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ORIGINAL ARTICLE Apgar Scores and Long-Term Risk of Epilepsy Yuelian Sun, Mogens Vestergaard, Carsten Bocker Pedersen, Jakob Christensen, t and Jorn Olsens Background: Low Apgar scores are associated with high risk of 100,000 person-years in industrialized countries. There are neonatal death, cerebral palsy, and mental retardation, but the many causes of epilepsy in childhood, including brain tu association between Apgar scores and long-term risk of epilepsy mors, cerebral palsy, and infections. However, for most of remains unresolved epilepsy cases, no clear antecedents have been identified. Methods. We carried out a population-based cohort study of Studies of twins indicate that both genetic and environmental factors play a role in the etiology of epilepsy. Few studies 1,538, 732 live newborns in Denmark between 1 January 1978 and have evaluated the effect of environmental factors originating 31 December 2002 by using national registers. The Apgar scores at or 5 minutes were recorded by midwives following standardized birth weight, preterm birth, toxemias, vaginal bleeding ng in early life; some, 4. but not all, -o have suggested that low procedures. We obtained information on epilepsy by linking the cohort with the National Hospital Register Cohort members were duration of labor may be part of the etiology of epilepsy followed from birth until onset of epilepsy, death, emigration, or 31 Apgar score evaluates newborns based on 5 signs: heart December 2002. whichever came first rate, respiratory effort, reflex irritability, muscle tone, and skin color during the first minutes of life. Each item is Results: The incidence rate of epilepsy increased consistently with scored with a value of 0, 1, or 2, and a total score of 10 3 and 86 per 100,000 person-years for those with a score of 10, the high risk of neonatal death, cerebral palsy, and mental retar- 5. 8-8.8). The incidence rate ratios of epilepsy associated with low dation. One study has reported a higher risk of epilepsy Apgar scores were particularly high in early childhood but remained among children with low Apgar scores, but did not address high into adulthood. The association did not change after excluding this association in detail children with cerebral palsy, congenital malformations, or a parental The aim of this study was to estimate the association history of epilepsy. between low Apgar scores and epilepsy in childhood and Conclusions: Neonates with a suboptimal ave a early adulthood by using a population-based cohort. An higher risk of epilepsy that lasts into adult life findings association between low Apgar scores and epilepsy would suggest that prenatal or perinatal factors play a larger role in the support the hypothesis that prenatal or perinatal factors play etiology of epilepsy than has previously been recognized. a role in the etiology of epilepsy ( Epidemiology2006;17:296-301) METHODS unprovoked seizures. The incidence rate is high in at\ poPulation Sti sy is a serious brain disorder characterized by recur- tem7 to identify all live newborns in Denmark between 1 hildhood,low in adulthood, and high again late in life. I January 1978 and 31 December 2002. They were followed from birth until the onset of epilepsy, death, emigration, or 31 The overall incidence rates range between 40 and 10 per December 2002, whichever came first. The information on deaths and emigration comes from the Danish Civil Regi Submitted 21 June 2005; accepted 14 October 2005 tration System. All live-born children in Denmark are as- From*The Danish Epidemiology Science Centre, Department of Epidemi- signed a unique personal identification number(civil registry ology, Institute of Public Health, and the tNational Centre for Registe based Research, Uni of Aarhus, Aarhus, Denmark; the #Depart- number), which is stored in the Civil Registration System ment of Neurology and Department of Clinical Pharmacology, Aarhus The civil registry number is used as an identification key to University Hospital, Aarhus, Denmark; and the SSchool of Public Health, individual information in all national registers, and it enables Department of Epidemiology, University of California at Los Angeles, accurate linkage of information between registers at the individual level. The study was approved by the Danish Data This study was supported by the Danish National Research Foundation, the Protection Agency. Epidemiology Science Centre, Assessment of Apgar Scores Department of Epidemiology, of Aarhus, Vennelyst Boule- ard 6. DK-8000 Aarhus C. D Information on Apgar scores was obtained from the mail: ys@soci. au. dk. Copyright o 2006 by Lippincott Williams Wilkins Danish Medical Birth Register. Information on Apgar ISSN:1044-398306/1703-0296 scores at 5 minutes after birth was available during the entire DOI:10.1097/01.ede.000020847847401.b6 study period, but information on Apgar scores at 1 minute Epidemiology Volume 17, Number 3, May 2006 第57页 Copyright o Lippincott Williams Wilkins. Unauthorized reproduction of this article is prohibited

ORIGINAL ARTICLE Apgar Scores and Long-Term Risk of Epilepsy Yuelian Sun,* Mogens Vestergaard,* Carsten Bøcker Pedersen,† Jakob Christensen,‡ and Jørn Olsen§ Background: Low Apgar scores are associated with high risk of neonatal death, cerebral palsy, and mental retardation, but the association between Apgar scores and long-term risk of epilepsy remains unresolved. Methods: We carried out a population-based cohort study of 1,538,732 live newborns in Denmark between 1 January 1978 and 31 December 2002 by using national registers. The Apgar scores at 1 or 5 minutes were recorded by midwives following standardized procedures. We obtained information on epilepsy by linking the cohort with the National Hospital Register. Cohort members were followed from birth until onset of epilepsy, death, emigration, or 31 December 2002, whichever came first. Results: The incidence rate of epilepsy increased consistently with decreasing Apgar scores. The incidence rate of epilepsy was 628 per 100,000 person-years for those with 5-minute Apgar scores of 1 to 3 and 86 per 100,000 person-years for those with a score of 10; the resulting incidence rate ratio was 7.1 (95% confidence interval 5.8 – 8.8). The incidence rate ratios of epilepsy associated with low Apgar scores were particularly high in early childhood but remained high into adulthood. The association did not change after excluding children with cerebral palsy, congenital malformations, or a parental history of epilepsy. Conclusions: Neonates with a suboptimal Apgar score have a higher risk of epilepsy that lasts into adult life. These findings suggest that prenatal or perinatal factors play a larger role in the etiology of epilepsy than has previously been recognized. (Epidemiology 2006;17: 296 –301) Epilepsy is a serious brain disorder characterized by recurrent, unprovoked seizures. The incidence rate is high in early childhood, low in adulthood, and high again late in life.1 The overall incidence rates range between 40 and 70 per 100,000 person-years in industrialized countries.2 There are many causes of epilepsy in childhood, including brain tumors, cerebral palsy, and infections. However, for most of epilepsy cases, no clear antecedents have been identified. Studies of twins indicate that both genetic and environmental factors play a role in the etiology of epilepsy.3 Few studies have evaluated the effect of environmental factors originating in early life; some,4,5 but not all,6 –10 have suggested that low birth weight, preterm birth, toxemias, vaginal bleeding, and duration of labor may be part of the etiology of epilepsy. Apgar score evaluates newborns based on 5 signs: heart rate, respiratory effort, reflex irritability, muscle tone, and skin color during the first minutes of life.11 Each item is scored with a value of 0, 1, or 2, and a total score of 10 indicates that the baby is “in the best possible condition.”11 Studies have shown that low Apgar scores are associated with high risk of neonatal death, cerebral palsy, and mental retardation.12–16 One study has reported a higher risk of epilepsy among children with low Apgar scores, but did not address this association in detail.14 The aim of this study was to estimate the association between low Apgar scores and epilepsy in childhood and early adulthood by using a population-based cohort. An association between low Apgar scores and epilepsy would support the hypothesis that prenatal or perinatal factors play a role in the etiology of epilepsy. METHODS Study Population We used data from the Danish Civil Registration System17 to identify all live newborns in Denmark between 1 January 1978 and 31 December 2002. They were followed from birth until the onset of epilepsy, death, emigration, or 31 December 2002, whichever came first. The information on deaths and emigration comes from the Danish Civil Registration System. All live-born children in Denmark are assigned a unique personal identification number (civil registry number), which is stored in the Civil Registration System. The civil registry number is used as an identification key to individual information in all national registers, and it enables accurate linkage of information between registers at the individual level. The study was approved by the Danish Data Protection Agency. Assessment of Apgar Scores Information on Apgar scores was obtained from the Danish Medical Birth Register.18 Information on Apgar scores at 5 minutes after birth was available during the entire study period, but information on Apgar scores at 1 minute Submitted 21 June 2005; accepted 14 October 2005. From *The Danish Epidemiology Science Centre, Department of Epidemiology, Institute of Public Health, and the †National Centre for Registerbased Research, University of Aarhus, Aarhus, Denmark; the ‡Department of Neurology and Department of Clinical Pharmacology, Aarhus University Hospital, Aarhus, Denmark; and the §School of Public Health, Department of Epidemiology, University of California at Los Angeles, Los Angeles, CA. This study was supported by the Danish National Research Foundation, the Danish Medical Research Council (22-02-0363, 22-02-0207), and the Danish Rector’s Conference. Correspondence: Yuelian Sun, The Danish Epidemiology Science Centre, Department of Epidemiology, University of Aarhus, Vennelyst Boulevard 6, DK-8000 Aarhus C, Denmark. E-mail: ys@soci.au.dk. Copyright © 2006 by Lippincott Williams & Wilkins ISSN: 1044-3983/06/1703-0296 DOI: 10.1097/01.ede.0000208478.47401.b6 296 Epidemiology • Volume 17, Number 3, May 2006 第 57 页

Epidemiology. Volume 17, Number 3, May 2006 Apgar Scores and Risk of Epilepsy after birth was accessible only for children born between 1978 and 1996. Midwives recorded Apgar scores after birth TABLE 1. Incidence Rates of Epilepsy According to Selected Characteristics of the Study Population, Denmark, 1978-2002 following standardized procedures. More than 95% of al births in Denmark take place in public hospitals, and mid- ncidence Rat wives report Apgar scores to the registry from the remaining Person-Years No of Persons per 100, 000 home births following the hospital procedures Characteristics at risk With Epilepsy Person-Year Assessment of Epilepsy B Information on epilepsy was obtained from the Na 9,202445 95.0 8,751,255 7717 tional Hospital Register that contains information on all discharges from Danish hospitals since 1977. Outpatients Gestational age(weeks) 305.5 have been included in the register since 1995. Diagnostic Very preterm 146637 information in the National Hospital Register was based on Preterm(33-36) 80,516 he International Classification of Diseases. &th revision Term(37-41) 14,370,16 D-8)from 1977 to 1993, and the International Classifica Posten(≥42) 1,471,843 tion of Diseases, 1 Oth revision(ICD-10) from 1994 to 2002 Cohort members were classified with epilepsy if they had Birth order been hospitalized or had been in outpatient care with a 8,124,750 7548 diagnosis of epilepsy (ICD-8: 345; ICD-10: G40-G41). The 2nd+ 9828950 time of onset of epilepsy was defined as the first day of Multiple birth Single birth 17,533,469 Data Analys Twin or more 419,903 104.3 Unknown The incidence rate ratio of epilepsy was estimated by a Maternal age(years) log-linear Poisson regression model- with the GENMOD 656.046 procedure in SAs version 8.1(SAS institute, Cary, NC). All incidence rate ratios were adjusted for age and its interaction 4,611,950 4528 with sex and for calendar year. Age and calendar year were 25-29 7053,083 treated as time-dependent variables. Age was categorized in 4.165.921 3669 1466.700 from the first birthday to the 19th birthday, and then age intervals of 20-21 and 22-25 as the oldest 2 groups. Calendar Ye 915 year was categorized in a 1-year period from 1978-2002. P 17, 15,855 values were based on likelihood ratio tests and 95% confi dence intervals( CIs)were calculated using Walds test. The 259.1 adjusted score test suggested that the regression models were Uncertain% Unknown not subject to overdispersion 87,508 141.7 17,587,074 RESULTS Parental history of epilepsy Mother 123,468 The study included 1, 538, 732 live-born children. Dur- Fath 100.343 ing 17, 953, 700 person-years of follow up, 16, 455 children Both 6855 were diagnosed with epilepsy corresponding to an average 17,728,284 incidence rate of 91.7 per 100,000 person-years. Table 1 shows the incidence rate of epilepsy according to the selected Congenit formation was suspected but not confirmed. The information about congenital malformation was missing. characteristics of the population The incidence rate of epilepsy increased consistently with decreasing 1-and 5-minute Apgar scores, especially for 5-minute Apgar scores (Table 2). In our study population, 3 at both 1 and 5 minutes had the highest incidence rate ratio 2466(0.16%)had a 5-minute Apgar score of l to 3 and 9047 of 8.03(95%CI=6. 19-10.42)compared with children with (0.59%)of 4 to 6. The average incidence rate of epilepsy an Apgar score of 10 at both measures(Table 3) was 628 per 100,000 person-years for those with 5-minute Incidence rate ratios of epilepsy differed in preterm and Apgar scores of l to 3 and 86 for those with a 5-minute term infants according to 5-minute Apgar scores (P for Apgar score of 10 interaction <0.001). The highest incidence rate ratios were The incidence rate ratios of epilepsy decreased when found among term infants (Table 4). the Apgar score improved from I to 5 minutes. However, the Infants with 5-minute Apgar scores of less than 10 had incidence rate ratios remained higher for infants with low higher incidence rate ratios of epilepsy throughout childhood 1-minute Apgar scores, even if their scores improved to 10 at and early adulthood compared with those with a score of 10 5 minutes compared with children with an Apgar score of 10 The highest incidence rate ratios were found, however, during at both 1 and 5 minutes. Children with Apgar scores of 1 to the first year of life(Fig. 1) o 2006 Lippincott Williams Wilkins 第58页 Copyright c Lippincott Williams& Wilkins. Unauthorized reproduction of this article is prohibited

after birth was accessible only for children born between 1978 and 1996. Midwives recorded Apgar scores after birth following standardized procedures. More than 95% of all births in Denmark take place in public hospitals, and midwives report Apgar scores to the registry from the remaining home births following the hospital procedures. Assessment of Epilepsy Information on epilepsy was obtained from the National Hospital Register that contains information on all discharges from Danish hospitals since 1977.19 Outpatients have been included in the register since 1995. Diagnostic information in the National Hospital Register was based on the International Classification of Diseases, 8th revision (ICD-8) from 1977 to 1993, and the International Classification of Diseases, 10th revision (ICD-10) from 1994 to 2002. Cohort members were classified with epilepsy if they had been hospitalized or had been in outpatient care with a diagnosis of epilepsy (ICD-8: 345; ICD-10: G40 –G41). The time of onset of epilepsy was defined as the first day of contact with the hospital. Data Analysis The incidence rate ratio of epilepsy was estimated by a log-linear Poisson regression model20 with the GENMOD procedure in SAS version 8.1 (SAS institute, Cary, NC). All incidence rate ratios were adjusted for age and its interaction with sex and for calendar year. Age and calendar year were treated as time-dependent variables.21 Age was categorized in 3-month intervals in the first year of life, in 1-year age levels from the first birthday to the 19th birthday, and then age intervals of 20 –21 and 22–25 as the oldest 2 groups. Calendar year was categorized in a 1-year period from 1978 –2002. P values were based on likelihood ratio tests and 95% confi- dence intervals (CIs) were calculated using Wald’s test.21 The adjusted score test suggested that the regression models were not subject to overdispersion.22 RESULTS The study included 1,538,732 live-born children. During 17,953,700 person-years of follow up, 16,455 children were diagnosed with epilepsy corresponding to an average incidence rate of 91.7 per 100,000 person-years. Table 1 shows the incidence rate of epilepsy according to the selected characteristics of the population. The incidence rate of epilepsy increased consistently with decreasing 1- and 5-minute Apgar scores, especially for 5-minute Apgar scores (Table 2). In our study population, 2466 (0.16%) had a 5-minute Apgar score of 1 to 3 and 9047 (0.59%) of 4 to 6. The average incidence rate of epilepsy was 628 per 100,000 person-years for those with 5-minute Apgar scores of 1 to 3 and 86 for those with a 5-minute Apgar score of 10. The incidence rate ratios of epilepsy decreased when the Apgar score improved from 1 to 5 minutes. However, the incidence rate ratios remained higher for infants with low 1-minute Apgar scores, even if their scores improved to 10 at 5 minutes compared with children with an Apgar score of 10 at both 1 and 5 minutes. Children with Apgar scores of 1 to 3 at both 1 and 5 minutes had the highest incidence rate ratio of 8.03 (95% CI 6.19 –10.42) compared with children with an Apgar score of 10 at both measures (Table 3). Incidence rate ratios of epilepsy differed in preterm and term infants according to 5-minute Apgar scores (P for interaction 0.001). The highest incidence rate ratios were found among term infants (Table 4). Infants with 5-minute Apgar scores of less than 10 had higher incidence rate ratios of epilepsy throughout childhood and early adulthood compared with those with a score of 10. The highest incidence rate ratios were found, however, during the first year of life (Fig. 1). TABLE 1. Incidence Rates of Epilepsy According to Selected Characteristics of the Study Population, Denmark, 1978 –2002 Characteristics Person-Years at Risk No. of Persons With Epilepsy Incidence Rate per 100,000 Person-Years Sex Boys 9,202,445 8738 95.0 Girls 8,751,255 7717 88.2 Gestational age (weeks) Very preterm (33) 146,637 448 305.5 Preterm (33–36) 680,516 981 144.2 Term (37–41) 14,370,165 12,721 88.5 Postterm (42) 1,471,843 1356 92.1 Unknown 1,284,540 949 73.9 Birth order 1st 8,124,750 7548 92.9 2nd 9,828,950 8907 90.6 Multiple birth Single birth 17,533,469 16,017 91.4 Twin or more 419,903 438 104.3 Unknown 327 0 0.0 Maternal age (years) 20 656,046 794 121.0 20–24 4,611,950 4528 98.2 25–29 7,053,083 6158 87.3 30–34 4,165,921 3669 88.1 35 1,466,700 1306 89.0 Cerebral palsy Yes 30,915 600 1940.8 No 17,922,785 15,855 88.5 Congenital malformation Yes 250,121 648 259.1 Uncertain* 28,998 40 137.9 Unknown† 87,508 124 141.7 No 17,587,074 15,643 88.9 Parental history of epilepsy Mother 123,468 397 321.5 Father 100,343 221 220.2 Both 1605 11 685.5 Neither 17,728,284 15,826 89.3 *Congenital malformation was suspected but not confirmed. † The information about congenital malformation was missing. Epidemiology • Volume 17, Number 3, May 2006 Apgar Scores and Risk of Epilepsy © 2006 Lippincott Williams & Wilkins 297 第 58 页

Sun et al Epidemiology. Volume 17, Number 3, May 2006 TABLE 2. Incidence Rate Ratios of Epilepsy According to Apgar Scores at 1 and 5 Minutes After Birth, Denmark, 1978-2002 I-Min Apgar Scores Min Apgar Scores Apgar Scores No, of Cases IRR(95% CI) No of cases IRR(95% CD 14,2 987 1.04(1.00-1.09) 1.45(1.35-1.56 1193 1.30(1.22-1.38) 1.89(1.72-2.07 143(1.32-1.55) 221 213 244(2.13-2.78) 1.81(1.69-1.95) 4.22(3.78-4.72) 14(5.798.81) 241(1.97-2.95) 219 208(1.61-2.70) 148(1.26-1.73) 0 1.58(139-1.78) scores were accessible from I January 1978 to 31 December 1996. ar year, age, and sex. APgar scores were registered as zero, including children who were transferred to intensive care immediately after birth. IR indicates incidence rate per 100, 000 person-years: IRR, incidence rate ratio. nce Rate Ratios*(95% CI)of Epilepsy According to Combinations of Apgar Scores at 1 and 5 Min, Denmark, 5-Min Apgar Scores 1-Min Apgar Scores 1-3 4-6 7 0.81(0.37-1.81)1.00 1.52(0.84-2.75)1.20(1.02-141)1.03(0.98-1.08) 1.52(1.15-2.01)1.56(1.36-1.80)1.23(1.15-1.32) 286(1.98-4.15)1.61(1.29201)1.69(1.45-1.96)1.24(1.12-1.38) 401(3.29-4.88)224(1.85-2.72)207(180-2.39)1.70(1.45-1.99)1.31(1.15-1.48) 1-3 803(6.19-10.42)464(3.94-5.4 2.24(1.63-3.08)3.20(2.44-4.19)1.60(1.05-243)165(1.18-232) Reference category. ApRar a (not applicable)indicates the number of person-years at risk was less than 5000, corresponding to fewer than 5 expected cases based on a hypothesis of no association between TABLE 4. Association of 5-Min Apgar Scores With Epilepsy for Babies Born Preterm and Term, Denmark, 1978-2002 Preterm Infants(<37 wk) Term Infants (37-41 wk) 5-Min Apgar Scores No of Cases IRR*(95% Ci) No. of Cases IrR*(95% Ci) 11,416 1.42(1.21-1.67 1.34(1.23-1.46) 1.71(1.41-2.08) 66(1.47-1.88) 1.80(1.38-2.34) 2.37(2.00-281) 75 2.52(1.99-3.18) 441(3.83-5.07) 757 8.68(6.73-11.18) Adjusted for calendar year, age, and sex. Reference category. The association between 5-minute Apgar scores and From 1995 to 2002, 9500 people were diagnosed with epilepsy did not change after excluding infants with cerebral epilepsy, including 1466(15%)only in an inpatient setting, palsy (n= 600), with confirmed or suspected congenital 3443(36%)only in an outpatient setting, and 4591(48%)in malformations(n =812), with parental history of epilepsy both settings. The incidence rates of epilepsy increased when (n= 629), or with any of the 3 ions(Table 5) outpatients were included, especially for children with an 298 c 2006 Lippincott Williams c wilkins 第59页 Copyright c Lippincott Williams& Wilkins. Unauthorized reproduction of this article is prohibited

The association between 5-minute Apgar scores and epilepsy did not change after excluding infants with cerebral palsy (n 600), with confirmed or suspected congenital malformations (n 812), with parental history of epilepsy (n 629), or with any of the 3 conditions (Table 5). From 1995 to 2002, 9500 people were diagnosed with epilepsy, including 1466 (15%) only in an inpatient setting, 3443 (36%) only in an outpatient setting, and 4591 (48%) in both settings. The incidence rates of epilepsy increased when outpatients were included, especially for children with an TABLE 2. Incidence Rate Ratios of Epilepsy According to Apgar Scores at 1 and 5 Minutes After Birth, Denmark, 1978 –2002 Apgar Scores 1-Min Apgar Scores* 5-Min Apgar Scores No. of Cases IR IRR† (95% CI) No. of Cases IR IRR† (95% CI) 10‡ 8998 80 1.00 14,281 86 1.00 9 2606 86 1.04 (1.00–1.09) 791 129 1.45 (1.35–1.56) 8 1193 106 1.30 (1.22–1.38) 441 166 1.89 (1.72–2.07) 7 654 118 1.43 (1.32–1.55) 221 213 2.44 (2.13–2.78) 4–6 819 149 1.81 (1.69–1.95) 319 369 4.22 (3.78–4.72) 1–3 380 286 3.43 (3.10–3.80) 88 628 7.14 (5.79–8.81) 0§ 97 234 2.41 (1.97–2.95) 58 219 2.08 (1.61–2.70) Missing 153 108 1.48 (1.26–1.73) 256 130 1.58 (1.39–1.78) *One-minute Apgar scores were accessible from 1 January 1978 to 31 December 1996. † Adjusted for calendar year, age, and sex. ‡ Reference category. § Apgar scores were registered as zero, including children who were transferred to intensive care immediately after birth. Apgar scores were missing for unknown reasons. IR indicates incidence rate per 100, 000 person-years; IRR, incidence rate ratio. TABLE 3. Incidence Rate Ratios* (95% CI) of Epilepsy According to Combinations of Apgar Scores at 1 and 5 Min, Denmark, 1978 –1996† 1-Min Apgar Scores 5-Min Apgar Scores 1–3 4–6 7 8 9 10 10 NA NA NA NA 0.81 (0.37–1.81) 1.00‡ 9 NA NA NA 1.52 (0.84–2.75) 1.20 (1.02–1.41) 1.03 (0.98–1.08) 8 NA NA NA 1.52 (1.15–2.01) 1.56 (1.36–1.80) 1.23 (1.15–1.32) 7 NA NA 2.86 (1.98–4.15) 1.61 (1.29–2.01) 1.69 (1.45–1.96) 1.24 (1.12–1.38) 4–6 NA 4.01 (3.29–4.88) 2.24 (1.85–2.72) 2.07 (1.80–2.39) 1.70 (1.45–1.99) 1.31 (1.15–1.48) 1–3 8.03 (6.19–10.42) 4.64 (3.94–5.46) 2.24 (1.63–3.08) 3.20 (2.44–4.19) 1.60 (1.05–2.43) 1.65 (1.18–2.32) *Adjusted for calendar year, age and sex. † Data on Apgar scores at one minute were not recorded after 1996. ‡ Reference category. NA (not applicable) indicates the number of person-years at risk was less than 5000, corresponding to fewer than 5 expected cases based on a hypothesis of no association between Apgar score and the risk of epilepsy. TABLE 4. Association of 5-Min Apgar Scores With Epilepsy for Babies Born Preterm and Term, Denmark, 1978 –2002 5-Min Apgar Scores Preterm Infants (<37 wk) Term Infants (37–41 wk) No. of Cases IR IRR* (95% CI) No. of Cases IR IRR* (95% CI) 10† 909 147 1.00 11,416 85 1.00 9 176 207 1.42 (1.21–1.67) 518 117 1.34 (1.23–1.46) 8 118 247 1.71 (1.41–2.08) 257 144 1.66 (1.47–1.88) 7 59 254 1.80 (1.38–2.34) 133 204 2.37 (2.00–2.81) 4–6 75 356 2.52 (1.99–3.18) 197 381 4.41 (3.83–5.07) 1–3 17 423 2.98 (1.84–4.81) 60 757 8.68 (6.73–11.18) *Adjusted for calendar year, age, and sex. † Reference category. Sun et al Epidemiology • Volume 17, Number 3, May 2006 298 © 2006 Lippincott Williams & Wilkins 第 59 页

Epidemiology. Volume 17, Number 3, May 2006 Apgar Scores and Risk of Apgar score of 10, whereas incidence rate ratios of children 三细部 with low Apgar score decreased slightly (Table 6) DISCUSSION The incidence rate of epilepsy increased consistently with decreasing 1-and 5-minute Apgar scores for children born at term or born preterm. The incidence rates of epilepsy decreased when the Apgar scores increased from 1 to 5 minutes, but they remained higher than those of children who had an Apgar score of 10 at both measures. The incidence rate ratios of neonates with low 5-minute Apgar score were particularly high in early childhood and continued to be high throughout the study period of up to 25 years. This associa- tion was not confounded by cerebral palsy, congenital mal 345678910 11 12 13 141525 formations, or a parental history of epilepsy Age (years) The association between Apgar scores and epilepsy has FIGURE 1. Incidence rate ratios and 95% Cls of epilepsy for been the subject of few studies. A case-control study indi- children with 5-minute Apgar scores of 1-6 and 7-9 accord- cated that low Apgar score is a risk factor for first unprovoked ing to age. Adjusted for calendar year, age, and sex. The afebrile seizures among children,and one large population reference group consists of children with a 5-minute Apgar based study showed that children with a 5-minute Apgar score of 1o score below 7 had a higher risk of epilepsy. Our results are TABLE 5. Association of 5-Min Apgar Scores With Epilepsy Among Children Without CP, CM, and PHE* Denmark. 1978-2002 Among Children Among Children Without Congenital Without Any of Without Cerebral Palsy ony of adler the 3 Conditions 5-Min Apgar Scores IRRT(95% CD) IRR’(95%CD IRR(95%CD IRRT(95%CI 39(1.29-1.49) 1.42(1.32-1.53) 45(1.35-1.56)1.35(1.24-1.46) 1.79(1.62-1.98) 78(1.61-1.97 1.90(1.72-2.09) 1.68(1.51-1.87) 222(1.93-2.57) 3.46(3.05-3.92) 4.03(3.59-4.54) 4.31(3.85-4.82)3.37(295-3.86) 1-3 59647-75586498573599958(45-751 CP CM. and PHE indicate cerebral palsy, congenital malformation, parental history of epilepsy, respectivel Adjusted for calendar year, age, and ser Reference category. ABLE 6. Association of 5-Min Apgar Scores With Epilepsy, Including and Excluding Outpatients Denmark. 1995-2002 Inpatients and Outpatients Inpatients* 5-Min Apgar Scores No, of Cases IR IRR(95% CD) IRR(95% CD) 91.31.00 57.31.00 432 120.81.28(1.16-1.41) 817135(1.20-1.52) 10.71.87(1.60-2.18) 17641.90(1.57-2.31) 133.2228(1.82-2.85) 32783.52(3.01-4.12) 250.1425(3.55-5.08) 7756.24(4.67-8.33 460.0789(5.71-10.91) ere refer to patients of epilepsy who were ever treated in an inpatient setting during study period. ADjusted for calendar year, age, and fReference category o 2006 Lippincott Williams Wilkins 299 第60页 Copyright c Lippincott Williams& Wilkins. Unauthorized reproduction of this article is prohibited

Apgar score of 10, whereas incidence rate ratios of children with low Apgar score decreased slightly (Table 6). DISCUSSION The incidence rate of epilepsy increased consistently with decreasing 1- and 5-minute Apgar scores for children born at term or born preterm. The incidence rates of epilepsy decreased when the Apgar scores increased from 1 to 5 minutes, but they remained higher than those of children who had an Apgar score of 10 at both measures. The incidence rate ratios of neonates with low 5-minute Apgar score were particularly high in early childhood and continued to be high throughout the study period of up to 25 years. This association was not confounded by cerebral palsy, congenital malformations, or a parental history of epilepsy. The association between Apgar scores and epilepsy has been the subject of few studies. A case– control study indicated that low Apgar score is a risk factor for first unprovoked afebrile seizures among children,23 and one large populationbased study showed that children with a 5-minute Apgar score below 7 had a higher risk of epilepsy.14 Our results are FIGURE 1. Incidence rate ratios and 95% CIs of epilepsy for children with 5-minute Apgar scores of 1– 6 and 7–9 according to age. Adjusted for calendar year, age, and sex. The reference group consists of children with a 5-minute Apgar score of 10. TABLE 5. Association of 5-Min Apgar Scores With Epilepsy Among Children Without CP, CM, and PHE,* Denmark, 1978 –2002 5-Min Apgar Scores Among Children Without Cerebral Palsy Among Children Without Congenital Malformation Among Children Without Parental History of Epilepsy Among Children Without Any of the 3 Conditions IRR† (95% CI) IRR† (95% CI) IRR† (95% CI) IRR† (95% CI) 10‡ 1.00 1.00 1.00 1.00 9 1.39 (1.29–1.49) 1.42 (1.32–1.53) 1.45 (1.35–1.56) 1.35 (1.24–1.46) 8 1.79 (1.62–1.98) 1.78 (1.61–1.97) 1.90 (1.72–2.09) 1.68 (1.51–1.87) 7 2.13 (1.84–2.46) 2.22 (1.93–2.57) 2.46 (2.15–2.82) 1.92 (1.64–2.25) 4–6 3.46 (3.05–3.92) 4.03 (3.59–4.54) 4.31 (3.85–4.82) 3.37 (2.95–3.86) 1–3 5.96 (4.70–7.55) 6.86 (5.49–8.57) 7.35 (5.95–9.09) 5.81 (4.50–7.51) *CP, CM, and PHE indicate cerebral palsy, congenital malformation, parental history of epilepsy, respectively. † Adjusted for calendar year, age, and sex. ‡ Reference category. TABLE 6. Association of 5-Min Apgar Scores With Epilepsy, Including and Excluding Outpatients, Denmark, 1995–2002 5-Min Apgar Scores Inpatients and Outpatients Inpatients* No. of Cases IR IRR† (95% CI) No. of Cases IR IRR† (95% CI) 10‡ 8362 91.3 1.00 5255 57.3 1.00 9 432 120.8 1.28 (1.16–1.41) 293 81.7 1.35 (1.20–1.52) 8 234 153.8 1.65 (1.44–1.87) 169 110.7 1.87 (1.60–2.18) 7 103 176.4 1.90 (1.57–2.31) 78 133.2 2.28 (1.82–2.85) 4–6 159 327.8 3.52 (3.01–4.12) 122 250.1 4.25 (3.55–5.08) 1–3 46 577.5 6.24 (4.67–8.33) 37 460.0 7.89 (5.71–10.91) *Inpatients here refer to patients of epilepsy who were ever treated in an inpatient setting during study period. † Adjusted for calendar year, age, and sex. ‡ Reference category. Epidemiology • Volume 17, Number 3, May 2006 Apgar Scores and Risk of Epilepsy © 2006 Lippincott Williams & Wilkins 299 第 60 页

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