poa15018_647_652.pdf

ARTICLE

Infant Pertussis Epidemiology and Implicationsfor Tetanus Toxoid, Reduced Diphtheria Toxoid,and Acellular Pertussis (Tdap) Vaccination

King County, Washington, 2002 Through 2007

Matthew P. Hanson, MD, DTM&H; Tao S. Kwan-Gett, MD, MPH; Atar Baer, PhD;Krista Rietberg, MPH; Mara Ohrt, MPH; Jeffrey S. Duchin, MD

Objectives: To describe the epidemiology of infantpertussis in King County, Washington, and to betterunderstand the implications for tetanus toxoid,reduced diphtheria toxoid, and acellular pertussis(Tdap) vaccination among older children, adolescents,and adults.

Design: Retrospective analysis of reported pertussis casesamong infants younger than 1 year, January 1, 2002,through December 31, 2007.

Setting: King County, Washington.

Participants: Reported pertussis cases among infantsyounger than 1 year between 2002 and 2007.

Main Outcome Measures: Bordetella pertussis froma household member or close contact was the primaryexposure. The main outcome measures were age and vac-cination status, incidence by race/ethnicity, suspected ex-posure, and Tdap eligibility of household members andclose contacts.

Results: Among 176 confirmed cases of infants with per-tussis,themedianagewas3months(agerange,0-11months);80.1%wereyounger than6months.Seventy-sevenpercentwereage-appropriatelyvaccinated.Between2002and2007,theoverallmeanannual incidencewas136casesper100 000infantpopulation.Comparedwithameanannual incidenceof73casesper100 000infantpopulationamongwhites, theincidencewas246casesper100 000infantpopulationamongblacks (rate ratio [RR], 3.37; 95% confidence interval [CI],2.59-4.44)and194casesper100000infantpopulationamongHispanics (RR,2.66;95%CI,2.02-3.53).Householdswerethe suspected exposure location for 70.0% of cases. Casehouseholds had a median of 3 (range, 1-15) Tdap-eligiblepersons.

Conclusions: The burden of infant pertussis in KingCounty, Washington, was high between 2002 and 2007,especially among racial/ethnic minorities. Tdap vacci-nation of eligible household members and close con-tacts should be promoted as an additional means of pro-tecting infants from pertussis.

Arch Pediatr Adolesc Med. 2011;165(7):647-652

P ERTUSSIS IS A CONTAGIOUS RE-spiratory tract illness causedby infection of the nasophar-ynx with the gram-negativecoccobacillus Bordetella per-

tussis. The illness is characterized by a par-oxysmal cough, followed by an inspira-tory whoop and posttussive vomiting. Thecough can last for weeks, but fever is usu-ally absent or of low grade. Infants hav-ing pertussis can be seen with apnea andcyanosis, whereas older children, adoles-cents, and adults may have symptoms simi-lar to those of a common viral respiratorytract illness. Most important, infants aremore likely to experience serious compli-cations of pertussis infection (eg, pneu-monia, encephalopathy, and seizures) thatlead to hospitalization and death.1,2

Before the introduction of whole-cell per-tussis vaccine for children in the 1940s, an

estimated 160 000 pertussis cases and morethan 5000 deaths occurred annually in theUnited States.3 During the 4 decades afterintroduction of whole-cell pertussis vac-cine, pertussis incidence declined dramati-cally, reaching an all-time low in 1976, withonly 1010 cases reported.4 Since then, anddespite continued vaccination efforts, re-ported pertussis cases have been on the rise.5

This increase in the number of reportedcases peaked in 2004 with 25 827 cases.6 Re-ported cases for 2005 were 25 616, similarto 2004, but in 2006 decreased to 15 632cases.7,8 For infants younger than 1 year, thereported annual incidence of pertussis in2005 was 97 cases per 100 000 infant popu-lation compared with 8.7 cases per 100 000overall population.7

The Advisory Committee on Immuni-zation Practices recommends that infantsshould receive the first 3 diphtheria and teta-

Author Affiliations: EpidemicIntelligence Service, Centers forDisease Control and Prevention,Atlanta, Georgia (Dr Hanson);Public Health–Seattle & KingCounty, Communicable DiseaseEpidemiology andImmunization Section(Drs Hanson, Kwan-Gett, Baer,and Duchin and Ms Rietberg),and Division of InfectiousDiseases, Department ofMedicine, University ofWashington (Dr Duchin),Seattle; and ImmunizationProgram, Section ofEpidemiology, Division ofPublic Health, Department ofHealth and Social Services, Stateof Alaska, Anchorage(Ms Ohrt). Dr Hanson is nowwith the Global HealthProgram, Bill & Melinda GatesFoundation, Seattle.

ARCH PEDIATR ADOLESC MED/ VOL 165 (NO. 7), JULY 2011 WWW.ARCHPEDIATRICS.COM647

©2011 American Medical Association. All rights reserved.

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nus toxoids and acellular pertussis (DTaP) vaccinations atages 2, 4, and 6 months.9,10 Additional doses are recom-mended at ages 15 to 18 months and 4 to 6 years. The ef-ficacy of 3 doses of DTaP is 80% to 85% against confirmedcases of pertussis as defined by the World Health Organi-zation (paroxysmal cough for �21 days and confirmed byculture, serology, or an epidemiologic link to a confirmedcase).11-13 Vaccine efficacy after 1 or 2 doses of DTaP is notclearly defined but seems to increase with each successivedose. Therefore, infants younger than 6 months are par-ticularly vulnerable to pertussis: they are the age groupamong whom pertussis disease is most severe, and they arenot well protected even if they are age-appropriately vac-cinated because they have not yet received 3 DTaP doses.

An additional tool is needed to offer protection toyoung infants during this period when they are most vul-nerable. Two new vaccines, developed for older chil-dren, adolescents, and adults, show promise in this re-gard. These vaccines combine tetanus toxoid, reduceddiphtheria toxoid, and acellular pertussis (Tdap) and werelicensed in the United States by the Food and Drug Ad-ministration in 2005. One of the Tdap vaccines, Adacel,was produced by Sanofi Pasteur (Lyon, France) and waslicensed for persons aged 11 to 64 years. The other Tdapvaccine, Boostrix, was produced by GlaxoSmithKline(London, England) and was licensed for persons aged 10to 18 years. Tdap was designed for older children, ado-lescents, and adults, populations regarded as the majorreservoirs for pertussis transmission to infants.14 In 2005,a single dose of Tdap (to replace a single dose of tetanustoxoid and reduced diphtheria toxoid vaccine [Td] if thelast booster vaccination for Td was administered �10years earlier) was recommended by the Advisory Com-mittee on Immunization Practice for routine use amongolder children and adolescents aged 11 to 18 years andadults aged 19 to 64 years.15,16 In 2008, the Advisory Com-mittee on Immunization Practice and the American Col-lege of Obstetricians and Gynecologists recommendedTdap vaccination in previously unvaccinated women dur-ing the immediate postpartum period.17

We reviewed reported cases of infant pertussis in KingCounty, Washington, between 2002 and 2007. Objec-tives of the study were to describe the epidemiology ofthis disease, to assess the burden of presumed house-hold transmission, and to evaluate the eligibility for Tdapvaccination of household members and close contacts ofinfants with confirmed pertussis.

METHODS

Notifiable disease surveillance data from Public Health–Seattle & King County served as the primary data source forthis study. Cases were reported from multiple sources, includ-ing laboratories, health care providers (ie, physicians, nurse prac-titioners, and nurses), hospitals, and clinics. After a pertussiscase is reported to Public Health–Seattle & King County, pub-lic health personnel investigate to gather information on de-mographics, vaccination status, clinical course, contacts, andthe need for public health intervention. Records of pertussiscase investigations among infants younger than 1 year re-ported from January 1, 2002, through December 31, 2007, werereviewed for this study.

We used the 1997 Centers for Disease Control and Preven-tion–Council of State and Territorial Epidemiologists case defi-nition and classification criteria to define confirmed and prob-able cases of pertussis.18 To meet clinical case definition, theperson must have a cough that lasts 2 weeks or longer with atleast 1 of the following: paroxysmal coughing, posttussive vom-iting, or an inspiratory whoop. Laboratory confirmation, usingspecimens obtained from a nasopharyngeal swab or aspirate,requires isolation of B pertussis from culture or a positive re-sult for B pertussis DNA by polymerase chain reaction (PCR).A confirmed pertussis case must meet 1 of the following 3 sce-narios: (1) a cough of any duration with isolation of B pertus-sis by culture, (2) a cough that meets the clinical case defini-tion and is confirmed by a positive result for B pertussis DNAby PCR, or (3) a cough that meets the clinical case definitionand is epidemiologically linked to a case confirmed by cultureor PCR. A probable pertussis case meets the clinical case defi-nition but is not laboratory confirmed or epidemiologicallylinked to a case confirmed by culture or PCR. We also used alocally defined classification, a possible pertussis case, for per-sons with a compatible clinical illness and in whom the healthcare provider was suspecting pertussis but who did not qualifyto be classified as a confirmed or probable case. All cases of per-tussis were followed up by public health personnel until cri-teria for the case definition were met and not necessarily forthe full duration of cough.

For this study, infants were considered age-appropriatelyvaccinated if they received dose 1 of DTaP before age 3 months,dose 2 before age 5 months, and dose 3 before age 7 months.Household members and close contacts were considered Tdapeligible if they were aged 11 to 64 years; data were unavailableon the number of Tdap-eligible household members and closecontacts who actually had received Tdap before the infant’s on-set of illness. Household members were defined as living in thesame housing unit as the pertussis case infant. The definitionof close contacts was determined on a case-by-case basis. Anexample of a close contact would be direct face-to-face con-tact or close proximity for a prolonged period to a patient withpertussis during his or her contagious period. The suspectedsource of pertussis transmission was determined during caseinvestigations by local public health personnel on the basis ofthe presence of symptoms compatible with pertussis in a house-hold member or other close contact of a case infant before on-set of symptoms in the patient.

County census data between 2002 and 2007 were the sourcefor King County infant population size. Analysis was per-formed using commercially available statistical software (SPSS14.0; SPSS Inc, Chicago, Illinois; and STATA 10.0; StataCorpLP, College Station, Texas).

RESULTS

Two hundred fifty-eight pertussis cases among infantsyounger than 1 year were reported to Public Health–Seattle & King County between 2002 and 2007. Of thesecases, 176 were classified as confirmed, 19 as probable,and 63 as possible cases. Among confirmed cases, 83(47.2%) were confirmed by culture, and 88 (50.0%) wereconfirmed by PCR.

Among 176 confirmed cases of infants younger than1 year with pertussis, the median age was 3 months (agerange, 0-11 months); 141 patients (80.1%) were youngerthan 6 months, and 95 patients (54.0%) were male. Theprimary language spoken by the parents of infants withpertussis was English for 151 cases (86.0%) and Span-ish for 21 cases (11.9%). Of 176 confirmed patients, 71




(40.3%) were white, 30 (17.0%) were black, 30 (17.0%)were Hispanic, 20 (11.4%) were Asian or Pacific Is-lander, and 25 (14.2%) were of unknown or other race/ethnicity.

The overall mean annual incidence for confirmedcases between 2002 and 2007 was 136 cases per100 000 infant population (range by year, 56-238 casesper 100 000 infant population). Black infants had thehighest incidence among all racial/ethnic groups, with246 cases per 100 000 infant population (range by year,149-388 cases per 100 000 infant population) and a rateratio (RR) of 3.37 (95% confidence interval [CI], 2.59-4.44), compared with whites. At the other end of thespectrum, whites had 73 cases per 100 000 infant popu-lation (range by year, 37-160 cases per 100 000 infantpopulation). Among Hispanics, the annual incidencewas 194 cases per 100 000 infant population (range byyear, 76-309 cases per 100 000 infant population), withan RR of 2.66 (95% CI, 2.02-3.53) compared withwhites. For Asian or Pacific Islanders, the annual inci-

dence was 112 cases per 100 000 infant population(range by year, 0-275 cases per 100 000 infant popula-tion), with an RR of 1.53 (95% CI, 1.13-2.09) comparedwith whites (Table 1). No clear trends were identifiedover time, overall or in any racial/ethnic group. Year-to-year variations are given in Table 1, with a peak in con-firmed cases seen in 2005.

Vaccination status was known in 175 of 176 case in-fants (99.4%).Amongtheseconfirmedpatients,135(77.1%)had been appropriately vaccinated with DTaP. Given thatthe median age of patients was 3 months, the median num-ber of DTaP doses received before onset of illness was 1(range, 0-4) (Table 2). For 41 infants who were not age-appropriately vaccinated, philosophical exemption wasprovided as a reason in 8 cases (19.5%), and the reason wasunknown in 27 cases (65.9%). Numbers of DTaP doses re-ceived before onset of illness among the age groups (0-1,2-3, 4-5, and 6-11 months) are given in Table 3.

By definition, all 176 confirmed cases included a cough,and 170 patients (97.0%) had a paroxysmal cough(Table 4). Other signs and symptoms included post-tussive vomiting in 144 infants (81.8%), apnea in 139(79.0%), cyanosis in 74 (42.0%), and inspiratory whoopin 46 (26.1%).

A median of 2 (range, 1-7) medical visits and a medianof 11.5 days (range, 1-57 days) from the onset of symp-toms elapsed before the diagnosis of pertussis was made.Among 176 confirmed cases, 80 patients (45.5%) were hos-pitalized, and the median length of stay among these was4.5 days (range, 1-36 days). The median age of 80 hospi-talized infants was 2 months (age range, 0-11 months) com-pared with a median age of 4 months (age range, 1-11months) for 96 nonhospitalized infants. Sixteen of 80 hos-pitalized infants (20.0%) required intensive care. The mostcommon complication was pneumonia, reported in 14 of176 infants (8.0%). No deaths were reported.

Households were the suspected exposure location for123 infants (70.0%); 43 infants (24.4%) had an un-known exposure. Among 176 confirmed cases, 991 house-

Table 1. Cases of Infant Pertussis in King County,Washington, 2002 Through 2007a

VariableConfirmed

Cases

Confirmed Casesper 100 000 Infant

Population per Year

Overall 176 1362002 12 562003 34 1602004 26 1222005 51 2382006 24 1112007 29 132

Black 30 2462002 3 1492003 4 2012004 5 2472005 5 2472006 8 3882007 5 239

Hispanic 30 1942002 3 1182003 5 2002004 5 1932005 8 3092006 2 762007 7 264

Asian or Pacific Islander 20 1122002 0 02003 8 2752004 3 1012005 4 1352006 3 992007 2 65

White 71 732002 6 372003 12 742004 9 562005 26 1602006 7 432007 11 66

aTwenty-five infants were of unknown race/ethnicity or one other thanthose listed. Compared with whites, the rate ratios (95% confidenceintervals) were 3.37 (2.59-4.44) for blacks, 2.66 (2.02-3.53) for Hispanics,and 1.53 (1.13-2.09) for Asian or Pacific Islanders.

Table 2. Vaccination Status, Suspected Exposure,and Time to Diagnosis Among Infants With ConfirmedPertussis in King County, Washington, 2002 Through 2007

VariableValue

(n=176)

No. of DTaP doses at onset of illness, median (range) 1 (0-4)Age-appropriately vaccinated, No. (%) 135 (76.7)Reason not age-appropriately vaccinated, No. (%) (n=41)

Unknown 27 (65.9)Philosophical exemption 8 (19.5)Parental refusal 2 (4.9)Religious exemption 1 (2.4)Other 3 (7.3)

Suspected exposure, No. (%)Household 123 (69.9)Unknown 43 (24.4)Outbreak related 23 (13.1)

Time from onset of illness to diagnosis,median (range), d

11.5 (1-57)

No. of medical visits until diagnosis, median (range) 2 (1-7)

Abbreviation: DTaP, diphtheria and tetanus toxoids and acellular pertussis.




hold members and close contacts were reported to havehad contact with the infant before onset of illness. A me-dian of 5 (range, 2-29) household members and close con-tacts was reported per infant. Among household mem-bers and close contacts, 376 persons reportedly hadrespiratory tract symptoms (ie, a prolonged cough) be-fore onset of illness in the infant, with a median of 2 per-sons (range, 0-12) per case. A median of 3 (range, 1-15)household members and close contacts per case (a totalof 472 throughout the study period) were aged 11 to 64years and Tdap eligible. Hispanics had the most Tdap-eligible household members and close contacts (n=157),with a median of 4 (range, 3-16) household members andclose contacts per case.

COMMENT

Between 2002 and 2007, the incidence of infant pertus-sis in King County, Washington, was higher than the na-tional mean; for example, in 2005, the King County in-cidence was more than twice that of the incidence in theUnited States.7 This high rate of infant pertussis oc-curred despite immunization coverage rates in KingCounty that have been comparable to or higher than thenational mean for pertussis-containing vaccine during thestudy period.19 Whether this higher incidence of re-ported infant pertussis in King County is attributable to

superior pertussis diagnosis, better notifiable disease re-porting, or regional differences in endemic rates of per-tussis is unknown. Regardless of the cause, the higherincidence requires additional tools and strategies to ad-dress this issue.

Vaccine efficacy after the third dose of DTaP, admin-istered at 6 months, is 80% to 85%.11-13 In our study, 80.1%of confirmed cases of infant pertussis occurred amonginfants younger than 6 months and too young to havereceived the first 3 DTaP doses. This observation rein-forces the need to use strategies in addition to the 3 rou-tine DTaP doses during infancy to decrease the risk forpertussis transmission to infants.

We determined that the household was the sus-pected source of pertussis transmission to infants in 70.0%of confirmed cases. This is consistent with previous stud-ies20,21 in which family members were the source of per-tussis transmission to infants in at least 75% of cases inwhere a source could be identified. Notably, we deter-mined that approximately 50% of household membersand close contacts of infants with pertussis were Tdapeligible (ie, they were aged 11-64 years), presenting a criti-cal opportunity to decrease transmission through vacci-nation with Tdap. Because we had no vaccination histo-ries for household members and close contacts, we couldnot subtract from this estimate those household mem-bers and close contacts who had been vaccinated withTd in the previous 10 years.

Given that the parents of infants with pertussis oftenhave been identified as the source of infection, the Ad-visory Committee on Immunization Practice and theAmerican College of Obstetricians and Gynecologists haverecommended Tdap vaccination of previously unvacci-nated women during the immediate postpartum pe-riod.17,22 In addition to postpartum women, all older chil-dren, adolescents, and adults who are close contacts ofor are in the same households as infants should be tar-geted for Tdap vaccination. During our study, we alsoobserved increased pertussis incidence among racial/ethnic minorities, especially black and Hispanic infantscompared with white infants, highlighting the need forTdap vaccination efforts to decrease the burden of dis-ease among these populations. This increased incidenceamong racial/ethnic minorities also underscores the needfor additional analysis to evaluate characteristics that dif-fer among these groups. Areas for further study could in-clude an evaluation of differences among racial/ethnic mi-norities with regard to vaccination status, suspectedexposure, time from onset of illness to diagnosis, num-

Table 3. DTaP Vaccination Status of Infants With Confirmed Pertussis by Age Group in King County, Washington, 2002 Through 2007

Age, mo TotalUnknown Vaccination

Status

No. of DTaP Doses

0 1 2 3 4

0-1 32 0 32 . . . . . . . . . . . .2-3 60 0 34 26 . . . . . . . . .4-5 49 1 3 32 13 . . . . . .6-11 35 0 8 7 4 15 1Total 176 1 77 65 17 15 1

Abbreviation: DTaP, diphtheria and tetanus toxoids and acellular pertussis.

Table 4. Signs, Symptoms, and Complications AmongInfants With Confirmed Pertussis in King County,Washington, 2002 Through 2007

VariableTotal, No. (%)

(n=176)

Cougha 176 (100.0)Paroxysmal cough 170 (97.0)Posttussive vomiting 144 (81.8)Apnea 139 (79.0)Cyanosis 74 (42.0)Inspiratory whoop 46 (26.1)Hospitalizationb 80 (45.5)Pneumonia 14 (8.0)Seizure 1 (0.6)Encephalopathy 1 (0.6)Death 0

aThe median duration is 17 days (range, 3-62 days), which is likely anunderestimate given that cases were followed up by public health personnelonly until case definition was met and not for the full duration of cough.

bThe median length of stay is 4.5 days (range, 1-36 days).




ber of visits to a health care provider until diagnosis, andhospitalization.

A notable finding was the high rate of philosophicalexemptions among infants who were not age-appropriately vaccinated. Increased incidence of pertus-sis has been reported among communities with high ratesof philosophical exemptions.23-26 These exemptions arelegal in many states, including Washington, where philo-sophical exemptions have been increasing in recent years.Some parents who have refused vaccination for their chil-dren on philosophical grounds might also be resistant toTdap vaccination for themselves. Therefore, the poten-tial effect of philosophical exemptions on Tdap vaccina-tion efforts among household members and close con-tacts of infants should be monitored.

A limitation of this study is that we had no data onTdap vaccination status of household members and closecontacts (such information is now collected, beginningJanuary 1, 2009). However, because most of the studyperiod predated the recommendation for Tdap vaccina-tion of older children, adolescents, and adults and be-cause of the typically slow uptake of new vaccine rec-ommendations among these age groups, we believe thatmost older children, adolescent, and adult contacts of ourpatients had not received the Tdap vaccine. In supportof this assertion are results from the 2006 and 2007 Na-tional Immunization Survey, in which Tdap vaccina-tion coverage among adolescents aged 13 to 17 years was10.8% (range, 9.4%-12.3%) in 2006 and 30.4% (range,28.2%-32.7%) in 2007.27,28 Other study limitations arerelated to the manner in which case investigations areconducted by public health personnel. Assessment of asuspected source of pertussis transmission on the basisof symptoms compatible with pertussis is subjective. Be-cause follow-up occurred only until the case definitionwas satisfied, we might have underestimated the dura-tion of patient symptoms.

In summary, in a community with high rates of in-fant pertussis, particularly among black and Hispanic in-fants, a substantial proportion of household and otherclose contacts of pertussis case infants is eligible for Tdapvaccination. Clinicians and public health professionalsshould promote Tdap vaccination of older children, ado-lescents, and adults who are close contacts of infants orare in the same households as infants and should con-sider targeted outreach to communities at increased risk.

Accepted for Publication: January 12, 2011.Correspondence: Matthew P. Hanson, MD, DTM&H,Global Health Program, Bill & Melinda Gates Founda-tion, 500 Fifth Ave N, Seattle, WA 98109.Author Contributions: Study concept and design: Han-son and Duchin. Acquisition of data: Rietberg, Ohrt, andDuchin. Analysis and interpretation of data: Hanson, Kwan-Gett, Baer, and Duchin. Drafting of the manuscript: Han-son and Duchin. Critical revision of the manuscript for im-portant intellectual content: Hanson, Kwan-Gett, Baer,Rietberg, Ohrt, and Duchin. Statistical analysis: Hansonand Baer. Obtained funding: Duchin. Administrative, tech-nical, and material support: Duchin. Study supervision:Kwan-Gett and Duchin.Financial Disclosure: None reported.

Additional Contributions: Data collection and manu-script preparation were completed as part of normal jobduties by Centers for Disease Control and Prevention andPublic Health–Seattle & King County staff. We thank allof the public health personnel who assisted in conduct-ing the thorough case investigations that made this ret-rospective analysis possible. In particular, we thank thelate Linda L. Vrtis, RN, for her tireless dedication, atten-tion to detail, and career spent improving the health ofthe public.

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28. Centers for Disease Control and Prevention (CDC). Vaccination coverage amongadolescents aged 13-17 years—United States, 2007. MMWR Morb Mortal WklyRep. 2008;57(40):1100-1103.

Announcement

Trial Registration Required. In concert with the Inter-national Committee of Medical Journal Editors (ICMJE),Archives of Pediatrics and Adolescent Medicine will re-quire, as a condition of consideration for publication,registration of all trials in a public trials registry (such ashttp://ClinicalTrials.gov). Trials must be registered at orbefore the onset of patient enrollment. This policy ap-plies to any clinical trial starting enrollment after July 1,2005. The trial registration number should be suppliedat the time of submission.

For details about this new policy, and for informa-tion on how the ICMJE defines a clinical trial, see theeditorials by DeAngelis et al in the September 8, 2004(2004;292:1363-1364) and June 15, 2005 (2005;293:2927-2929) issues of JAMA. Also see the Instructions toAuthors on our Web site: www.archpediatrics.com.




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