- Email: [email protected]
Provider Response to Different Formats of the Adult Immunization Schedule
Provider Response to Different Formats of the Adult Immunization Schedule Matthew M. Davis, MD, MAPP, Lakshmi K. Halasyamani, MD, Vishnu-Priya Sneller, MBBS, PhD, MSPH, Kathy R. Bishop, MHSA, Sarah J. Clark, MPH Background: Providers’ failure to administer vaccines in accordance with established recommendations is a well-recognized barrier to national immunization efforts. This study evaluated the ease of use of two different formats of the Centers for Disease Control and Prevention’s (CDC) adult immunization schedule by physicians in private practice, where the majority of adult immunizations are administered. Methods:
A series of focus groups was conducted with 94 physicians and other clinical staff in 11 private practices (family medicine and internal medicine) in six U.S. cities. Each session was based on a structured set of questions that explored barriers to adult immunizations, followed by three mock clinical scenarios to examine how each of two graphical depictions of the 2003–2004 adult immunization schedule (one from the CDC’s Advisory Committee on Immunization Practices, and the other from the Immunization Action Coalition) might facilitate assessments of recommended immunizations. Group dialogue and individual participants’ written responses to the scenarios and the alternate schedule formats were analyzed.
Results:
Providers perceived multiple barriers to adult immunization independent of immunization schedule formats, chiefly patients’ low interest in immunization and refusal of vaccines. Most participants were not familiar with either format of CDC’s adult immunization schedule before the study, but quickly developed strong preferences for one versus the other (usually the second format that they encountered). About half of the providers changed their vaccine recommendations for clinical scenarios when they consulted either schedule format, although some of the changes were not clinically appropriate. Participants suggested several ways to enhance the availability of the information contained in the schedule formats, especially through electronic means.
Conclusions: This qualitative study suggests ways in which graphic depictions of an adult immunization schedule may address adult immunization barriers. Greater provider familiarity with schedule formats will be critical to their appropriate application in clinical encounters. (Am J Prev Med 2005;29(1):34 – 40) © 2005 American Journal of Preventive Medicine
Introduction
N
ational vaccination rates for adult immunizations such as influenza and pneumococcal vaccines currently fall well below target levels set in Healthy People 2010, especially among people aged ⱖ19 years with chronic conditions.1–5 A wellrecognized barrier to immunization is providers’ From the Child Health Evaluation and Research Unit, Division of General Pediatrics (Davis, Bishop, Clark), Division of General Internal Medicine (Davis, Halasyamani) and Gerald R. Ford School of Public Policy (Davis), University of Michigan, Ann Arbor, Michigan; and Department of Internal Medicine, St. Joseph Mercy Hospital (Halasyamani), Ann Arbor, Michigan; and National Immunization Program, Centers for Disease Control and Prevention (Sneller), Atlanta, Georgia Address correspondence and reprint requests to: Matthew M. Davis, MD, MAPP, University of Michigan, Divisions of General Pediatrics and General Internal Medicine, 300 NIB, 6C23, Ann Arbor MI 48109-0456. E-mail: [email protected].
34
failure to administer vaccines in accordance with established recommendations. Office-based immunization promotion strategies such as reminder systems, physician performance audits with feedback, and standing orders for immunizations have been shown to be effective,6 –9 but not broadly adopted.9,10 In 2002, in an effort to improve providers’ knowledge about adult immunization recommendations and to facilitate routine immunizations for adults through consolidation of existing recommendations in a graphic format, the Advisory Committee on Immunization Practices (ACIP) of the Centers for Disease Control and Prevention (CDC) issued an adult immunization schedule in a format similar to the well-established child and adolescent immunization schedule11 (Figure 1). The Immunization Action Coalition (IAC), a CDC-funded partner for immunization news dissemination, independently developed
Am J Prev Med 2005;29(1) © 2005 American Journal of Preventive Medicine • Published by Elsevier Inc.
0749-3797/05/$–see front matter doi:10.1016/j.amepre.2005.03.009
Figure 1. 2003–2004 Adult immunization schedule of the Advisory Committee on Immunization Practices.
Am J Prev Med 2005;29(1)
35
Proposed New Format Recommended Adult Immunization Schedule, United States, 2003-2004 Table 1: Recommendations by Age Group Age
50-64 years
19-49 years
▲
z▲
Vaccine
Tetanus, diphtheria*
65+ years
Booster every 10 years1 following completion of primary series
Measles, mumps, rubella*
1-2 doses 2 if born after 1956
Vaccines below line are for selected populations
Annually
Annually for selected populations3
Influenza
1-2 doses for selected populations4
Pneumococcal
1 dose; 2nd dose for selected populations
Hepatitis A
2 doses (0, 6-12 months) for selected populations5
Hepatitis B*
3 doses (0, 1-2, 4-6 months) for selected populations6 2 doses (0, 4-8 wks) for selected populations7
Varicella*
1 or more doses for selected populations8
Meningococcal See footnotes on reverse side
Table 2: Recommendations by Medical Condition Pregnancy
Diabetes, heart disease, chronic pulmonary disease, chronic liver disease, including chronic alcoholism
Congenital immunodeficiency, leukemia, lymphoma, generalized malignancy, therapy with alkylating agents, antimetabolites, radiation or large amounts of corticosteroids
Kidney failure, recipients of hemodialysis or clotting factor concentrates
Asplenia (including elective splenectomy) and terminal complement component deficiencies
Use if indicated 1
Use if indicated 1
Use if indicated 1
Use if indicated 1
Use if indicated 1
Use if indicated
Contraindicated
Use if indicated
Use if indicated
2
Use if indicated 2
▲
Vaccine
▲
Medical Condition
Tetanus, diphtheria* Measles, mumps, rubella*
Use if indicated 1 Contraindicated
2
2
2
2
HIV infection
Influenza
Recommended 3
Recommended 3
Recommended 3
Recommended 3
Recommended 3
Recommended 3
Pneumococcal
Use if indicated 4
Recommended 4
Recommended 4
Recommended 4
Recommended 4
Recommended 4
Hepatitis A
Use if indicated 5
Use if indicated 5
Use if indicated 5
Use if indicated 5
Use if indicated 5
Use if indicated 5
Hepatitis B*
Use if indicated
Use if indicated
Use if indicated
Recommended
Use if indicated
Use if indicated 6
Varicella* Meningococcal H. influenzae type b*
6
6
6
6
6
Contraindicated 7
Use if indicated 7
Contraindicated 7
Use if indicated 7
Use if indicated 7
Contraindicated 7
Use if indicated 8
Use if indicated 8
Use if indicated 8
Use if indicated 8
Recommended 8
Use if indicated 8
Not recommended
Not recommended
Recommended 9
Not recommended
Recommended 9
Recommended 9
See footnotes on reverse side * Covered by the Vaccine Injury Compensation Program. For information on how to file a claim, call (800) 338-2382 or visit www.hrsa.gov/osp/vicp. To file a claim for vaccine injury, write: U.S. Court of Federal Claims, 717 Madison Place, N.W., Washington D.C. 20005 or call (202) 219-9657.
Endorsements to be placed here in the future. Figure 2. 2003–2004 Adult immunization schedule of the Immunization Action Coalition.
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American Journal of Preventive Medicine, Volume 29, Number 1
Footnotes for Table 1 and Table 2 1. Tetanus and Diphtheria (Td): Initiate or complete a primary series to all adults who have not received 3 doses of tetanus- and diphtheria-containing vaccine; give the first 2 doses at least 4 wks apart and the 3rd dose, 6-12 mos after the 2nd. Give a Td booster to those in whom 10 yrs have elapsed since completion of the primary series or since their last booster dose. For wound management protocols, see complete ACIP statement. 2. Measles, Mumps, Rubella (MMR): Give 1 dose of MMR to all adults born in 1957 or later who do not have documentation of at least one dose of live virus vaccine given at 1 yr of age or later, either as separate antigens or in combination, or other acceptable evidence of immunity. An additional dose of measles-containing vaccine, preferably as MMR, is recommended for adults born >1957 who a) were previously vaccinated with killed measles vaccine, b) were vaccinated with an unknown vaccine between 1963 and 1967, c) are students in post-secondary educational institutions, d) work in a health care facility, or e) plan to travel internationally. Give 1 dose of rubella-containing vaccine (preferably as MMR) to nonpregnant women of childbearing age who do not have documentation of rubella vaccination or lab evidence of immunity. Counsel women to avoid becoming pregnant for 4 wks after vaccination with MMR. Withhold MMR or other measlescontaining vaccines from HIV-infected persons with severe immunosuppression. 3. Influenza (Inf): Give 1 dose of influenza vaccine annually to all adults >50 yrs of age, as well as those <50 yrs who a) have a chronic disorder of the cardiovascular or pulmonary system, including asthma, b) have required regular medical follow-up or hospitalization during the preceding year due to chronic metabolic diseases (including diabetes mellitus), renal dysfunction, hemoglobinopathies, immunosuppression (including immunosuppression caused by medications or by human immunodeficiency virus [HIV]), c) will be in the 2nd or 3rd trimester of pregnancy during the influenza season, d) are a healthcare worker; e) reside in a nursing home or other long-term care facility, f) are likely to transmit influenza to persons at high-risk (household contacts and caregivers of children birth to 23 mos of age, or persons of all ages with high-risk conditions), or g) wish to reduce their chances of becoming ill with influenza. Only healthy, non-pregnant persons 549 yrs of age may receive live attenuated influenza vaccine. Inactivated influenza vaccine is preferred for persons with close contact with immunosuppressed persons. 4. Pneumococcal polysaccharide (PPV): Give PPV to all adults >65 yrs of age as well as others <65 yrs with a) a chronic disorder of the pulmonary system, excluding asthma, b) chronic cardiovascular disease, c) diabetes mellitus, d) alcoholism, e) chronic liver dis-ease including liver disease as a result of alcohol abuse (cirrhosis), f) cochlear implant (if candidate, vaccinate at least 2 wks before surgery), g) functional or anatomic asplenia (e.g., sickle cell disease or splenectomy [if elective splenectomy, vaccinate at least 2 wks before surgery]), or h) an immunocompromising condition (e.g., HIV infection [vaccinate as close to diagnosis as possible when CD4 cell counts are highest], leukemia, lymphoma, Hodgkins disease, multiple myeloma, generalized malignancy, chronic renal failure, nephrotic syndrome, or other conditions associated with immuno-suppression (e.g., organ or bone marrow transplantation), or i) those receiving immunosuppressive chemotherapy including long-term corticosteroids. In addition, give PPV to Alaskan Natives and certain American Indian populations. Revaccinate 5 yrs later if person is at highest risk of fatal pneumococcal infection or rapid antibody loss (groups g, h, & i) or if
Reporting Adverse Reactions
Report adverse reactions to vaccines through the federal Vaccine Adverse Event Reporting System. For information on reporting reactions following vaccines, please visit www.vaers.org or call the 24-hour national toll-free information line (800) 822-7967.
the person is >65 yrs and the first dose was given at <65 yrs and >5 yrs have elapsed since the previous dose. 5. Hepatitis A (HepA): Give a 2-dose HepA vaccine series to adults who a) will be traveling to or working in countries that have high or intermediate endemnicity of hepatitis A (all except Canada, Japan, Australia, New Zealand, and Western Europe), b) have clotting-factor disorders or chronic liver disease, c) are male and have sex with men, d) use injecting or noninjecting illegal drugs, or e) work with HAVinfected primates or with HAV in a research laboratory setting. 6. Hepatitis B (HepB): Give a 3-dose HepB vaccine series to adults who a) are healthcare or public-safety workers with exposure to blood in the workplace, b) are in training in schools of medicine, dentistry, nursing, laboratory technology, and other allied health professions, c) are injecting drug users, d) have had more than one sex partner in the previous 6 mos, e) have had a recently acquired sexuallytransmitted disease (STD), f) are clients in STD clinics, g) are males and have sex with men, h) are household contacts or sex partners of persons with chronic HBV infection, i) are clients or staff of institutions for the developmentally disabled, j) will be traveling to a countries having high or intermediate prevalence of chronic HBV infection for more than 6 mos, k) are inmates of a correctional facilities, l) are receiving clotting-factor concentrates, or m) are on hemodialysis (use special formulation or a double dose [see complete ACIPstatement]) or who are going to be starting dialysis in the months ahead. 7. Varicella (Var): Vaccinate all persons who do not have a reliable clinical history of varicella infection or serological evidence of varicella zoster virus (VZV) infection. Make special efforts to vaccinate adults who a) are healthcare workers or family contacts of immunocompromised persons, b) live or work in environments where transmission of VZV is likely (e.g., teachers of young children, day care employees, residents and staff members in institutional settings) or can occur (e.g., college students, inmates and staff members or correctional institutions, military personnel), c) are women and not pregnant now but may become pregnant in the future, or d) are planning to travel internationally. Do not vaccinate pregnant women or women attempting to become pregnant in the next 4 wks. Persons with impaired humoral but not cellular immunity may be vaccinated. 8. Meningococcal (Men): Give quadrivalent polysaccharide meningococcal vaccine to adults who a) have a terminal complement component deficiency, b) anatomic or functional asplenia (if elective splenectomy, vaccinate at least 2 wks before surgery), or c) are planning to travel to a country in which disease is hyperendemic or epidemic (e.g., the meningitis belt of sub-Saharan Africa or to Mecca, Saudi Arabia for the Hajj). Revaccination at 3-5 yrs may be indicated for persons who continue to be at high risk of infection (e.g., persons residing in areas where disease is epidemic). Counsel college freshmen, especially those who live in dormitories, regarding their risk of meningococcal disease and the availability of a vaccine that can decrease the risk of infection. 9. Haemophilus influenzae type b (Hib): Give a single 0.5 mL dose of Hib vaccine to all adults at increased risk for invasive Hib disease, including those with a) functional or anatomic asplenia (e.g., sickle-cell disease, postsplenectomy [if elective splenectomy, vaccinate at least 2 wks before surgery]), b) immunodeficiency (in particular, persons with IgG2 subclass deficiency), c) immunosuppression from cancer chemotherapy, and d) infection with HIV. Adults with Hodgkins disease should be vaccinated at least 2 wks before the initiation of chemotherapy or, if this is not possible, >3 mos after the end of chemotherapy.
References
These recommendations are based on those of the U.S. Public Health Services Advisory Committee on Immunization Practices (ACIP). For the complete ACIP statement, go to www.cdc.gov/nip/publications/ACIP-list.htm.
For additional information about vaccines, including precautions and contraindications for immunization and vaccine shortages, please visit the National Immunization Program Website at www.cdc.gov/nip or call the CDCs National Immunization Information Hotline at (800) 232-2522 (English) or (800) 232-0233 (Spanish).
Figure 2. 2003–2004 Adult immunization schedule of the Immunization Action Coalition (continued).
a different graphic depiction of the same CDC adult immunization recommendations (Figure 2) (D Peterson, Immunization Action Coalition, St. Paul, MN, personal communication, 2003).
The objectives of this qualitative study were to evaluate the potential benefits and problems in the use of these different adult immunization schedule formats, and to suggest methods for implemenAm J Prev Med 2005;29(1)
37
Table 1. Clinical case scenarios for adult immunizations, presented to study participants Scenario 1
Scenario 2 Scenario 3
A healthy 27-year-old hospital-based phlebotomist with no prior history of varicella disease or previous vaccination against measles/mumps/rubella who visits the office in November. A 55-year-old male chef with HIV disease who visits the office in December. A 43-year-old female with a history of splenectomy, disabled by severe peripheral neuropathy and on dialysis for end-stage renal disease secondary to diabetes mellitus type 1 who visits the office in November.
tation and dissemination of different schedule formats.
Methods Sample The study team convened focus groups at 11 private internal medicine and family medicine practices in six metropolitan areas (Ann Arbor, Chicago, Cleveland, Houston, Minneapolis/ St. Paul, Salt Lake City). All providers involved with immunization were invited, for a total of 94 participants (35 physicians; 59 nonphysicians including nurse practitioners, nurses, physician assistants, and medical assistants). The family medicine practices administered vaccines to children and adults.
Data Collection Each focus group session began with discussion of providers’ general approaches to adult immunizations and the challenges to administering recommended immunizations to adult patients. Participants were then asked to consider three clinical scenarios (Table 1), for each of which they initially indicated their vaccine recommendations on a response card and then reconsidered their choices using one of the two formats of the adult immunization schedule. After each schedule format was used once for each of the first two cases, participants were asked to complete the third case with the schedule format that they preferred. As the scenarios were discussed with each group, participants noted whether they changed their immunization recommendations. The order of presentation of the ACIP versus the IAC format was alternated at sequential practices, so as not to bias findings related to increasing provider familiarity with the schedule formats over the course of the focus groups. For four respondents, clinical obligations prevented them from answering all scenarios. Project staff followed up with participants from each practice several weeks after the focus group session, in order to discuss the extent to which the adult immunization schedules (either format) had been incorporated into practice. This study was approved by the Institutional Review Board of the University of Michigan Medical School. Study subjects were each provided a modest honorarium for their participation. Data were collected in 2003–2004 and were analyzed in 2004.
38
Results Practice Approaches and Barriers to Adult Immunizations Respondent practices indicated that they most frequently consider adult immunizations when the patient has an injury (nine practices), during routine physicals,7 during the influenza season,7 when a patient presents with a chronic condition,6 and for school or travel.6 Cited barriers to adult immunization were similar across sites as well, including perceptions that patients generally lack cues to appropriate vaccinations,11 and that patients refuse the shots for a variety of reasons.11 Several practices also commented that patients often do not understand why shots are necessary and do not perceive substantive value from vaccinations.7
Provider Use of Adult Immunization Schedule Formats Scenario 1. Among 93 respondents to this scenario, 46 (49%) changed their recommendations after using an adult immunization schedule. The most common type of change (n⫽13) was that respondents indicated that they would recommend pneumococcal vaccine to this individual (not correct). Common clinically appropriate changes were to recommend measles–mumps–rubella (MMR) if not already immunized (10), recommend a tetanus– diphtheria booster (9), and recommend varicella vaccine if not immune (7). Scenario 2. Among 94 respondents for this scenario, 50 (53%) changed their recommendations after using an adult immunization schedule. The most common change (n⫽18) was to remove varicella vaccine from their recommendations (correct). Other common correct changes included removing MMR from their recommendations (9), and adding pneumococcal (5) and influenza vaccine recommendations (4). Scenario 3. For this scenario, 51 (57%) preferred the ACIP format, and 39 (43%) preferred the IAC format; importantly, 73% of all participants chose the second format presented to them. The most common reason cited for choosing the ACIP or the IAC format was the perception that the graphic presentation of one was easier to read or follow than the other. Notably, there were no substantive differences in the preference of physician versus nonphysician staff for the ACIP versus the IAC format. The ACIP format was preferred by participants who found color codes easier to follow. The IAC format was preferred by participants who found colors a distraction and preferred text explanations.
American Journal of Preventive Medicine, Volume 29, Number 1
Provider Suggestions for Enhancing Adult Immunization Schedule Formats Several providers suggested that CDC should enlarge the schedule to “wall size” and issue copies to practices for posting on the walls of exam rooms or waiting room, in order to prompt providers and patients alike to consider adult immunizations. Others suggested posting the schedule format in several different locations around the office, such as the check-in desk and nursing station. Providers who use handheld computers suggested adding a point-and-click functionality into the electronic schedule interface so that providers could click on vaccine names and chronic conditions and see the relevant footnotes immediately. Other providers suggested developing an interactive decision tool that would prompt providers to ask specific questions of patients, and then inform providers about the appropriate immunizations for patients based on patient data.
Subsequent Use of the Adult Immunization Schedules Participants at eight practices provided information 1 to 2 months after the focus group sessions were conducted. At four practices, providers indicated that having the adult immunization schedule increased awareness regarding indications for adult immunizations. Some providers noted that they discussed immunizations more often in their discussions with patients, while others said that they had posted the schedule in exam rooms, the nursing station, or the vaccine-preparation area. Another practice reported that their preferred schedule format was a focus of recent separate physician and nonphysician staff meetings. At the other four practices, providers said that provision of the adult immunization schedule had not altered their clinical efforts regarding vaccines.
Discussion The focus-group approach employed in this study provided several valuable insights about current common approaches to adult immunizations in private, community-based family medicine and internal medicine practices. Providers’ comments about barriers to immunizations corresponded well to published studies of provider perspectives on challenges to immunizing adults,6 –10 and led us to believe that the study participants were similar to the general healthcare provider community for adult patients. Importantly, providers appeared more inclined to attribute low vaccination rates to patient rather than provider factors, which contrasted with the study finding that about half of the
providers changed their vaccine recommendations when they were provided information through the adult immunization schedules. In general, providers’ responses indicate many opportunities to study the implementation of adult immunization recommendations using graphic adult immunization schedules as tools, perhaps supplemented by programs that inform and motivate both providers and patients.
Use of Adult Immunization Schedules In aggregate, study participants did not clearly prefer either the ACIP or IAC format of the adult immunization schedule. There were strongly expressed positive and negative statements about both schedules, sometimes directly contradicting each other. This suggests that there may not be one “best” schedule format that meets the needs of all providers. Rather, various formats of the same recommendations may better meet the needs of a diverse group of providers with diverse training backgrounds and preferences. If confirmed in broader provider studies in the future, this finding underscores the importance of “field testing” different formats for immunization reference materials and maintaining more than one version of reference materials if there is no clearly demonstrated preference in the target audience of providers. The adult immunization schedule graphic has potential value as a resource for improving the quality of patient care, but with the caveat that providers’ occasionally inappropriate application of information in the schedule is likely attributable to general unfamiliarity with the schedule format. This interpretation is supported by the fact that the majority of respondents preferred the second format presented to them, regardless of whether it was the IAC or ACIP format. Therefore, beyond development of schedule formats as decision aids, there is an apparent need to educate providers in their use. Subsequent to the focus groups, half of the practices reported that the adult immunization schedule formats were effective prompts regarding adult vaccination efforts, while the remainder had not changed their vaccination emphasis. This finding underscores the point that the availability of an adult immunization schedule itself will be insufficient to prompt the broad spectrum of internal medicine and family medicine practices to change their approaches to adult vaccination, especially among practitioners for whom adult immunization remains a low priority.
Limitations The limitations of qualitative studies are inherent in their design. The study sample was not intended to be representative of the larger population of adult immunization providers in the United States. Rather, the goal Am J Prev Med 2005;29(1)
39
What This Study Adds . . . Adult immunization rates lag far behind childhood rates; whether an immunization schedule would serve as a helpful resource or prompt for adult health care providers is unknown. In this study, providers frequently changed their immunization recommendations for clinical vignettes based on information contained in the adult schedules, suggesting that the schedules may help improve rates of timely and appropriate vaccination for adults. Moreover, providers indicated no clear preference for different presentation formats of the schedule, indicating that more than one format may help in dissemination of such information.
was to explore providers’ potential use of new adult immunization schedule formats that had not previously been examined. The findings suggest avenues for future study, particularly regarding providers’ accurate interpretation of information provided in graphic schedules, and the extent to which the incorporation of different schedule formats into routine provider practice may contribute to decreased barriers to immunization and higher adult vaccination rates. Broader publication and dissemination of the adult schedule may also prompt adults in the general public to ask healthcare providers about vaccines appropriate for them.
Conclusions Our study findings shed valuable light on adult healthcare providers’ perceptions of barriers to adult immunizations and their potential application of information included in recently issued adult immunization schedule formats to improve vaccine delivery, but also underscore the importance of educating providers about the appropriate use of such schedule formats in the timepressured healthcare environment. While the advent of adult immunization schedule formats may not lead directly to vastly improved adult vaccination rates be-
40
cause barriers to immunization are complex and multifactorial, providers do value a central resource for adult immunization information. Lessons learned from efforts to urge providers to incorporate adult immunization recommendations in their practices—such as the value of a single set of recommendations presented in different formats—may also be transferable to other efforts to educate healthcare providers in the future. This work was funded by the Centers for Disease Control and Prevention through a cooperative agreement with the Association of Teachers of Preventive Medicine. We are grateful to the practices and providers who participated in this study for their time and insights. We also acknowledge the research assistance of Emily Kennedy. No financial conflict of interest was reported by the authors of this paper.
References 1. Centers for Disease Control and Prevention. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices. MMWR Recomm Rep 2003;52:1–36. 2. Singleton JA, Greby SM, Wooten KG, Walker FJ, Strikas R. Influenza, pneumococcal, and tetanus toxoid vaccination of adults – United States, 1993-1997. MMWR Surveill Summ 2000;49:39 –52. 3. Centers for Disease Control and Prevention. Influenza and pneumococcal vaccination levels among persons aged ⱖ65 years. MMWR Morb Mortal Wkly Rep 2002;51:1019 –24. 4. Centers for Disease Control and Prevention. Preventive-care practices among persons with diabetes—United States, 1995 and 2001. MMWR Morb Mortal Wkly Rep 2002;51:965–9. 5. U.S. Department of Health and Human Services. Healthy people 2010, conference ed. 2 vols. Washington DC: U.S. Department of Health and Human Services, 2000. 6. Briss PA, Rodewald LR, Hinman AR, et al. Reviews of evidence regarding interventions to improve vaccination coverage in children, adolescents, and adults. Am J Prev Med 2000;18(suppl 1):97–140. 7. Shefer A, Briss P, Rodewald L, et al. Improving immunization coverage rates: an evidence-based review of the literature. Epidemiol Rev 1999;21:96 –142. 8. Szilagyi P, Vann J, Bordley C, et al. Interventions aimed at improving immunization rates. Cochrane Database of Systematic Reviews, 4:CD003941, 2002. 9. Szilagyi PG, Bordley C, Vann JC, et al. Effect of patient reminder/recall interventions on immunization rates: a review. JAMA 2000;284:1820 –7. 10. Davis MM, McMahon SR, Santoli JM, Schwartz B, Clark SJ. A national survey of physician practices regarding influenza vaccine. J Gen Intern Med 2002;17:670 – 6. 11. Centers for Disease Control and Prevention. Recommended adult immunization schedule, United States, 2002–2003. MMWR Morb Mortal Wkly Rep 2002;51:904 – 8.
American Journal of Preventive Medicine, Volume 29, Number 1
A series of focus groups was conducted with 94 physicians and other clinical staff in 11 private practices (family medicine and internal medicine) in six U.S. cities. Each session was based on a structured set of questions that explored barriers to adult immunizations, followed by three mock clinical scenarios to examine how each of two graphical depictions of the 2003–2004 adult immunization schedule (one from the CDC’s Advisory Committee on Immunization Practices, and the other from the Immunization Action Coalition) might facilitate assessments of recommended immunizations. Group dialogue and individual participants’ written responses to the scenarios and the alternate schedule formats were analyzed.
Results:
Providers perceived multiple barriers to adult immunization independent of immunization schedule formats, chiefly patients’ low interest in immunization and refusal of vaccines. Most participants were not familiar with either format of CDC’s adult immunization schedule before the study, but quickly developed strong preferences for one versus the other (usually the second format that they encountered). About half of the providers changed their vaccine recommendations for clinical scenarios when they consulted either schedule format, although some of the changes were not clinically appropriate. Participants suggested several ways to enhance the availability of the information contained in the schedule formats, especially through electronic means.
Conclusions: This qualitative study suggests ways in which graphic depictions of an adult immunization schedule may address adult immunization barriers. Greater provider familiarity with schedule formats will be critical to their appropriate application in clinical encounters. (Am J Prev Med 2005;29(1):34 – 40) © 2005 American Journal of Preventive Medicine
Introduction
N
ational vaccination rates for adult immunizations such as influenza and pneumococcal vaccines currently fall well below target levels set in Healthy People 2010, especially among people aged ⱖ19 years with chronic conditions.1–5 A wellrecognized barrier to immunization is providers’ From the Child Health Evaluation and Research Unit, Division of General Pediatrics (Davis, Bishop, Clark), Division of General Internal Medicine (Davis, Halasyamani) and Gerald R. Ford School of Public Policy (Davis), University of Michigan, Ann Arbor, Michigan; and Department of Internal Medicine, St. Joseph Mercy Hospital (Halasyamani), Ann Arbor, Michigan; and National Immunization Program, Centers for Disease Control and Prevention (Sneller), Atlanta, Georgia Address correspondence and reprint requests to: Matthew M. Davis, MD, MAPP, University of Michigan, Divisions of General Pediatrics and General Internal Medicine, 300 NIB, 6C23, Ann Arbor MI 48109-0456. E-mail: [email protected].
34
failure to administer vaccines in accordance with established recommendations. Office-based immunization promotion strategies such as reminder systems, physician performance audits with feedback, and standing orders for immunizations have been shown to be effective,6 –9 but not broadly adopted.9,10 In 2002, in an effort to improve providers’ knowledge about adult immunization recommendations and to facilitate routine immunizations for adults through consolidation of existing recommendations in a graphic format, the Advisory Committee on Immunization Practices (ACIP) of the Centers for Disease Control and Prevention (CDC) issued an adult immunization schedule in a format similar to the well-established child and adolescent immunization schedule11 (Figure 1). The Immunization Action Coalition (IAC), a CDC-funded partner for immunization news dissemination, independently developed
Am J Prev Med 2005;29(1) © 2005 American Journal of Preventive Medicine • Published by Elsevier Inc.
0749-3797/05/$–see front matter doi:10.1016/j.amepre.2005.03.009
Figure 1. 2003–2004 Adult immunization schedule of the Advisory Committee on Immunization Practices.
Am J Prev Med 2005;29(1)
35
Proposed New Format Recommended Adult Immunization Schedule, United States, 2003-2004 Table 1: Recommendations by Age Group Age
50-64 years
19-49 years
▲
z▲
Vaccine
Tetanus, diphtheria*
65+ years
Booster every 10 years1 following completion of primary series
Measles, mumps, rubella*
1-2 doses 2 if born after 1956
Vaccines below line are for selected populations
Annually
Annually for selected populations3
Influenza
1-2 doses for selected populations4
Pneumococcal
1 dose; 2nd dose for selected populations
Hepatitis A
2 doses (0, 6-12 months) for selected populations5
Hepatitis B*
3 doses (0, 1-2, 4-6 months) for selected populations6 2 doses (0, 4-8 wks) for selected populations7
Varicella*
1 or more doses for selected populations8
Meningococcal See footnotes on reverse side
Table 2: Recommendations by Medical Condition Pregnancy
Diabetes, heart disease, chronic pulmonary disease, chronic liver disease, including chronic alcoholism
Congenital immunodeficiency, leukemia, lymphoma, generalized malignancy, therapy with alkylating agents, antimetabolites, radiation or large amounts of corticosteroids
Kidney failure, recipients of hemodialysis or clotting factor concentrates
Asplenia (including elective splenectomy) and terminal complement component deficiencies
Use if indicated 1
Use if indicated 1
Use if indicated 1
Use if indicated 1
Use if indicated 1
Use if indicated
Contraindicated
Use if indicated
Use if indicated
2
Use if indicated 2
▲
Vaccine
▲
Medical Condition
Tetanus, diphtheria* Measles, mumps, rubella*
Use if indicated 1 Contraindicated
2
2
2
2
HIV infection
Influenza
Recommended 3
Recommended 3
Recommended 3
Recommended 3
Recommended 3
Recommended 3
Pneumococcal
Use if indicated 4
Recommended 4
Recommended 4
Recommended 4
Recommended 4
Recommended 4
Hepatitis A
Use if indicated 5
Use if indicated 5
Use if indicated 5
Use if indicated 5
Use if indicated 5
Use if indicated 5
Hepatitis B*
Use if indicated
Use if indicated
Use if indicated
Recommended
Use if indicated
Use if indicated 6
Varicella* Meningococcal H. influenzae type b*
6
6
6
6
6
Contraindicated 7
Use if indicated 7
Contraindicated 7
Use if indicated 7
Use if indicated 7
Contraindicated 7
Use if indicated 8
Use if indicated 8
Use if indicated 8
Use if indicated 8
Recommended 8
Use if indicated 8
Not recommended
Not recommended
Recommended 9
Not recommended
Recommended 9
Recommended 9
See footnotes on reverse side * Covered by the Vaccine Injury Compensation Program. For information on how to file a claim, call (800) 338-2382 or visit www.hrsa.gov/osp/vicp. To file a claim for vaccine injury, write: U.S. Court of Federal Claims, 717 Madison Place, N.W., Washington D.C. 20005 or call (202) 219-9657.
Endorsements to be placed here in the future. Figure 2. 2003–2004 Adult immunization schedule of the Immunization Action Coalition.
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Footnotes for Table 1 and Table 2 1. Tetanus and Diphtheria (Td): Initiate or complete a primary series to all adults who have not received 3 doses of tetanus- and diphtheria-containing vaccine; give the first 2 doses at least 4 wks apart and the 3rd dose, 6-12 mos after the 2nd. Give a Td booster to those in whom 10 yrs have elapsed since completion of the primary series or since their last booster dose. For wound management protocols, see complete ACIP statement. 2. Measles, Mumps, Rubella (MMR): Give 1 dose of MMR to all adults born in 1957 or later who do not have documentation of at least one dose of live virus vaccine given at 1 yr of age or later, either as separate antigens or in combination, or other acceptable evidence of immunity. An additional dose of measles-containing vaccine, preferably as MMR, is recommended for adults born >1957 who a) were previously vaccinated with killed measles vaccine, b) were vaccinated with an unknown vaccine between 1963 and 1967, c) are students in post-secondary educational institutions, d) work in a health care facility, or e) plan to travel internationally. Give 1 dose of rubella-containing vaccine (preferably as MMR) to nonpregnant women of childbearing age who do not have documentation of rubella vaccination or lab evidence of immunity. Counsel women to avoid becoming pregnant for 4 wks after vaccination with MMR. Withhold MMR or other measlescontaining vaccines from HIV-infected persons with severe immunosuppression. 3. Influenza (Inf): Give 1 dose of influenza vaccine annually to all adults >50 yrs of age, as well as those <50 yrs who a) have a chronic disorder of the cardiovascular or pulmonary system, including asthma, b) have required regular medical follow-up or hospitalization during the preceding year due to chronic metabolic diseases (including diabetes mellitus), renal dysfunction, hemoglobinopathies, immunosuppression (including immunosuppression caused by medications or by human immunodeficiency virus [HIV]), c) will be in the 2nd or 3rd trimester of pregnancy during the influenza season, d) are a healthcare worker; e) reside in a nursing home or other long-term care facility, f) are likely to transmit influenza to persons at high-risk (household contacts and caregivers of children birth to 23 mos of age, or persons of all ages with high-risk conditions), or g) wish to reduce their chances of becoming ill with influenza. Only healthy, non-pregnant persons 549 yrs of age may receive live attenuated influenza vaccine. Inactivated influenza vaccine is preferred for persons with close contact with immunosuppressed persons. 4. Pneumococcal polysaccharide (PPV): Give PPV to all adults >65 yrs of age as well as others <65 yrs with a) a chronic disorder of the pulmonary system, excluding asthma, b) chronic cardiovascular disease, c) diabetes mellitus, d) alcoholism, e) chronic liver dis-ease including liver disease as a result of alcohol abuse (cirrhosis), f) cochlear implant (if candidate, vaccinate at least 2 wks before surgery), g) functional or anatomic asplenia (e.g., sickle cell disease or splenectomy [if elective splenectomy, vaccinate at least 2 wks before surgery]), or h) an immunocompromising condition (e.g., HIV infection [vaccinate as close to diagnosis as possible when CD4 cell counts are highest], leukemia, lymphoma, Hodgkins disease, multiple myeloma, generalized malignancy, chronic renal failure, nephrotic syndrome, or other conditions associated with immuno-suppression (e.g., organ or bone marrow transplantation), or i) those receiving immunosuppressive chemotherapy including long-term corticosteroids. In addition, give PPV to Alaskan Natives and certain American Indian populations. Revaccinate 5 yrs later if person is at highest risk of fatal pneumococcal infection or rapid antibody loss (groups g, h, & i) or if
Reporting Adverse Reactions
Report adverse reactions to vaccines through the federal Vaccine Adverse Event Reporting System. For information on reporting reactions following vaccines, please visit www.vaers.org or call the 24-hour national toll-free information line (800) 822-7967.
the person is >65 yrs and the first dose was given at <65 yrs and >5 yrs have elapsed since the previous dose. 5. Hepatitis A (HepA): Give a 2-dose HepA vaccine series to adults who a) will be traveling to or working in countries that have high or intermediate endemnicity of hepatitis A (all except Canada, Japan, Australia, New Zealand, and Western Europe), b) have clotting-factor disorders or chronic liver disease, c) are male and have sex with men, d) use injecting or noninjecting illegal drugs, or e) work with HAVinfected primates or with HAV in a research laboratory setting. 6. Hepatitis B (HepB): Give a 3-dose HepB vaccine series to adults who a) are healthcare or public-safety workers with exposure to blood in the workplace, b) are in training in schools of medicine, dentistry, nursing, laboratory technology, and other allied health professions, c) are injecting drug users, d) have had more than one sex partner in the previous 6 mos, e) have had a recently acquired sexuallytransmitted disease (STD), f) are clients in STD clinics, g) are males and have sex with men, h) are household contacts or sex partners of persons with chronic HBV infection, i) are clients or staff of institutions for the developmentally disabled, j) will be traveling to a countries having high or intermediate prevalence of chronic HBV infection for more than 6 mos, k) are inmates of a correctional facilities, l) are receiving clotting-factor concentrates, or m) are on hemodialysis (use special formulation or a double dose [see complete ACIPstatement]) or who are going to be starting dialysis in the months ahead. 7. Varicella (Var): Vaccinate all persons who do not have a reliable clinical history of varicella infection or serological evidence of varicella zoster virus (VZV) infection. Make special efforts to vaccinate adults who a) are healthcare workers or family contacts of immunocompromised persons, b) live or work in environments where transmission of VZV is likely (e.g., teachers of young children, day care employees, residents and staff members in institutional settings) or can occur (e.g., college students, inmates and staff members or correctional institutions, military personnel), c) are women and not pregnant now but may become pregnant in the future, or d) are planning to travel internationally. Do not vaccinate pregnant women or women attempting to become pregnant in the next 4 wks. Persons with impaired humoral but not cellular immunity may be vaccinated. 8. Meningococcal (Men): Give quadrivalent polysaccharide meningococcal vaccine to adults who a) have a terminal complement component deficiency, b) anatomic or functional asplenia (if elective splenectomy, vaccinate at least 2 wks before surgery), or c) are planning to travel to a country in which disease is hyperendemic or epidemic (e.g., the meningitis belt of sub-Saharan Africa or to Mecca, Saudi Arabia for the Hajj). Revaccination at 3-5 yrs may be indicated for persons who continue to be at high risk of infection (e.g., persons residing in areas where disease is epidemic). Counsel college freshmen, especially those who live in dormitories, regarding their risk of meningococcal disease and the availability of a vaccine that can decrease the risk of infection. 9. Haemophilus influenzae type b (Hib): Give a single 0.5 mL dose of Hib vaccine to all adults at increased risk for invasive Hib disease, including those with a) functional or anatomic asplenia (e.g., sickle-cell disease, postsplenectomy [if elective splenectomy, vaccinate at least 2 wks before surgery]), b) immunodeficiency (in particular, persons with IgG2 subclass deficiency), c) immunosuppression from cancer chemotherapy, and d) infection with HIV. Adults with Hodgkins disease should be vaccinated at least 2 wks before the initiation of chemotherapy or, if this is not possible, >3 mos after the end of chemotherapy.
References
These recommendations are based on those of the U.S. Public Health Services Advisory Committee on Immunization Practices (ACIP). For the complete ACIP statement, go to www.cdc.gov/nip/publications/ACIP-list.htm.
For additional information about vaccines, including precautions and contraindications for immunization and vaccine shortages, please visit the National Immunization Program Website at www.cdc.gov/nip or call the CDCs National Immunization Information Hotline at (800) 232-2522 (English) or (800) 232-0233 (Spanish).
Figure 2. 2003–2004 Adult immunization schedule of the Immunization Action Coalition (continued).
a different graphic depiction of the same CDC adult immunization recommendations (Figure 2) (D Peterson, Immunization Action Coalition, St. Paul, MN, personal communication, 2003).
The objectives of this qualitative study were to evaluate the potential benefits and problems in the use of these different adult immunization schedule formats, and to suggest methods for implemenAm J Prev Med 2005;29(1)
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Table 1. Clinical case scenarios for adult immunizations, presented to study participants Scenario 1
Scenario 2 Scenario 3
A healthy 27-year-old hospital-based phlebotomist with no prior history of varicella disease or previous vaccination against measles/mumps/rubella who visits the office in November. A 55-year-old male chef with HIV disease who visits the office in December. A 43-year-old female with a history of splenectomy, disabled by severe peripheral neuropathy and on dialysis for end-stage renal disease secondary to diabetes mellitus type 1 who visits the office in November.
tation and dissemination of different schedule formats.
Methods Sample The study team convened focus groups at 11 private internal medicine and family medicine practices in six metropolitan areas (Ann Arbor, Chicago, Cleveland, Houston, Minneapolis/ St. Paul, Salt Lake City). All providers involved with immunization were invited, for a total of 94 participants (35 physicians; 59 nonphysicians including nurse practitioners, nurses, physician assistants, and medical assistants). The family medicine practices administered vaccines to children and adults.
Data Collection Each focus group session began with discussion of providers’ general approaches to adult immunizations and the challenges to administering recommended immunizations to adult patients. Participants were then asked to consider three clinical scenarios (Table 1), for each of which they initially indicated their vaccine recommendations on a response card and then reconsidered their choices using one of the two formats of the adult immunization schedule. After each schedule format was used once for each of the first two cases, participants were asked to complete the third case with the schedule format that they preferred. As the scenarios were discussed with each group, participants noted whether they changed their immunization recommendations. The order of presentation of the ACIP versus the IAC format was alternated at sequential practices, so as not to bias findings related to increasing provider familiarity with the schedule formats over the course of the focus groups. For four respondents, clinical obligations prevented them from answering all scenarios. Project staff followed up with participants from each practice several weeks after the focus group session, in order to discuss the extent to which the adult immunization schedules (either format) had been incorporated into practice. This study was approved by the Institutional Review Board of the University of Michigan Medical School. Study subjects were each provided a modest honorarium for their participation. Data were collected in 2003–2004 and were analyzed in 2004.
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Results Practice Approaches and Barriers to Adult Immunizations Respondent practices indicated that they most frequently consider adult immunizations when the patient has an injury (nine practices), during routine physicals,7 during the influenza season,7 when a patient presents with a chronic condition,6 and for school or travel.6 Cited barriers to adult immunization were similar across sites as well, including perceptions that patients generally lack cues to appropriate vaccinations,11 and that patients refuse the shots for a variety of reasons.11 Several practices also commented that patients often do not understand why shots are necessary and do not perceive substantive value from vaccinations.7
Provider Use of Adult Immunization Schedule Formats Scenario 1. Among 93 respondents to this scenario, 46 (49%) changed their recommendations after using an adult immunization schedule. The most common type of change (n⫽13) was that respondents indicated that they would recommend pneumococcal vaccine to this individual (not correct). Common clinically appropriate changes were to recommend measles–mumps–rubella (MMR) if not already immunized (10), recommend a tetanus– diphtheria booster (9), and recommend varicella vaccine if not immune (7). Scenario 2. Among 94 respondents for this scenario, 50 (53%) changed their recommendations after using an adult immunization schedule. The most common change (n⫽18) was to remove varicella vaccine from their recommendations (correct). Other common correct changes included removing MMR from their recommendations (9), and adding pneumococcal (5) and influenza vaccine recommendations (4). Scenario 3. For this scenario, 51 (57%) preferred the ACIP format, and 39 (43%) preferred the IAC format; importantly, 73% of all participants chose the second format presented to them. The most common reason cited for choosing the ACIP or the IAC format was the perception that the graphic presentation of one was easier to read or follow than the other. Notably, there were no substantive differences in the preference of physician versus nonphysician staff for the ACIP versus the IAC format. The ACIP format was preferred by participants who found color codes easier to follow. The IAC format was preferred by participants who found colors a distraction and preferred text explanations.
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Provider Suggestions for Enhancing Adult Immunization Schedule Formats Several providers suggested that CDC should enlarge the schedule to “wall size” and issue copies to practices for posting on the walls of exam rooms or waiting room, in order to prompt providers and patients alike to consider adult immunizations. Others suggested posting the schedule format in several different locations around the office, such as the check-in desk and nursing station. Providers who use handheld computers suggested adding a point-and-click functionality into the electronic schedule interface so that providers could click on vaccine names and chronic conditions and see the relevant footnotes immediately. Other providers suggested developing an interactive decision tool that would prompt providers to ask specific questions of patients, and then inform providers about the appropriate immunizations for patients based on patient data.
Subsequent Use of the Adult Immunization Schedules Participants at eight practices provided information 1 to 2 months after the focus group sessions were conducted. At four practices, providers indicated that having the adult immunization schedule increased awareness regarding indications for adult immunizations. Some providers noted that they discussed immunizations more often in their discussions with patients, while others said that they had posted the schedule in exam rooms, the nursing station, or the vaccine-preparation area. Another practice reported that their preferred schedule format was a focus of recent separate physician and nonphysician staff meetings. At the other four practices, providers said that provision of the adult immunization schedule had not altered their clinical efforts regarding vaccines.
Discussion The focus-group approach employed in this study provided several valuable insights about current common approaches to adult immunizations in private, community-based family medicine and internal medicine practices. Providers’ comments about barriers to immunizations corresponded well to published studies of provider perspectives on challenges to immunizing adults,6 –10 and led us to believe that the study participants were similar to the general healthcare provider community for adult patients. Importantly, providers appeared more inclined to attribute low vaccination rates to patient rather than provider factors, which contrasted with the study finding that about half of the
providers changed their vaccine recommendations when they were provided information through the adult immunization schedules. In general, providers’ responses indicate many opportunities to study the implementation of adult immunization recommendations using graphic adult immunization schedules as tools, perhaps supplemented by programs that inform and motivate both providers and patients.
Use of Adult Immunization Schedules In aggregate, study participants did not clearly prefer either the ACIP or IAC format of the adult immunization schedule. There were strongly expressed positive and negative statements about both schedules, sometimes directly contradicting each other. This suggests that there may not be one “best” schedule format that meets the needs of all providers. Rather, various formats of the same recommendations may better meet the needs of a diverse group of providers with diverse training backgrounds and preferences. If confirmed in broader provider studies in the future, this finding underscores the importance of “field testing” different formats for immunization reference materials and maintaining more than one version of reference materials if there is no clearly demonstrated preference in the target audience of providers. The adult immunization schedule graphic has potential value as a resource for improving the quality of patient care, but with the caveat that providers’ occasionally inappropriate application of information in the schedule is likely attributable to general unfamiliarity with the schedule format. This interpretation is supported by the fact that the majority of respondents preferred the second format presented to them, regardless of whether it was the IAC or ACIP format. Therefore, beyond development of schedule formats as decision aids, there is an apparent need to educate providers in their use. Subsequent to the focus groups, half of the practices reported that the adult immunization schedule formats were effective prompts regarding adult vaccination efforts, while the remainder had not changed their vaccination emphasis. This finding underscores the point that the availability of an adult immunization schedule itself will be insufficient to prompt the broad spectrum of internal medicine and family medicine practices to change their approaches to adult vaccination, especially among practitioners for whom adult immunization remains a low priority.
Limitations The limitations of qualitative studies are inherent in their design. The study sample was not intended to be representative of the larger population of adult immunization providers in the United States. Rather, the goal Am J Prev Med 2005;29(1)
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What This Study Adds . . . Adult immunization rates lag far behind childhood rates; whether an immunization schedule would serve as a helpful resource or prompt for adult health care providers is unknown. In this study, providers frequently changed their immunization recommendations for clinical vignettes based on information contained in the adult schedules, suggesting that the schedules may help improve rates of timely and appropriate vaccination for adults. Moreover, providers indicated no clear preference for different presentation formats of the schedule, indicating that more than one format may help in dissemination of such information.
was to explore providers’ potential use of new adult immunization schedule formats that had not previously been examined. The findings suggest avenues for future study, particularly regarding providers’ accurate interpretation of information provided in graphic schedules, and the extent to which the incorporation of different schedule formats into routine provider practice may contribute to decreased barriers to immunization and higher adult vaccination rates. Broader publication and dissemination of the adult schedule may also prompt adults in the general public to ask healthcare providers about vaccines appropriate for them.
Conclusions Our study findings shed valuable light on adult healthcare providers’ perceptions of barriers to adult immunizations and their potential application of information included in recently issued adult immunization schedule formats to improve vaccine delivery, but also underscore the importance of educating providers about the appropriate use of such schedule formats in the timepressured healthcare environment. While the advent of adult immunization schedule formats may not lead directly to vastly improved adult vaccination rates be-
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cause barriers to immunization are complex and multifactorial, providers do value a central resource for adult immunization information. Lessons learned from efforts to urge providers to incorporate adult immunization recommendations in their practices—such as the value of a single set of recommendations presented in different formats—may also be transferable to other efforts to educate healthcare providers in the future. This work was funded by the Centers for Disease Control and Prevention through a cooperative agreement with the Association of Teachers of Preventive Medicine. We are grateful to the practices and providers who participated in this study for their time and insights. We also acknowledge the research assistance of Emily Kennedy. No financial conflict of interest was reported by the authors of this paper.
References 1. Centers for Disease Control and Prevention. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices. MMWR Recomm Rep 2003;52:1–36. 2. Singleton JA, Greby SM, Wooten KG, Walker FJ, Strikas R. Influenza, pneumococcal, and tetanus toxoid vaccination of adults – United States, 1993-1997. MMWR Surveill Summ 2000;49:39 –52. 3. Centers for Disease Control and Prevention. Influenza and pneumococcal vaccination levels among persons aged ⱖ65 years. MMWR Morb Mortal Wkly Rep 2002;51:1019 –24. 4. Centers for Disease Control and Prevention. Preventive-care practices among persons with diabetes—United States, 1995 and 2001. MMWR Morb Mortal Wkly Rep 2002;51:965–9. 5. U.S. Department of Health and Human Services. Healthy people 2010, conference ed. 2 vols. Washington DC: U.S. Department of Health and Human Services, 2000. 6. Briss PA, Rodewald LR, Hinman AR, et al. Reviews of evidence regarding interventions to improve vaccination coverage in children, adolescents, and adults. Am J Prev Med 2000;18(suppl 1):97–140. 7. Shefer A, Briss P, Rodewald L, et al. Improving immunization coverage rates: an evidence-based review of the literature. Epidemiol Rev 1999;21:96 –142. 8. Szilagyi P, Vann J, Bordley C, et al. Interventions aimed at improving immunization rates. Cochrane Database of Systematic Reviews, 4:CD003941, 2002. 9. Szilagyi PG, Bordley C, Vann JC, et al. Effect of patient reminder/recall interventions on immunization rates: a review. JAMA 2000;284:1820 –7. 10. Davis MM, McMahon SR, Santoli JM, Schwartz B, Clark SJ. A national survey of physician practices regarding influenza vaccine. J Gen Intern Med 2002;17:670 – 6. 11. Centers for Disease Control and Prevention. Recommended adult immunization schedule, United States, 2002–2003. MMWR Morb Mortal Wkly Rep 2002;51:904 – 8.
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