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Malclllal (_'Jgareilo Slllokillg alld In\'La.sivc Mcningococcal Disease: Cohort Study Among Youn~ Children Metropolitan Atlanta, 1089-1996 of b4cl,2rial [llCiiH!glllS and :,c[nz¢cmm the U:nled ~"l;llCS Approx~m;~lcl~ cases of 1IlC01tlgOCOCCal dlsc4>C occtlr The chsca>c lq ellen dc~astalin7. < ,t>c'-t.tt.t[ hydroccph;llu, and nicllt,~ .Hid ;:lt~-it<l! and is~auscd hv org,misms of d~al~sl >ero~motip t~ IllClllH~Oc'Ot-t'i d[hi poorly Ill]~tll~O~elllc ill chil~r0n yOtillgOl Illodiliyihlc rl~k i';ttlOl's it)l Norway. [~ngland. {l~t] [hc' l.'r:ttc'd ait.ld Wc rep. rl }lCIC lliu Icsull~ belT+ceil cl~aroll¢ SlllOklllg dur~n~ prc7- nancy and {,lher malernal and Jill;ill acleris{ics ar',d Ibc risk el devc-h~ul7 during c-arlv childhood In lhl> cigareilc .ilelhod~ \kc Ll>cd a rcqrosp¢ctive c~)horl des;i~t'l II1 I he OCCIIFIUBk'C tll ~p~:r;Ithc Illc'III~OL'(ice{II tt{>c'~tSk" Ill d coholl el climldlcn bor:~ in the tot~b I)eKalh. {)ouglax. ~"tllhq~. I }winneu. pcrlod(~'ptcn~bcr ;I, 199(>) kkc u>cd (lcor- i0Nc).,indl)cccmbc~ l]. lO~5 Thedealhccr- I)l~toq el Repn~ducnxe I{eTlhh, N3huil iI (enler Med:cmc. t in,>r) (rlllVCrslly ~ch.lo) of ~lcdlcioe. May i c~99 \:OI ~'). No 5 325307769

Malernal ,~moking and Meningococe~l Disease who died through September 31, 1996, `',,'ere linked to the corresponding birth certificates. Initial linking was based on last names and b/rth dates of children, and further matching and validation were done by children's first names, mothers" maiden names, and fathers' last names. The birth and death certificates were matched for more than 90% of the eligi- b~e children. Data from prospective surveil- lance for invasive meningococcal disease~ were used to identify cases of invasive meningococcal disease in these children. Cases of meningococcal disease were linked to the birth~:teath file by matching first and last names and date of birth. Children for whom information was missing were excluded from analysis. The study cohort consisted of 283 291 children who were assumed to have resided in metropolitan Atlanta throughout the study period. The duration of follow-up was defined as the period between birth and diag- nosis of meningococcal disease for children who developed the disease; the period between birth and death for children who died during follow-up without developing meningococcal disease; and the period between birth and September 31, 1996, or the third birthday, whichever camc first, for the rest of the cohort. Children whose birth certificates ,,,,'ere not matched to either death certificates or surveillance records for the meningococcal disease group were assumed to be alive and not to have devel- oped meningococcal disease. Identification qf Case~s A case of invasive meningococcal dis- ease was defined by the isolation ofN menin- gttidts from either the blood or the cere- brospinal fluid of the patient. Isolates were serogrouped by standard laboratory tech- niques. Cases were identified as part of a lab- oratory-based surveillance project for meningococcal and other invasive bacterial infections in metropolitan Atlanta,~ ~s an area with 32 hospitals and a population of 2 344 514 ( 1990 census). Initial case reports `',,ere obtained from hospital laboratories and infection-control practitioners. Laboratories were audited every. 6 months to identi~, unrc- ported cases and validate reported cases. Medical records of all audited patients `'`';ere also reviewed. Information Regarding lnJhnt and Maternal Characteristics Characteristics of infants and mothers were obtained from the birth certificate data file. Selected infant characteristics included sex, birthweight (<2500 g, _>2500 g), and ges- tation at birth (<37 weeks, >_37 weeks). Assessed maternal characteristics included age at delivery (<20 years, >20 years), race (White, Black, other), education (<12 years, _>12 years), marital status (married, not mat- ned), and smoking of cigarettes din-rag preg- nancy (yes/no: if yes, the number of ciga- rettes smoked daily). The birth certificate and Georgia Medicaid claims databases were linked to detemaine the so~ce of payment for prenatal care and deliver' (Medicaid or other source). These variables were chosen because they may be confounders of an association between maternal smoking and sporadic meningococcal disease among children. Analysis Age-specific incidence was determined by the number ofc~.ses per total person-years of follow-up for each year of age. Univariate relationships between selected infant and maternal characteristics and invasive meningococcal disease were assessed by using the Fisher exact test. Variables lbund to be significantly associated with invasive mcningococcal disease were entered in a multivariate model. To account for variable lengths of follow-up, Cox proportional haz- ards analysis was used to identify indepen- dent associations between selected risk factors and menmgococcal disease. The proportional hazard assumption was assessed graphically by the SAS procedure LIFETEST~ and by a test for the interaction between maternal s~noking and time since the infant's birth.' Models were fitted by means of the SAS TABLE I--Incidence of Invaslve Meningococcal Disease by Age of Infant: Metropolitan Atlanta, Ga, 1989-1996 Age Interval No. of Person-Years No. of Incidence Ratea of Children, y Chitdrer~ of Follow-Up Cases (95% Confidence Interval) 0-I 283 291 279 761 36 12.8 (9.3, 17.8) 1-2 270 191 248 985 5 2.0 (0.8, 4.8} 2-3 228 534 207 692 6 2.9 (1,3, 6.4) ~lncidence of invasive meningococcal disease per 100 000 person-years. procedure PtIREG ~ Potential intc~actiOos bev, veen maternal race and maternaI smok- ing dunng pregnancy and bc~een maternal race and maternal education were also assessed. Because no cases occ~ed in chi l- dren of mothers whose race was clarified as "'other." info~ation ~om chil&en of White women and Black women was used in haz- ~ds analysis. Results Fifty-five cases were identified. Two cases were in children born outside metro- politan Allanta, and these cases were excluded. Four cases could not be linked to births in the study area or in Georgia, per- haps because of migration into the study area fi-om another state. Information on maternal smoking during pregnancy was not available for these children. Information on maternal smoking durmg pregnancy or maternal edu- cation level was missing for 2 other cases. After we made these exclusions, we ana- lyzed data fi-om 47 cases. Serogroup B N meningitidis accounted for 17 oft.he 47 cases (36%); 10 cases (21%) were serogroup C, 5 cases (1 I%) were serogroup Y, and 1 case (2%) was serogroup W t 35. Serogroup information was not avail- able for 14 cases. Meningitis ~,as diagnosed for 18 cases (38%). Four of the 47 cases (9%) died of meningococcal disease. No meningococcal disease outbreaks or secondary cases were noted in me~opoIitan Atlanta during the study penc~t. 'Fhe age-.~'cific incidence was highest tbr children 1 year or younger(Table l). The proportion of children who acquired invasive menmgococcal disease did not differ significantly by sex, gestation at birth, abnor- mal conditions, or mother's race, but several WaNes were significant in univariate analy- ses (Table 2 ). The proportion of children acquiring meningococcal disease was greater for teenaged mothers than older mothers (0.04% vs 0.01%, P= .003); unmarried moth- ers than manned mothers (0.03% vs 0.01%. P .008); mothers whose prenatal care and/or delivery, was paid for by Medicaid than moth- crs whose prenatal care and/or delivery was paid for by another insurer (0.03% vs 0.01%, P - .002); mothers with fewer than 12 years of educatioo than mothers with more than 12 years of education (0.04% vs <0.01%, P - .00001 ); and mothers who reported smok- ing during pregnancy than mothers who reported not smoking during pregnancy (0.05% vs 0.01%, P = .00001 ). Among children of White mothers, the proportion acquiring meningococcal dis- ease was significantly higher for those whose mothers were young, not married, May 1999, Vol. 89, No. 5 American Journal of Public Health 713 325307770

Vusuf et al. TABLE 2--Univariate Relation Between Selected Infant and Maternal Characteristics and Invasive Menlngococcal Disease: Metropolitan Atlanta, Ga, 1989-1996 All Children (n = 283 291) White Children (n = 163 501) Black Children (n -- 110 770) No. of No. With Meningo- No. of No. With Meningo- Children cocca~ Disease (%) Children coccal Disease (%) No. of No. With Meningo- Characteristic Children coccal Disease (%) Sex of child Female 138 367 1 g (0.01) 79 506 13 (002) 54 480 6 (0.01) Male 144 924 28 (0.02) 83 995 18 (0.02) 56 290 10 (0.02) Birlhweight, g <2500 23 397 6 (0.03) 9137 4 (0.04) 13 664 2 (0.01) _>2500 259 894 41 (0.02) 154 364 27 (0.02) 97 106 14 (0.01) Gestation at birth, wk <37 29 517 7 (0.02) 12 893 4 (0.03) 15 962 3 (0.02) _>37 253 774 40 (0,02) ! 50 608 27 (0.02) 94 808 13 (0.01 ) Abnormal conditions in newDornb Yes 10 460 3 (0.03) 5196 2 (0.04) 5024 1 (0.02) No 272 831 44 (0.02) 158 305 29 (0.02) 105 746 15 (0.01) Mother's race White 163 501 31 (0.02) ............ Black 110 770 16 (0.01) ............ Other/unknown 9 020 0 (0.00) ........... Mother's age at delivery, y <20 34 398 13 (0.04)" 12 550 10 (0.08)~ 21 367 3 (0.01) _>20 248 893 34 (0.01) 150 951 21 (0 01) 89 403 13 (0.01) Mother's marffa[ status Marrie0 191 614 23 (0.01)a 140 918 18 (0.01)" 42 708 5 (0.01) Not married 91 677 24 (0.03) 22 583 13 (0.06) 68 062 11 (0.02) Mother received Medicaid Yes 76 712 23 (0.03)" 25 834 17 (0.07)" 49 059 6 (0.01) No 206 579 24 (0.01) 137 667 14 (0.01) 61 711 10 (0.02) Mother's education, y <12 48 668 21 (0.04)a 23 766 16 (0.07)a 23 280 5 (0.02) _>12 234 623 26 (0.01) 139 735 15 (0.01) 87 490 11 (0.01) Mother smoked during pregnancy Yes 29 267 16 (0.05)a 19 883 11 (0.06)a 9 234 5 (0.05)a No 254 024 31 (0.01) 143 618 20 (0.01) 101 536 11 (0.01) aProportions of children acquiring mening,:x=occal infection are significantly different ~etween at least 2 levels of the characteristic (Fisher exact test, P< .05). ~Abnormal conditions diagnosed in the newborn inctuded anemia, injury during birth, fetal alcohol syndrome, respiratory distress syndrome, meconium aspiration syndrome, seizures, and other or urclassified conditions. received Medicaid, or had fewer than 12 years of education (Table 2). For children of White mothers and African American mothers, the proportion acquiring meningococcal disease was significantly increased by maternal cigarette smoking during pregnancy. Cox proportional hazards analysis indicated that children of mothers who smoked during pregnancy were 2,9 times more likely to acquire meningococcal dis- ease than were children of mothers who dig not smoke during pregnancy (Table 3). No significant interaction between race and maternal smoking status was found in determining risk for meningococcal dis- ease (data not shown), In addition, exami- nation of maternal smoking as a time-vary- ing covariate (data not shown) indicated that the association between maternal ciga- rette smoking and risk for meningococcal disease did not significantly differ (P = .552) between a child's first year of 714 American Journal of Public Health life and the second and third years of life. After the effect of smoking during preg- nancy was accounted for, no significant dose response relation between the num- ber of cigarettes smoked and risk for meningococcal disease was found (data not shown). Compared with children of moth- ers with 12 or more years of education, children of mothers with fewer than 12 years of education were 2.1 times more likely to acquire meningococcal disease. Although inleraction between race and maternal education level was significant in determining the risk for meningococcal disease (data not shown), the number of cases was too small to allow reliable deter- ruination of risk by race. The fraction of meningococcal disease attributable to exposure to cigarelte smoke (for which maternal smoking during preg- nancy was a proxy) was similar for all chil- dren, of both White mothers and African American mothers (Table 4). Discussion Our findings are consistent with the results of previous studies~ ~z and indicate that exposure to maternal cigarette smoking is a risk factor tbr sporadic meningococcal disease in young children. The rate of inva- sive mcningococcal disease was 5 times higher for children of mothers who reported smoking during pregnancy than tbr children of mothers who did not smoke during preg- nancy. This relation persisted when children of White mothers and children of African American mothers were examined separately. Maternal cigarette smoking during preg- nancy was also independently associated with invasive meningococcal disease in mul- tivariate analysis. After factors reflecting social and economic status were adjusted for, children of mothers who smoked during pregnancy were 2.9 times more likely to acquire invasive meningococcal disease than were children of mothers who did not smoke May 1999, Vol. 89. No. 5 325307771

TABLE 3--Associations of Selected Infant and Maternal Characteristics to Invasive Meningococcal Disease In Early Childhood: Metropolitan Atlanta, Ga, 1989-1996 Characteristic Risk Ratioa 95% Confidence Interval Mother's age, y: <20 vs _>20 (reference) 1.52 Mother's race: White vs Black (reference) 1.8 Mother received Medicaid 1.54 Mother married 0.70 Mother smoked during pregnancy 2.93b Mother's education, y: <1 2 vs >12 (reterence) 2.07~ 0.71,3.25 0.87, 3.58 0.80, 2.99 O.33, 1.45 1.52, 5.66 1.02, 4.20 "Risk Ratio estimated by Cox proportional hazards model. All characteristics are adjusted for other characteristics in the table. TABLE 4---Attributable Fraction of Invaslve Meningococcal Disease Among Children Due to Maternal Cigarette Smoking During Pregnancy: Metropolitan Atlanta, Ga, 1989-1996 Fraction Attributable to Maternal Smoking All children 0.26 Children of White mothers 0.26 Children of African American mothers 0.25 aAttributable fraction was calculated with the following formula: attributable fraction = [(incidence among all children in the cohort) - (incidence among children of mothers who did not smoke)] / [incidence among atl children in the cohort]. Incidence = number of cases per 100 000 person-years. during pregnanc): Approximately one quarter of invasive meningococcal disease among children could be attributed to passive expo- sure to cigarette smoke. Several case-control studies" ~z have linked exposure to cigarette smoke with inva- sive meningococcal disease. In one study in the United Kingdom, children younger than 5 years who were exposed to cigarette smoke at home were 4.5 times ~nore likely to acquire meningococcal disease than were controls.9 These differences remained statistically sig- nificant even after control for social class. A dose-response relation was found between the number of cigarettes s~noked at home and the likelihood of invasive meningococcal disease. Fischer et al. have reported that dur- ing an outbreak of serogroup B disease in the Pacific Northwest among children younger lhan 18 years, cigarette smoking by the mother was the strongest independent risk factor (odds ratio - 3.8) for invasive meningococcal disease) Mechanisms that may determine the increased risk of meningococcal disease as a result of cigarette smoke exposure include the deleterious effects of cigarette smoke on mucosal integrity and the irrtmune system,s Cigarette smoke depresses respiratory mucus secretion and bronchial ciliary activ- ity and may reduce the effectiveness of the respiratory mucosa to act as a protective barrier against bacterial pathogens. Exposure to cigarette smoke adversely affects macrophage activity and neutrophil func- tion:~ 23 and may indirectly increase the risk for meningococcal infection by predispos- ing children to viral respiratory infections.2~ Concurrent viral upper respiratory tract infections have been linked to meningo- coccal diseascfls 27 Several studies have implicated cigarette smoking as a risk factor for increased nasopharyngeal carriage of N meningitidis.~4"v~-3* Therefore, children exposed to smokers may have a high likeli- hood of exposure to the pathogen, a high rate of carriage acquisition, or prolonged carriage of N memngitidis. The age-specific incidence we found (highest for infants I year and younger) was consistent with previous reports that meningococcal attack rates are highest dur- ing the first year of life, t': The incidence among I- to 2-year-old and 2- to 3-year-old children (2.0 and 2.9 per 100000 person- years, respectively) were also consistent with previous estimates. ~'~ National esti- mates for annual incidence of meningococ- cal disease for people of all ages is about 1 in 100 000 persons.Ls~ Our finding that serogroups B and C accounted for most cases was also consistent with national esti- mates reported close to or during the time of our surveillance,~'3~ Although meningococcat disease has been reported to have a higher incidence Maternal Smoking and Meningoen¢cal Disease among males than females aqd among Blacks than Whites,Ls5 we found no signifi- cant association by sex or race. Previous studies have reported an association be~veen low socioeconomic status and meningococ- cal disease6"~s~'37 because of an increased likelihood of acquiring meningococcal infec- tion through factors such as increased house- hold crowding and poor nutrition.6"9"38~° The level of educational attainment is commonly used as a proxy for socioeconomic statusf In our cohort, low maternal education level was independently associated with increased risk for invasive meningococcal disease for young children. Young maternal age at deliv- ery, being an unmarried mother, and receiv- ing Medicaid are also associated with low socioeconomic status, and in our cohort these factors were univariately associated with meningococcal disease in all children and in children of White mothers. One limitation of this study is that the number of cases of invasive meningococcal disease was small, considering the breadth of the study population. We did not account for out-migration from the study area and may have missed counting some meningococcal cases. However, because the incidence of the disease was very low and the median follow- up duration for most children was 3 years (most cases occurred within the first year of life), movement of participants out of the study area is unlikely to have strongly influ- enced our findings. Another limitation is that cigareue smo "king by the mother during preg- nancy was identified through self-reported information acquired from birth certificates. A total of 10.3% of all mothers were reported to have smoked during pregnancy, and the rate was higher among White mothers than Black mothers ( 12.2% vs 8.3%). Using data from a postdelivery mail survey of a sample of women who gave birth in Georgia, epi- demiologists recently estimated that about 34% of women who smoke during pregnancy do not have this tact documented on the childk birth ceaificate,a2 In addition, under- reporting of smoking may be greater among Black women and women with higher educa- tion levels.~z However, underreporting of maternal smoking would bias the potential association between smoking and meningo- coccal disease toward the null. Because we could not directly measure the passive exposure of children to cigarette smoke, we assumed that mothers who reported smoking during pregnancy continued to smoke after giving birth. Studies have shown that most women who smoke at any time during pregnancy do so throughout preg- nancy, and among those who quit smoking during pregnancy, most relapse shortly after giving birth.~z-4s Relapsers who report they May 1999, Vol. 89, No. 5 American Journal of Public Health 715 325307772

~'usuf et did not smoke during pregnancy would decrease the apparent magratude of the idenli- fled risk between passive tobacco smoke exposure and mcningococcal disease. Thus, a concerned mother may stop smoking during pregnancy and be reported as a nonsmoker, but she may resume smoking after delivery and unknowingly place her infant at increased risk for im~.sive meningococcal disease. The~ findings, in addition to the fact that adverse health effects during infancy can result from exposure to cigarette smoke in utero,~ suggest that our findings are valid. Further, this study did not account tbr the exposure of children to cigarette smoke from persons in the household other than the mother. One s~ength of ottr study is that all resi- dent cases of invasive meningococcal disease ~vere identified through a laboratory-based active surveillance system, and periodic audits were used to optimize the accuracy of detection. Studies have shown that, compared with passive surveillance systems, laboratory- based active surveillance for meningococcal disease is more accurate and able to identi~¢ twice as many cases.~:~s The use of birth cer- tificate data allowed the examination of sev- eral infant and maternal characteristics; the reporting accuracy of a number of these has already been evaluated. Our study illustrates how the linking of information ~om birth and death certificate databases to data from a pop- ulalion-based surveillance system for disease can be used to follow a birth cohort. For low-- incidence diseases, this methodology may provide a simple, low-cost, yet powerful approach tbr assessing population-based rote.,; by selected characteristics, computing relative risks, and examining trends. Moreover, this methodology pcrntits an efficienl approach to evaluating the effect of strategies to reduce: risk lhctors such as maternal smoking and auk changes in their association with meningo- coccal or other disease. Maternal smoking during pregnancy has been associated with several adverse health effects on the fetus and infant, including pre- maturib', low birthweight, and sudden infant death syndrome.*~ Studies have shown that passive exposure to cigarene smoke increases a child's susceptibility to various infec- tions.~ s~ Our findings support recent reporls linking exposure to cigarelte smoke with increased risk tbr invasive meningococcal disease in young children, and they add to the impetus for promoting smoking cessation among pregnant women and mothers. Health care providers and the general public need to be informed that cigarette smoking may be a strong risk factor for meningococcal disease. Smoking prevention can form an integral part of efforts to prevent meningococcal dis- ease. At least 2 Web sites ~Universil2¢ of Illi- 716 American Joumaal of Public Health nois at Urbana and National Meningitis Trust Fund) provide information on meningitis pre- vention and indicate that avoidance of expo- sure to cigarette smoke may' reduce the risk for acquiring the disease. Because the associ- ation between exposure to cigarette smoke and invasive meningococcal disease has implications lbr public health, this research should be replicated in other geographic areas where meningococcal disease surveil- lance is occurring ~ Contributors H. R. Yusufplanned the study, analyzed the data, and wxote the paper. R.W. Rochat and D. S Stephens co- supervised study planning and implemematton W S Baughman developed the meningococcal d~seasc active st~rveillance database and assisted with stud~ design. P. M. Gargiullo assisted with stat~slical analysis and study design. B A Perkins assisted with planning of study and interpretation of results M.D. Brar~tley assisted with matching birth and death record databases to develop a follow-up cohort, matching meningococcal cases lo the cohorl. and designing the study. R. W. Rochat, D S Stephens, W. S. Baughman, P. M Garg~allo, P, A Perkins, and M. D. Brantley contributed to wm~tng the paper. All 7 aulhors are guar,rnltas for the integrity of the research Acknowledgments Wc gratefully thank the following institutions and individuals lbr the assistance and support lhey pro- vided to this study: Georgia Emerging Infectiou., Diseases Program, Atlanta, and hospitals and staffot the Atlanta Acll,,c Surveillance Progran~ References Jack,on [z~. "¢V~nger JD. Laboratory-based s~tr- veillance for meningococcal disease in selected areas, United States, 1989 1991. MMWR Mm4~ Mortal Whir Rep 1993;42tSS-2):21-~,t) 2 Fortnum HM. Davis AC. Epidemiology of bac- terial meningitis..4rch Dis" Chtld. 1993:68 763 767. 3 Pinner RW. 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