The Cost of Containing One Case of Measles: The Economic Impact on the Public Health Infrastructure—Iowa, 2004
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《小儿科》
Epidemiology and Surveillance Division, National Immunization Program, Centers for Disease Control and Prevention, Atlanta, Georgia
Iowa Department of Public Health, Des Moines, Iowa
ABSTRACT
Background. In February 2004, students from a college in Iowa, with a high proportion of nonmedical exemptions to vaccination, traveled to India; one fourth of the students contracted measles while there. One exposed, susceptible student returned home during his infectious period, necessitating 2 months of containment efforts in Iowa.
Objective. The objective of this study was to measure the direct costs of measles containment from a public health system perspective.
Methods. We evaluated activities performed, personnel time/materials allocated, and direct costs incurred in 2004 US dollars by the Iowa public health infrastructure. The study period was defined as March 5, 2004 (when the Iowa Department of Public Health was first contacted about the case), through May 12, 2004 (when a final meeting was held on the containment effort).
Results. A total of 2525 hours of personnel time were expended to review flight manifests, contact exposed passengers, set up vaccination clinics, trace >1000 potentially exposed contacts, and institute and enforce quarantine orders for vaccination refusers. Two thousand twenty-five phone calls were received from the public, and 2243 miles were driven by staff. The temporal distribution of personnel time was characterized by marked peaks at the report of potential secondary cases. The total estimated cost was $ 142452.
Conclusions. The direct cost to the public health infrastructure of containing 1 case of measles was far greater than the estimated cost of uncomplicated individual illness (less than $100). Economic analyses of vaccine-preventable diseases may need to go beyond the costs of individual illness to account for the costs of protecting society.
Key Words: measles economic evaluation measles-mumps-rubella vaccines
Abbreviations: IDPH, Iowa Department of Public Health
Measles is a highly infectious, acute viral disease that can cause severe pneumonia, diarrhea, encephalitis, and death. An estimated 30 to 40 million cases and 750000 measles deaths occur annually worldwide.1 In the United States, <100 cases occurred annually during 2002–2003, 82% of which were import-associated.2 The success of the US measles-elimination program is based on high levels of preschool vaccination coverage (>90% by the age of 3 years)3 and the widespread requirement by states of 2 doses of measles vaccine for school entry.4 However, exemptions for religious or philosophical reasons are permitted in most states.5 Those who are exempt from receiving the vaccine are >22 times more likely to acquire measles than those who do receive it and create a 2- to 66-fold increased risk of measles for those who are not exempt from the vaccine mandates in the same community.6
In February 2004, a group of 28 college students from a community in Iowa with a high proportion of nonmedical exemptions to vaccination traveled together to India, where 44000 cases of measles were reported in 2003,7 although the true number is certainly much higher. All 6 students without receipt of at least 1 dose of measles vaccination contracted measles in India. The Iowa Department of Public Health (IDPH) recommended that students with measles stay in India during their infectious period to avoid potential spread during prolonged airline flights. Nonimmune contacts were asked to stay until the end of their potential incubation period. Despite the IDPH recommendations, 1 exposed unvaccinated student returned to Iowa earlier than requested. During his travel, involving connections in 2 busy airports, he developed a cough and conjunctivitis. Shortly after arrival in Iowa, he developed a rash and saw a physician who reported the case to the IDPH, and measles was subsequently laboratory-confirmed.8 This was the first measles case in Iowa since 1996 and occurred in a community with a high proportion of persons with nonmedical exemptions to vaccination. In this community, only 59% of the students attending primary/secondary school were fully vaccinated, compared with the statewide average of 97%. The IDPH began an intensive measles-containment effort, at the end of which spread was limited to 2 secondary cases: 1 unvaccinated close, personal contact of the index case patient and a person who had received 2 valid doses of measles-containing vaccine but who had sat next to the index case patient on a small airplane for 2 hours. None of the 3 people with measles were hospitalized or had known complications.
Conventional economic analyses often are confined to the costs incurred by the patient.9,10 However, the costs incurred by the 3 Iowa patients seemed to be small (none were hospitalized or had known complications) compared with the costs incurred by the public health system in preventing spread to others. In this study, we examined the economic impact of measles-containment efforts on Iowa public health institutions.
METHODS
The study was performed from a public health system perspective and evaluated activities performed, personnel time/materials allocated, and direct costs incurred in 2004 US dollars by the Iowa public health infrastructure. Public health activities performed by the University of Iowa Hospitals and Clinics in collaboration with the Johnson County Health Department were also included in the analysis. The study period was defined as March 5, 2004 (when the IDPH was first contacted about the students returning from India) through May 12, 2004 (when a final meeting was held on the containment effort). For activities, we obtained chronological descriptions from each involved institution. Resources allocated to specific response activities were identified when available. Personnel time was based on hours allocated to containment obtained from written chronological reports and personal interviews with the personnel in the involved institutions. For costs, an instrument focusing on major containment cost categories was administered to outbreak managers from the IDPH, county health departments, and other health institutions. Personnel time was converted to costs by using the reported gross wage of each individual, plus fringe benefits when available. Overhead costs were based on the number of person-hours and each institution's accounting method. Counts and unitary costs were obtained for phone calls, vaccine, immunoglobulin, and miles traveled. Because the study evaluated containment costs, we did not attempt to measure the direct costs of disease for the 3 cases of measles.
RESULTS
Activities
Containment activities included subpoenaing flight manifests, contacting Iowa-resident passengers concerning postexposure prophylaxis, communicating with other states concerning non–Iowa-resident passengers, issuance of press releases, issuance of health advisories to alert physicians and enhance surveillance, collaboration with the Centers for Disease Control and Prevention, and establishment of special measles-vaccination clinics. A toll-free measles-information phone line registered >2000 calls.
One of the 2 secondary case patients of measles had traveled during the infectious period with 60 other children from the community's school and attending adults to a neighboring town for an academic competition with >1000 other children. Three vaccination clinics were held in different locations for these contacts and others. Seven persons refused postexposure vaccination and were placed under quarantine, and some of these persons required the intervention of law-enforcement authorities. The other secondary case patient of measles had made 4 visits to 3 clinics during the infectious period. All potentially exposed medical staff and patients were contacted to assess measles immunity by using standards of the Advisory Committee on Immunization Practices criteria (adequate vaccination with measles-containing vaccine, laboratory proof of immunity, birth before 1957, or documentation of physician-diagnosed measles).11 Laboratory testing for immunity was performed at the Public Health Laboratory for Iowa using the Zeus Scientific enzyme-linked immunosorbent assay IgG for measles. Those lacking evidence of immunity were offered vaccination at a special vaccination clinic. Two exposed, susceptible health care workers did not receive postexposure vaccination within the recommended time period and were placed into voluntary home quarantine for 2 weeks.
Personnel Time/Materials
Approximately 2500 hours of personnel time were expended, of which 60% was devoted to emergency response, with approximately half incurred by the IDPH (Table 1). The temporal distribution of personnel time was characterized by marked peaks when the 2 secondary cases were reported, with subsequent smaller peaks at report of other rash illnesses for which measles was subsequently ruled out (Fig 1).
Costs
The total estimated cost was $ 142452, of which 75% was attributable to personnel costs and overhead, with the IDPH incurring 64% (Table 1).
DISCUSSION
The direct cost of an individual case of measles has been estimated to range from $70 (no complications) to $30000 (encephalitis), with an expected cost of $704.12 In this outbreak, the single primary patient and the 2 secondary case patients experienced no known complications; thus, the direct costs attributable to their illnesses may have been <$500. Our study suggests that the costs to the Iowa public health infrastructure of preventing the spread of disease from these cases were >$140000. This figure is an underestimate. We did not evaluate private-sector costs (eg, physicians and hospitals increasing disease surveillance and vaccination activity), costs outside of health institutions (eg, school, police), indirect costs (eg, impact on other public health programs in Iowa by diversion of resources into measles containment), or any costs outside Iowa (eg, other states contacting exposed passengers and setting up vaccination clinics, quarantine stations, airlines providing manifests and interacting with health authorities, Centers for Disease Control and Prevention staff time).
On the other hand, containment efforts would have been easier if high rates of vaccine acceptance had been present in the local community. Additionally, Iowa does not currently have a prematriculation vaccination requirement for college attendance. States enforcing such requirements have historically had lower rates of measles outbreaks in colleges.13 Vaccinations were administered to persons already needing vaccinations and thus may not ultimately represent incremental costs. Public-sector–containment costs cannot be translated directly into increased demands on public funds, because most personnel time was salaried at a fixed level.
Large community outbreaks have been associated with low rates of measles vaccination in countries such as the United Kingdom,14,15 Ireland,16,17 and Italy.18 Measles outbreaks in communities with low vaccination coverage due to exemptions have been described previously.19,20 However, the costs of containing a community-wide outbreak can easily run into the millions of dollars even in the absence of vaccine refusal.21 Using an expected cost of $704 per measles case, the containment efforts would have been cost-saving if they had prevented an outbreak of 200 measles cases. Because 40% of the local community was unvaccinated, an outbreak of as many as 1000 cases might have occurred.
The results of our analysis also raise some health-care issues that should be considered by primary care providers in the United States: (1) the importance of knowledge of immunization rates and segments of the undervaccinated population in the community that they serve; (2) the necessity of a travel-history assessment to detect diseases that are not common in the United States; and (3) the value of early diagnosis and reporting to the public health authorities of vaccine-preventable diseases that may now be uncommon because of effective implementation of vaccination programs.
The vigorous containment efforts developed during this outbreak were probably cost-saving and may have been life-saving. The containment costs of 1 measles case in this outbreak were high. Such costs are more likely to be evident in countries that are close to measles elimination, because the direct disease costs may be minimal. However, containment costs are rarely included in economic decision analyses, in part because these costs may be difficult to assign to an individual. Our study suggests that such analyses may need to go beyond the costs of individual illness to account for the costs of protecting society, particularly when countries are close to elimination.
ACKNOWLEDGMENTS
The Iowa Measles Response Team consists of the following members. Johnson County Department of Public Health: Kathryn "Kot" Flora, Annette Scheib, Meghan Harris, and Ralph Wilmoth; Jefferson County Public Health: Vickie McKeever, Sue Robinson, Linda Sharp, Peggy Hickenbottom, and Gary Roth; Linn County Public Health: Marty Ralston, Tom Hart, John Erceg, and Vickie Smith; University of Iowa Hospitals and Clinics: Loreen A. Herwaldt, Jean Pottinger, Sherry David, Stacy Coffman, Sandy Von Behren, Stephanie Holley, Sheri Swartzendruber, Todd Wiblin, Daniel Diekema, Charles Helms, Phil Polgreen, and Melissa Ward; Iowa Department of Public Health: Dawn Hughes, Chris Taylor, Elizabeth Miller, Josh Yoakam, Judy Goddard, Mary Rexroat, Pam Deichmann, Mary Jones, Sarah Brend, Tricia Kitzman, Jim Goodrich, Don Callahan, and Teri Thornton; Iowa Attorney General's Office: Heather Adams; and University Hygienic Laboratory: Lucy DesJardin and Tom Gahan.
We thank Dr Terri Hyde for collaboration in this study.
FOOTNOTES
Accepted Feb 2, 2005.
No conflict of interest declared.
REFERENCES
Centers for Disease Control and Prevention. Epidemiology of measles—United States, 2001–2003. MMWR Morb Mortal Wkly Rep.2004; 53 :713 –716
Centers for Disease Control and Prevention. National, state, and urban area vaccination levels among children aged 19–35 months—United States, 2003. MMWR Morb Mortal Wkly Rep.2004; 53 :658 –661
Centers for Disease Control and Prevention. State Immunization Requirements 2001–2002. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention;2002
Centers for Disease Control and Prevention, National Vaccine Advisory Committee. Report of the NVAC Working Group on Philosophical Exemptions, Minutes of the National Vaccine Advisory Committee, January 13, 1998. Atlanta, GA: National Vaccine Program Office;1998 :1 –5
Feikin D, Lezotte DC, Hamman RF, Salmon DA, Chen RT, Hoffman RF. Individual and community risks of measles and pertussis associated with personal exemptions to immunization. JAMA.2000; 284 :3145 –3150
Centers for Disease Control and Prevention. Imported measles case associated with nonmedical vaccine exemption—Iowa, March 2004. MMWR Morb Mortal Wkly Rep.2004; 53 :244 –246
White CC, Koplan JP, Orenstein WA. Benefits and costs of immunization for measles, mumps and rubella. Am J Public Health.1985; 75 :739 –744
Hatziandreu EJ, Brown RE, Halpern MT. A Cost-Benefit Analysis of the Measles-Mumps-Rubella (MMR) Vaccine. Report From the Medical Technology Assessment and Policy Research Program. Arlington, VA: US Department of Health and Human Services, Centers for Public Health Research and Evaluation;1994
Watson JC, Hadler SC, Dykewicz CA, Reef S, Phillips L. Measles, mumps, and rubella—vaccine use and strategies for elimination of measles, rubella, and congenital rubella syndrome and control of mumps: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep.1998; 47 (RR-8):1–57
Zhou F, Reef S, Massoudi M, et al. An economic analysis of the current universal 2-dose measles-mumps-rubella vaccination program in the United States. J Infect Dis.2004; 189 (suppl 1):S131–S145
Baughman AL, Williams WW, Atkinson WL, Cook LG, Collins MJ. The impact of college prematriculation immunization requirements on risk for measles outbreaks [published correction appears in JAMA. 1994;272:1822]. JAMA.1994; 272 :1127 –1132
Jansen VAA, Stollenwerk N, Jensen HV, Ramsay ME, Edmunds WJ, Rhodes CJ. Measles outbreaks in a population with declining vaccine uptake. Science.2003; 301 :804
Coughlan S, Connell J, Cohen B, Jin L, Hall W. Suboptimal measles-mumps-rubella vaccination coverage facilitates an imported measles outbreak in ireland. Clin Infect Dis.2002; 35 :84 –86
McBrien J, Murphy J, Gill D, Cronin M, O'Donovan C, Cafferkey MT. Measles outbreak in Dublin, 2000. Pediatr Infect Dis J.2002; 22 :580 –584
Centers for Disease Control and Prevention. Measles epidemic attributed to inadequate vaccination coverage—Campania, Italy, 2002. MMWR Morb Mortal Wkly Rep.2003; 52 :1044 –1047
Sutter RW, Markowitz LE, Bennetch JM, Morris W, Zell ER, Preblud SR. Measles among the Amish: a comparative study of measles severity in primary and secondary cases in households. J Infect Dis.1991; 163 :12 –16
van den Hof S, Meffre CM, Conyn-van Spaendonck MA, Woonink F, de Melker HE, van Binnendijk RS. Measles outbreak in a community with very low vaccine coverage, the Netherlands. Emerg Infect Dis.2001; 7 (3 suppl):593–597
Robertson SE, Markowitz LE, Berry DA, Dini EF, Orenstein WA. A million dollar measles outbreak: epidemiology, risk factors, and a selective revaccination strategy. Public Health Rep.1992; 107 :24 –31(Gustavo H. Dayan, MD, Ism)
Iowa Department of Public Health, Des Moines, Iowa
ABSTRACT
Background. In February 2004, students from a college in Iowa, with a high proportion of nonmedical exemptions to vaccination, traveled to India; one fourth of the students contracted measles while there. One exposed, susceptible student returned home during his infectious period, necessitating 2 months of containment efforts in Iowa.
Objective. The objective of this study was to measure the direct costs of measles containment from a public health system perspective.
Methods. We evaluated activities performed, personnel time/materials allocated, and direct costs incurred in 2004 US dollars by the Iowa public health infrastructure. The study period was defined as March 5, 2004 (when the Iowa Department of Public Health was first contacted about the case), through May 12, 2004 (when a final meeting was held on the containment effort).
Results. A total of 2525 hours of personnel time were expended to review flight manifests, contact exposed passengers, set up vaccination clinics, trace >1000 potentially exposed contacts, and institute and enforce quarantine orders for vaccination refusers. Two thousand twenty-five phone calls were received from the public, and 2243 miles were driven by staff. The temporal distribution of personnel time was characterized by marked peaks at the report of potential secondary cases. The total estimated cost was $ 142452.
Conclusions. The direct cost to the public health infrastructure of containing 1 case of measles was far greater than the estimated cost of uncomplicated individual illness (less than $100). Economic analyses of vaccine-preventable diseases may need to go beyond the costs of individual illness to account for the costs of protecting society.
Key Words: measles economic evaluation measles-mumps-rubella vaccines
Abbreviations: IDPH, Iowa Department of Public Health
Measles is a highly infectious, acute viral disease that can cause severe pneumonia, diarrhea, encephalitis, and death. An estimated 30 to 40 million cases and 750000 measles deaths occur annually worldwide.1 In the United States, <100 cases occurred annually during 2002–2003, 82% of which were import-associated.2 The success of the US measles-elimination program is based on high levels of preschool vaccination coverage (>90% by the age of 3 years)3 and the widespread requirement by states of 2 doses of measles vaccine for school entry.4 However, exemptions for religious or philosophical reasons are permitted in most states.5 Those who are exempt from receiving the vaccine are >22 times more likely to acquire measles than those who do receive it and create a 2- to 66-fold increased risk of measles for those who are not exempt from the vaccine mandates in the same community.6
In February 2004, a group of 28 college students from a community in Iowa with a high proportion of nonmedical exemptions to vaccination traveled together to India, where 44000 cases of measles were reported in 2003,7 although the true number is certainly much higher. All 6 students without receipt of at least 1 dose of measles vaccination contracted measles in India. The Iowa Department of Public Health (IDPH) recommended that students with measles stay in India during their infectious period to avoid potential spread during prolonged airline flights. Nonimmune contacts were asked to stay until the end of their potential incubation period. Despite the IDPH recommendations, 1 exposed unvaccinated student returned to Iowa earlier than requested. During his travel, involving connections in 2 busy airports, he developed a cough and conjunctivitis. Shortly after arrival in Iowa, he developed a rash and saw a physician who reported the case to the IDPH, and measles was subsequently laboratory-confirmed.8 This was the first measles case in Iowa since 1996 and occurred in a community with a high proportion of persons with nonmedical exemptions to vaccination. In this community, only 59% of the students attending primary/secondary school were fully vaccinated, compared with the statewide average of 97%. The IDPH began an intensive measles-containment effort, at the end of which spread was limited to 2 secondary cases: 1 unvaccinated close, personal contact of the index case patient and a person who had received 2 valid doses of measles-containing vaccine but who had sat next to the index case patient on a small airplane for 2 hours. None of the 3 people with measles were hospitalized or had known complications.
Conventional economic analyses often are confined to the costs incurred by the patient.9,10 However, the costs incurred by the 3 Iowa patients seemed to be small (none were hospitalized or had known complications) compared with the costs incurred by the public health system in preventing spread to others. In this study, we examined the economic impact of measles-containment efforts on Iowa public health institutions.
METHODS
The study was performed from a public health system perspective and evaluated activities performed, personnel time/materials allocated, and direct costs incurred in 2004 US dollars by the Iowa public health infrastructure. Public health activities performed by the University of Iowa Hospitals and Clinics in collaboration with the Johnson County Health Department were also included in the analysis. The study period was defined as March 5, 2004 (when the IDPH was first contacted about the students returning from India) through May 12, 2004 (when a final meeting was held on the containment effort). For activities, we obtained chronological descriptions from each involved institution. Resources allocated to specific response activities were identified when available. Personnel time was based on hours allocated to containment obtained from written chronological reports and personal interviews with the personnel in the involved institutions. For costs, an instrument focusing on major containment cost categories was administered to outbreak managers from the IDPH, county health departments, and other health institutions. Personnel time was converted to costs by using the reported gross wage of each individual, plus fringe benefits when available. Overhead costs were based on the number of person-hours and each institution's accounting method. Counts and unitary costs were obtained for phone calls, vaccine, immunoglobulin, and miles traveled. Because the study evaluated containment costs, we did not attempt to measure the direct costs of disease for the 3 cases of measles.
RESULTS
Activities
Containment activities included subpoenaing flight manifests, contacting Iowa-resident passengers concerning postexposure prophylaxis, communicating with other states concerning non–Iowa-resident passengers, issuance of press releases, issuance of health advisories to alert physicians and enhance surveillance, collaboration with the Centers for Disease Control and Prevention, and establishment of special measles-vaccination clinics. A toll-free measles-information phone line registered >2000 calls.
One of the 2 secondary case patients of measles had traveled during the infectious period with 60 other children from the community's school and attending adults to a neighboring town for an academic competition with >1000 other children. Three vaccination clinics were held in different locations for these contacts and others. Seven persons refused postexposure vaccination and were placed under quarantine, and some of these persons required the intervention of law-enforcement authorities. The other secondary case patient of measles had made 4 visits to 3 clinics during the infectious period. All potentially exposed medical staff and patients were contacted to assess measles immunity by using standards of the Advisory Committee on Immunization Practices criteria (adequate vaccination with measles-containing vaccine, laboratory proof of immunity, birth before 1957, or documentation of physician-diagnosed measles).11 Laboratory testing for immunity was performed at the Public Health Laboratory for Iowa using the Zeus Scientific enzyme-linked immunosorbent assay IgG for measles. Those lacking evidence of immunity were offered vaccination at a special vaccination clinic. Two exposed, susceptible health care workers did not receive postexposure vaccination within the recommended time period and were placed into voluntary home quarantine for 2 weeks.
Personnel Time/Materials
Approximately 2500 hours of personnel time were expended, of which 60% was devoted to emergency response, with approximately half incurred by the IDPH (Table 1). The temporal distribution of personnel time was characterized by marked peaks when the 2 secondary cases were reported, with subsequent smaller peaks at report of other rash illnesses for which measles was subsequently ruled out (Fig 1).
Costs
The total estimated cost was $ 142452, of which 75% was attributable to personnel costs and overhead, with the IDPH incurring 64% (Table 1).
DISCUSSION
The direct cost of an individual case of measles has been estimated to range from $70 (no complications) to $30000 (encephalitis), with an expected cost of $704.12 In this outbreak, the single primary patient and the 2 secondary case patients experienced no known complications; thus, the direct costs attributable to their illnesses may have been <$500. Our study suggests that the costs to the Iowa public health infrastructure of preventing the spread of disease from these cases were >$140000. This figure is an underestimate. We did not evaluate private-sector costs (eg, physicians and hospitals increasing disease surveillance and vaccination activity), costs outside of health institutions (eg, school, police), indirect costs (eg, impact on other public health programs in Iowa by diversion of resources into measles containment), or any costs outside Iowa (eg, other states contacting exposed passengers and setting up vaccination clinics, quarantine stations, airlines providing manifests and interacting with health authorities, Centers for Disease Control and Prevention staff time).
On the other hand, containment efforts would have been easier if high rates of vaccine acceptance had been present in the local community. Additionally, Iowa does not currently have a prematriculation vaccination requirement for college attendance. States enforcing such requirements have historically had lower rates of measles outbreaks in colleges.13 Vaccinations were administered to persons already needing vaccinations and thus may not ultimately represent incremental costs. Public-sector–containment costs cannot be translated directly into increased demands on public funds, because most personnel time was salaried at a fixed level.
Large community outbreaks have been associated with low rates of measles vaccination in countries such as the United Kingdom,14,15 Ireland,16,17 and Italy.18 Measles outbreaks in communities with low vaccination coverage due to exemptions have been described previously.19,20 However, the costs of containing a community-wide outbreak can easily run into the millions of dollars even in the absence of vaccine refusal.21 Using an expected cost of $704 per measles case, the containment efforts would have been cost-saving if they had prevented an outbreak of 200 measles cases. Because 40% of the local community was unvaccinated, an outbreak of as many as 1000 cases might have occurred.
The results of our analysis also raise some health-care issues that should be considered by primary care providers in the United States: (1) the importance of knowledge of immunization rates and segments of the undervaccinated population in the community that they serve; (2) the necessity of a travel-history assessment to detect diseases that are not common in the United States; and (3) the value of early diagnosis and reporting to the public health authorities of vaccine-preventable diseases that may now be uncommon because of effective implementation of vaccination programs.
The vigorous containment efforts developed during this outbreak were probably cost-saving and may have been life-saving. The containment costs of 1 measles case in this outbreak were high. Such costs are more likely to be evident in countries that are close to measles elimination, because the direct disease costs may be minimal. However, containment costs are rarely included in economic decision analyses, in part because these costs may be difficult to assign to an individual. Our study suggests that such analyses may need to go beyond the costs of individual illness to account for the costs of protecting society, particularly when countries are close to elimination.
ACKNOWLEDGMENTS
The Iowa Measles Response Team consists of the following members. Johnson County Department of Public Health: Kathryn "Kot" Flora, Annette Scheib, Meghan Harris, and Ralph Wilmoth; Jefferson County Public Health: Vickie McKeever, Sue Robinson, Linda Sharp, Peggy Hickenbottom, and Gary Roth; Linn County Public Health: Marty Ralston, Tom Hart, John Erceg, and Vickie Smith; University of Iowa Hospitals and Clinics: Loreen A. Herwaldt, Jean Pottinger, Sherry David, Stacy Coffman, Sandy Von Behren, Stephanie Holley, Sheri Swartzendruber, Todd Wiblin, Daniel Diekema, Charles Helms, Phil Polgreen, and Melissa Ward; Iowa Department of Public Health: Dawn Hughes, Chris Taylor, Elizabeth Miller, Josh Yoakam, Judy Goddard, Mary Rexroat, Pam Deichmann, Mary Jones, Sarah Brend, Tricia Kitzman, Jim Goodrich, Don Callahan, and Teri Thornton; Iowa Attorney General's Office: Heather Adams; and University Hygienic Laboratory: Lucy DesJardin and Tom Gahan.
We thank Dr Terri Hyde for collaboration in this study.
FOOTNOTES
Accepted Feb 2, 2005.
No conflict of interest declared.
REFERENCES
Centers for Disease Control and Prevention. Epidemiology of measles—United States, 2001–2003. MMWR Morb Mortal Wkly Rep.2004; 53 :713 –716
Centers for Disease Control and Prevention. National, state, and urban area vaccination levels among children aged 19–35 months—United States, 2003. MMWR Morb Mortal Wkly Rep.2004; 53 :658 –661
Centers for Disease Control and Prevention. State Immunization Requirements 2001–2002. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention;2002
Centers for Disease Control and Prevention, National Vaccine Advisory Committee. Report of the NVAC Working Group on Philosophical Exemptions, Minutes of the National Vaccine Advisory Committee, January 13, 1998. Atlanta, GA: National Vaccine Program Office;1998 :1 –5
Feikin D, Lezotte DC, Hamman RF, Salmon DA, Chen RT, Hoffman RF. Individual and community risks of measles and pertussis associated with personal exemptions to immunization. JAMA.2000; 284 :3145 –3150
Centers for Disease Control and Prevention. Imported measles case associated with nonmedical vaccine exemption—Iowa, March 2004. MMWR Morb Mortal Wkly Rep.2004; 53 :244 –246
White CC, Koplan JP, Orenstein WA. Benefits and costs of immunization for measles, mumps and rubella. Am J Public Health.1985; 75 :739 –744
Hatziandreu EJ, Brown RE, Halpern MT. A Cost-Benefit Analysis of the Measles-Mumps-Rubella (MMR) Vaccine. Report From the Medical Technology Assessment and Policy Research Program. Arlington, VA: US Department of Health and Human Services, Centers for Public Health Research and Evaluation;1994
Watson JC, Hadler SC, Dykewicz CA, Reef S, Phillips L. Measles, mumps, and rubella—vaccine use and strategies for elimination of measles, rubella, and congenital rubella syndrome and control of mumps: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep.1998; 47 (RR-8):1–57
Zhou F, Reef S, Massoudi M, et al. An economic analysis of the current universal 2-dose measles-mumps-rubella vaccination program in the United States. J Infect Dis.2004; 189 (suppl 1):S131–S145
Baughman AL, Williams WW, Atkinson WL, Cook LG, Collins MJ. The impact of college prematriculation immunization requirements on risk for measles outbreaks [published correction appears in JAMA. 1994;272:1822]. JAMA.1994; 272 :1127 –1132
Jansen VAA, Stollenwerk N, Jensen HV, Ramsay ME, Edmunds WJ, Rhodes CJ. Measles outbreaks in a population with declining vaccine uptake. Science.2003; 301 :804
Coughlan S, Connell J, Cohen B, Jin L, Hall W. Suboptimal measles-mumps-rubella vaccination coverage facilitates an imported measles outbreak in ireland. Clin Infect Dis.2002; 35 :84 –86
McBrien J, Murphy J, Gill D, Cronin M, O'Donovan C, Cafferkey MT. Measles outbreak in Dublin, 2000. Pediatr Infect Dis J.2002; 22 :580 –584
Centers for Disease Control and Prevention. Measles epidemic attributed to inadequate vaccination coverage—Campania, Italy, 2002. MMWR Morb Mortal Wkly Rep.2003; 52 :1044 –1047
Sutter RW, Markowitz LE, Bennetch JM, Morris W, Zell ER, Preblud SR. Measles among the Amish: a comparative study of measles severity in primary and secondary cases in households. J Infect Dis.1991; 163 :12 –16
van den Hof S, Meffre CM, Conyn-van Spaendonck MA, Woonink F, de Melker HE, van Binnendijk RS. Measles outbreak in a community with very low vaccine coverage, the Netherlands. Emerg Infect Dis.2001; 7 (3 suppl):593–597
Robertson SE, Markowitz LE, Berry DA, Dini EF, Orenstein WA. A million dollar measles outbreak: epidemiology, risk factors, and a selective revaccination strategy. Public Health Rep.1992; 107 :24 –31(Gustavo H. Dayan, MD, Ism)