Hopkins University School of Medicine (M.C.A., P.K.D.), and the Department of Pediatric Nursing, Johns Hopkins Hospital (A.E.D.), both in Baltimore.
Address reprint requests to Dr. Allen at the Johns Hopkins Hospital, CMSC 210, 601 N. Wolfe St., Baltimore, MD 21287-3200.
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600 vs. >600 g), gestational age (
