Abstract
This article proposes an innovative, theoretically-driven intervention to reduce risk from human papillomavirus (HPV). This lessening of HPV risk would lead to a reduction in the rate of cervical cancer. Aims of this article are to introduce a culturally appropriate model (PEN-3) that may facilitate vaccine uptake among vulnerable populations and to ascertain whether culturally appropriate health education delivered by nurses could be included in vaccine education programs.
Keywords: Nurses, Cultural, Immunization, Health Education, Schools
Tanya and Tommie are 17-year-old twins who live with their parents. Both parents are attentive to their children’s needs. Their father manages a call center and the mother works as a desk clerk at a local hotel. Due to high cost neither parent opted into a family health insurance. The twins spend their after school time at basketball practice. As a result of their Catholic upbringing and their parents’ discomfort with having “the Talk,” the children are not skilled in sexual communication. They understands that engaging in sex without birth control can result in a pregnancy, but do not know much about STIs—how they are contracted and how they can be avoided. They are not aware that a persistent human papillomavirus (HPV) infection may lead to cervical or penile cancer. The topics of HPV and cancer never came up in high school health class or at home. A year later, they are college students. Tanya has come to student health to request information about birth control and a cervical cancer prevention shot that she read about in a magazine.
Introduction
As cervical cancer prevention technologies and vaccine science evolve, so does the need for utilizing nurse expertise in these areas. Nurses serve as a core source of vaccine information.5,16 Nurses recognize that vaccine costs for non-insured or underinsured children are covered by the Vaccines for Children Program (VCP). Nurses also know that not all adolescents are receiving all the recommended immunizations for their age group.
The Healthy People 2010 vaccination goal of 90% coverage among adolescents aged 13–15 years was not met with respect to the HPV vaccines.1 Although HPV vaccination rates are increasing each year, only 27% of teenage girls completed the recommended three-dose series in 2009. Among teenage girls who completed the series, 23.1% were Black and 23.4% were Hispanic. These findings suggest that barriers to completing the vaccine series exist, but particularly for members of certain ethnic groups. One of these barriers is insufficient knowledge about the importance of completing the vaccine regimen.5, 14
In this article, the authors introduce a culturally appropriate model, PEN-3, that nurses can follow to achieve the goal of increasing HPV vaccine knowledge and use. The authors envision that culturally appropriate HPV vaccination education delivered in nontraditional settings (e.g., schools) by nurses, and reinforced in every health visit, may help increase vaccine completion rates.1, 5, 8, 19
THE HPV VACCINES
The link between HPV and cervical cancer is so strong that the International Agency for Research on Cancer (part of WHO) has officially acknowledged HPV as a high-risk human carcinogen.2 In 2006, the first quadrivalent HPV vaccine (Gardasil®) targeting HPV strains 6, 11, 16, and 18 was approved by the FDA in females aged 9–26 years3; in 2009 approved in males aged 9–26. Cervarix, a bivalent HPV vaccine was approved in 2009 (Table 1).3 Despite 5 years of HPV vaccine availability, vaccination completion rates are lower than projected by the new Healthy People 2020 objective of 80% coverage.4 The fee for the HPV vaccine is paid for by private insurance and by the VCP.
TABLE 1.
SUMMARY ON HPV VACCINES
| HPV 16/18 vaccine | HPV 6/11/16/18 vaccine | |
|---|---|---|
|
| ||
| Manufacturer | GlaxoSmithKline | Gardasil |
|
| ||
| Volume | 0.5mL per dose | 0.5mL per dose |
|
| ||
| Schedule | 0, 1, 6 months | 0, 2, 6 months |
|
| ||
| Focus | Cervical Cancer | Cancer and STD ❖ |
|
| ||
| Recommended Age | ||
| • Females | 9–26 years | 9–26 years |
| • Males | Not FDA approved | 9–26 years |
Adapted from: Giannini SL, Hanon E, Fourneau MA et al. Superior immune response induced by vaccination with HPV 16/18 L1 VLP formulated with either AS04 or aluminium salt only formulation. Poster B68. Presented at: Frontiers in Cancer Prevention Research, a meeting of American Association for Cancer Research (AACR), Baltimore, Maryland, 30 October–2 November 2005 and Fernandez JM, Hoeffler J.P. [eds], Gene Expression Systems. Using nature for the art of expression. Academic Press, San Diego, 1999.
To be most effective, the HPV vaccine is given as a three shot regimen in children before the onset of sexual activity. The best antibody response occurs in children aged 12 years or younger.1–4 If the topic of vaccinations were discussed by nurses with both students and their parents in the school setting, decisions about vaccinations could be made in an enlightened environment.8, 13, 15
In practice, however, the burden for decision making regarding immunizations for children, falls almost exclusively on parents.4,5 Nurses have an opportunity to educate parents and students about the risk of contracting HPV and ways to prevent it.16 Both students and their parents may be highly influenced by their interactions with a nurse.16 To be most effective in decreasing the burdens of HPV and cervical cancer, nurse interventions must be culturally appropriate and include parental involvement.17–19
Studies describing disparities related to the initiation and continuation of the HPV vaccine series while understanding the important role nurses play in the health and wellbeing of children were reviewed. The authors performed a review of the literature using data generated from PsychINFO, Medline, and CINAHL.
OVERVIEW
Certain populations—for example, those of low socioeconomic status, some minorities, and those with public health insurance—are more likely to initiate the HPV vaccinations but less likely to complete the recommended three dose series.4 Incomplete vaccination series may result in suboptimal disease protection.6 This fact has raised questions about the degree to which HPV vaccination will lower cervical cancer rates in individuals who do not complete the three dose regimen.3,6 Cervical cancer protection from 1 or 2 doses of the HPV vaccine is still unclear.7,14 From observation full series completion of the bivalent vaccine provides protection up to 6.4 years and the quadrivalent vaccine is up to 8.5 years. Nurses’ instructions about and reinforcement of the need for completing the HPV vaccine series are critical.5
Factors specific to minority parents’ barriers to vaccines include not having knowledge to make informed decisions.8–10 Of note, ~20% of minority members in this country live below the poverty line and are uninsured.11 Poor and uninsured persons may be less aware of their risks and more likely to be treated for cancer at later stages of disease—and, thus, more likely to die of cancer.10,11
Nurse and HPV Knowledge
Nurses are more likely than teachers or guidance counselors to hold beliefs supporting the usefulness and safety of vaccinations and are often sought out by students and parents for their expertise about health-related concerns.13–15 Nurses have formal healthcare training and knowledge to advise parents and students about immunizations. Parents and students who receive correct information about vaccines may utilize vaccine services frequently and consistently.15,16
Because nurses have contact with students and parents on a regular basis, they are ideal primary contacts for immunization-related information. Nurses can also address real and perceived barriers that may influence parents’ and students’ readiness to initiate and complete the HPV vaccine regimen.15–18
CULTURAL EMPOWERMENT
The PEN-3 model identifies the target audience, whether the student(s), parents and/or nurses, while also exploring supporting factors and beliefs including perceptions, enablers and nurturers, to adapting health behaviors, and maintaining a cultural awareness and empowered environment is best suited for a HPV vaccine program.
To assess vaccine acceptance by and communication with the target population, an explanatory theory based on the PEN-3 model is used (Figure).19 The PEN-3 model has been tested and validated as a culturally appropriate model.19,20 The PEN-3 has been described as “the best articulated model to date on cultural competence and healthcare.”21,22
FIGURE.
HYPOTHESIZED APPLICATION OF PEN-3 MODEL FOR HPV VACCINE ACCEPTANCE
There are three interrelated and interdependent dimensions of health (otherwise known as PEN-3; Box). These dimensions are broadly characterized as (1) “cultural identity” (identification of the target audience) including the Person, Extended family, and Neighborhood; (2) “relationships and expectations” (exploration of target audience’s supporting factors and beliefs), including Perceptions, Enablers, and Nurturers; and (3) “cultural empowerment” (both positive and negative), including Positive, Existential, and Negative.19,20
BOX. PEN 3 MODEL.

Adapted from Airhihenbuwa C.Health and Culture: Beyond the Western Paradigm. Thousand Oaks, CA: Sage; 1995.
The author surveys such aspects of the health education as person, extended family, and neighborhood; discusses the elements that inform an educational diagnosis of health behavior, including perceptions, enablers, and nurturers; and considers the cultural appropriateness of health behavior, examining positive, negative, and existential beliefs.19,20 Perceptions are thought to hinder or promote family members’ motivations to change health-related beliefs. Enablers may facilitate changes in perceptions or behavior, or they may generate barriers to change. An example of a positive enabler is the Vaccine for Children’s Programs, which enables low-income parents to have their school-age children vaccinated against HPV free of charge. Nurturers are the supporting factors that a person may receive from central significant others. Nurturers can be the parents’ respect for nurses, who in turn encourage parents to exercise their decision-making power to have their child vaccinated. Dimension 3, Neighborhoods, is committed to promoting health and preventing disease in neighborhoods and communities.19,20
Neighborhoods contains three subcategories (positive, existential, and negative) and encompasses the cultural correctness of health beliefs. Positives are necessary health practices that empower individuals, families, neighbors, and communities to improve their health status.16 An indication of success for this category would be increased awareness of the HPV vaccine. The second category, termed existential, includes different health practices (e.g., prayer, traditions), values, and beliefs that may influence decisions about HPV prevention and support for the vaccine. Negatives include myths and misperceptions and engaging in unprotected sexual intercourse.16
THE ROLE OF NURSES
Nurses guided by the PEN-3 model can play a critical role in this outreach. For example, nurses could offer seminars to students and parents about the basics of HPV and the HPV vaccine. The nurses can use dimensions of the PEN-3 model in informing parents’ and students’ decision-making process. Nurses can also develop a survey to evaluate parents’ and students’ knowledge about and attitudes toward the HPV vaccine both before and after the seminar (Table 2).
TABLE 2.
SAMPLE SURVEY ITEMS GUIDED BY THE PEN-3 MODEL
| Circle yes or no or answer the question on the line provided. |
| Relationships & Expectations (Perception, Enablers, Nurturers) |
| Yes No ■ I believe that vaccines are important for children. |
| Yes No ■ I know that the Vaccines for Children Program will pay for the vaccine if my child is younger than 19 years old. |
| Yes No ■ I have received the recommendation of my healthcare practitioner for my child to receive the HPV vaccine. |
| For students: This is what my parents say about the vaccine:
|
| For students and parents: This is what other family members say about the vaccine:
|
| Cultural Empowerment (Positives, Existential, Negatives) |
| Yes No ■ Religion plays a part in my decision making about the HPV vaccine. |
| Yes No ■ Prayer will protect me from cervical cancer. |
| Yes No ■ Folk healers can protect me from cervical cancer. |
| Yes No ■ HPV is not serious enough for a vaccine. |
| Yes No ■ Cervical cancer is something that is meant to be. |
| Yes No ■ Alternative choices (eg, herbs, teas, rubs) play an important role in preventing cervical cancer. |
| Yes No ■ I believe new vaccines are created to make money for the government. |
A study could then be designed to assess the effectiveness of nurses’ educational interventions. Success could be defined as increased rates of HPV vaccination knowledge, including compliance with the full course of vaccination. Using these sources might result in an underestimate of the true vaccination rate because some parents who have their children vaccinated at a county health department or other medical facility may fail to inform the school of this activity. Use of online registries could enhance the information-sharing process, providing more accurate information about vaccination rates.
COLLABORATION
A model of cultural competence such as the PEN-3, which has been verified and duplicated, is an invaluable resource for health promotion and education. In the school setting, nurses can apply this model when they instruct students and parents about HPV and the HPV vaccine.
To reduce HPV infection rates, and, ultimately, cervical cancer rates, a one-size-fits-all approach is not adequate. Nurses must impart information in a way that takes into account their listeners’ cultural values and beliefs.19 Nurses have been identified by many young women as an approachable and informative resource regarding not only HPV vaccination but also STIs in general.19,23.25
CONCLUSION
Nurses are well suited to educate students and parents about transmission and prevention of HPV infection. Nurses can promote the common professional ideal of providing holistic care and advocacy for patients. It is critical to encourage the collaboration and creative brainstorming to develop education programs that can significantly reduce HPV infection and transmission and increase HPV vaccine uptake and series completion.
Footnotes
The authors [Johnson-Mallard, Thomas, Lengacher, Barta & Kostas-Polston] state that they do not have a financial interest in or other relationship with any commercial product named in this article.
Contributor Information
Versie Johnson-Mallard, Email: vejohnso@health.usf.edu, Robert Wood Johnson Nurse Faculty Scholar, 12901 Bruce B. Downs Blvd. MDC 22 Tampa, FL, 33612, Office: (813) 974-7210, Institution: University of South Florida.
Tami L. Thomas, Email: tami.thomas@emory.edu, CPNPRWJ Nurse Faculty Scholar, Emory University, Atlanta Georgia, 1520 Clifton Road NE, Room 256, Atlanta, GA 30032, Office Number: 404-727-6922.
Elizabeth A. Kostas-Polston, Email: epolston@health.usf.edu, RWJF Nurse Faculty Scholar 2010-2013, USF College of Nursing | 12901 Bruce B. Downs, Blvd | MDC22 | Tampa, FL 33612-4799.
Michelle Barta, Email: mbarta1@health.usf.edu, Pharmacy student, University of South Florida, 12901 Bruce B. Downs Blvd, MDC22, Tampa, Florida, 33612-4766.
Cecile A. Lengacher, University of South Florida, College of Nursing, 12901 Bruce B. Downs Blvd, MDC22, Tampa, Florida, 33612-4766, Office: 813-974-9147.
Desiree Rivers, Email: drivers@health.usf.edu, College of Medicine, University of South Florida, 12901 Bruce B. Downs Blvd, MDC 13, Tampa, FL 33612, Tel. (813) 974-2140.
References
- 1.Healthy People. Three Dose HPV Vaccine for Females by Age 13 to 15 Years. 2010 http://www.healthypeople.gov/2010/About/
- 2.International Agency for Research on Cancer. Epidemiology and Biology Cluster (EBC) World Health Organization, Biennial Report 2006–2007; pp. 33–40. [Google Scholar]
- 3.US Food and Drug Administration. Vaccines, Blood & Biologics Gardasil. 2010 http://www.fda.gov/BiologicsBloodVaccines/Vaccines/ApprovedProducts/ucm094042.htm.
- 4.Centers for Disease Control and Prevention. National, state, and local area vaccination coverage among adolescents aged 13–17 years—United States, 2009. Morbid Mortal Wkly Rep. 2010 Aug 20;59(32):1018–1023. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5836a2.htm. [PubMed] [Google Scholar]
- 5.Zimet GD, Mays RM, Sturn LA, et al. Parental attitudes about sexually transmitted vaccination for their adolescent children. Arch Pediatr Adolesc Med. 2005;159(2):132–137. doi: 10.1001/archpedi.159.2.132. [DOI] [PubMed] [Google Scholar]
- 6.Chao C, Velicer C, Slezak JM, Jacobsen SJ. Correlates for completion of 3-dose regimen of HPV vaccine in female members of a management care organization. Mayo Clin Proc. 2009;84(10):864–870. doi: 10.4065/84.10.864. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Frazer IH. Measuring serum antibody to human papillomavirus following infection or vaccination. Gynecol Oncol. 2010;118(1 suppl):S8–S11. doi: 10.1016/j.ygyno.2010.04.003. [DOI] [PubMed] [Google Scholar]
- 8.Kahn JK, Ding L, Huang B, et al. Mothers’ intention for their daughters and themselves to receive the human papillomavirus vaccine: a national study of nurses. Pediatrics. 2009;123(6):1439–1445. doi: 10.1542/peds.2008-1536. [DOI] [PubMed] [Google Scholar]
- 9.Middleman AB, Robertson LM, Young C, et al. Predictors of time to completion of the hepatitis B vaccination series among adolescents. J Adolesc Health. 1999;25(5):323–327. doi: 10.1016/s1054-139x(99)00063-4. [DOI] [PubMed] [Google Scholar]
- 10.Erwin DO, Johnson VA, Trevino M, et al. A comparison of African American and Latina social network as indicators for culturally tailoring: a breast and cervical cancer education intervention. Cancer. 2007;109(2 suppl):368–377. doi: 10.1002/cncr.22356. [DOI] [PubMed] [Google Scholar]
- 11.Farley TA. Sexually transmitted disease in the Southeastern United States: location, race, and social context. Sex Transm Dis. 2006;33(7 suppl):S58–S64. doi: 10.1097/01.olq.0000175378.20009.5a. [DOI] [PubMed] [Google Scholar]
- 12.Glanz K, Croyle RT, Chollette VY, Pinn VW. Cancer-related health disparities in women. Am J Public Health. 2003;93(2):292–298. doi: 10.2105/ajph.93.2.292. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Shui I, Kennedy A, Wooten K, et al. Factors influencing African-American mothers’ concerns about immunization safety: a summary of focus group findings. J Natl Med Assoc. 2005;97(5):657–666. [PMC free article] [PubMed] [Google Scholar]
- 14.Centers for Disease Control and Prevention. Youth risk behavior surveillance—United States, 2007. Morbid Mortality Wkly Rep. 2008;57(SS04):1–131. http://www.cdc.gov/mmwr/preview/mmwrhtml/ss5704a1.htm. [PubMed] [Google Scholar]
- 15.Salmon DA, Moulton LH, Omer SB, et al. Knowledge, attitude, and beliefs of school nurses and personnel and associations with nonmedical immunization exemptions. Pediatrics. 2004;113(6):e552–e559. doi: 10.1542/peds.113.6.e552. [DOI] [PubMed] [Google Scholar]
- 16.National Association of School Nurses. Immunizations Position Statement. Revised September 2010. http://www.nasn.org/Default.aspx?tabid=225.
- 17.Ryan KM. Health promotion of faculty and staff: the school nurse’s role. J Sch Nurs. 2008;24(4):183–189. doi: 10.1177/1059840508319551. [DOI] [PubMed] [Google Scholar]
- 18.Bennett MP. Ethics and the HPV vaccine: considerations for school nurses. J Sch Nurs. 2008;24(5):275–283. doi: 10.1177/1059840508322380. [DOI] [PubMed] [Google Scholar]
- 19.Airhihenbuwa CO. Health and Culture: Beyond the Western Paradigm. Thousand Oaks, CA: Sage; 1995. [Google Scholar]
- 20.Cowdery JE, Parker S, Webster JD. The Application of the PEN-3 Model in the Development of an HIV Prevention Intervention Aimed at Reducing Health Disparities Among African American Adults. Presented at: National HIV Prevention Conference; June 12–15, 2005; Atlanta, Georgia. http://www.aegis.com/conferences/NHIVPC/2005/MP-099.html. [Google Scholar]
- 21.Airhihenbuwa C. Health and Culture: Beyond the Western Paradigm. Thousand Oaks, CA: Sage; 1995. [Google Scholar]
- 22.Airhihenbuwa C, DiClemente J, Wingood M, Lowe A. HIV/AIDS education and prevention among African-Americans: a focus on culture. AIDS Educ Prev. 1992;4(3):267–276. [PubMed] [Google Scholar]
- 23.Goodman RM, Yoo S, Jack L., Jr Applying comprehensive community-based approaches in diabetes prevention: rationale, principles and models. J Public Health Manag Pract. 2006;12(6):545–555. doi: 10.1097/00124784-200611000-00008. [DOI] [PubMed] [Google Scholar]
- 24.American Academy of Nurse Practitioners. The Voice of the Nurse Practitioner: Annual Report. 2009 http://www.aanp.org/NR/rdonlyres/97CD0283-59DF-4964-819B-61E58864B4F8/0/AnnualReport2009.pdf.
- 25.Haebler J. Inside ANA. Headlines from the hill. Legislating HPV vaccine a state tale. American Nurse Today. 2007;2 (11):18. [Google Scholar]

