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The incidence of cerebral palsy
CLINICAL SECTION Clinical Opinion The incidence of cerebral palsy Mortimer G. Rosen, MD, and Janet C. Dickinson, BSN , MSW New York, Ne w York The clinician is often held responsible for obstetric events that are suspected of being related to cerebral palsy. To review the incidence of cerebral palsy and to aid the clinician in this situation, a search of published studies was conducted . Composite rates of cerebral palsy in different birth weight infants and cerebral palsy with and without serious mental retardation were calculated . The cumulative incidence rate at the age of 5 to 7 years was 2.7 cases of cerebral palsy for 1000 birth cohorts. Approximately 36% of all cerebral palsy occurred in the infant < 2500 gm. Serious mental retardation (intelligence quotient < 50) accompanied cerebral palsy approximately 30% of the time for the term infant and 18% of the time when the infant was < 2500 gm. On the basis of a past estimation that 70% of cerebral palsy is of antepartum or unknown origin, the term infant at risk for intrapartum-attributed cerebral palsy may be about 1 in 2000 term births. (AM J OBST8 GVNECOL 1992;167:417-23.)
Key words: Cer ebral palsy, incidence , mental re ta rdation Cerebra l pa lsy continues to pose a diagnostic and therapeutic d ilemma for the obstetrician beca use its various causes are poorl y u nd erstood . Electronic fetal monito ring, init iated in the ea rl y 1960s , raised hopes tha t some cases of cerebral pa lsy cou ld be p reve nted through a better mean s of eva luation of the fetus du ring labor. T od ay, studies continue to find a lack of associat ion between intrap art um fetal monitor ing and lon g-term neurologic outcome. ' Co n fou nding the incide nce issue is the fact that obs tetric p ractices and ne onatal intensive care have changed . With increased infant survival, increased ne urologic morbid ity may occu r mor e frequen tly, offsetting the overall effects of clinical practice changes! This review attem pted to evaluate current morbidit y data with res pect to the rates of cerebral palsy. Past stu d ies have genera lly found a prevalence rate of abo ut 2 per 1000 livin g infants at 7 to 10 years o f age, with ser ious mental retardation (in tellige nce quotient [IQ] < 50 ) present in 20 % to 30 % of these children.' The lar gest United States study, th e Co llaborative Perinatal Project, foun d a cerebra l pa lsy cumulative incidence ra te (which includes children with cerebral palsy who died) of 4.6 per 1000 of infants at 7 years of age! The question raise d in this review was whether th e cumuFrom the Department of Obstetrics and Gynecology, Sloane H ospital f or Women of Columbia Presbyterian M edical Center and the College of Physicians and Surgeons of Columbia University. R eprints not available.
611137971
lative incid ence of cerebral palsy has changed d uring the past 10 years, specifica lly the cu mulative incid ence in the term infant.
Methods A Med line search was conducted of all original En glish langua ge studies pu blished since 1980, with major in fa nt neu rologic damage as an end point. Unfortunatel y, although these stu dies were p ublished since 19 80, the birth dates of th e pop ulation s often went back to the 1950s. Few re cent stu d ies of the combination of mental re tard ation and cerebral pa lsy were found ; therefore studies conducted before 1980 were included when that aspect is discussed . Where poss ible, in some of the tables the birth d ates were indicated ra ther than the publicatio n d ates of the stud ies, so that the reader could consi der the possible differences in ne on atal care in the d ifferent tim e pe riods. To be includ ed in ana lyses, studies had to provide adequate raw n umbers to determine the denominator for th e rates of cerebral pa lsy either in the total population or by birth weight. Cu mu lative inciden ce at the age of 4 to 7 years was used beca use it pro vide s more information th an either a straight incidence or prevale nce rate. The cu mulative incidence rate use d all bir ths during a set period of time as the denomina tor , and n ume rator included infants with cerebral palsy who had die d . Including infants who had died has been recommended to provide as com plete a picture of cere bral palsy as possible." Prevalence ra te was not used,
417
418
Rosen and Dickinson
August 1992 Am J Obstet Gyne col
Table I. Cu mulative inciden ce of cerebral palsy per 1000 live births Study
y ear pu blished
Birth years
Country
Length of foll ow-up (yr)
R ate, excluding acquired (per 1000)
J arvis et al.? Nelson and Ellenberg" Emond et al. 10 Hagberg et al."t Holst et al.[. Dowding and Barry[3t Stanley and Watson" Riikonen et al." T or fs et al." Pharoah et al. [7 Meberg" Composite rate
1985 1986 1989 1989 1989 1988 1988 1989 1990 1990 1990
1972-197 5 1959-1966 1970 1979-1982 1978 1979-1981 1979-1981 1978-1982 1959-19 66 1984 1980-1984
Eng land Unite d States* En gland Sweden Denmark Irel and West Australia Finland California Eng land Norw ay
5 7 7 4 4 4 5 5 5 5 4
1.8 4.6 2.5 2.2 4.9 1.9 2.3 2.5 2.0§ 1.9 2.1 2.7
*Collaborative Perinatal Projec t. t Exciuded deaths before age 2. t Exciuded all congenital anom alies. §Did not indicate whether deaths were included.
because it can var y tremendousl y depending on the age of diagnosis and the len gth of time of survival. In the ColIaborative Perinatal Proj ect 15% of the children diagnosed with cerebral pals y at 12 months had died by the age of 7 years."" Studies with folIow-up at different ages, between 4 and 7 years, were qualified by stating the different ages. Cases of cerebral palsy th at were obviously cau sed post natalIy were excluded. Studies usualI y did not differentiate cerebral palsy by degree of handicap, so a stu dy's diagnosis of cerebral palsy was accepted. Figures fro m the Collaborative Perinatal Project were included to provide comparisons and becaus e that study constituted a large and essentially singular United States cerebral palsy incidence study. The figures from th e Collaborative Perinatal Project included both infants who had a diagnosis of cerebral palsy who had died and cases of cerebral palsy th at the y defined as mild (not requiring bracing, wheelchair, etc .)" because we decided th at their "mild" category would be included in alI cases of cerebra l palsy in other studies. We primarily used later published reports abou t the ColIaborative Perinat al Project because thes e categories were included. Earlier reports that excluded de aths and "mild" cerebral palsy yielded a 2.5 per 1000 rate." For types of cerebral palsy, the denominator is alI cases of cerebral palsy. When discussing the different types of cerebral palsy, th e most frequently used categories of cerebral palsy included diplegia (or paraplegia), a form of cerebral palsy where the legs are pri maril y affected ; hemiplegia, where onl y one side of the body is affected ; and quadriplegia (or tetraplegia), where three or all four limbs are affected . Extrapyramidal (or dyskinetic) cerebral palsy, including choreoathetotic and dysto nic and ataxia, was included as much as possib le whe n stu dies had th is as a distinct category.
The anal yses of cerebral palsy by birth weight were done with live births at that birth weight as denominators . Because studies used either cerebral pals y or mental retardation as starting points, both types of stud ies were considered. Howe ver , when considering studies using mental retardation as the starting point, th e primary focus was that proportion of the mentally retarded who also had cerebral palsy. Mental retardation not associated with cerebral palsy was not reviewed. Results
Excluding cases that had an obvious postnatal origin, 10 studies published since 1980 determined the cumu lative incidence rates for cerebral palsy,,"'-17 (Table I). The average cumulative incidence rate of these studies was 2.7 per 1000 livebirths. Table II describes studies that included the breakdown by type of cerebral palsy.B,9,I[.l3,17-19Years of birth, not publication, are given. Not alI the previously discussed studies were included, because not all had breakdown by type of cerebral palsy. The avera ge proportion s of the different types of cerebral palsy of all with cerebral palsy were 34% diplegia, 30 % hemiplegia, 20 % qu adriplegia, and 16% extrap yramidal. Table III includes studies that grouped cerebral palsy by birth weight." 4, s, H-17, 20 Years of birth, rather than dates of publication, are indicated for the reasons previously stated. The average pr op ortions of cerebral palsy by birth weight of all children with cerebral palsy were 36% for those weighing <2500 gm and 64% for children weighing > 2499 gm . Some of these studies an alyzed cerebral palsy rates by smaller increments of birth weight" [I , [ 3 , 14 , [6 , [ 7 (Table IV) . The increments varied too much to do an exact comparison, but the figures are helpful to determine any trends in the incidence by birth weight.
Incidence of cerebral palsy 419
Volume 167 Number 2
Table II. Distribution of cerebral palsy by type* Study
Nelson and Ellenberg"] Pharoah et aLI7 Dowding and Barry" Dale and Stanley'? Riikonen et al. 15 Hagberg et al. 11 Jarvis et al." Composite rates
Country
1959-1966 1984 1979-1981 1971-1975 1978-1982 1979-1982 1972-1975
United States England Ireland Australia Finland Sweden England
Hemiplegia (%)
Quadriplegia (%)
Extrapyramidal (%)
29 40 25 22 29 36 29 30
24 27 10 32 3:j: 7:j: 39 20
14 11 27 5 24 15 9 16
32 24 38 39 44 41 l8§ 34
*Denominators are all cases of cerebral palsy. Rows may not total 100% because some types of cerebral palsy were excluded. tBased on survivors. :j:Used term tetraplegia. §Used term paraplegia.
Table III. Distribution of cerebral palsy by birth weight* Country
<2500 gm (%)
>2499 gm (%)
Overalliow-birth-weight births (%)
United Statest England West Australia Denmark England Norway Sweden Ireland Finland Japan California
33 47 32 40 26 27 38 32 52 52 17 36
67 53 68 60 74 73 62 68 49 48 83 64
9.2 6.7
Study
Nelson and Ellenberg" Pharoah et aLI7 Stanley and Watsonl 4 Holst et aLI2 Jarvis et al. 9 Meberg'"
Hagberg et al. II Dowding and Barry" Riikonen et al. 15 Saito et aL20 Torfs et al." Composite rates
1959-1966 1984 1979-1981 1978 1972-1975 1980-1984 1979-1982 1979-1981 1978-1982 1963-1976 1959-1966
4.1:j:
3.5
7.0 4.2 4.0 5.1 4.0 4.5 6.8 5.3
*Denominator is cases of cerebral palsy. tCollaborative Perinatal Project. :j:Figure from Dale et al, 19 Some studies analyzed trends of cumulative incidences of cerebral palsy over periods of time"!': 13-17. 19 (Fig. 1). Some studies found recent minor decreases, others found almost no change in rate, and other studies found recent minor increases. When there was a minor increase, the type of cerebral palsy that increased the most was diplegia or cerebral palsy among lowbirth-weight (LBW) infants. A few studies analyzed the occurrence of serious mental retardation among children with cerebral palsy. Table V provides the figures from those studies. 18.21. 22 The average rate of serious mental retardation (IQ <50) along with cerebral palsy for all birth weights was 25%, 18% for infants weighing <2500 gm, and 30% for those >2499. A few studies analyzed the occurrence of cerebral palsy among children with serious mental retardation.":" These figures are based on children surviving at the time of the study (prevalence). The composite rate for the studies of all cases of mental retardation with cerebral palsy was 16.8% (Table VI). McLaren and Bryson" reviewed studies for the presence of cerebral palsy in the seriously mentally retarded. They encountered difficulties due to differences in methodology and
a frequent lack of differentiation between disorders; for example, neurologic, motor, and sensory disorders may have been combined. Four studies were sufficiently specific enough to be analyzed.v" Kielv" analyzed two other studies'";" for the occurrence of cerebral palsy in populations with serious mental retardation. Because of methodologic differences used in the studies, this composite rate should be considered as an approximation. Comment
One task in standardizing studies was to consider when the follow-up was done and when the diagnosis of brain damage was made. Nelson and Ellenberg" 7 pointed out the difficulty of comparing studies because of the variation in timings of follow-up. Studies generally grouped all degrees of cerebral palsy together; however; milder cases often were not known until the child entered school and as many as 50% of patients diagnosed at 12 months were free of motor handicap at 7 years of age. A cumulative incidence rate addresses the problem of loss of cases through deaths. There was a problem with the lack of data on births that occurred in the past 10 years. The only reviewed
420
Rosen and Dickinson
August 1992
Am
J Obstet Gynecol
Table IV. Rate of cerebral palsy by birth weight (per 1000) Study
Rate in infants <1000 gm
Dowding and Barry" Meberg'" Hagberg" Jarvis et al.9 Pharoah et al. 17 Stanley and Watson 14
20.2
Rate in infants 1000-1499 gm
Rate in infants 1500-1999 gm
Rate in infants 2000-2499 s»
46.7 13* 90* 3.5* 44* 26.9*
15.7
3.2 14* 6 7.4* 9.7* 8
30 17.2
*Includes the lower-birth-weight group.
Table V. Percentages of serious mental retardation (IQ <50) in cases of cerebral palsy by birth weight*
Country
(%)
Rate of serious mental retardation in <2500 gm with cerebral palsy (%)
United Statest Sweden England
26 14 36 25
15 13 27 18
Rate in all weights Study
Age (yr)
Nelson and Broman" Hagberg et al." Pharoah et al. IB Composite rate
7 4
5 (mean)
Rate of serious mental retardation in >2499 gm with cerebral palsy (%)
33 16 40 30
*Includes infants or children who died (cumulative incidence). tCollaborative Perinatal Project.
Table VI. Percentage of cerebral palsy in those with serious mental retardation (IQ <50)*
Study
McQueen et al." Jacobsen and janicki" Gustavson et al." Mclfonald'" Oregon State Board of Health 27 Drillien et al. 2Bt Composite rate
Age (yr)
With cerebral palsy in serious mental retardation Country or state population (%)
7-10
Canada New York
15.4 15.8
5-16 10
<20
Sweden Quebec Oregon
18.6 12.8 15.8
7.5-14.5
Scotland
22.9 1,6.8
<21
*Surviving at time of study. tIQ <55.
studies where births did occur solely in the 1980s were the Meberg study" and the Pharoah et al." studies. Some studies, published quite recently, were based on births from as far back as the 1960s or earlier, before the use of neonatal intensive care and before the means were established to prevent erythroblastosis fetalis. With the advent of neonatal intensive care units in the 1970s, the survival of very-low-birth-weight infants has improved. The average survival rate beyond the neonatal period for the <1500-gm infant in developed countries was 15% to 40% in the early 1970s and 60% to 75% in the mid-1980s. 31 Although there is concern that, with this increased survival, the incidence of ce-
rebral palsy among LBW infants has increased, we found the rate to be fairly stable at about 15 per 1000 LBW births «2500 gm) since the 1950s (Fig. 1). For the very-low-birth-weight infant « 1500 gm) this rate is higher. Studies found rates of cerebral palsy of 13 to 90 per 1000 for neonatal survivors of 500 to 1500 gm at birth (Table IV). Other studies have had findings of a stable rate of neurologic impairment along with an increased survival rate for very-low-birth-weight babies. A review by Hagberg et at. '2 found that where a country had a higher perinatal mortality rate to begin with and a greater drop in perinatal mortality rate with the advent of improved neonatal care, the rate of cerebral palsy did not increase noticeably. However, when the rate was lower to begin with and neonatal care has been used with increasingly smaller babies, the cerebral palsy rate has increased to a greater extent. The implication is that babies who have needed minimal to moderate improved neonatal care to survive tend to have low morbidity, whereas the much smaller babies who need intensive, long-term care to survive are more likely to have permanent neurologic problems. Hagberg et aJ.32 sees a 40 times higher live-birth prevalence of cerebral palsy in the very-low-birth-weight infant than in the normal-birth-weight infant. One problem we encountered was the cutoff point for LBW babies. Some studies included the 2500 gm infant in the LBW group and others did not. This discrepancy could significantly change the final figure. Another problem was the interchangeable use of the terms LBW and preterrn." With these problems, the figures on cerebral palsy by birth weight are a close approximation of cerebral palsy by birth weight. An average
Incidence of cerebral palsy 421
Volume 167 Number 2
3.5 .----------------------~ 3
2.5
- - - - - - - - - - - - -
- - - - -
1.5 '- - - - - - - - - . . . . 1
0.5
-
.
_
-
- -
- . -. -
- .. -
OL..-_--J._ _--J.._ _...I-_ _..I...-_ _L-.-_--l._ _--L_---I
1950
1970
1960
1980
9RUKDNEN (FINLAND)
+EUOND*(ENGLAND)
"STANLEY (W. AUST)
.JARVIS (ENGLAND)
*UEBERG (NORWAY)
.PHAROAH (ENGLAND) .HAGBERG (SWEDEN) -DOWDING (IRELAND)
35 r - - - - - - - - - - - - - - - - - - - - - - - - , 30 ~25
'"
- ... - ... - -
. - - ..... - ..... - .... - - ..
---. ---------. ------. -----. -----
20 -"
-- ... - ... -
15
5
. - - . - - ... _ ..
~ ~ ~ ~ ~ . . . -_ . . -
-"'-
O'--_---L.-_--JL--_-L-_----l._ _- L - _ - - L_ _...L.-_---.l
1950
1960
.. DALE (W. AUST) • EMOND* (ENGLAND)
1970
1980
* PHAROAH (ENGLAND) B RIIKONEN (FINLAND)
* MEBERG (NORWAY)
~ DOWDING (IRELAND)
Fig. 1. Rates of cerebral palsy for all birth weights per 1000 live births (tojJ) and per 1000 live births <2500 gm (bollom). Asterisk, Neonatal survivors.
of 36% of all cerebral palsy occurred in the LBW population. Therefore approximately 5.3% of the birth population contributed 36% of the cases of cerebral palsy. When studies providing cerebral palsy rates over periods of time are considered, the rate for infants weighing >2499 gm was stable at 1 to 1.5 per 1000 births of infants of that birth weight. Our composite figure, which includes more studies, was 1.8. There appeared to be some consistency in the rates
of cerebral palsy for the different birth weights, so one would think that overall rates could be tentatively extrapolated on the basis of a combination of the LBW rate, which is higher in the United States and has remained relatively unchanged at about 6.8%,33 and the survival of these infants. Because the percentage of LBW infants varies from country to country, we would then expect the percentage of cerebral palsy occurring ing FHR l3-sympathetic and parasympathetic tone, re-
422 Rosen and Dickinson
in different birth weights to vary in a similar fashion. However, this was not the case. Other variables seemed to be involved. Besides the socioeconomic and ethnic compositions of the population that appear to be associated with LBW, one also needs to consider health policies in and within different countries concerning access to prenatal care and the resuscitation and treatment of very small newborns. As early as 1897, Freud noted that there appeared to be different types of cerebral palsy that probably had different origins, so they should be studied separately. Others have reiterated this message more recently. 18 Birth weights and types of cerebral palsy seem to be intertwined so it is difficult to discuss one without discussing the other. Diplegia, which occurs more often among infants of LBW, was 34% of all cerebral palsy cases, whereas LBW infants were 36% of all cases of cerebral palsy (although these two do not completely overlap). The rates of serious mental retardation (IQ <50) occurring along with cerebral palsy also differed by birth weight. The composite rate of serious mental retardation in those with cerebral palsy was 25% for all birth weights, 18% for LBW, and 30% for those weighing >2499 gm. Therefore 75% of all children with cerebral palsy have IQs >50 with most of those having IQs >70, and the occurrence of serious mental retardation is more common with the normal-birth-weight infants who have cerebral palsy. Among all infants with serious mental retardation, the rate of cerebral palsy was approximately 16.8%. However, the sources of the populations for this last figure need to be considered. Many of these studies were based on institutionalized populations. Also, because these studies were based on survivors, it underestimates the overall incidence. Thus we may estimate that intrapartum cause for cerebral palsy is <0.5 per 1000 term births and that active prevention for those infants awaits better understanding of cause of the disease, because the usual monitoring methods in labor do not allow for that diagnosis.' It is more probable that understanding and preventing premature birth and better means of antepartum surveillance are more likely to contribute to the prevention of cerebral palsy. To the obstetrician the incidence of cerebal palsy has major clinical meaning. It is clear that the target population for cerebral palsy still hovers at about 2.7 per 1000 live births at 4 to 10 years of age. About 36% of cerebral palsy will have origins in infants weighing <2500 gm, with increasing risk for cerebral palsy with each decrement in infant birth weight. The emphasis in research should be on finding causes of and solutions for early prenatal problems that contribute to births at very low weights, to births of small-for-gestational-age infants, and to births of otherwise prenatally damaged
August 1992 Am J Obstet Gynecol
infants. Tort reform needs to acknowledge these unknowns in the etiology of cerebral palsy, so the clinician can be enabled to practice his or her best without having to do so defensively. In the term infant the incidence of cerebral palsy will be about 1.8 per 1000 of children with that birth weight. Thus the target for more than 90% of all deliveries is small. It is also important to understand that past estimates of origins of cerebral palsy for term infants are divided into perinatal (25% to 30%) causes and the remainder probably prenatal or unknown causes. A portion of those with perinatal causes will be intrapartum causes. REFERENCES 1. Grant A, Joy M, O'Brien N, Hennessey E, MacDonald D. Cerebral palsy among children born during the Dublin randomised trial of intrapartum monitoring. Lancet 1989;2: 1233-6. 2. Torfs CP, Vanden Berg BJ, Oechsli FW, Cummins S. Prenatal and perinatal factors in the etiology of cerebral palsy. J Pediatr 1990;116:615-9. 3. FreemanJM, ed. Prenatal and perinatal factors associated with brain disorders. Hyattsville, Maryland: National Institutes of Health, 1985, NIH publication no 85-1149. 4. Nelson KB, Ellenberg JH. Antecedents of cerebral palsy. Multivariate analysis of risks. N Engl J Med 1986;315: 81-6. 5. Paneth N, Kiely J. The frequency of cerebral palsy: a review of population studies in industrialized nations since 1950. In: Stanley F, Alberman E, eds. The epidemiology of cerebral palsy. London: Spastic International Medical, 1984. 6. Nelson KB, Ellenberg JH. Obstetric complications as risk factors for cerebral palsy or seizure disorders. JAMA 1984;251: 1843-8. 7. Nelson KB, Ellenberg JH. Children who "outgrew" cerebral palsy. Pediatrics 1982;69:529-36. 8. Nelson KB, EllenbergJH. Epidemiology of cerebral palsy. Adv Neurol 1978;19:421-35. 9. Jarvis SN, Holloway JS, Hey EN. Increase in cerebral palsy in normal birthweight babies. Arch Dis Child 1985;60:1113-21. 10. Emond A, Golding J, Peckham C. Cerebral palsy in two national cohort studies. Arch Dis Child 1989;64:848-52. 11. Hagberg B, Hagberg G, Olow I, Von Wendt L. The changing panorama of cerebral palsy in Sweden. V. The birth year period 1979-82. Acta Pediatr Scand 1989;78:283-90. 12. Holst K, Andersen E, Philip J, Hennigsen I. Antenatal and perinatal conditions correlated to handicap among 4year-old children. Am J Perinatol 1989;6:258-67. 13. Dowding VM, Barry C. Cerebral palsy: changing patterns of birthweight and gestational age (1976/81). Irish Med J 1988;81:25-8. 14. Stanley FJ, Watson L. The cerebral palsies in Western Australia: trends, 1968-81. AM J OBSTET GVNECOL 1988;158:89-93. 15. Riikonen R, Raumavirta S, Sinivuori E, Seppala T. Changing pattern of cerebral palsy in the southwest region of Finland. Acta Pediatr Scand 1989;78:581-7. 16. Meberg A. Declining incidence of low birth weight-impact on perinatal mortality and incidence of cerebral palsy. J Perinatol Med 1990;18:195-200. 17. Pharoah POD, Cooke T, Cooke RWI, Rosenbloom L. Birthweight specific trends in cerebral palsy. Arch Dis Child 1990;65:602-6. 18. Pharoah POD, Cooke T, Rosenbloom L, Cooke RWI. Effects of birth weig-ht, g-estational age, and maternal ob-
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19.
20. 21. 22. 23.
24. 25.
stetric history on birth prevalence of cerebral palsy. Arch Dis Child 1987;62: 1035-40. Dale A, Stanley FJ. An epidemiological study of cerebral palsy in Western Australia, 1956-75. II. Spastic cerebral palsy and perinatal factors. Dev Med Child Neurol 1980;22: 13-25. Saito T, Fujii T, Tango T. Prediction of the development of cerebral palsy from perinatal risk factors. Brain Dev 1983;5:1-8. Nelson KB, Broman SH. Perinatal risk factors in children with serious motor and mental handicaps. Ann Neurol 1977;2:371-7. Hagberg B, Hagberg G, Olow I. The changing panorama of cerebral palsy in Sweden. IV. Epidemiologic trends 1959-1978. Acta Pediatr Scand 1984;73:433-40. McQueen PC, Spence MW, Garner JB, Pereira LH, Winsor EJT. Prevalence of major mental retardation and associated disabilities in the Canadian Maritime Provinces. AmJ Ment Def 1987;91:460-6. Jacobson JW, Janicki MP. Observed prevalence of multiple developmental disabilities. Ment Retardation 1983;21:87-94. Gustavson KH, Holmgren G, Jonsell R, Son Blomquist HK. Severe mental retardation in children in a northern Swedish county. .I Ment Def Res 1977;21:161-81.
Incidence of cerebral palsy 423
26. McDonald AD. Severely retarded children in Quebec: prevalences, causes, and care. Am .I Ment Def 1973;78:205-15. 27. Oregon State Board of Health. Mental retardation prevalence in Oregon. Portland, Oregon: Publication of the Oregon State Board of Health, 1962. 28. Drillien CM, Jameson S, Wilkinson EM. Studies in mental handicap. I. Prevalence and distribution by clinical type and severity of defect. Arch Dis Child 1966;41 :528-38. 29. McLaren .I, Bryson SE. Review of recent epidemiological studies of mental retardation: prevalence, associated disorders, and etiology. AmJ Ment Retard 1987;92:243-54. 30. Kiely M. The prevalence of mental retardation. Epidemiol Rev 1987;9:194-218. 31. Heinonen K, Hakulinen A, .Iokela V. Survival of the smallest. Lancet 1988;2:204-6. 32. Hagberg B, Hagberg G, Zetterstrom R. Decreasing perinatal mortality-increase in cerebral palsy morbidity? Acta Pediatr Scand 1989;78:664-70. 33. United States Department of Health and Human Services. Health status of minorities and low-income groups. 3rd ed. Hyattsville, Maryland: USDHHS, 1991:108.
Key words: Cer ebral palsy, incidence , mental re ta rdation Cerebra l pa lsy continues to pose a diagnostic and therapeutic d ilemma for the obstetrician beca use its various causes are poorl y u nd erstood . Electronic fetal monito ring, init iated in the ea rl y 1960s , raised hopes tha t some cases of cerebral pa lsy cou ld be p reve nted through a better mean s of eva luation of the fetus du ring labor. T od ay, studies continue to find a lack of associat ion between intrap art um fetal monitor ing and lon g-term neurologic outcome. ' Co n fou nding the incide nce issue is the fact that obs tetric p ractices and ne onatal intensive care have changed . With increased infant survival, increased ne urologic morbid ity may occu r mor e frequen tly, offsetting the overall effects of clinical practice changes! This review attem pted to evaluate current morbidit y data with res pect to the rates of cerebral palsy. Past stu d ies have genera lly found a prevalence rate of abo ut 2 per 1000 livin g infants at 7 to 10 years o f age, with ser ious mental retardation (in tellige nce quotient [IQ] < 50 ) present in 20 % to 30 % of these children.' The lar gest United States study, th e Co llaborative Perinatal Project, foun d a cerebra l pa lsy cumulative incidence ra te (which includes children with cerebral palsy who died) of 4.6 per 1000 of infants at 7 years of age! The question raise d in this review was whether th e cumuFrom the Department of Obstetrics and Gynecology, Sloane H ospital f or Women of Columbia Presbyterian M edical Center and the College of Physicians and Surgeons of Columbia University. R eprints not available.
611137971
lative incid ence of cerebral palsy has changed d uring the past 10 years, specifica lly the cu mulative incid ence in the term infant.
Methods A Med line search was conducted of all original En glish langua ge studies pu blished since 1980, with major in fa nt neu rologic damage as an end point. Unfortunatel y, although these stu dies were p ublished since 19 80, the birth dates of th e pop ulation s often went back to the 1950s. Few re cent stu d ies of the combination of mental re tard ation and cerebral pa lsy were found ; therefore studies conducted before 1980 were included when that aspect is discussed . Where poss ible, in some of the tables the birth d ates were indicated ra ther than the publicatio n d ates of the stud ies, so that the reader could consi der the possible differences in ne on atal care in the d ifferent tim e pe riods. To be includ ed in ana lyses, studies had to provide adequate raw n umbers to determine the denominator for th e rates of cerebral pa lsy either in the total population or by birth weight. Cu mu lative inciden ce at the age of 4 to 7 years was used beca use it pro vide s more information th an either a straight incidence or prevale nce rate. The cu mulative incidence rate use d all bir ths during a set period of time as the denomina tor , and n ume rator included infants with cerebral palsy who had die d . Including infants who had died has been recommended to provide as com plete a picture of cere bral palsy as possible." Prevalence ra te was not used,
417
418
Rosen and Dickinson
August 1992 Am J Obstet Gyne col
Table I. Cu mulative inciden ce of cerebral palsy per 1000 live births Study
y ear pu blished
Birth years
Country
Length of foll ow-up (yr)
R ate, excluding acquired (per 1000)
J arvis et al.? Nelson and Ellenberg" Emond et al. 10 Hagberg et al."t Holst et al.[. Dowding and Barry[3t Stanley and Watson" Riikonen et al." T or fs et al." Pharoah et al. [7 Meberg" Composite rate
1985 1986 1989 1989 1989 1988 1988 1989 1990 1990 1990
1972-197 5 1959-1966 1970 1979-1982 1978 1979-1981 1979-1981 1978-1982 1959-19 66 1984 1980-1984
Eng land Unite d States* En gland Sweden Denmark Irel and West Australia Finland California Eng land Norw ay
5 7 7 4 4 4 5 5 5 5 4
1.8 4.6 2.5 2.2 4.9 1.9 2.3 2.5 2.0§ 1.9 2.1 2.7
*Collaborative Perinatal Projec t. t Exciuded deaths before age 2. t Exciuded all congenital anom alies. §Did not indicate whether deaths were included.
because it can var y tremendousl y depending on the age of diagnosis and the len gth of time of survival. In the ColIaborative Perinatal Proj ect 15% of the children diagnosed with cerebral pals y at 12 months had died by the age of 7 years."" Studies with folIow-up at different ages, between 4 and 7 years, were qualified by stating the different ages. Cases of cerebral palsy th at were obviously cau sed post natalIy were excluded. Studies usualI y did not differentiate cerebral palsy by degree of handicap, so a stu dy's diagnosis of cerebral palsy was accepted. Figures fro m the Collaborative Perinatal Project were included to provide comparisons and becaus e that study constituted a large and essentially singular United States cerebral palsy incidence study. The figures from th e Collaborative Perinatal Project included both infants who had a diagnosis of cerebral palsy who had died and cases of cerebral palsy th at the y defined as mild (not requiring bracing, wheelchair, etc .)" because we decided th at their "mild" category would be included in alI cases of cerebra l palsy in other studies. We primarily used later published reports abou t the ColIaborative Perinat al Project because thes e categories were included. Earlier reports that excluded de aths and "mild" cerebral palsy yielded a 2.5 per 1000 rate." For types of cerebral palsy, the denominator is alI cases of cerebral palsy. When discussing the different types of cerebral palsy, th e most frequently used categories of cerebral palsy included diplegia (or paraplegia), a form of cerebral palsy where the legs are pri maril y affected ; hemiplegia, where onl y one side of the body is affected ; and quadriplegia (or tetraplegia), where three or all four limbs are affected . Extrapyramidal (or dyskinetic) cerebral palsy, including choreoathetotic and dysto nic and ataxia, was included as much as possib le whe n stu dies had th is as a distinct category.
The anal yses of cerebral palsy by birth weight were done with live births at that birth weight as denominators . Because studies used either cerebral pals y or mental retardation as starting points, both types of stud ies were considered. Howe ver , when considering studies using mental retardation as the starting point, th e primary focus was that proportion of the mentally retarded who also had cerebral palsy. Mental retardation not associated with cerebral palsy was not reviewed. Results
Excluding cases that had an obvious postnatal origin, 10 studies published since 1980 determined the cumu lative incidence rates for cerebral palsy,,"'-17 (Table I). The average cumulative incidence rate of these studies was 2.7 per 1000 livebirths. Table II describes studies that included the breakdown by type of cerebral palsy.B,9,I[.l3,17-19Years of birth, not publication, are given. Not alI the previously discussed studies were included, because not all had breakdown by type of cerebral palsy. The avera ge proportion s of the different types of cerebral palsy of all with cerebral palsy were 34% diplegia, 30 % hemiplegia, 20 % qu adriplegia, and 16% extrap yramidal. Table III includes studies that grouped cerebral palsy by birth weight." 4, s, H-17, 20 Years of birth, rather than dates of publication, are indicated for the reasons previously stated. The average pr op ortions of cerebral palsy by birth weight of all children with cerebral palsy were 36% for those weighing <2500 gm and 64% for children weighing > 2499 gm . Some of these studies an alyzed cerebral palsy rates by smaller increments of birth weight" [I , [ 3 , 14 , [6 , [ 7 (Table IV) . The increments varied too much to do an exact comparison, but the figures are helpful to determine any trends in the incidence by birth weight.
Incidence of cerebral palsy 419
Volume 167 Number 2
Table II. Distribution of cerebral palsy by type* Study
Nelson and Ellenberg"] Pharoah et aLI7 Dowding and Barry" Dale and Stanley'? Riikonen et al. 15 Hagberg et al. 11 Jarvis et al." Composite rates
Country
1959-1966 1984 1979-1981 1971-1975 1978-1982 1979-1982 1972-1975
United States England Ireland Australia Finland Sweden England
Hemiplegia (%)
Quadriplegia (%)
Extrapyramidal (%)
29 40 25 22 29 36 29 30
24 27 10 32 3:j: 7:j: 39 20
14 11 27 5 24 15 9 16
32 24 38 39 44 41 l8§ 34
*Denominators are all cases of cerebral palsy. Rows may not total 100% because some types of cerebral palsy were excluded. tBased on survivors. :j:Used term tetraplegia. §Used term paraplegia.
Table III. Distribution of cerebral palsy by birth weight* Country
<2500 gm (%)
>2499 gm (%)
Overalliow-birth-weight births (%)
United Statest England West Australia Denmark England Norway Sweden Ireland Finland Japan California
33 47 32 40 26 27 38 32 52 52 17 36
67 53 68 60 74 73 62 68 49 48 83 64
9.2 6.7
Study
Nelson and Ellenberg" Pharoah et aLI7 Stanley and Watsonl 4 Holst et aLI2 Jarvis et al. 9 Meberg'"
Hagberg et al. II Dowding and Barry" Riikonen et al. 15 Saito et aL20 Torfs et al." Composite rates
1959-1966 1984 1979-1981 1978 1972-1975 1980-1984 1979-1982 1979-1981 1978-1982 1963-1976 1959-1966
4.1:j:
3.5
7.0 4.2 4.0 5.1 4.0 4.5 6.8 5.3
*Denominator is cases of cerebral palsy. tCollaborative Perinatal Project. :j:Figure from Dale et al, 19 Some studies analyzed trends of cumulative incidences of cerebral palsy over periods of time"!': 13-17. 19 (Fig. 1). Some studies found recent minor decreases, others found almost no change in rate, and other studies found recent minor increases. When there was a minor increase, the type of cerebral palsy that increased the most was diplegia or cerebral palsy among lowbirth-weight (LBW) infants. A few studies analyzed the occurrence of serious mental retardation among children with cerebral palsy. Table V provides the figures from those studies. 18.21. 22 The average rate of serious mental retardation (IQ <50) along with cerebral palsy for all birth weights was 25%, 18% for infants weighing <2500 gm, and 30% for those >2499. A few studies analyzed the occurrence of cerebral palsy among children with serious mental retardation.":" These figures are based on children surviving at the time of the study (prevalence). The composite rate for the studies of all cases of mental retardation with cerebral palsy was 16.8% (Table VI). McLaren and Bryson" reviewed studies for the presence of cerebral palsy in the seriously mentally retarded. They encountered difficulties due to differences in methodology and
a frequent lack of differentiation between disorders; for example, neurologic, motor, and sensory disorders may have been combined. Four studies were sufficiently specific enough to be analyzed.v" Kielv" analyzed two other studies'";" for the occurrence of cerebral palsy in populations with serious mental retardation. Because of methodologic differences used in the studies, this composite rate should be considered as an approximation. Comment
One task in standardizing studies was to consider when the follow-up was done and when the diagnosis of brain damage was made. Nelson and Ellenberg" 7 pointed out the difficulty of comparing studies because of the variation in timings of follow-up. Studies generally grouped all degrees of cerebral palsy together; however; milder cases often were not known until the child entered school and as many as 50% of patients diagnosed at 12 months were free of motor handicap at 7 years of age. A cumulative incidence rate addresses the problem of loss of cases through deaths. There was a problem with the lack of data on births that occurred in the past 10 years. The only reviewed
420
Rosen and Dickinson
August 1992
Am
J Obstet Gynecol
Table IV. Rate of cerebral palsy by birth weight (per 1000) Study
Rate in infants <1000 gm
Dowding and Barry" Meberg'" Hagberg" Jarvis et al.9 Pharoah et al. 17 Stanley and Watson 14
20.2
Rate in infants 1000-1499 gm
Rate in infants 1500-1999 gm
Rate in infants 2000-2499 s»
46.7 13* 90* 3.5* 44* 26.9*
15.7
3.2 14* 6 7.4* 9.7* 8
30 17.2
*Includes the lower-birth-weight group.
Table V. Percentages of serious mental retardation (IQ <50) in cases of cerebral palsy by birth weight*
Country
(%)
Rate of serious mental retardation in <2500 gm with cerebral palsy (%)
United Statest Sweden England
26 14 36 25
15 13 27 18
Rate in all weights Study
Age (yr)
Nelson and Broman" Hagberg et al." Pharoah et al. IB Composite rate
7 4
5 (mean)
Rate of serious mental retardation in >2499 gm with cerebral palsy (%)
33 16 40 30
*Includes infants or children who died (cumulative incidence). tCollaborative Perinatal Project.
Table VI. Percentage of cerebral palsy in those with serious mental retardation (IQ <50)*
Study
McQueen et al." Jacobsen and janicki" Gustavson et al." Mclfonald'" Oregon State Board of Health 27 Drillien et al. 2Bt Composite rate
Age (yr)
With cerebral palsy in serious mental retardation Country or state population (%)
7-10
Canada New York
15.4 15.8
5-16 10
<20
Sweden Quebec Oregon
18.6 12.8 15.8
7.5-14.5
Scotland
22.9 1,6.8
<21
*Surviving at time of study. tIQ <55.
studies where births did occur solely in the 1980s were the Meberg study" and the Pharoah et al." studies. Some studies, published quite recently, were based on births from as far back as the 1960s or earlier, before the use of neonatal intensive care and before the means were established to prevent erythroblastosis fetalis. With the advent of neonatal intensive care units in the 1970s, the survival of very-low-birth-weight infants has improved. The average survival rate beyond the neonatal period for the <1500-gm infant in developed countries was 15% to 40% in the early 1970s and 60% to 75% in the mid-1980s. 31 Although there is concern that, with this increased survival, the incidence of ce-
rebral palsy among LBW infants has increased, we found the rate to be fairly stable at about 15 per 1000 LBW births «2500 gm) since the 1950s (Fig. 1). For the very-low-birth-weight infant « 1500 gm) this rate is higher. Studies found rates of cerebral palsy of 13 to 90 per 1000 for neonatal survivors of 500 to 1500 gm at birth (Table IV). Other studies have had findings of a stable rate of neurologic impairment along with an increased survival rate for very-low-birth-weight babies. A review by Hagberg et at. '2 found that where a country had a higher perinatal mortality rate to begin with and a greater drop in perinatal mortality rate with the advent of improved neonatal care, the rate of cerebral palsy did not increase noticeably. However, when the rate was lower to begin with and neonatal care has been used with increasingly smaller babies, the cerebral palsy rate has increased to a greater extent. The implication is that babies who have needed minimal to moderate improved neonatal care to survive tend to have low morbidity, whereas the much smaller babies who need intensive, long-term care to survive are more likely to have permanent neurologic problems. Hagberg et aJ.32 sees a 40 times higher live-birth prevalence of cerebral palsy in the very-low-birth-weight infant than in the normal-birth-weight infant. One problem we encountered was the cutoff point for LBW babies. Some studies included the 2500 gm infant in the LBW group and others did not. This discrepancy could significantly change the final figure. Another problem was the interchangeable use of the terms LBW and preterrn." With these problems, the figures on cerebral palsy by birth weight are a close approximation of cerebral palsy by birth weight. An average
Incidence of cerebral palsy 421
Volume 167 Number 2
3.5 .----------------------~ 3
2.5
- - - - - - - - - - - - -
- - - - -
1.5 '- - - - - - - - - . . . . 1
0.5
-
.
_
-
- -
- . -. -
- .. -
OL..-_--J._ _--J.._ _...I-_ _..I...-_ _L-.-_--l._ _--L_---I
1950
1970
1960
1980
9RUKDNEN (FINLAND)
+EUOND*(ENGLAND)
"STANLEY (W. AUST)
.JARVIS (ENGLAND)
*UEBERG (NORWAY)
.PHAROAH (ENGLAND) .HAGBERG (SWEDEN) -DOWDING (IRELAND)
35 r - - - - - - - - - - - - - - - - - - - - - - - - , 30 ~25
'"
- ... - ... - -
. - - ..... - ..... - .... - - ..
---. ---------. ------. -----. -----
20 -"
-- ... - ... -
15
5
. - - . - - ... _ ..
~ ~ ~ ~ ~ . . . -_ . . -
-"'-
O'--_---L.-_--JL--_-L-_----l._ _- L - _ - - L_ _...L.-_---.l
1950
1960
.. DALE (W. AUST) • EMOND* (ENGLAND)
1970
1980
* PHAROAH (ENGLAND) B RIIKONEN (FINLAND)
* MEBERG (NORWAY)
~ DOWDING (IRELAND)
Fig. 1. Rates of cerebral palsy for all birth weights per 1000 live births (tojJ) and per 1000 live births <2500 gm (bollom). Asterisk, Neonatal survivors.
of 36% of all cerebral palsy occurred in the LBW population. Therefore approximately 5.3% of the birth population contributed 36% of the cases of cerebral palsy. When studies providing cerebral palsy rates over periods of time are considered, the rate for infants weighing >2499 gm was stable at 1 to 1.5 per 1000 births of infants of that birth weight. Our composite figure, which includes more studies, was 1.8. There appeared to be some consistency in the rates
of cerebral palsy for the different birth weights, so one would think that overall rates could be tentatively extrapolated on the basis of a combination of the LBW rate, which is higher in the United States and has remained relatively unchanged at about 6.8%,33 and the survival of these infants. Because the percentage of LBW infants varies from country to country, we would then expect the percentage of cerebral palsy occurring ing FHR l3-sympathetic and parasympathetic tone, re-
422 Rosen and Dickinson
in different birth weights to vary in a similar fashion. However, this was not the case. Other variables seemed to be involved. Besides the socioeconomic and ethnic compositions of the population that appear to be associated with LBW, one also needs to consider health policies in and within different countries concerning access to prenatal care and the resuscitation and treatment of very small newborns. As early as 1897, Freud noted that there appeared to be different types of cerebral palsy that probably had different origins, so they should be studied separately. Others have reiterated this message more recently. 18 Birth weights and types of cerebral palsy seem to be intertwined so it is difficult to discuss one without discussing the other. Diplegia, which occurs more often among infants of LBW, was 34% of all cerebral palsy cases, whereas LBW infants were 36% of all cases of cerebral palsy (although these two do not completely overlap). The rates of serious mental retardation (IQ <50) occurring along with cerebral palsy also differed by birth weight. The composite rate of serious mental retardation in those with cerebral palsy was 25% for all birth weights, 18% for LBW, and 30% for those weighing >2499 gm. Therefore 75% of all children with cerebral palsy have IQs >50 with most of those having IQs >70, and the occurrence of serious mental retardation is more common with the normal-birth-weight infants who have cerebral palsy. Among all infants with serious mental retardation, the rate of cerebral palsy was approximately 16.8%. However, the sources of the populations for this last figure need to be considered. Many of these studies were based on institutionalized populations. Also, because these studies were based on survivors, it underestimates the overall incidence. Thus we may estimate that intrapartum cause for cerebral palsy is <0.5 per 1000 term births and that active prevention for those infants awaits better understanding of cause of the disease, because the usual monitoring methods in labor do not allow for that diagnosis.' It is more probable that understanding and preventing premature birth and better means of antepartum surveillance are more likely to contribute to the prevention of cerebral palsy. To the obstetrician the incidence of cerebal palsy has major clinical meaning. It is clear that the target population for cerebral palsy still hovers at about 2.7 per 1000 live births at 4 to 10 years of age. About 36% of cerebral palsy will have origins in infants weighing <2500 gm, with increasing risk for cerebral palsy with each decrement in infant birth weight. The emphasis in research should be on finding causes of and solutions for early prenatal problems that contribute to births at very low weights, to births of small-for-gestational-age infants, and to births of otherwise prenatally damaged
August 1992 Am J Obstet Gynecol
infants. Tort reform needs to acknowledge these unknowns in the etiology of cerebral palsy, so the clinician can be enabled to practice his or her best without having to do so defensively. In the term infant the incidence of cerebral palsy will be about 1.8 per 1000 of children with that birth weight. Thus the target for more than 90% of all deliveries is small. It is also important to understand that past estimates of origins of cerebral palsy for term infants are divided into perinatal (25% to 30%) causes and the remainder probably prenatal or unknown causes. A portion of those with perinatal causes will be intrapartum causes. REFERENCES 1. Grant A, Joy M, O'Brien N, Hennessey E, MacDonald D. Cerebral palsy among children born during the Dublin randomised trial of intrapartum monitoring. Lancet 1989;2: 1233-6. 2. Torfs CP, Vanden Berg BJ, Oechsli FW, Cummins S. Prenatal and perinatal factors in the etiology of cerebral palsy. J Pediatr 1990;116:615-9. 3. FreemanJM, ed. Prenatal and perinatal factors associated with brain disorders. Hyattsville, Maryland: National Institutes of Health, 1985, NIH publication no 85-1149. 4. Nelson KB, Ellenberg JH. Antecedents of cerebral palsy. Multivariate analysis of risks. N Engl J Med 1986;315: 81-6. 5. Paneth N, Kiely J. The frequency of cerebral palsy: a review of population studies in industrialized nations since 1950. In: Stanley F, Alberman E, eds. The epidemiology of cerebral palsy. London: Spastic International Medical, 1984. 6. Nelson KB, Ellenberg JH. Obstetric complications as risk factors for cerebral palsy or seizure disorders. JAMA 1984;251: 1843-8. 7. Nelson KB, Ellenberg JH. Children who "outgrew" cerebral palsy. Pediatrics 1982;69:529-36. 8. Nelson KB, EllenbergJH. Epidemiology of cerebral palsy. Adv Neurol 1978;19:421-35. 9. Jarvis SN, Holloway JS, Hey EN. Increase in cerebral palsy in normal birthweight babies. Arch Dis Child 1985;60:1113-21. 10. Emond A, Golding J, Peckham C. Cerebral palsy in two national cohort studies. Arch Dis Child 1989;64:848-52. 11. Hagberg B, Hagberg G, Olow I, Von Wendt L. The changing panorama of cerebral palsy in Sweden. V. The birth year period 1979-82. Acta Pediatr Scand 1989;78:283-90. 12. Holst K, Andersen E, Philip J, Hennigsen I. Antenatal and perinatal conditions correlated to handicap among 4year-old children. Am J Perinatol 1989;6:258-67. 13. Dowding VM, Barry C. Cerebral palsy: changing patterns of birthweight and gestational age (1976/81). Irish Med J 1988;81:25-8. 14. Stanley FJ, Watson L. The cerebral palsies in Western Australia: trends, 1968-81. AM J OBSTET GVNECOL 1988;158:89-93. 15. Riikonen R, Raumavirta S, Sinivuori E, Seppala T. Changing pattern of cerebral palsy in the southwest region of Finland. Acta Pediatr Scand 1989;78:581-7. 16. Meberg A. Declining incidence of low birth weight-impact on perinatal mortality and incidence of cerebral palsy. J Perinatol Med 1990;18:195-200. 17. Pharoah POD, Cooke T, Cooke RWI, Rosenbloom L. Birthweight specific trends in cerebral palsy. Arch Dis Child 1990;65:602-6. 18. Pharoah POD, Cooke T, Rosenbloom L, Cooke RWI. Effects of birth weig-ht, g-estational age, and maternal ob-
Volume 167 "umber 2
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stetric history on birth prevalence of cerebral palsy. Arch Dis Child 1987;62: 1035-40. Dale A, Stanley FJ. An epidemiological study of cerebral palsy in Western Australia, 1956-75. II. Spastic cerebral palsy and perinatal factors. Dev Med Child Neurol 1980;22: 13-25. Saito T, Fujii T, Tango T. Prediction of the development of cerebral palsy from perinatal risk factors. Brain Dev 1983;5:1-8. Nelson KB, Broman SH. Perinatal risk factors in children with serious motor and mental handicaps. Ann Neurol 1977;2:371-7. Hagberg B, Hagberg G, Olow I. The changing panorama of cerebral palsy in Sweden. IV. Epidemiologic trends 1959-1978. Acta Pediatr Scand 1984;73:433-40. McQueen PC, Spence MW, Garner JB, Pereira LH, Winsor EJT. Prevalence of major mental retardation and associated disabilities in the Canadian Maritime Provinces. AmJ Ment Def 1987;91:460-6. Jacobson JW, Janicki MP. Observed prevalence of multiple developmental disabilities. Ment Retardation 1983;21:87-94. Gustavson KH, Holmgren G, Jonsell R, Son Blomquist HK. Severe mental retardation in children in a northern Swedish county. .I Ment Def Res 1977;21:161-81.
Incidence of cerebral palsy 423
26. McDonald AD. Severely retarded children in Quebec: prevalences, causes, and care. Am .I Ment Def 1973;78:205-15. 27. Oregon State Board of Health. Mental retardation prevalence in Oregon. Portland, Oregon: Publication of the Oregon State Board of Health, 1962. 28. Drillien CM, Jameson S, Wilkinson EM. Studies in mental handicap. I. Prevalence and distribution by clinical type and severity of defect. Arch Dis Child 1966;41 :528-38. 29. McLaren .I, Bryson SE. Review of recent epidemiological studies of mental retardation: prevalence, associated disorders, and etiology. AmJ Ment Retard 1987;92:243-54. 30. Kiely M. The prevalence of mental retardation. Epidemiol Rev 1987;9:194-218. 31. Heinonen K, Hakulinen A, .Iokela V. Survival of the smallest. Lancet 1988;2:204-6. 32. Hagberg B, Hagberg G, Zetterstrom R. Decreasing perinatal mortality-increase in cerebral palsy morbidity? Acta Pediatr Scand 1989;78:664-70. 33. United States Department of Health and Human Services. Health status of minorities and low-income groups. 3rd ed. Hyattsville, Maryland: USDHHS, 1991:108.