Published online November 1, 2007
PEDIATRICS Vol. 120 No. 5 November 2007, pp. e1165-e1173 (doi:10.1542/peds.2007-0037)
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ARTICLE

Effect of Vaccine Shortages on Timeliness of Pneumococcal Conjugate Vaccination: Results From the 2001–2005 National Immunization Survey

Philip J. Smith, PhDa, J. Pekka Nuorti, MD, DSca, James A. Singleton, MSa, Zhen Zhao, PhDa and Kirk M. Wolter, PhDb

a National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia
b National Opinion Research Center and University of Chicago, Chicago, Illinois


    ABSTRACT
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
BACKGROUND. In September 2001 and again in February 2004, the Centers for Disease Control and Prevention announced shortages in the supply of the pneumococcal conjugate vaccine. We describe the effects of the pneumococcal conjugate vaccine shortages in 2001–2003 and 2004 on the timeliness of vaccination uptake for quarterly birth cohorts affected by the shortages.

METHODS. A total of 102478 19- to 35-month-old children were sampled by the National Immunization Survey between 2001 and 2005. Provider-reported vaccination histories were used to evaluate whether children had been administered ≥4 doses of pneumococcal conjugate vaccine by 16 months of age.

RESULTS. Among successive birth cohorts affected by the first shortage, estimated coverage of ≥4 doses of pneumococcal conjugate vaccine by 16 months declined significantly from 28.8% to 18.2%. As the first shortage ended, estimated coverage of ≥4 doses of pneumococcal conjugate vaccine by 16 months increased steadily with each successive birth cohort to 40.2%. From the onset of the second shortage, estimated coverage of ≥4 doses of pneumococcal conjugate vaccine by 16 months declined steadily and significantly to 13.7%. As many as 27% of parents whose child was affected by the first shortage reported that their child's vaccination provider had delayed the administration of pneumococcal conjugate vaccine doses. Of those parents who said that a pneumococcal conjugate vaccine dose was delayed and whose child was not administered ≥4 doses, 2.9% received a reminder notice from the provider to schedule administration of those delayed doses, and 0.2% had an appointment to receive those delayed or missed doses.

CONCLUSIONS. Vaccine shortages can result in delayed or missed doses and can have a dramatic impact on the vaccine coverage of children. Vaccination providers need to communicate effectively with parents so that doses that are delayed or missed during a vaccine shortage are administered when the shortage is resolved.


Key Words: childhood immunization • surveillance and monitoring

Abbreviations: PCV7—pneumococcal conjugate vaccine • ACIP—Advisory Committee on Immunization Practices • CI—confidence interval • CDC—Centers for Disease Control and Prevention • NIS—National Immunization Survey • RDD—random-digit dialing • MSA—metropolitan statistical area

Streptococcus pneumoniae is a leading cause of bacteremia, sepsis, meningitis, pneumonia, sinusitis, and acute otitis media in young children.1 In February 2000 a 7-valent pneumococcal conjugate vaccine (PCV7), Prevnar (Wyeth-Ayerst Pharmaceuticals, Marrietta, PA), was licensed. A total of 4 doses of PCV7 at ages 2, 4, 6, and 12 to 15 months was subsequently recommended for routine administration young children by the American Academy of Pediatrics in August 20002 and the Advisory Committee on Immunization Practices (ACIP) in October 2000.1 The routinely recommended PCV7 4-dose series has been 97% effective (95% confidence interval [CI]: 76%–100%) against invasive disease caused by serotypes represented in the vaccine, and effectiveness in children who received 3 doses before 12 months of age has been 87% (95% CI: 71%–94%).3

In August 2001, deliveries of the vaccine were delayed, resulting in the first shortage of PCV7,4 and in December 2001, the ACIP recommended deferring the fourth dose of the vaccine for health children.5 In May 2003, the Centers for Disease Control and Prevention (CDC) reported that PCV7 production and deliveries had become sufficiently adequate to permit a return to the 4-dose schedule.6

However, in December 2003, the CDC reported that it had received notice from the only US supplier of PCV7 that production constraints could cause delays in shipments. Subsequently, in February 2004, the CDC recommended that health care providers temporarily suspend routine use of the fourth dose of PCV7 to conserve the vaccine and minimize the likelihood of shortages,7 and then in March 2004, the CDC recommended that all health care providers temporarily suspend routine administration of both the third and fourth doses of PCV7 to healthy children.3 In September 2004, the CDC announced the end of the second PCV7 shortage because of the increased production capacity of the US supplier of PCV7 and reinstated the original American Academy of Pediatrics and ACIP recommendation of a 4-dose schedule to be completed by 16 months of age.8

Little is known about the impact of the shortages on the timeliness of PCV7 vaccinations. Because the routine schedule recommends 3 doses of PCV7 by 7 months of age and 4 doses by 16 months, we evaluated the impact of vaccine shortages on the uptake of ≥3 doses of PCV7 by 7 months and ≥4 doses of PCV7 by 16 months of age. Also, we present estimated coverage of ≥3 and ≥4 doses of PCV4 by 24 months to evaluate subsequent uptake after those recommended ages. We also identified the characteristics of children whose PCV7 coverage was significantly lower as a result of the shortages. Finally, we examined the extent to which the parents of children affected by PCV7 shortages had reported delayed PCV7 doses, had an appointment to receive missed doses, or had ever received reminder notices to get missed doses.


    METHODS
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Design of the National Immunization Survey
Data collected from 102478 19- to 35-month-old children sampled by the 2001, 2002, 2003, 2004, and 2005 National Immunization Survey (NIS) were analyzed. The NIS is a survey of US children 19 to 35 months of age conducted by the CDC for the purposes of monitoring vaccination coverage rates in the United States. Data collection in the NIS occurs in 2 phases, including a list-assisted random-digit dialing (RDD) survey of households with land-line telephones that have children 19 to 35 months of age, followed by a vaccination provider record check. Cellular telephone numbers are not included in the list of telephone numbers from which the RDD sample is obtained. When a household with an age-eligible child is identified in the RDD phase of the survey, an RDD interview is conducted that collects demographic information about each age-eligible child in the household, demographic information about the age-eligible child's mother, and sociodemographic information about the household. At the end of the RDD interview, consent is requested for contacting the age-eligible children's vaccination providers. If consent is given, the provider record-check phase of the NIS is conducted. In the provider record-check phase, all of the vaccination providers named by the RDD respondent are contacted by mail to obtain the age-eligible child's provider-reported vaccination history. Provider-reported vaccination histories obtained from the provider record check were used to evaluate the vaccination status of children sampled in the NIS. The NIS was reviewed and approved by the institutional review board at the CDC in 2001 and 2006. Zell et al9 and Smith et al1012 provide a detailed description of the statistical methods used by the NIS.

NIS Coverage of the Population of Children 19 to 35 Months of Age and Survey Response Rates
Between 2001 and 2005, among households with children 19 to 35 months of age, the percentage of 19- to 35-month-old children who lived in a household with a land-line telephone was ~90%. The response rate of the NIS is the product of 3 proportions: (1) the estimated percentage of households that reported in the NIS RDD interview as having a 19- to 35-month-old child among those that actually have a 19- to 35-month-old child, (2) the Council of American Survey Research Organizations13 rate of the RDD portion of the NIS, and (3) the percentage of sampled children for whom a provider-reported vaccination history is obtained in the NIS provider record check that is sufficiently detailed to accept as a complete report.12 The Council of American Survey Research Organizations rate is the multiplicative product of the resolution completion rate, the screener completion rate, and the RDD interview completion rate. The resolution completion rate is the proportion of telephone numbers determined to be residential, nonresidential, or nonworking among all telephone numbers in the released NIS sample; the screener completion rate is the proportion of telephone number callers who completed the NIS screening interview among all of the resolved residential telephone numbers; and the RDD interview completion rate is the proportion of households that completed the NIS interview among all of the households with ≥1 child who was 19 to 35 months of age.

For the survey years that we studied, among households that had a land-line telephone and a 19- to 35-month-old child, the estimated percentages of households that reported having a 19- to 35-month-old child in the RDD portion of the NIS ranged from 74% and 70%, and the Council of American Survey Research Organizations rates ranged from 69% to 76%. Among parents of age-eligible children who had a completed NIS RDD interview, the percentages of children who had a sufficiently detailed vaccination history returned from vaccination providers to accept as a complete report ranged from 62% to 68%.

Statistical Analyses of the Timeliness of PCV7 Administration
Studies have demonstrated that the recommended PCV7 4-dose series administered before 16 months of age has very high effectiveness against invasive disease caused by serotypes represented in the vaccine.1 Although the ACIP specified alternative vaccination schedules for older infants and for catch-up doses during the initial uptake of the vaccine, we evaluated PCV7 uptake by the ACIP vaccination schedule for previously unvaccinated infants that recommends the routine administration of 4 doses of PCV7 by 16 months of age.1 During the PCV7 shortages, most of the children who were affected were between 2 and 15 months of age, the youngest and oldest ages at which doses are recommended in the routine 4-dose schedule. To measure the temporal effect of PCV7 shortages on the timeliness of PCV vaccination coverage among children affected by those shortages, we evaluated PCV7 coverage for quarterly birth cohorts. The quarterly birth cohort of each sampled child was defined by the year and quarter in which they were born. For each quarterly birth cohort, we estimated the percentage of children who were administered ≥4 doses of PCV7 by 16 and 24 months of age and the percentage of children who were administered ≥3 doses of PCV7 by 7 and 24 months of age.

To examine the extent to which parents of children affected by PCV7 shortage had reported a delayed PCV7 dose, had an appointment to receive missed doses, or had ever received reminder notices to get missed doses, we used data collected from the 2840 children sampled in the first vaccine shortage module of the NIS. Because the vaccine shortage module collected data between the second quarter of 2003 and the fourth quarter of 2003 from 19- to 35-month-old children, information collected in that module included data from quarterly birth cohorts who were to be administered the recommended PCV7 vaccination schedule during the first PCV7 shortage that was announced in August 2001 and lasted until May 2003.

In all of our analyses, we used SAS software survey procedures (SAS Institute, Inc, Cary, NC)14 that allow the sampling weights, sampling design of the NIS, independence of sampling from year to year, and clustering within households to be taken into account in our statistical analyses. For each quarterly birth cohort, we used a cohort-age model described by Smith et al15 to estimate the percentages of children who had received ≥4 PCV7 doses by 16 and 24 months of age and ≥3 PCV7 doses by 7 and 24 months of age. The statistical significance of differences between estimated percentages was evaluated using z-score tests.


    RESULTS
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Decreases in ≥4-Dose PCV7 Coverage by 16 Months During the Vaccine Shortages
Children affected by the first PCV7 shortage belonged to quarterly birth cohorts that were born approximately between the fourth quarter of 2000 and the fourth quarter of 2001 (Fig 1). Subsequent to the peak in vaccination coverage that preceded the first shortage, ≥4-dose PCV7 coverage by 16 months of age declined significantly (P < .05) from 28.8% (95% CI: ±1.9%) for the quarterly birth cohort born in the third quarter of 2000 to 18.2% (95% CI: ±1.7%) for the quarterly birth cohort born in the second quarter of 2001. Also, children affected by the second PCV7 shortage belonged to quarterly birth cohorts that were born approximately between the fourth quarter of 2002 and the third quarter of 2003 (Fig 1). Subsequent to the second peak in vaccination coverage that preceded the second shortage, ≥4-dose PCV7 coverage declined significantly (P < .05) from 40.1% (95% CI: ±2.8%) for the birth cohort born in the fourth quarter of 2002 to 13.7% (95% CI: ±1.2%) for the birth cohort born in the second quarter of 2003.


Figure 1
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FIGURE 1 Estimated vaccination coverage of ≥4 doses of PCV7 by 16 (dashed line) and 24 (dotted line) months of age among selected birth cohorts. Sample sizes for the coverage estimates at 16 months are listed directly below the estimate, and sample sizes for the coverage estimates at 24 months are listed directly above the estimate. Data are from the 2001–2005 NIS.

 
Late Doses of ≥4 Doses of PCV7 Administered by 24 Months
For all of the quarterly birth cohorts, coverage of ≥4 doses of PCV7 increased appreciably between 16 and 24 months of age (Fig 1). This increase was ~13% during the first PCV7 shortage and ~34% during the second shortage. However, during the first shortage, uptake of ≥4 doses of PCV7 by 24 months of age remained flat at ~33%. However, during the second shortage, coverage of ≥4 doses of PCV7 by 24 months decreased significantly from 51.2% (95% CI: ±3.4%) to 36.4% (95% CI: ±3.0%; P < .05).

≥3 Doses of PCV7 Coverage by 7 and 24 months
Vaccination coverage of ≥3 doses of PCV7 by 7 months of age was affected by the 2 PCV7 shortages (Fig 2). Subsequent to the first peak in vaccination coverage preceding the first shortage, ≥3-dose PCV7 coverage by 7 months of age declined significantly (P < .05) from 43.2% (95% CI: ±2.2%) for the quarterly birth cohort born in the first quarter of 2001 to 27.7% (95% CI: ±2.1%) for the quarterly birth cohort born in the second quarter of 2002. Subsequent to the second peak in vaccination coverage preceding the second shortage, ≥3-dose PCV7 coverage declined significantly (P < .05) from 56.9% (95% CI: ±2.9) for the birth cohort born in the second quarter of 2003 to 15.9% (95% CI: ±2.8%) for the birth cohort born in the fourth quarter of 2003.


Figure 2
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FIGURE 2 Estimated vaccination coverage of ≥3 doses of PCV7 by 7 (dashed line) and 24 (dotted line) months of age among selected birth cohorts. Sample sizes for the coverage estimates at 7 months are listed directly below the estimate, and sample sizes for the coverage estimates at 24 months are listed directly above the estimate. Data are from the 2001–2005 NIS.

 
For all of the quarterly birth cohorts, vaccination coverage of ≥3 doses of PCV7 increased appreciably between 7 and 24 months of age (Fig 2). During the first PCV7 shortage, this increase was ~30% for birth cohorts. However, during the second PCV7 shortage, this increase was as much as 65%.

Association Between ≥4 Doses of PCV7 by 16 Months of Age and Characteristics of Children Affected by the First PCV7 Shortage
Among children affected by the first PCV7 shortage, the quarterly birth cohort born in the second quarter of 2001 had the lowest percentage of children administered ≥4 doses of PCV7 by 16 months of age. Among children in that birth cohort, Hispanic, non-Hispanic black, and non-Hispanic American Indian children had significantly lower vaccination coverage than non-Hispanic white children; foreign-born children had significantly lower vaccination coverage than native-born children; and children who had received their vaccine doses from all public, hospital, military, or mixed-type providers had significantly lower vaccination coverage than children who received all of their doses from a private vaccination provider (Table 1).


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TABLE 1 Estimated Percentage of Children Who Received ≥4 Doses of PCV7 by 16 and 24 Months of Age for the Birth Cohorts With Lowest Coverage During the First and Second PCV7 Shortages According to Selected Child, Maternal, and Household Characteristics: NIS 2001–2005

 
Also, children whose mother was never married or widowed/divorced/separated had significantly lower vaccination coverage than children whose mother was married; children whose mother had ≤12 years of schooling or had not completed college had significantly lower vaccination coverage than children whose mother was a college graduate; children whose mother preferred to speak Spanish during the NIS telephone interview had significantly lower vaccination coverage than those whose mother spoke English; and children whose mother was ≤29 years of age had a significantly lower vaccination coverage than those whose mother was ≥30 years of age.

Finally, children living in a household with annual income that was <135% of the federal poverty level had significantly lower vaccination coverage than children living in a household with an annual income above the 135% the federal poverty level; children who lived in a household with ≥2 children ≤18 years of age had significantly lower vaccination coverage than children with 1 child; and children who lived in a noncentral city metropolitan statistical area (MSA) or in a non-MSA had significantly lower vaccination coverage than children who lived in a central city MSA.

With respect to late doses received by 24 months of age, nearly all of the child, maternal, and household characteristics found to be statistically significant in explaining the variation in the percentage of children receiving ≥4 doses of PCV7 by 16 months were significant in explaining the variation in the percentage of children receiving ≥4 doses of PCV7 by 24 months (Table 1).

Association Between Coverage of ≥4 Doses of PCV7 by 16 Months of Age and Characteristics of Children Affected by the Second PCV7 Shortage
Among children affected by the second PCV7 shortage, the quarterly birth cohort born in the second quarter of 2003 had the lowest percentage of children administered ≥4 doses of PCV7 by 16 months of age. Compared with the quarterly birth cohort born in the second quarter of 2001, for the quarterly birth cohort born in the second quarter of 2003, there were relatively few factors associated with variation in vaccination coverage with ≥4 doses of PCV7 by 16 months of age. In particular, children's race/ethnicity was not significantly associated with variation in estimated vaccination coverage of ≥4 doses of PCV7 by 16 months of age (Table 1).

However, foreign-born children had significantly lower vaccination coverage than native born children; and children who were administered all of their PCV7 doses at a public facility had significantly lower coverage than children who were administered all of their PCV7 doses at a private facility. Also, children whose mother had >12 years of education but not a college degree had significantly lower estimated coverage than children whose mother had a college degree. Finally, among children born in the second quarter of 2003, there were no household characteristics found to be significantly associated with variation in ≥4-dose PCV7 coverage by 16 months of age.

However, with respect to receiving ≥4 doses of PCV7 by 24 months, for children belonging to the quarterly birth cohort born in the second quarter of 2003, nearly all of the child, maternal, and household characteristics found to be statistically significant in explaining the variation in the percentage of children receiving ≥4 doses of PCV7 by 16 months of age among children born in the second quarter of 2001 reappeared as being statistically significant (Table 1).

Reminder/Recall Efforts to Administer Delayed and Missed Doses
Compared with the birth cohort born in the second quarter of 2000 that was scheduled to receive all of the recommended doses of PCV7 before the first shortage, birth cohorts that were scheduled to receive doses of PCV7 during the first shortage had significantly higher percentages of parents reporting that PCV7 doses had been delayed because the child's vaccination provider told them that he/she was out of the vaccine (P < .05; Table 2). Among parents who reported a delay in administration of a PCV7 dose to their child and whose child had not received ≥4 doses of PCV7 by the time of NIS RDD interview, only 2.9% (95% CI: ±2.6%) reported receiving a postcard, letter, or telephone call to remind them to bring their child back to the vaccination provider for this vaccine dose that was delayed, and 0.2% (95% CI: ±0.5%) reported having an appointment to have the missed PCV7 doses administered to their child.


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TABLE 2 Estimated Percentage of Households Reporting That a PCV7 Dose Had Ever Been Delayed by Quarterly Birth Cohort: NIS Vaccination Shortage Module

 

    DISCUSSION
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
In evaluating the impact of the 2 PCV7 shortages, we have shown that after the peaks in estimated vaccination coverage that preceded the 2 PCV7 vaccine shortages, coverage of ≥4 doses of PCV7 by 16 months of age declined steeply by 10.6% (95% CI: ±2.6%) in the first shortage and then by 26.4% (95% CI: ±3.0%) among quarterly birth cohorts affected by the second shortage. Our findings show that there was a large number of late doses administered to quarterly birth cohorts who were affected by the PCV7 shortages. However, we also found that a large percentage of children affected by the shortages had not received ≥4 doses of PCV7 by 24 months.16 Despite the shortages and associated lower coverage and delay of recommended doses, incidence of invasive pneumococcal disease has declined in young children after the introduction of PCV7.17,18 The additional disease burden that could have been prevented in the absence of the shortages is unknown, particularly among birth cohorts that were affected most by the shortage and among children who never received catch-up doses.

Also, we found disparities in estimated ≥4-dose PCV7 coverage between non-Hispanic white children and Hispanic, non-Hispanic black, and non-Hispanic American Indian children. In particular, the disparities we observed are similar to those observed in other reports on vaccination coverage surveillance19 and are often attributable to barriers to accessing primary care, such as not having health insurance,20 not having a medical home,21 or living in a location that is inconvenient to public or private clinics where vaccines are routinely administered.21 These disparities were found in the estimated vaccination coverage of ≥4 doses of PCV7 by 16 and 24 months during the first shortage and by 24 months in the second shortage. Although we did not find a disparity in the estimated coverage of ≥4 doses by 16 months between racial/ethnic groups in the second shortage, children who received all of the doses at a public facility had significantly lower estimated coverage than children who received all of the doses at a private facility.

In other research,22 a survey of 1412 vaccination providers found that 64% reported having a system to track children for whom PCV7 doses were deferred because of the shortages or because of the reduced number of vaccine doses recommended during the PCV7 shortages.7,23,24 However, our findings showed that, among children who had not received 4 doses of PCV7 and whose parent reported a delay in administration of a PCV7 dose, <1% reported that they had been contacted by their child's vaccination provider to have those missed doses administered. How might the discrepancy in the findings between the vaccination provider survey and the findings from the NIS be reconciled? Perhaps some provider's systems were not used to track children for whom PCV7 doses were deferred because of the shortages, or perhaps parents did not remember receiving the message or the messages received by parents from providers to recall children who missed doses was misunderstood or misinterpreted. Additional research is needed to evaluate the effectiveness of provider efforts to catch up vaccinations deferred during a vaccine shortage.

Our study has several strengths. The results of our study are based on data from a large national survey. Data from the survey can be used to monitor the number and percentage of children who may be susceptible to vaccine-preventable diseases because they are not vaccinated or are undervaccinated as a result of delayed or missed doses during vaccine shortages.

The NIS response rate suggests one potential limitation of our work: because of the potential for selection bias resulting from multiple levels of nonresponse to the NIS, our statistical estimates of vaccination coverage may not accurately represent that of the entire target population of children 19 to 35 months of age in the United States. Although weighting adjustments12 were used to mitigate the potential for selection bias resulting from nonresponse, the effectiveness of those adjustments is unknown. If response to the NIS is associated with higher vaccination coverage or greater access to vaccinations during vaccine shortages, our estimates may underestimate the impact of the PCV7 vaccine shortage to the extent that the weighting adjustments do not adequately account for those factors. However, research by Bartlett et al25 has shown that estimates of vaccination coverage obtained from the National Health Interview Survey are nearly identical to those obtained from the NIS. Because the National Health Interview Survey is a door-to-door survey with interviews that are administered face to face, there is no bias in their estimates that can be attributed to households not having land-line telephones. Because the NIS estimates have been nearly identical to the estimates obtained from the National Health Interview Survey, there is empirical evidence that the statistical adjustments used to account for that potential source of selection bias work adequately in the NIS.

Another limitation of our work is that, although the ACIP specified alternative vaccination schedules for older infants and for catch-up doses during the initial uptake of the vaccine, in our work we evaluated PCV7 uptake by the ACIP vaccination schedule for previously unvaccinated infants that recommends the routine administration of 4 doses of PCV7 by 16 months of age and did not account for the possibility that some vaccination providers followed the alternative schedules that required fewer doses to be administered. In analyses not presented in this article, we have accounted for this nuance and found that results did not change appreciably, however.

A steady and reliable supply of childhood vaccines is critical to combating vaccine preventable diseases. Since 2000, there have been shortages of the tetanus and diphtheria booster vaccine26; the influenza vaccine27; the measles, mumps, and rubella vaccine28; the varicella vaccine28; PCV74,7; and, more recently, the meningococcal conjugate vaccine.29 These shortages have demonstrated the vulnerability of the vaccine supply.

Manufacturing a vaccine is a complex, highly controlled process that can take several months to over a year, and, thus, increasing the number of doses that are available to be administered can take time. Because there is frequently just 1 manufacturer producing a particular vaccine, even short-term disruptions in a manufacturer's production volume may create a shortage that may result in underimmunization. Rodewald et al30 have described 4 measures that the CDC takes to improve vaccine supply. First, the demand for vaccine production is heavily influenced by recommendations of the Advisory Committee on Immunization Practices that develops written recommendations for the routine administration of vaccines to the pediatric and adult populations, along with schedules regarding the appropriate periodicity and dosage. Second, the CDC negotiates a federal contract that uses federal and state funds to purchase ~56% of the recommended childhood vaccines distributed in the United States. Third, the CDC administers grants to states to help in implementing and promoting immunization programs to improve vaccine coverage rates. Fourth, the CDC administers some stockpiles of vaccines to be used for disruptions in production and surges in demand.

The General Accounting Office has recommended coordinating efforts between government and industry to increase and maintain vaccine stockpiles that will be available to all children during shortages, monitoring childhood vaccine inventory in state Vaccine for Children depots that can be used by all children during periods of vaccine shortages, and monitoring the delivery of vaccines to stockpiles and adequacy of the amount of vaccines in those stockpiles.31 Vaccine stockpiles can be used to interrupt disease outbreak situations and to ameliorate short-term production problems. In light of recent vaccine shortages and increased concerns about an influenza pandemic or bioterrorism event, expansion of the CDC's stockpiles has become a pressing public health need.

In addition to strengthening vaccine stockpiles, we believe that effective communication between vaccine providers and parents during vaccine shortages about when missed vaccines can be caught up is crucial. It is known that vaccination providers are the single most important source of information where parents seek advice about vaccines.32,33 Also, efforts to remind parents when pediatric vaccines are due or to recall parents when vaccines are overdue have been demonstrated to be effective in increasing vaccination coverage rates.34 Guidelines communicating with parents about other barriers to vaccination, such as concerns about vaccine safety, have been published.35 In our current era of recurrent vaccine shortages, it is desirable that additional guidelines be published for pediatricians that describe how to communicate effectively with parents about vaccine shortages and how to establish an effective plan with parents to make up missed or deferred doses for their children.


    CONCLUSIONS
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Children who miss doses that are not caught up during or after periods of vaccine shortage represent a pool of children who are at increased risk of acquiring and transmitting vaccine-preventable diseases. Our findings suggest that, during the initial uptake of a newly introduced vaccine, a vaccine shortage can have a significant effect on the vaccination coverage of birth cohorts affected by the shortage. Furthermore, children belonging to minority race/ethnic groups and other children who have characteristics or live in circumstances that are traditionally associated with low vaccination coverage may be impacted more greatly by the shortage.


    FOOTNOTES
 
Accepted Apr 17, 2007.

Address correspondence to Philip J. Smith, PhD, Centers for Disease Control and Prevention, National Immunization Program, MS E-32, 1600 Clifton Rd, NE, Atlanta, GA 30333. E-mail: pzs6{at}cdc.gov

The authors have indicated they have no financial relationships relevant to this article to disclose.


    REFERENCES
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

  1. Centers for Disease Control and Prevention. Preventing pneumococcal disease among infants and young children. Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 2000;49(RR-9) :1 –38. Available at: www.cdc.gov/mmwr/preview/mmwrhtml/rr4909a1.htm. Accessed April 9, 2007
  2. American Academy of Pediatrics, Committee on Infectious Diseases. Policy statement: recommendations for the prevention of pneumococcal infections, including the use of pneumococcal conjugate vaccine (Prevnar), pneumococcal polysaccharide vaccine, and antibiotic prophylaxis. Pediatrics. 2000;106 :362 –366[Abstract/Free Full Text]
  3. Centers for Disease Control and Prevention. Notice to readers: updated recommendations on the use of pneumococcal conjugate vaccine: suspension of recommendation for third and fourth dose. MMWR Morb Mortal Wkly Rep. 2004;53 :177 –178. Available at: www.cdc.gov/mmwr/preview/mmwrhtml/mm5308a5.htm. Accessed April 9, 2007[Medline]
  4. Centers for Disease Control and Prevention. Notice to readers: decreased availability of pneumococcal conjugate vaccine. MMWR Morb Mortal Wkly Rep. 2001;50 :783 –784. Available at: www.cdc.gov/mmwr/preview/mmwrhtml/mm5036a3.htm. Accessed April 9, 2007
  5. Centers for Disease Control and Prevention. Notice to readers: updated recommendations on the use of pneumococcal conjugate vaccine in a setting of vaccine shortage—Advisory Committee on Immunization Practices. MMWR Morb Mortal Wkly Rep. 2001;50 :1140 –1142. Available at: www.cdc.gov/mmwr/preview/mmwrhtml/mm5050a4.htm. Accessed April 9, 2007
  6. Centers for Disease Control and Prevention. Notice to readers: pneumococcal conjugate vaccine shortage resolved. MMWR Morb Mortal Wkly Rep. 2003;52 :446 –447. Available at: www.cdc.gov/mmwr/preview/mmwrhtml/mm5219a6.htm. Accessed April 9, 2007
  7. Centers for Disease Control and Prevention. Notice to readers: limited supply of pneumococcal conjugate vaccine: suspension of recommendation for fourth dose. MMWR Morb Mortal Wkly Rep. 2004;53 :108 –109. Available at http://www.cdc.gov/MMWR/preview/mmwrhtml/mm5305a6.htm. Accessed September 8, 2007
  8. Centers for Disease Control and Prevention. Notice to readers: pneumococcal conjugate vaccine shortage resolved. MMWR Morb Mortal Wkly Rep. 2004;53 :851 –852. Available at: www.cdc.gov/mmwr/preview/mmwrhtml/mm5336a8.htm. Accessed April 9, 2007
  9. Zell ER, Ezzati-Rice TM, Battaglia MP, Wright RA. The National Immunization Survey: the methodology of a vaccination surveillance system. Pub Health Rep. 2000;115 :65 –77[CrossRef][Web of Science][Medline]
  10. Smith PJ, Battaglia MP, Huggins VJ, et al. Overview of the sampling design and statistical methods used in the National Immunization Survey. Am J Prev Med. 2001;20(4 suppl) :17 –24
  11. Smith PJ, Rao JNK, Battaglia MP, et al. Compensating for nonresponse bias in the national immunization survey using response propensities. Vital Health Stat. 2001;(133) :2 . Available at: www.cdc.gov/nchs/data/series/sr_02/sr02_133.pdf. Accessed April 9, 2007
  12. Smith PJ, Hoaglin DC, Battaglia MP, et al. Statistical Methodology of the National Immunization Survey: 1994–2002. Vital Health Stat. 2005;(138) :2 . Available at: www.cdc.gov/nchs/data/series/sr_02/sr02_138.pdf. Accessed April 9, 2007
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PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics

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P. J. Smith, N. Jain, J. Stevenson, N. Mannikko, and N.-A. Molinari
Progress in Timely Vaccination Coverage Among Children Living in Low-Income Households
Arch Pediatr Adolesc Med, May 1, 2009; 163(5): 462 - 468.
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