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Costs of Illness Due to Bordetella pertussis in Families
Lucia H. Lee, MD;
Michael E. Pichichero, MD
Arch Fam Med. 2000;9:989-996.
ABSTRACT
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Objective To assess costs of pertussis morbidity among families in a community setting.
Design Prospective survey.
Results Sixty-nine families (87 individuals) were studied. Twelve of 14 families with household contacts included an ill adolescent or parent. This individual was the first identified pertussis case within the household in 8 families. A family member required an average of 1.6 visits before (range, 0-7 visits) and after (range, 0-9 visits) pertussis was diagnosed; children younger than 1 year needed 2.5 and 2 visits, respectively. Symptomatic improvement occurred after a mean of 31 days (range, 4-134 days) after pertussis diagnosis and full recovery after a mean of 66 days (range, 5-383 days). Adults experienced the longest recovery time (median, 93 days) compared with other age groups. The average medical costs for an infant, child, adolescent, and adult were $2822, $308, $254, and $181, respectively. Parents lost an average of 6 workdays (range, 1-35 days) to care for an ill child; for these parents, costs associated with work loss averaged $767 per family. An average of 1.7 and 0.7 lost workdays accrued to bring an ill child to a physician's office and the emergency department, respectively. A majority (58%) of parents working while family members were ill with pertussis reported decreased work productivity ranging from 25% to 99%. Work-related costs contributed more than 60% of the overall costs of pertussis.
Conclusions The adverse financial effect of pertussis on 69 families in Monroe County, New York, was $145 903 ($2115 per family) and supports the need for booster immunizations in adolescents and adults.
INTRODUCTION
PERTUSSIS CAN occur in all members of a family. Within a family, adolescents and adults are potential sources of pertussis for children, and targeting immunization of adolescents and adults may reduce illness in younger family members by decreasing child exposure to infectious adults.1 Routine vaccination in adolescents and adults has important public health implications, especially in the United States, where the number of reported pertussis cases for adolescents and adults has been increasing during the last 2 decades.2-6 A clear definition of costs associated with pertussis morbidity and mortality and the potential savings due to routine immunization in this population are important factors to consider if such a strategy would be beneficial. At present, little information is available that examines the economic burden of pertussis within a family.
MATERIALS AND METHODS
STUDY DESIGN
The 18-month study (January to December 1995, and July to December 1996) was conducted at a time during which pertussis was a reportable disease in Rochester, NY. Pertussis cases were prospectively identified by the Monroe County Health Department (MCHD) and by 1 of us (M.E.P.) at a private pediatric practice (Elmwood Pediatric Group [EPG], Rochester). Families with pertussis cases were contacted and detailed information about the symptoms, immunizations, treatment, and duration of illness in the individual(s), as well as parental work loss and work productivity, was obtained. Appropriate number of doses and timing of immunizations was verified from medical records obtained from physicians' offices. Infants, children, adolescents, and adults were defined as younger than 1 year, 1 to 9 years old, 10 to 20 years old, and older than 21 years, respectively.
Pertussis cases at MCHD were defined by 1 or more of the following criteria: (1) documented positive culture for Bordetella pertussis; (2) documented positive direct fluorescent antibody results if exposed to a culture-positive and symptomatic household contact; and (3) symptoms fulfilling the Centers for Disease Control and Prevention (CDC) clinical criteria (cough for >14 days otherwise unexplained or for >7 days with paroxysms or whooping epidemiologically linked to a laboratory confirmed case).7 In addition, cases at EPG were identified using serologic criteria as an adjunct method to confirm pertussis: a 4-fold or greater change in agglutinin or immunoglobulin G (IgG) antibody to pertussis toxin (PT), filamentous hemagglutinin (FHA), or pertactin (PRN) geometric mean value during a time period (acute to convalescent), or 2 different antibody test values from a single serum sample that resulted in greater than or equal to 3 SD above the mean value of the control population.
An index case was considered to be a person in a household with the earliest onset of cough. A family member was considered a household contact if he or she fulfilled the clinical case definition and was epidemiologically linked to a laboratory-confirmed case. An index case was inferred to be the source within a household if his or her coughing illness was not epidemiologically linked to a previously identified laboratory-confirmed pertussis case at school or work.
LABORATORY ANALYSIS
Serologic confirmation of pertussis by agglutinating antibody was assayed by the whole-cell microagglutination technique of Manclark and Meade.8 Standard human antiserum lot B262, which was used as a reference (titer 1:512), and B pertussis antigen (strain BB460) were provided by Bruce Meade, MD (Office of Biologics, Research, and Review, US Food and Drug Administration, Bethesda, Md). Immunoglobulin G antibodies to PT, FHA, and PRN were measured by enzyme-linked immunosorbent assay and compared with Office of Biologics, Research, and Review human pertussis antiserum lot 3 (PT and FHA) and 4 (PRN) by the method of Meade et al.9 Purified antigen was a gift from SmithKline Beecham (Rixensart, Belgium). The same assays were performed for the control population of 360 healthy, noncoughing, fully immunized children and adults living in Rochester. A serologically confirmed pertussis case was based on a 4-fold or greater change in agglutinin or IgG antibody to PT, FHA, or PRN geometric mean values during a time period (acute to convalescent), or 2 different antibody test values from a single serum sample that each resulted in values greater than or equal to 3 SD above the mean value of the control population (Table 1).
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Table 1. Serologic Values Used to Define Single Serum Serologic Positivity*
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QUESTIONNAIRE
Once an individual with pertussis was identified, a questionnaire was mailed within 2 weeks to the family. Questionnaires were not sent out between January and June 1996 because a study coordinator assigned to this project had a time commitment shift. Information gathered included the cost of visits to medical facilities (office, emergency department [ED], hospital), laboratory testing, antibiotic treatment and prophylaxis, and symptomatic medications, work loss, and additional arrangements for child care. Parents were asked to report the amount of decreased work productivity that was due to a family member being ill with pertussis or to their own illness with pertussis. The percentage of tasks achieved in the work setting was semiquantitatively based on the amount of work accomplished during a full workday prior to the onset of pertussis in the family. Productivity was defined as the ability to complete the same amount of responsibilities (100%), a noticeable but not consistent decrease in ability to complete responsibilities (75%), consistent decrease in ability to complete responsibilities (50%), inability to complete the majority of responsibilities (25%), or inability to complete responsibilities (0%). Adults, adolescents, and parents of children with pertussis also reported the time to improvement and to full recovery from illness. If the questionnaire was not returned within 4 weeks, contact by telephone was attempted and a second questionnaire was sent to families interested in completing the questionnaire. If a family member was still symptomatic at the time of questionnaire return, a study coordinator maintained periodic telephone contact and a record of the information until complete recovery occurred. To improve the reliability of parent/patient recall during illness recovery, a minimum of 3 telephone calls were made to follow-up the completion of each questionnaire.
COST CALCULATIONS
The direct cost of a private acute illness visit was based on an average charge of $45 per visit, which was the average charge for this type of visit in Rochester. Actual charges for ED visits, hospitalizations, and laboratory tests were verified from billing department records and were included in our analysis. Antibiotic cost was based on the sum of the average wholesale price of the least expensive brand of each drug and a $2 pharmacy-dispensing fee per drug. Indirect costs of pertussis were estimated to include a loss of 2 hours from work for an office visit, 3 hours from work for an ED visit, and 8 hours from work per hospital day. Salary loss was estimated to be $20.50 per hour of lost work, a charge that was based on the average hourly earnings in Rochester in 1992.10
RESULTS
During the 18-month study period, 172 individuals among 130 families fulfilled the case definition for pertussis. One hundred thirty-five cases were identified through MCHD and 37 cases through EPG. Of the MCHD cases, B pertussis was confirmed by culture or direct fluorescent antibody in 92 individuals, and 3 individuals had a 4-fold increase in acute to convalescent titers to pertussis components. Forty cases met the CDC clinical definition of pertussis but were not confirmed by laboratory tests (Table 2). Of the EPG cases, B pertussis was confirmed in 5 EPG cases by microbiologic methods or by a 4-fold antibody rise to pertussis components. Twenty-seven cases were confirmed by single serum serologic testing; 10 of these 27 individuals also fulfilled the CDC clinical case definition of pertussis. Ten individuals had a positive single serum antibody titer to all 4 pertussis antigens, 8 individuals had a positive antibody titer to 3 pertussis antigens, and 9 individuals had a positive antibody titer to 2 pertussis antigens. Five cases fulfilled the CDC clinical case definition but were not confirmed by laboratory tests (Table 2).
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Table 2. Confirmed Pertussis Cases*
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Pertussis occurred in 97 children (55%) and 25 infants (14%); 20 infants (11%) were younger than 6 months. Of 119 cases for whom immunization records were available, 90% of children and infants were appropriately vaccinated against pertussis based on the immunization schedule recommended by the Advisory Committee on Immunization Practices. Seventy-three of these 119 individuals were laboratory-confirmed cases who were appropriately immunized, and included 17 infants younger than 6 months.
A questionnaire reply was obtained from 69 families (87 individuals) with identified pertussis. A 66% and 65% questionnaire response rate was achieved in 1995 and 1996, respectively. In 54 households (78%), a single family member developed pertussis. Ten families reported 2 siblings or a parent and child with pertussis; for 6 families, the onset of symptoms in family members developed 7 or more days apart. Four families reported 3 or more concurrently ill household members; among 3 of these families, symptoms in subsequent household members developed 11 to 14 days after the individual with the earliest symptoms. Twelve (86%) of 14 families with household contacts included an ill adolescent or parent; this individual was the first identified pertussis case within the household in 8 families. Five (83%) of 6 adults with pertussis were women; no sex differences were noted among the other age groups.
Pertussis was diagnosed after an average of 1.6 visits (range, 0-7 visits) to the office physician in all cases; the same average number of visits was needed for follow-up (range, 0-9 visits). Of all age groups, infants required more visits to an office physician; an average of 2.5 visits (range, 1-6 visits) was needed before a diagnosis of pertussis was made and an average of 2 visits (range, 0-6 visits) was needed for follow-up. The number of physician office visits by age and the number of concurrently ill family members with pertussis are presented in Table 3.
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Table 3. Pertussis Diagnosis and Follow-up
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Symptomatic improvement occurred a mean of 31 days (range, 4-134 days) after diagnosis, and full recovery occurred after a mean of 66 days (range, 5-383 days). Adults had the longest recovery time (median, 93 days) compared with infants, children, and adolescents (median, 75, 56, and 74 days, respectively). Full recovery from pertussis took an average of 1.6 times longer when 3 or more family members were ill with pertussis than when 2 or fewer family members were ill. The median length of time from onset of pertussis symptoms until subjective clinical improvement and full recovery is presented in Table 3.
PERTUSSIS COSTS AMONG WORKING PARENTS
Thirty-one of 78 parents working outside the home lost workdays to care for an ill family member at home. For these parents, costs associated with work loss averaged $767 per family; each parent lost an average of 6 workdays (range, 1-35 days). A cumulative total of 145 lost workdays amounted to a cost of $23 780 (Table 4). Parents of 4 hospitalized infants lost an average of 6 workdays (range, 3-10 days); costs associated with work loss to care for these hospitalized infants averaged $1025 per family. Parents bringing an ill family member to a physician's office lost an average of 1.7 workdays (range, 0.3-3.3 days), which amounted to a loss of $9881. Working parents of an infant or child with pertussis who underwent an ED evaluation took an average of 0.7 days (range, 0.4-1.1 days) off from work with a loss of $554. The remaining 43 working parents lost no workdays, but decreased productivity was reported among most of these adults (Table 5). Eighteen working parents (42%) reported 100% productivity. Thirty-seven percent, 9%, and 12% of working parents reported greater than or equal to 75% to 99%, 50% to 74% and less than or equal to 25% to 49% productivity, respectively. Six adults working outside the home were ill with pertussis themselves. The estimated total cost due to decreased work productivity was $68 470. One family reported $340 in additional child care costs.
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Table 4. Costs Among Working Parents
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Table 5. Productivity Among 42 Working Parents With No Lost Workdays
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MEDICAL COSTS
A total of 9 ED visits were reported among the 69 families. Seven ED visits were required by 4 infants, and 2 ED visits were required by 1 child. Of all age groups, 4 infants required hospitalization. The average direct and indirect medical costs, excluding the costs for work loss for home care, decreased productivity, and household prophylaxis for an infant, child, adolescent, and adult, were $2822, $308, $254, and $181, respectively. The overall costs of pertussis illness among 69 families are presented in Table 6.
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Table 6. Costs for 87 Pertussis Cases in Monroe County, New York*
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Of note, 67 (77%) of 87 family members received a macrolide or trimethoprim/sulfamethoxazole for treatment of pertussis; only 32 of the appropriately treated household members (48%) received a 14-day regimen. Five individuals (6%) were given a macrolide for longer than 14 days. One individual received an inappropriate antibiotic only, and 6 individuals (7%) were administered antibiotics inappropriately before a macrolide was prescribed. No antibiotics were given to 2 family members with identified pertussis.
Eighty-five (98%) of the 87 family members had medical insurance. Eighty-one individuals (95%) had insurance from a health maintenance organization and 4 individuals (5%) had Medicaid. An average of 84% (range, 25%-100%) of the direct medical costs were covered by insurance.
COMMENT
In this study, 40% of pertussis cases occurred among adolescents and adults. Transmission of B pertussis to family contacts from an adolescent or adult source occurred often. Eighty-six percent of families with more than 1 identified pertussis case included an ill adolescent or parent; of these families, an adolescent or parent was the source of infection 67% of the time. Adults who developed pertussis had close contact with their children. Fifty percent of affected adults were homemakers or worked at home, and 5 of 6 adult cases were women.
The burden of pertussis among families is substantial due both to the economic expenditures required to care for ill family members and to the prolonged recovery from illness. Adults had the longest recovery time (median, 93 days) compared with infants, children, and adolescents (median, 75, 56, and 74 days, respectively). During this period, adolescents and adults may act as a reservoir for pertussis, resulting in transmission of pertussis to infants and young children at home,11-13 adolescents at school, or other adults at work.14-17 The average number of visits required for pertussis diagnosis was age-dependent, with infants requiring more frequent visits. When more than 1 pertussis case occurred within a family, a diagnosis was not suspected any earlier in other family members than in the index case. Among children, medical expenditures were predominantly allocated toward physician office visits rather than ED visits or hospitalizations. The direct cost for physician office visits ($5175 for 41 cases) accounted for 41% of the overall medical costs for this age group. The highest morbidity associated with pertussis occurred among infants ($2822 per case), largely due to the hospitalization of 4 infants.
A substantial proportion of the overall medical cost for pertussis was due to indirect costs from salary wages lost from decreased work productivity. Of those parents who did not take actual time off from work, only 42% were fully productive in the work setting. Parents were least productive ( 25%-49% lost work productivity) when more than 1 family member became ill with pertussis, or when an infant required hospitalization. Of the working parents who were ill from pertussis themselves, none reported 100% work productivity. Total indirect costs due to time taken from work to bring an ill child to physician office visits or ED visits, or to care for a hospitalized infant, amounted to $9881, $554, and $4100, respectively, in lost salary wages. The overall cost of decreased work productivity was $68 470, which accounted for 46% of the overall costs for 87 cases of pertussis (Table 6).
A simple estimate of cost-effectiveness of an adolescent immunization program was determined. We based our calculation on a 10% wastage rate for vaccines delivered during an immunization campaign, the cost of an acellular pertussis vaccine in the private sector (http://www.cdc.gov/nip/vfc/cdc_vac_price_list.htm), a prorated vaccine administration cost of $518 (since a catch-up vaccination [eg, hepatitis B] could be given at the same visit), and disease prevention according to the prevalence of pertussis per case. The cost of immunizing all adolescents in Monroe County would be $203 404, which exceeds the cost of averting pertussis in adolescents ($6347). When the costs of preventing pertussis in infants ($328 128) and children ($5887) are included, a strategy of immunizing adolescents is worth considering.
This study has several limitations. Sixty-six families (90 individuals) did not respond to the questionnaire; 91% were children and adolescents, with an equal distribution among each of these groups. The number of adults who did and did not participate in the survey was similar. Of the available immunization records for nonparticipants, 90% of cases were appropriately immunized. Culture or direct fluorescent antibody confirmed the diagnosis of pertussis illness in 60% of nonparticipating individuals; 11 nonparticipants were diagnosed by serologic tests alone. Seventy-six percent of pertussis cases were confirmed by laboratory tests; the remainder of cases were identified by the CDC clinical definition of pertussis without confirmed laboratory testing. Although the demographic characteristics, immunization status, and number of confirmed pertussis cases was similar for questionnaire participants compared with nonparticipants, selection bias may have resulted from families with more severe disease; these families may have been more motivated to complete the questionnaire. Second, since the CDC clinical definition is sensitive but not specific, inclusion of these cases may have led to an overestimation of the costs attributed to pertussis. Pertussis is difficult to recognize until classic symptoms such as paroxysmal cough and whoop occur. The sensitivity of bacteriologic confirmation decreases progressively during this stage compared with the ability to isolate B pertussis during the catarrhal stage.19 Isolation of B pertussis by culture is also reduced among completely vaccinated persons and those who have received a macrolide prior to obtaining culture.20-21 Since facilities and materials were available to perform single serum serologic testing, this method was used as an adjunct diagnostic method for cases seen at EPG. Adequate staffing was not available to offer this diagnostic method for all identified cases of pertussis in Monroe County; likewise, single serum serologic testing was not included in the diagnostic services provided by the MCHD. Bordetella pertussis was confirmed in 5 EPG cases by microbiologic methods or by a 4-fold antibody rise to pertussis components. Twenty-seven cases were confirmed by single serum serologic testing; 10 of these 27 individuals also fulfilled the CDC clinical case definition. A positive IgG response to PT was elicited in 26 cases. The use of the single serum serologic technique to establish a pertussis diagnosis is controversial and harmonization of this technique (eg, pertussis antigens, isotypes) to confirm pertussis has not yet been established. Single serum serologic testing would be useful when large-scale collection of paired specimens, such as in a state health department diagnostic program, is not practical. Obtaining paired specimens is not practical. In addition, paired serum specimens would not be useful to yield a timely diagnosis when evaluating the extent of disease outbreak or when the diagnostic sensitivity of microbiologic methods is expected to be low. Single serum serologic testing has been used by previous investigators to establish a pertussis diagnosis,11, 14, 17, 22-23 particularly the use of IgG antibody to PT.5, 24 The sensitivity and specificity of this method depends on selected cutoff values. If the cutoff values of mean titers of IgG antibody to PT were set at greater than 2 SDs and 3 SDs, 2.5% and 0.5% of individuals without pertussis, respectively, would fulfill the criteria for serologic diagnosis by statistical chance.17 We chose to define a serologically confirmed pertussis case by the more stringent of the 2 criteria. The cutoff value was established from a large control population of fully immunized healthy persons. Serum samples were obtained from a broad age range since a single serologic mean value is not accurate across all age groups. Lastly, we required 2 different pertussis antibody test values above this cutoff to minimize the chances of including false-positive cases. In fact, the antibody values of the serologically confirmed pertussis cases were very high-titered and exceeded 3 SDs by 1- to 98-fold. We did not measure IgA responses because these responses may not have significantly increased the diagnostic sensitivity of single serum serologic testing with the stringent criteria used in our study. Including single serum serologic testing as part of a pertussis case definition would increase the ability to diagnose pertussis among culture-negative cases. An increase in reported pertussis cases therefore may not reflect a true increase in disease, but rather the use of additional laboratory methods to confirm pertussis. The reliance on serologic confirmation of pertussis using FHA and pertactin antibodies may be affected by infection with Bordetella parapertussis or cross-reacting antigens from nonencapsulated Haemophilus influenzae,25 and may in turn affect the true number of pertussis cases. Three EPG cases confirmed by single serum serologic testing alone responded to our questionnaire. The contribution of these cases to the overall questionnaire response rate is minimal and thus does not significantly affect the analysis of costs associated with pertussis morbidity.
The costs of decreased work productivity account for a significant proportion of the overall estimated cost of pertussis. A conservative selection of parents with salaried positions and tangible parameters such as an average hourly earning for Rochester were used to calculate the costs associated with decreased work productivity. While traditional employee benefits such as health insurance and pensions are ubiquitous, not everyone is entitled to a flexible work schedule, paid parental leave, or undifferentiated leave (eg, paid sick leave for family illness). Employee benefits, when combined with earnings, have been shown to stratify the workplace such that female, nonwhite, and young workers are disproportionately clustered in jobs yielding the lowest benefit coverage.26-27 In addition, of parents who did not achieve a high school education, only 17% received paid leave.28 Use of sick leave for family needs, as opposed to "flextime," represents a productivity loss to an employer that cannot be recompensed.29 Thus, regardless of whether sick leave is paid or unpaid, this time is a permanent loss to the employer. Nevertheless, we acknowledge in a literal sense the possibility that the actual earning loss of working parents in our study is less than our calculated cost of work lost due to paid sick leave and that actual costs incurred would provide an authentic assessment of work loss. However, our calculations used tangible parameters to provide a reasonable approach for estimating the costs of pertussis among working parents. Other investigators30 have also used this approach. We acknowledge that these cost calculations are only estimates and that costs related to an amount of productive output per day would provide a more objective measure of work productivity.
We recognize that neither natural disease nor complete vaccination according to the currently recommended pediatric immunization schedule confers lifelong immunity. Although the pertussis antibody level may decrease as early as 5 years after complete vaccination, the time period of waning immunity ranges from 7 to 12 years after complete vaccination.31-32 These results suggest that adolescents may benefit from vaccination. The recommended administration of booster vaccinations could be as frequent as every 5 years but has yet to be determined. It is possible that vaccination of susceptible adolescents may shift the incidence of pertussis to other age groups. Continued epidemiologic surveillance would be a reasonable approach to these issues.
In conclusion, the adverse financial effect of pertussis on families is substantial. Lost days and decreased work productivity account for a large proportion of the overall costs. Reduced spread of pertussis within a family may improve with immunization of adolescents and adults.33-34
AUTHOR INFORMATION
Accepted for publication September 13, 2000.
Supported by contract AI05049 from the National Institutes of Allergy and Infectious Diseases, Bethesda, Md.
Presented in part at the 37th Annual Meeting of the Infectious Diseases Society of America, Philadelphia, Pa, November 19, 1999.
This article expresses the views of the authors and is not intended to represent the opinions of the Food and Drug Administration.
Corresponding author and reprints: Lucia H. Lee, MD, Center for Biologics Evaluation and Research, Food and Drug Administration, HFM 475, Suite 370N, 1401 Rockville Pike, Rockville, MD 20852 (e-mail: leel{at}cber.fda.gov).
From the Center for Biologics Evaluation and Research, Food and Drug Administration, Rockville, Md (Dr Lee); and the Department of Microbiology and Immunology, University of Rochester Medical Center, Rochester, NY (Dr Pichichero).
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Rationale for Use of Tdap Booster Vaccines for Adolescent Immunization: Overview of Efficacy, Safety, and Clinical Use
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Pichichero et al.
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