Use of birth certificates and surveillance data to characterize reported pertussis among Texas infants and young children, 1995 to 2000.

Background: Pertussis morbidity is increasing, especially among young infants and children, who are more likely to be hospitalized and have more severe complications. Maternal and pediatric factors associated with underimmunization and hospitalization for pertussis are poorly understood, but young maternal age and low birth weight have been associated with pertussis among young infants.

Methods: We used pertussis surveillance data, matching cases to the birth certificates of 416 Texas infants and children reported as pertussis cases during 1995 to 2000. Maternal/pediatric information gathered from birth certificates included birth weight, gestational age, and maternal factors (age, birthplace and education level, prenatal care, and previous live birth). We assessed the immunization status of the cases and maternal/pediatric factors associated with underimmunization with a pertussis-containing vaccine and hospitalization using descriptive statistics and logistic regression.

Results: The 416 cases represented 20% of the pertussis morbidity in Texas from 1995 through 2000. Most children had not been vaccinated (275 [66%]), even though 374 (90%) were old enough for at least one dose. Among those 374 children, only those younger than 6 months were associated with underimmunization (odds ratio [OR], 9.98; 95% confidence interval [CI], 6.24-15.97). Most patients (253 [61%]) were hospitalized. Hospitalization was associated with complications of apnea (OR, 2.13; 95% CI, 1.39-2.38), pneumonia (OR, 5.26; 95% CI, 2.94-11.59), and age younger than 6 months (OR, 2.11; 95% CI, 1.38-3.23).

Conclusion: More than two-thirds of the children reported as pertussis cases were old enough to have at least one dose of a pertussis-containing vaccine but were not immunized. Maternal and pediatric characteristics on birth certificates were not useful in predicting either underimmunization or hospitalization for pertussis complications. More current assessments of maternal and pediatric characteristics should be part of pertussis contact investigations.

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Pertussis is an ancient disease that today continues to cause major morbidity and mortality for several reasons. Adults and adolescents are now known to be a source of infection for children too young to be immunized appropriately, (1) but booster doses are not yet recommended for persons older than 7 years of age. (2) The number of pertussis cases has risen steadily since 1976, especially among infants too young to have received three doses of pertussis-containing vaccine. (3)

Infants younger than 7 months of age are at special risk of acquiring pertussis because immunity is short-lived, meaning maternal antibodies that cross the placenta are not protective for infants. (4) In addition, the three-dose primary series is not completed until 6 months of age. (2) Developing a detailed picture to explain why such increases have occurred is difficult because routine pertussis surveillance does not capture pediatric and maternal factors that might be possible risk factors both for pertussis disease and delayed vaccination. Possible risk factors for pertussis disease include prematurity, (5) young maternal age, (6) family size, (7) and low birth weight. (8) An additional factor might be poor vaccine coverage, which could be especially relevant for Texas, where up-to-date vaccination has been as low as 11%. (9) Low-birth-weight infants (10), (11) and infants admitted to neonatal intensive care units (11), (12) have been found less likely to be adequately vaccinated with a pertussis-containing vaccine, a factor that could contribute to pertussis morbidity. Other studies have associated poor immunization levels with birth order, (13), (14) inadequate prenatal care, (14), (15) adolescent mothers, (16) and single-parent households. (13), (16)

The Texas Department of Health (TDH) has used data from birth certificates to provide supplemental information about maternal and prenatal characteristics in the surveillance of communicable disease. Such vital statistics data have been used to assess immunization status of children born to human immunodeficiency virus-infected mothers, (17) assess underimmunization of Texas children reported as measles cases, (14) and assess risk factors for congenital syphilis. (18) In this study, we used vital statistics data to supplement pertussis surveillance data to examine maternal and pediatric factors that might explain pertussis morbidity and mortality in children younger than 2 years of age.

Methods

Pertussis cases are routinely reported to the Immunization Division at the Texas Department of Health. Data routinely collected in a pertussis case report (19) include age, gender, race/ethnicity, place of residence, numbers of doses of pertussis vaccine administered, dates that such doses were administered, and complications of pertussis. These include apnea, hospitalization, seizures, encephalopathy, pneumonia, and death.

Birth certificate data that could be useful in supplementary surveillance include infant birth weight, birth city, maternal age, education (high school graduate versus not completing high school), place of birth (United States versus foreign), marital status, prenatal care (for the pregnancy involving the child reported as pertussis case), and previous live births. All these items are routinely collected on the Texas birth certificates.

For the calendar years 1995 through 2000, the Texas Immunization Program identified all cases of pertussis reported among Texas children aged 0 to 2 years. The pertussis surveillance database was used to generate each infant's name, date of birth, ethnicity, and gender. The immunization program performed four-for-four matching (surname, ethnicity, date of birth, and gender) with birth certificates, which also contained the mother's name. A final analysis data set containing both the pertussis and birth certificate information was created by the TDH with the names of infants and mothers stripped from the data set.

Definitions

We used prenatal care data in the birth certificates to calculate an index of inadequate/adequate prenatal care using the Kotelchuck index, (20), (21) a composite index based on two subscales. The first subscale considers the month of pregnancy during which a woman initially sought prenatal care (months 1-4 versus months 5-9). The second subscale assesses the percentage of recommended prenatal visits the mother had based on the infant's gestational age at birth. The composite index has categories of prenatal care: none, inadequate, intermediate, adequate, and adequate-plus. In the study analysis, a dichotomous variable was created for logistic regression. It compared the women who had no or inadequate prenatal care with those who had intermediate, adequate, or adequate-plus care. Low-birth-weight infants weighed less than 2,500 g. Premature infants were born before 37 weeks' gestation.

Statistical Analysis

The children reported as pertussis cases and their mothers were characterized using descriptive statistics, univariate analyses, and logistic regressions. The data set was used to describe characteristics of children and mothers, and in logistic regression models to assess risk factors associated with hospitalization and lack of any pertussis vaccination. In the univariate analysis and logistic regressions, we calculated odds ratios and 95% confidence intervals. Confidence intervals that did not overlap 1 were considered significant. The logistic regression was performed using all variables that were significant in the univariate analysis. One logistic regression was performed to assess risk factors associated with hospitalization for pertussis among all 416 cases. A second logistic regression analyzed possible risk factors associated with a lack of any immunizations with a pertussis-containing vaccine among 374 cases old enough to have been vaccinated. EpiInfo version 6 (22) was used for data entry and descriptive statistics, and SAS version 6.12 (23) was used for multivariate logistic regression.

Results

Pediatric and Maternal Characteristics

During the 6-year period, 416 children aged 0 to 2 years were reported as pertussis cases, representing 20% of the 2,045 cases reported to the Centers for Disease Control and Prevention by the TDH. (24) Of the 416 cases, 392 (93%) were culture confirmed for Bordetella pertussis. The pediatric cases were equally distributed between male and female (208 [50%]), their racial distribution was predominantly Hispanic (223 [54%]), and most had one or more older siblings (262 [63%]). A minority of children were reported to have been low birth weight (32 [8%]) or to have been premature at birth (58 [14%]).

The cases were reported from 70 Texas counties, but the majority (261 [63%]) were from the state's large metropolitan areas (cities with at least 250,000 population). Harris County (Houston) reported 51 (12%) cases; Bexar County (San Antonio), 70 (17%); Dallas County (Dallas), 68 (16%); Tarrant County (Ft. Worth), 28 (7%); Travis County (Austin), 21 (5%); and Nueces (Corpus Christi), 23 (6%).

The median maternal age was 24.8 years (range, 14-42 years). Relatively large proportions of mothers were unmarried (167 [40%]) and had not finished high school (190 [46%]). Most mothers had been born in the United States (337 [81%]). A minority of mothers were adolescents (97 [23%]) and had no or inadequate prenatal care (90 [22%]) according to the Kotelchuck guidelines.

Immunization and Pertussis Complications

Most children had not received any doses of diphtheria/tetanus/pertussis (275 [66%]), even though 374 (90%) were old enough to have had at least one dose of a pertussis-containing vaccine. Only 13 (12%) of the 105 children who were 7 months of age or older and thus eligible to complete the three-dose series had done so. The age distribution and vaccine status of the cases are shown in Table 1.

Among the large metropolitan counties that reported most pertussis cases, vaccination coverage was poor. The numbers of cases and numbers who were not immunized with a pertussis-containing vaccine are shown in Table 2. In those counties, between 38 and 80% of the children old enough to have been vaccinated had received no doses.

In univariate modeling, the only risk factor associated with being unimmunized against pertussis was age less than 6 months. That age remained significant in the multivariate model (Table 3).

Hospitalizations, Complications, and Deaths

Complications were common in this group of children; 253 (61%) were hospitalized with a median stay of 5 days (range, 1-42 days). A total of 209 children (50%) reported complications that included apnea (176 [42%]), pneumonia (62 [15%]), seizures (5 [1%]), and death (2 [0.5%]). No cases of encephalopathy were reported. Multiple complications occurred in 31 children: 26 had apnea and pneumonia; 4 had seizures and apnea; and 1 had apnea, pneumonia, and seizures. The two children who died were both Hispanic girls from West Texas. Both were 1 month of age, had apnea and pneumonia, and died after hospital admission. Neither infant was low birth weight or premature. In univariate modeling, hospital admission was associated with an age of less than 6 months; having no immunizations for pertussis; and complications of apnea, pneumonia, and seizures. No maternal characteristics were associated with a risk of hospitalization. Apnea, pneumonia, and age younger than 6 months remained significant in the multivariate model (Table 4).

Discussion

Texas reported 1,057 pertussis cases during the 6-year study period, (24) 3% of the 34,560 pertussis cases reported nationally. Almost 40% of the Texas children reported as pertussis cases were 2 years of age or younger when reported. Two-thirds of the children had received no immunizations with pertussis-containing vaccines, although 90% were old enough to have received at least one dose and 60% of the children were hospitalized.

Using these population-based data and supplementary data from birth certificates, we have confirmed earlier studies regarding risk factors for hospitalization among pertussis cases and underimmunization with a pertussis-containing vaccine. Using the supplementary birth certificate data, we have also been unable to ascertain any new pediatric or maternal risk factors for hospitalization or underimmunization among children reported with pertussis.

Our finding that children 6 months of age or younger were likely to be admitted to the hospital replicates prior work done in Germany, France, Canada, and the United States. (6), (7), (25-28) In undertaking this study, we evaluated a number of maternal and pediatric characteristics that have been associated with pertussis disease (prematurity, low birth weight, young maternal age, and family size) and others that had not previously been associated with pertussis (child's place of residence, maternal birthplace, marital status, and maternal education). The lack of association between young maternal age and later birth order with pertussis hospitalization is surprising because young adults are considered a possible source of pertussis transmission (6), (29) and such transmission often occurs in larger families. (29-31) It is possible that we did not find such associations using birth certificate data because these data are not current or detailed enough to reflect the dynamics of pertussis transmission months to years after birth.

In this study, prematurity and low birth weight may not have been associated with pertussis hospitalization because those perinatal conditions existed only among a minority of the Texas cases. In addition, the infants' health at the time of exposure to pertussis may have been better than the precarious start in life that is indicated by prematurity and/or low birth weight. We had expected such an association could exist because low-birth-weight infants face a greater risk of rehospitalization in the first year of life. (32), (33)

Perhaps such maternal and pediatric factors can better be assessed in the interviews that are performed as part of a contact investigation of a pertussis case (34), (35) Asking about maternal and pediatric characteristics during a pertussis case investigation would be more timely than examining birth certificate data and might be useful in identifying especially high-risk contacts and should be evaluated in a prospective manner. Such an assessment might be useful as part of enhanced pertussis surveillance in Texas, where multiple out-breaks of pertussis have been reported in the past 2 years. (40), (41)

A second issue of concern identified in this study is that this population of infants and young children with pertussis was so poorly immunized. Even though 90% of the pertussis cases were old enough to have received at least one dose of a pertussis-containing vaccine, two-thirds of infants and children had not received any doses. Poor immunization rates have been reported in countries where pertussis immunization had been suspended (6), (7) and was being reintroduced. However, the Texas immunization coverage for children for any dose of pertussis-containing vaccine in this study is much lower than coverage reported in Chicago and Cincinnati, (26), (36) two cities where larger pertussis outbreaks were reported in the last decade. How much of the poor vaccine coverage noted among cases is due to poor immunization coverage among all Texas children is an issue that is difficult to assess. At one point in the early 1990s, immunization coverage in inner-city Houston was 11%, (9) the lowest of any major U.S. city. Immunization coverage has improved from that nadir, reaching a level of 55% in the mid-1990s (37) and 71% in 2000. (38) However, those levels are well below the U.S. goal of 90% immunization levels for all U.S. 2-year-olds. (39) The relationship between deficient immunization coverage in Texas and reported pertussis in young children merits more detailed study.

Summary

This study found that children 2 years of age or younger who are reported with pertussis in Texas are likely to be hospitalized, but that birth certificate data were not useful in identifying risk factors to predict such admissions. Updated maternal and pediatric information should be sought during the contact investigations done for pertussis cases, and a prospective evaluation of such efforts is merited. We also found that most Texas children reported as pertussis cases had received no doses of a pertussis-containing vaccine. The contribution of poor immunization coverage to the state's pertussis morbidity merits further study. Given the combination of pertussis outbreaks (40), (41) and a history of poor immunization against pertussis, it is possible that pertussis reporting in Texas is deficient.

The doctor may also learn more about the illness from the way the patient tells the story than from the story itself.

--James B. Herrick (1861-1954)

Table 1. Doses of pertussis-containing vaccine by
child's age at pertussis onset

                No. of doses

Age       0    1    2   3  4  Total

< 2 mo    42   -    -   -  -    42
2-3 mo   104   -    -   -  -   104
4-5 mo    57   22   -   1  -    80
6-12 mo   49   65   7   -  -   121
> 1 yr    23   18  13  14  1    69
Total    285  105  20  15  1   416

Table 2. Doses of pertussis-containing vaccine among
pertussis cases in urban Texas counties

                             No. of doses

County (largest city)     0   1  2  3  4  Total

Bexar (San Antonio)      45  18  3  3  1     70
Dallas (Dallas)          37  24  4  3  0     68
E1 Paso (E1 Paso)         1   1  0  0  0      2
Harris (Houston)         42   8  1  0  0     51
Nueces (Corpus Christi)  13   6  1  3  0     23
Tarrant (Ft. Worth)      18   8  1  1  0     28
Travis (Austin)          11   7  3  0  0     21

Table 3. Predictors of no immunizations among 374 infant pertussis cases
age-eligible for administration of a pertussis-containing vaccine,
1995-2000 (a)

                                                       Percent
Factor                                    Total no.  unimmunized

Infant characteristics
   Sex
     Male                                   187          63
     Female                                 187          62

   Age
     <6 mo                                  184          88
     [greater than or equal to]6 mo         190          38

   Race/ethnicity
     White                                  118          60
     Hispanic                               197          63
     Black                                   53          62
     Other                                    6          67

   Urban                                    345          62
   Rural                                     29          66

   LBW
     Yes                                     32          50
     No                                     342          63

   Premature
     Yes                                     55          62
     No                                     319          62

   Older siblings                           238          59
   Firstborn                                136          68

  Maternal characteristic
   Maternal age
     <20 yr                                  86          66
     [greater than or equal to]20 yr        288          61

   Married                                  222          59
   Unmarried                                152          68
   HS Dropout                               166          66
   HS Graduate                              208          59
   U.S.-born mother                         306          61
   Foreign-born mother                       68          66

   Prenatal care
     None/inadequate                         80          68
     adequate/adequate+                     294          61

   Pregnancy
     Complications                          121          62
     No complications                       253          62

Factor                                Crude OR (95% CI)

Infant characteristics
   Sex
     Male                               1.02 (0.66-1.59)
     Female                                  Ref

   Age
     <6 mo                             11.47 (6.58-20.14)
     [greater than or equal to]6 mo           Ref

   Race/ethnicity
     White                                    Ref
     Hispanic                           1.15 (0.70-1.89)
     Black                              1.09 (0.53-2.25)
     Other                              1.32 (0.18-15.15)

   Urban                                0.86 (0.36-2.02)
   Rural                                      Ref

   LBW
     Yes                                0.58 (0.26-1.26)
     No                                       Ref

   Premature
     Yes                                0.98 (0.52-1.84)
     No                                       Ref

   Older siblings                       0.66 (0.41-1.05)
   Firstborn                                  Ref

  Maternal characteristic
   Maternal age
     <20 yr                             1.24 (0.72-2.12)
     [greater than or equal to]20 yr          Ref

   Married                              0.67 (0.43-1.06)
   Unmarried                                  Ref
   HS Dropout                           1.30 (0.83-2.02)
   HS Graduate                                Ref
   U.S.-born mother                     0.81 (0.45-1.46)
   Foreign-born mother                        Ref

   Prenatal care
     None/inadequate                    1.33 (0.77-2.33)
     adequate/adequate+                       Ref

   Pregnancy
     Complications                      0.98 (0.61-1.57)
     No complications                         Ref

Factor                                Adjusted OR (95% CI)

Infant characteristics
   Sex
     Male
     Female

   Age
     <6 mo                            9.98 (6.24-15.97)
     [greater than or equal to]6 mo

   Race/ethnicity
     White
     Hispanic
     Black
     Other

   Urban
   Rural

   LBW
     Yes
     No

   Premature
     Yes
     No

   Older siblings
   Firstborn

  Maternal characteristic
   Maternal age
     <20 yr
     [greater than or equal to]20 yr

   Married
   Unmarried
   HS Dropout
   HS Graduate
   U.S.-born mother
   Foreign-born mother

   Prenatal care
     None/inadequate
     adequate/adequate+

   Pregnancy
     Complications
     No complications

(a) OR, odds ratio; CI, confidence interval; Ref, reference; LBW, low
birth weight; HS, high school.

Table 4. Predictors of hospital admissions among 416 infant pertussis
cases, Texas, 1995-2000 (a)

                                                 Proportion
Characteristics                       Total no.   admitted

Infant characteristics
   Sex
     Male                               208         48
     Female                             208         52

   Age
     <6 mo                              262         70
     [greater than or equal to]6 mo     154         49

   Race/ethnicity
     White                              127         62
     Hispanic                           223         62
     Black                               59         56
     Other                                7         71

   LBW
     Yes                                 32         75
     No                                 384         60

   Premature birth
     Yes                                 61         67
     No                                 358         59

   Older siblings                       262         62
   Firstborn                            163         56
   No pertussis shots                   275         67
   Pertussis shots                      141         50
   Apnea                                176         72
   No apnea                             240         53
   Pneumonia                             62         87
   No pneumonia                         354         56
   Seizure                                5         80
   No seizure                           410         61

  Maternal characteristics
   Maternal age
     <20 yr                              97         63
     [greater than or equal to]20 yr    319         61

   Married                              249         61
   Not married                          167         60
   HS dropout                           190         63
   HS graduate                          226         59
   U.S.-born mother                     337         59
   Foreign-born mother                   79         67

   Prenatal care
     None/inadequate                     88         63
     Adequate/adequate+                 326         61

   Pregnancy complications
     Yes                                136         60
     No                                 280         61

Characteristics                       Crude OR (95% CI)

Infant characteristics
   Sex
     Male                              0.83 (0.55-1.26)
     Female                                  Ref

   Age
     <6 mo                             2.23 (1.45-3.43)
     [greater than or equal to]6 mo          Ref

   Race/ethnicity
     White                                   Ref
     Hispanic                          0.99 (0.61-1.58)
     Black                             0.77 (0.39-1.51)
     Other                             1.52 (0.24-16.49)

   LBW
     Yes                               0.55 (0.23-1.28)
     No                                      Ref

   Premature birth
     Yes                               0.60 (0.31-1.14)
     No                                      Ref

   Older siblings                      1.12 (0.73-1.72)
   Firstborn                                 Ref
   No pertussis shots                  2.02 (1.31-3.12)
   Pertussis shots                           Ref
   Apnea                               2.24 (1.45-3.47)
   No apnea                                  Ref
   Pneumonia                           5.26 (2.33-12.33)
   No pneumonia                              Ref
   Seizure                             2.60 (0.25-128.94)
   No seizure                                Ref

  Maternal characteristics
   Maternal age
     <20 yr                            0.89 (0.54-1.46)
     [greater than or equal to]20 yr         Ref

   Married                             1.02 (0.67-1.56)
   Not married                               Ref
   HS dropout                          1.15 (0.76-1.74)
   HS graduate                               Ref
   U.S.-born mother                    0.72 (0.41-1.24)
   Foreign-born mother                       Ref

   Prenatal care
     None/inadequate                   1.02 (0.61-1.69)
     Adequate/adequate+                      Ref

   Pregnancy complications
     Yes                               0.97 (0.62-1.50)
     No                                      Ref

Characteristics                       Adjusted OR (95% CI)

Infant characteristics
   Sex
     Male
     Female

   Age
     <6 mo                              2.11 (1.38-3.23)
     [greater than or equal to]6 mo

   Race/ethnicity
     White
     Hispanic
     Black
     Other

   LBW
     Yes
     No

   Premature birth
     Yes
     No

   Older siblings
   Firstborn
   No pertussis shots
   Pertussis shots
   Apnea                                2.13 (1.38-3.28)
   No apnea
   Pneumonia                            5.26 (2.94-11.59)
   No pneumonia
   Seizure
   No seizure

  Maternal characteristics
   Maternal age
     <20 yr
     [greater than or equal to]20 yr

   Married
   Not married
   HS dropout
   HS graduate
   U.S.-born mother
   Foreign-born mother

   Prenatal care
     None/inadequate
     Adequate/adequate+

   Pregnancy complications
     Yes
     No

(a) OR, odds ratio; CI, confidence interval; LBW, low birth weight; HS,
high school; Ref, reference.

Accepted December 11, 2002.

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(36.) Kenyon TA, Izurieta H, Shulman ST, et al. Large outbreak of pertussis among young children in Chicago, 1993: Investigation of potential contributing factors and estimation of vaccine effectiveness. Pediatr Infect Dis J 1996;15:655-661.

(37.) Simpson DM, Suarez L. The immunization status of Texas children aged 3 to 24 months: Results of the 1994 Texas immunization survey. Tex Med 1996;92:60-65.

(38.) CDC. National, state and urban area vaccination covers levels among children aged 19-35 months: United States, 2000. MMWR 2001;50:636-641.

(39.) U.S. Department of Health and Human Services, Public Health Service. Healthy People 2000: National Health Promotion and Disease Prevention Objectives. Washington, DC, U.S. Government Printing office, 1990.

(40.) Texas Department of Health. Pertussis in Texas. Dis Prev News 2001;61:1-5.

(41.) Texas Department of Health. Surge in pertussis cases continues. Dis Prev News 2002;62:1-2.

RELATED ARTICLE: Key Points

* Birth certificate data contain information that has been used to identify risk factors for infectious diseases.

* Two-thirds of children old enough to be vaccinated had not received any doses of vaccine.

* Pertussis surveillance should include an assessment of maternal and pediatric factors that might be associated with transmission of pertussis.

Jan W. Pelosi, MPH, and Joann M. Schulte, DO

From the Immunization Division, Texas Department of Health, Austin, TX, and the Rollins School of Public Health, Emory University, Atlanta, GA.

Reprint requests to Joann M. Schulte, DO, Florida Department of Health, 4052 Bald Cypress Way, Bin A13, Tallahassee, FL 32399. Email: [e-mail]

Copyright [c] 2003 by The Southern Medical Association

0038-4348/03/9612-1231