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      Interventions to increase uptake of Human Papillomavirus (HPV) vaccination in minority populations: A systematic review

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          Highlights

          • Nine studies intervened on vaccination in racial/ethnic and sexual and gender minorities.

          • Education and reminders increased HPV vaccine series initiation and completion.

          • Lack of high-quality, adequately powered studies warrants further investigation.

          Abstract

          Minority youth represent a unique population for public health interventions given the social, economic, and cultural barriers they often face in accessing health services. Interventions to increase uptake of Human Papillomavirus (HPV) vaccination in minority youth have the potential to reduce disparities in HPV infection and HPV-related cancers. This systematic review assesses the effectiveness of interventions to increase HPV vaccine uptake, measured as vaccine series initiation and series completion, among adolescents and young adults, aged 9–26 years old, identifying as a racial and ethnic minority or sexual and gender minority (SGM) group in high-income countries.

          Of the 3013 citations produced by a systematic search of three electronic databases (PubMed, Embase, and Web of Science) in November 2018, nine studies involving 9749 participants were selected for inclusion. All studies were conducted in the United States and were published from 2015 to 2018. Interventions utilized education, vaccine appointment reminders, and negotiated interviewing to increase vaccination. Participants were Black or African American (44.4%), Asian (33.3%), Hispanic or Latinx (22.2%), American Indian or Alaska Native (11.1%), and SGM (22.2%). Studies enrolled parent–child dyads (33.3%), parents alone (11.1%), and youth alone (55.6%). Vaccine series initiation ranged from 11.1% to 84% and series completion ranged from 5.6% to 74.2% post-intervention. Educational and appointment reminder interventions may improve HPV vaccine series initiation and completion in minority youth in the U.S. Given the lack of high quality, adequately powered studies, further research is warranted to identify effective strategies for improving HPV vaccine uptake for minority populations.

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          Use of 9-Valent Human Papillomavirus (HPV) Vaccine: Updated HPV Vaccination Recommendations of the Advisory Committee on Immunization Practices

          During its February 2015 meeting, the Advisory Committee on Immunization Practices (ACIP) recommended 9-valent human papillomavirus (HPV) vaccine (9vHPV) (Gardasil 9, Merck and Co., Inc.) as one of three HPV vaccines that can be used for routine vaccination (Table 1). HPV vaccine is recommended for routine vaccination at age 11 or 12 years (1). ACIP also recommends vaccination for females aged 13 through 26 years and males aged 13 through 21 years not vaccinated previously. Vaccination is also recommended through age 26 years for men who have sex with men and for immunocompromised persons (including those with HIV infection) if not vaccinated previously (1). 9vHPV is a noninfectious, virus-like particle (VLP) vaccine. Similar to quadrivalent HPV vaccine (4vHPV), 9vHPV contains HPV 6, 11, 16, and 18 VLPs. In addition, 9vHPV contains HPV 31, 33, 45, 52, and 58 VLPs (2). 9vHPV was approved by the Food and Drug Administration (FDA) on December 10, 2014, for use in females aged 9 through 26 years and males aged 9 through 15 years (3). For these recommendations, ACIP reviewed additional data on 9vHPV in males aged 16 through 26 years (4). 9vHPV and 4vHPV are licensed for use in females and males. Bivalent HPV vaccine (2vHPV), which contains HPV 16, 18 VLPs, is licensed for use in females (1). This report summarizes evidence considered by ACIP in recommending 9vHPV as one of three HPV vaccines that can be used for vaccination and provides recommendations for vaccine use. Recommendations for routine use of vaccines in children, adolescents and adults are developed by the Advisory Committee on Immunization Practices (ACIP). ACIP is chartered as a federal advisory committee to provide expert external advice and guidance to the Director of the Centers for Disease Control and Prevention (CDC) on use of vaccines and related agents for the control of vaccine-preventable diseases in the civilian population of the United States. Recommendations for routine use of vaccines in children and adolescents are harmonized to the greatest extent possible with recommendations made by the American Academy of Pediatrics (AAP), the American Academy of Family Physicians (AAFP), and the American College of Obstetricians and Gynecologists (ACOG). Recommendations for routine use of vaccines in adults are harmonized with recommendations of AAFP, ACOG, and the American College of Physicians (ACP). ACIP recommendations approved by the CDC Director become agency guidelines on the date published in the Morbidity and Mortality Weekly Report (MMWR). Additional information about ACIP is available at http://www.cdc.gov/vaccines/acip/. Methods From October 2013 to February 2015, the ACIP HPV Vaccine Work Group reviewed clinical trial data assessing the efficacy, immunogenicity, and safety of 9vHPV, modeling data on cost-effectiveness of 9vHPV, and data on burden of type-specific HPV-associated disease in the United States. Summaries of reviewed evidence and Work Group discussions were presented to ACIP before recommendations were proposed. Recommendations were approved by ACIP in February 2015. Evidence supporting 9vHPV use was evaluated using the Grading of Recommendations, Assessment, Development, and Evaluation (GRADE) framework (5) and determined to be type 2 (moderate level of evidence) among females and 3 (low level of evidence) among males; the recommendation was categorized as a Category A recommendation (for all persons in an age- or risk-factor–based group) (6). HPV-Associated Disease HPV is associated with cervical, vulvar, and vaginal cancer in females, penile cancer in males, and anal cancer and oropharyngeal cancer in both females and males (7–10). The burden of HPV infection also includes cervical precancers, including cervical intraepithelial neoplasia grade 2 or 3 and adenocarcinoma in situ (≥CIN2). The majority of all HPV-associated cancers are caused by HPV 16 or 18, types targeted by 2vHPV, 4vHPV and 9vHPV (2,11,12). In the United States, approximately 64% of invasive HPV-associated cancers are attributable to HPV 16 or 18 (65% for females; 63% for males; approximately 21,300 cases annually) and 10% are attributable to the five additional types in 9vHPV: HPV 31, 33, 45, 52, and 58 (14% for females; 4% for males; approximately 3,400 cases annually) (1,12,13). HPV 16 or 18 account for 66% and the five additional types for about 15% of cervical cancers (12). Approximately 50% of ≥CIN2 are caused by HPV 16 or 18 and 25% by HPV 31, 33, 45, 52, or 58 (14). HPV 6 or 11 cause 90% of anogenital warts (condylomata) and most cases of recurrent respiratory papillomatosis (15). 9vHPV Efficacy, Immunogenicity, and Safety In a phase III efficacy trial comparing 9vHPV with 4vHPV among approximately 14,000 females aged 16 through 26 years, 9vHPV efficacy for prevention of ≥CIN2, vulvar intraepithelial neoplasia grade 2 or 3, and vaginal intraepithelial neoplasia grade 2 or 3 caused by HPV 31, 33, 45, 52, or 58 was 96.7% in the per protocol population* (Table 2) (2,16). Efficacy for prevention of ≥CIN2 caused by HPV 31, 33, 45, 52, or 58 was 96.3% and for 6-month persistent infection was 96.0% (16). Few cases were caused by HPV 6, 11, 16, or 18 in either vaccine group. Noninferior immunogenicity of 9vHPV compared with 4vHPV was used to infer efficacy for HPV 6, 11, 16, and 18. Geometric mean antibody titers (GMTs) 1 month after the third dose were noninferior for HPV 6, 11, 16, and 18; in the 9vHPV group, >99% seroconverted to all nine HPV vaccine types (Table 3). Two immunobridging trials were conducted. One compared 9vHPV in approximately 2,400 females and males aged 9 through 15 years with approximately 400 females aged 16 through 26 years. Over 99% seroconverted to all nine HPV vaccine types; GMTs were significantly higher in adolescents aged 9 through 15 years compared with females aged 16 through 26 years. In a comparison of 4vHPV with 9vHPV in approximately 600 adolescent females aged 9 through 15 years, 100% seroconverted to HPV 6, 11, 16, and 18 in both groups, and GMTs were noninferior in the 9vHPV group compared with the 4vHPV group. Immunogenicity in males aged 16 through 26 years was compared with females of the same age group in a separate study. In both females and males, >99% seroconverted to all nine HPV vaccine types, and GMTs in males were noninferior to those in females (4). The immunogenicity of concomitant and nonconcomitant administration of 9vHPV with quadrivalent meningococcal conjugate vaccine (Menactra, MenACWY-D) and tetanus, diphtheria, acellular pertussis vaccine (Adacel, Tdap) was evaluated. The GMTs were noninferior for all nine HPV vaccine types in the co-administered group (all p<0.001). For Menactra, the noninferiority criterion was met for all four serogroups, and for Adacel, for diphtheria, tetanus, and all four pertussis antigens. Safety has been evaluated in approximately 15,000 subjects in the 9vHPV clinical development program; approximately 13,000 subjects in six studies were included in the initial application submitted to FDA (2). The vaccine was well-tolerated, and most adverse events were injection site-related pain, swelling, and erythema that were mild to moderate in intensity. The safety profiles were similar in 4vHPV and 9vHPV vaccinees. Among females aged 9 through 26 years, 9vHPV recipients had more injection-site adverse events, including swelling (40.3% in the 9vHPV group compared with 29.1% in the 4vHPV group) and erythema (34.0% in the 9vHPV group compared with 25.8% in the 4vHPV group). Males had fewer injection site adverse events. In males aged 9 through 15 years, injection site swelling and erythema in 9vHPV recipients occurred in 26.9% and 24.9%, respectively. Rates of injection-site swelling and erythema both increased following each successive dose of 9vHPV. Health Impact and Cost Effectiveness Introduction of 9vHPV in both males and females was cost-saving when compared with 4vHPV for both sexes in a cost-effectiveness model that assumed 9vHPV cost $13 more per dose than 4vHPV. Cost-effectiveness ratios for 9vHPV remained favorable compared with 4vHPV (9vHPV was cost-saving in most scenarios, and the cost per quality-adjusted life year gained did not exceed $25,000 in any scenario) when varying assumptions about HPV natural history, cervical cancer screening, vaccine coverage, vaccine duration of protection, and health care costs, but were sensitive to 9vHPV cost assumptions (17). Because the additional five types in 9vHPV account for a higher proportion of HPV-associated cancers in females compared with males and cause cervical precancers, the additional protection from 9vHPV will mostly benefit females. Recommendations for Use of HPV Vaccines ACIP recommends that routine HPV vaccination be initiated at age 11 or 12 years. The vaccination series can be started beginning at age 9 years. Vaccination is also recommended for females aged 13 through 26 years and for males aged 13 through 21 years who have not been vaccinated previously or who have not completed the 3-dose series (1). Males aged 22 through 26 years may be vaccinated.† Vaccination of females is recommended with 2vHPV, 4vHPV (as long as this formulation is available), or 9vHPV. Vaccination of males is recommended with 4vHPV (as long as this formulation is available) or 9vHPV. 2vHPV, 4vHPV, and 9vHPV all protect against HPV 16 and 18, types that cause about 66% of cervical cancers and the majority of other HPV-attributable cancers in the United States (1,12). 9vHPV targets five additional cancer causing types, which account for about 15% of cervical cancers (12). 4vHPV and 9vHPV also protect against HPV 6 and 11, types that cause anogenital warts. What is currently recommended? The Advisory Committee on Immunization Practices (ACIP) recommends routine HPV vaccination at age 11 or 12 years. The vaccination series can be started beginning at age 9 years. Vaccination is also recommended for females aged 13 through 26 years and for males aged 13 through 21 years who have not been vaccinated previously or who have not completed the 3-dose series. Males aged 22 through 26 years may be vaccinated. ACIP recommends vaccination of men who have sex with men and immunocompromised persons through age 26 years if not vaccinated previously. Why are the recommendations being updated now? 9-valent HPV vaccine (9vHPV) was approved by the Food and Drug Administration on December 10, 2014. This vaccine targets HPV types 6, 11, 16, and 18, the types targeted by the quadrivalent HPV vaccine (4vHPV), as well as five additional types, HPV types 31, 33, 45, 52, and 58. ACIP reviewed results of a randomized trial among approximately 14,000 females aged 16 through 26 years that showed noninferior immunogenicity for the types shared by 4vHPV and 9vHPV and high efficacy for the five additional types. Other trials in the 9vHPV clinical development program included studies that compared antibody responses across age groups and females and males and concomitant vaccination studies. The evidence supporting 9vHPV vaccination was evaluated using the Grading of Recommendations, Assessment, Development, and Evaluation (GRADE) framework and determined to be type 2 (moderate level of evidence) among females and 3 (low level of evidence) among males; the recommendation was designated as a Category A recommendation (recommendation for all persons in an age- or risk-factor–based group). What are the new recommendations? 9vHPV, 4vHPV or 2vHPV can be used for routine vaccination of females aged 11 or 12 years and females through age 26 years who have not been vaccinated previously or who have not completed the 3-dose series. 9vHPV or 4vHPV can be used for routine vaccination of males aged 11 or 12 years and males through age 21 years who have not been vaccinated previously or who have not completed the 3-dose series. ACIP recommends either 9vHPV or 4vHPV vaccination for men who have sex with men and immunocompromised persons (including those with HIV infection) through age 26 years if not vaccinated previously. Administration 2vHPV, 4vHPV, and 9vHPV are each administered in a 3-dose schedule. The second dose is administered at least 1 to 2 months after the first dose, and the third dose at least 6 months after the first dose§ (1). If the vaccine schedule is interrupted, the vaccination series does not need to be restarted. If vaccination providers do not know or do not have available the HPV vaccine product previously administered, or are in settings transitioning to 9vHPV, any available HPV vaccine product may be used to continue or complete the series for females for protection against HPV 16 and 18; 9vHPV or 4vHPV may be used to continue or complete the series for males. There are no data on efficacy of fewer than 3 doses of 9vHPV. Special Populations HPV vaccination is recommended through age 26 years for men who have sex with men and for immunocompromised persons (including those with HIV infection) who have not been vaccinated previously or have not completed the 3-dose series. Precautions and Contraindications HPV vaccines are contraindicated for persons with a history of immediate hypersensitivity to any vaccine component. 4vHPV and 9vHPV are contraindicated for persons with a history of immediate hypersensitivity to yeast. 2vHPV should not be used in persons with anaphylactic latex allergy. HPV vaccines are not recommended for use in pregnant women (1). If a woman is found to be pregnant after initiating the vaccination series, the remainder of the 3-dose series should be delayed until completion of pregnancy. Pregnancy testing is not needed before vaccination. If a vaccine dose has been administered during pregnancy, no intervention is needed. A new pregnancy registry has been established for 9vHPV (2). Pregnancy registries for 4vHPV and 2vHPV have been closed with concurrence from FDA (1,18). Exposure during pregnancy can be reported to the respective manufacturer.¶ Patients and health care providers can report an exposure to HPV vaccine during pregnancy to the Vaccine Adverse Event Reporting System (VAERS). Adverse events occurring after administration of any vaccine should be reported to VAERS. Additional information about VAERS is available by telephone (1–800–822–7967) or online at http://vaers.hhs.gov. Cervical Cancer Screening Cervical cancer screening is recommended beginning at age 21 years and continuing through age 65 years for both vaccinated and unvaccinated women (19,20). Recommendations will continue to be evaluated as further postlicensure monitoring data become available. Future Policy Issues A clinical trial is ongoing to assess alternative dosing schedules of 9vHPV. ACIP will formally review the results as data become available. HPV vaccination should not be delayed pending availability of 9vHPV or of future clinical trial data.
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            Patient reminder and recall interventions to improve immunization rates

            Immunization rates for children and adults are rising, but coverage levels have not reached optimal goals. As a result, vaccine-preventable diseases still occur. In an era of increasing complexity of immunization schedules, rising expectations about the performance of primary care, and large demands on primary care providers, it is important to understand and promote interventions that work in primary care settings to increase immunization coverage. One common theme across immunization programs in many nations involves the challenge of implementing a population-based approach and identifying all eligible recipients, for example the children who should receive the measles vaccine. However, this issue is gradually being addressed through the availability of immunization registries and electronic health records. A second common theme is identifying the best strategies to promote high vaccination rates. Three types of strategies have been studied: (1) patient-oriented interventions, such as patient reminder or recall, (2) provider interventions, and (3) system interventions, such as school laws. One of the most prominent intervention strategies, and perhaps best studied, involves patient reminder or recall systems. This is an update of a previously published review.
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              Understanding suboptimal human papillomavirus vaccine uptake among ethnic minority girls.

              The introduction of human papillomavirus (HPV) vaccines represents a breakthrough in the primary prevention of cervical cancer. However, little is known about vaccination uptake and correlates among low-income, ethnic minority, and immigrant populations in the U.S. who may benefit most from the vaccine.
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                Author and article information

                Contributors
                Journal
                Prev Med Rep
                Preventive Medicine Reports
                2211-3355
                11 July 2020
                September 2020
                11 July 2020
                : 19
                : 101163
                Affiliations
                [a ]Department of Health Promotion Sciences, Mel and Enid Zukerman College of Public Health, University of Arizona, Tucson, AZ, USA
                [b ]Canyon Ranch Center for Prevention and Health Promotion, Department of Health Promotion Sciences, Mel and Enid Zukerman College of Public Health, University of Arizona, Tucson, AZ, USA
                [c ]Division of Public Health Practice and Translational Research, Mel and Enid Zukerman College of Public Health, University of Arizona, Tucson, AZ, USA
                Author notes
                [* ]Corresponding author at: Department of Health Promotion Sciences, Mel and Enid Zuckerman College of Public Health, University of Arizona, 1295 N Martin Ave., Tucson, AZ 85719, United States. jehiri@ 123456email.arizona.edu
                Article
                S2211-3355(20)30123-6 101163
                10.1016/j.pmedr.2020.101163
                7372149
                32714778
                8f94a730-d204-41c3-9151-f0d871bb3be1
                © 2020 The Authors. Published by Elsevier Inc.

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 20 June 2020
                : 27 June 2020
                : 4 July 2020
                Categories
                Review Article

                papillomavirus vaccine,cancer prevention,minority population,health disparities,intervention studies,systematic review

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