Cervical Cancer: Prevention and Early Detection

Seminars in Oncology Nursing, Vol 33, No 2 (May), 2017: pp 172-183

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CERVICAL CANCER: PREVENTION AND EARLY DETECTION THERESA A. KESSLER OBJECTIVE: To review effective methods of prevention that can be used to control the incidence of cervical cancer and detection strategies that can identify the precancerous lesions before they become true cancer.

DATA SOURCES: Current medical, scientific and nursing literature, and national and international guidelines of cervical cancer.

CONCLUSION: Nearly all cervical cancers are caused by specific types of human papillomavirus (HPV). Prophylactic vaccination for HPV provides the most effective method of primary prevention against HPV-related diseases. The use of the Pap test and HPV test, according to published guidelines, provides the most effective means of screening for cervical cancer.

IMPLICATIONS FOR NURSING PRACTICE: Nurses are in a key position to provide health education with the goal of supporting vaccine uptake and screening guidelines.

KEY WORDS: cervical cancer, early detection, HPV vaccination, cervical cancer screening, education.

Theresa A. Kessler, PhD, RN, ACNS-BC, CNE: Professor and Kreft Endowed Chair for the Advancement of Nursing Science, College of Nursing & Health Professions, Valparaiso University, Valparaiso, IN. Address correspondence to Theresa A. Kessler, PhD, RN, ACNS-BC, CNE, Advancement of Nursing Science, College of Nursing & Health Professions, Valparaiso University, 836 LaPorte Ave, Valparaiso, IN 46383. e-mail: [email protected] © 2017 Elsevier Inc. All rights reserved. 0749-2081 http://dx.doi.org/10.1016/j.soncn.2017.02.005

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ervical cancer is a global health concern. It ranks as the fourth most common female malignancy worldwide,1,2 with the incidence of cervical cancer at an estimated 527,624 women every year, with 265,672 deaths from the disease. 3 Cervical cancer accounts for 4% of all cancers diagnosed worldwide. When one considers health disparities, cervical cancer is the third most common cause of death worldwide for those women who live in low-resource or less developed countries. 1 In fact, nearly 84% of cervical cancer cases occurred in less

CERVICAL CANCER: PREVENTION AND EARLY DETECTION

developed countries, with the highest incidence in Africa, Latin America, and the Caribbean, and the lowest incidence in North America and Oceania.4,5 Women who are poor and live in rural areas of lowand middle-income countries, as well women who are poor and live in high-income countries, are at an increased risk of invasive cervical cancer; this increased risk is caused by a lack of access to prevention, screening, and treatment services.6 In the United States (US), cervical cancer ranks 14th in frequency among all cancers.7 However, disparities exist in the US as well. Incidence and death rates in the US are higher in areas with limited access to cervical cancer screening.8 For 2017, the American Cancer Society estimates that 12,820 new cases of invasive cervical cancer will be diagnosed in the US, with a projected 4,210 deaths in the same year.8,9 Nearly all cervical cancers are caused by human papillomavirus (HPV) infections. HPV is the most common sexually transmitted infection worldwide,10 and is the cause of nearly all cases of cervical cancer.10,11 Currently, approximately 79 million men and women in the US are infected with HPV and about 14 million will become newly infected each year.12 In the US, HPV is detected in 99.7% of cervical cancers,13 and more than 11,000 women develop cervical cancer as a result of HPV disease.12 Because precancerous lesions can be found by the Papanicolaou (Pap) test and treated and cured, cervical cancer is often detected before it becomes advanced. Early detection has led to lower incidence and death rates. Women treated with precancerous lesions have nearly a 100% 5-year survival rate.8,9 Even though secondary screening can prevent cervical cancer by detecting precancerous lesions, not all women receive the recommended screening nor receive the screening in a timely manner. In addition, an effective primary prevention strategy is available to combat cervical cancer. Both males and females should receive HPV vaccinations to prevent the development of cervical cancer; however, vaccination rates remain low.

HISTORY In the 1940s, cervical cancer was a major cause of death among women of childbearing age in the US. In the 1950s, the Pap test was introduced and effectively reduced the incidence of invasive cervical cancer. Between 1955 and 1992, US cer-

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vical cancer incidence and death rates declined by more than 60%.7,9 Epidemiologically, it was believed that cervical cancer might be caused by a sexually transmitted agent; however, this fact was not known until the 1980s.9 Between 1975 and 2012, cervical cancer incidence declined by over 50% because of widespread use of the Pap test.9 More recently, incidence rates have stabilized in whites younger than 50 years of age and declined by 3% per year in African Americans. For women over age 50, incidence has decreased by about 2% per year in whites and about 4% per year in African Americans.9 Today, women are more likely to be diagnosed with cervical precancer than invasive cervical cancer.9 Worldwide, during the past 30 years, cervical cancer mortality rates have fallen in most developing countries because of screening and treatment programs.6 However, during these same years, rates in most developing countries have risen or remained unchanged. These increased or steady rates have been because of limited access to health services, lack of awareness about cervical cancer and its screening recommendations, and the absence of screening and treatment program.6

ETIOLOGY As the causative agent for virtually all cases of cervical cancer, HPV can infect the genital areas of females and males, including the skin of the vulva, penis, and anus; the linings of the vagina, cervix, and rectum; and the linings of the mouth and throat.12 Unlike other sexually transmitted infections, most signs and symptoms of HPV are nonexistent; therefore, most individuals are unaware of the infection. There are more than 40 types of HPV that are sexually transmitted and will infect the epithelium of the skin or mucus membranes. Despite the fact that the immune system typically clears the virus from the body within 2 years, some individuals will have a persistent HPV infection that can cause various types of cancers and genital warts.14 “Low-risk” HPV types can cause warts on or around the genitals and anus of both females and males. Females may also have warts on the cervix and in the vagina. Because these genital HPV types rarely cause cancer, they are called “low-risk” viruses.11 The low-risk types include 6, 11, 42, 43, 44, 54, 61, 70, 72, and 81, while types 6 and 11 account for 90% to 100% of genital warts.15 It is estimated

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that approximately 20% to 50% of people with lowrisk infections may also have co-infections with what is known as “high-risk types.”15 High-risk HPV types cause cancer.11 Fifteen HPV types can cause cervical cancer16 and include types: 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 68, 73, and 82.15,16 The most frequent precancerous cervical lesions are cervical intra-epithelial neoplasm; these lesions can become invasive.17 Types 16 and 18 are the most oncogenic strains of the virus and are responsible for causing over 75% of cervical cancer cases and the majority of other genital cancers.11,14 The prevalence of high-risk HPV infections peak shortly after initiation of sexual intercourse.17 When high-risk HPV lingers and infects the cells of the vulva, vagina, penis, anus, or the oropharynx, it can cause cell changes or precancers.18 These precancers may eventually develop into cancer if they are not found and removed. These cancers are much less common than cervical cancer. Much less is known about how many people with HPV will develop cancer in these areas.

CANCER PREVENTION AND EARLY DETECTION Controlling the incidence of cervical cancer can be accomplished in two ways. One way is to prevent the precancers in the first place, and the second is to detect the precancers before they become true cancer.

RISK FACTORS While epidemiological case series have shown nearly 100% of cervical cancer cases test positive for HPV,19 only a small number of those with HPV will develop cervical cancer. Table 1 shows the various risk factors for HPV and cervical cancer. Approximately 90% of HPV infections are transient and are undetectable within 1 to 2 years.11 Women who have sex at an early age or who have many sexual partners or a partner with multiple sex partners are at increased risk for HPV infection and cervical cancer. However, women may become infected with HPV even with only one sexual partner. In fact, HPV infections are common in healthy women, but those infections rarely cause cervical cancer. Immunosuppression may also affect the incidence of HPV. Women who are positive for HIV are at a higher risk for HPV infection because precancerous changes may develop into invasive cancer faster. In addition, women who have AIDS have an increased risk for cervical cancer.11 In addition to the risks associated with HPV infection, cervical cancer may be influenced by other risk factors.11 Women who take immunosuppressive drugs are also at higher risk of developing cervical cancer. Infection with chlamydia has been linked to a higher risk of cervical cancer in women whose blood tests show signs of past or current chlamydia infection (compared with women with normal test results). Unfortunately, infection with chlamydia produces no symptoms; therefore, women

TABLE 1. Risk Factors for HPV and Cervical Cancer Risk factors for HPV First intercourse <18 years Multiple sex partners or having a partner with multiple partners Smoking Immunosuppression from medications or disease

HPV, human papillomavirus; HSV-2, herpes simplex virus 2.

Risk factors for cervical cancer HPV High risk: Types 16 and 18 Low risk: Types 6 and 11 Past or current chlamydia infection Infection with HSV-2 Diet low in fruits and vegetables Being overweight Smoking Use of combined oral contraceptives Three or more full-term pregnancies First full-term pregnancy before age 17 Low income or limited access to health care Positive family history for cervical cancer

CERVICAL CANCER: PREVENTION AND EARLY DETECTION

may not know that they are infected unless they are tested for chlamydia during a pelvic exam.11 Infection with herpes simplex virus 2 can be associated with chronic inflammation and microulcerative changes of the cervical epithelium that play an important role in initiation and progression of cancer.15 General lifestyle factors have been considered weak links to cervical cancer, including eating a diet low in fruits and vegetables and being overweight. Women who smoke cigarettes are twice as likely to get cervical cancer compared with non-smokers.20 Cancer-causing chemicals and tobacco by-products in cigarettes have been found in the cervical mucosa of women who smoke.20 These substances damage the DNA of cervical cells. Long-term use of combined oral contraceptives (COCs) has been associated with increased risk of cervical cancer; however, the risk decreases after the COCs are stopped. In one study, the risk of cervical cancer was doubled in women who took COCs longer than 5 years, but the risk returned to normal 10 years after COCs were stopped.21 Women with three or more full-term pregnancies have an increased risk of developing cervical cancer. The reason for this is unknown.21 Also, when a women has her first full-term pregnancy before age 17, she is almost two times more likely to get cervical cancer later in life than women who waited to get pregnant until after age 25.21 The use of diethylstilbestrol (DES) in mothers has been linked to cancer in their daughters, clear cell adenocarcinoma of the vagina more so than the cervix. However, there is an extremely low risk, only about one in every 1,000 women whose mothers took DES during pregnancy develop cancer, meaning about 99.9% of DES daughters do not develop these cancers.21 Having a family history of cervical cancer can increase risk two to three times higher than those with no family history.21 Some researchers suspect some of the familial tendency may be caused by an inherited condition that makes some women less able to fight off HPV infection compared with others.21 Lastly, poverty has been linked to cervical cancer. Women with low incomes or limited access to health care may not be screened or treated for cervical cancers and precancers.21

PREVENTION STRATEGIES Prevention of HPV infection is key to preventing cervical cancer; however, there is not one

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solution to prevent infection with all the different types of HPV. While the rate of HPV infection is high and there is no known cure for HPV, effective primary prevention is available. It is important that both females and males lower their risk with effective health behaviors and HPV vaccination. For females, prevention includes safe sex practices such as delaying sex until older, limiting the number of sex partners, and avoiding sex with someone who has had many other sex partners.22 Men must also avoid multiple sex partners and be aware that being uncircumcised increases the risk of being infected with HPV and passing it on to partners.22 However, circumcision does not completely protect against HPV infection; uncircumcised men can still be infected with HPV and pass it on to their partners. Men must use latex condoms the correct way every time they have sex. A condom can lower the risk of HPV infection; but areas that are not covered by a condom may still become infected.22 Combining these health behaviors with vaccination is important. HPV vaccines are safe, effective, and could prevent the majority of HPV-attributable cancers, if vaccination coverage is high.23

VACCINATION FOR HPV Prophylactic HPV vaccination provides the most effective method of primary prevention against cervical cancer. Vaccination for HPV has been available in the US since 2006. The Advisory Committee for Immunization Practices, the Center for Disease Control and Prevention, and the American Cancer Society provide recommendations regarding vaccination. All three groups recommend three doses for routine HPV vaccination for females and males ages 11 or 12 years, and catch-up vaccines for males through age 21 and for females through age 26.22,24 The vaccine is recommended for gay and bisexual males through age 26 and for females and males who have compromised immune systems through age 26, if they were not fully vaccinated when they were younger.16 Recommendations for vaccination in the US vary slightly from what is recommended by the World Health Organization. In 2014, the World Health Organization updated their recommendations and cited a vaccine schedule of two doses of the HPV vaccine for girls between 9 and 13 years of age.25 HPV vaccination should occur before the first sexual contact and prior to exposure to HPV; however, vaccination after the first sexual contact

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is recommended.26 Young adult females are of particular concern because HPV prevalence peaks in 20- to 24-year-old females, when almost 45% were found to be infected.27 Unfortunately, statistics for HPV prevalence may not provide the true rate of occurrence. Because HPV infections may clear quickly, the incidence of HPV may be even higher than reported. Therefore, routine HPV vaccination should decrease the burden of HPV-related diseases. Three vaccines are available for the prevention of HPV. In 2006, Gardasil (Merck & Co. Inc. Whitehouse Station, NJ, USA) was approved by the US Food and Drug Administration (FDA) as a quadrivalent vaccine (4vHPV) that prevents HPV types 6, 11, 16, and 18.28 In 2009, another vaccine, Cervarix (GSK-GlaxoSmithKline, Rixensart, Belgium), was released; it is a bivalent vaccine (2vHPV) that prevents HPV types 16 and 18, which can cause cervical cancer and precancerous lesions.29 In December 2014, the FDA approved Gardasil 9 (9-valent human papillomavirus vaccine [9vHPV]) for the prevention of diseases caused by nine types of HPV: 6, 11, 16, 18, 31, 33, 45, 52, and 58.28 Gardasil 9 added protection against five additional types of HPV beyond the quadrivalent vaccine; these additional types are responsible for approximately 20% of cervical cancers that are not covered by previously approved HPV vaccines.28 Gardasil 9 is approved for use in females ages 9 to 26 and in males ages 9 to 15. Vaccination of females is recommended with 2vHPV, 4vHPV, or 9vHPV, and vaccination of males is recommended with 4vHPV or 9vHPV.30

EARLY CANCER DETECTION/SCREENING GUIDELINES Because HPV vaccines cannot protect against established infections, nor do they protect against all types of HPV, women must still be screened for cervical cancer and follow cervical cancer screening guidelines. High-quality secondary screening with cytology or the Pap test is a simple and effective procedure. In the US, screening recommendations for the Pap test changed dramatically in 2012. Data shows abnormal Pap test results revert to normal even without treatment nine out of 10 times,15 and approximately 90% of HPV infections resolve on their own.7,31 Because of these factors, new screening guidelines were issued in 2012. The American Cancer Society, the American Society for Colposcopy and Cervical Pathology, and the American Society for Clinical Pathology aligned their screening guidelines with the US Preventive Services Task Force and the American College of Obstetricians and Gynecologists.17,32 Table 2 provides the screening guidelines. Preferred screening guidelines now state cervical cancer screening should begin at 21 years of age, regardless of sexual history,17 with a routine Pap test and should continue at 3-year intervals until the woman is 29 years of age.32 Between 30 and 65 years of age, women should receive the Pap test and the HPV test every 5 years. This cotesting is important because it lowers the rate of false-negatives. 32 An acceptable testing

TABLE 2. Cervical Cancer Screening Guidelines Age (yrs)

Recommendation

<21 21 to 29

No screening regardless of sexual initiation or other risk factors Cytology alone every 3 years No HPV testing as stand-alone or as a cotest with cytology Cytology plus HPV testing (cotest) every 5 years (preferred) Or Cytology alone every 3 years (acceptable) No screening if 3 consecutive negative cytology results or 2 consecutive negative cotests within the last 10 years, with the most recent test in the past 5 years

30 to 65

>65

Screening after hysterectomy with removal of the cervix is not recommended. HPV, human papillomavirus.

CERVICAL CANCER: PREVENTION AND EARLY DETECTION

alternative for women 30 to 65 is to have a Pap test cytology alone every 3 years. Once a woman is over 65 years of age, she no longer needs screening following an adequate negative prior screening history.32 Women who cotest HPV-positive and cytology-negative should repeat cotesting in 12 months or receive immediate HPV genotypespecific testing for HPV16 alone or for HPV16 and HPV18.32 If cotesting is positive for either repeat test, women should be referred to colposcopy. Women testing negative on both tests should return to routine screening.32 Women who have a history of cervical intraepithelial neoplasm 2 (CIN2) or a more severe diagnosis should continue routine screening for at least 20 years, even if it extends screening beyond 65 years of age.32 It is also recommended that women who are over 65 years and who also have had exposure to DES in utero, are immunosuppressed, positive for HIV, or have a history of an organ transplant should speak to their health care provider (HCP) for the best screening approach.15 Yearly screening is no longer recommended because of the higher rates of falsepositive results and the fact that there is little effect on subsequent cancer with the extended time between precancerous lesions and invasion.17 In the past, questions were raised about the efficacy of conventional versus liquid-based Pap testing. This concern has resolved in the US because automated liquid-based cytology has replaced conventional pap smears.15 A positive feature of liquidbased testing is that the same sample can be used to test for the presence of high-risk HPV types in addition to the cytology.33 HPV tests can forecast cervical cancer risk many years in the future and are currently recommended for use in conjunction with the Pap test for women 30 to 65 years of age. HPV testing alone should not be used in women under 30 years of age, nor should HPV testing be used in combination with cytology in women under 30 because of the higher rate of HPV infections in these women.17 Molecular tests for HPV assess for the high-risk HPV types that can lead to cervical cancer. There is no role for low-risk HPV testing in cervical cancer screening.32 The HPV tests better forecast the development of CIN3+ over the next 5 to 10 years more so than cytology alone32 and can identify women at risk for an uncommon type of cervical cancer (adenocarcinoma) that is often missed by the Pap test cytology.9

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BARRIERS TO PRIMARY AND SECONDARY PREVENTION HPV Vaccination Because HPV vaccination is key to preventing cervical cancer, it is important to examine the factors that influence vaccination behaviors. The percentage of females and males who have been vaccinated in the US has been low and has not reached levels of other recommended vaccines. In 2012, 17-yearold females were the most highly vaccinated age group, with only 44.5% of this age group receiving all three dosages.34 In 2013, only 36.9% of females aged 19 to 26 years reported receipt of ≥1 dosages of the HPV vaccine.34 Most female adolescents in commercial and Medicaid health plans do not currently receive the recommended vaccine dosages by 13 years of age.35 Even those already exposed to HPV should still be vaccinated because vaccination after exposure can still protect against other high-risk strains.27 In addition to low uptake of the HPV vaccine, unfortunately, young adults have reported low intentions of receiving the vaccine.26,36 There are multiple barriers to vaccination. These barriers include parental, provider, or systemlevel factors. In the US, parental consent is needed to vaccinate adolescents under the age of 18 years. Parents report lack of knowledge or needing more information before vaccinating their children,23,37 and report a concern about the vaccine’s effect on sexual behavior.37 Parents also believe their children are at a low risk of HPV infection and, as such, do not need the vaccine. In addition, parents view costs or financial concerns as barriers to vaccination.37 For parents of sons, perceived lack of direct benefit of the vaccine has led to low vaccination rates.37 Unfortunately there are also social disparities for vaccine series completion. Disproportionately more African American females and males and females living below or at the poverty level have lower rates of series completion.34 For young adults aged 19 to 26, perceived barriers to HPV vaccination are reported in the literature. Lack of knowledge is a barrier to HPV vaccine uptake.38-41 Other barriers include cost,37,38 concern about the safety of the vaccine,39,42,43 perceived low susceptibility to HPV,38 and low intention to receive the vaccine.36,43 A lack of provider recommendation has been a consistent barrier to increasing vaccination rates.44 HCPs may lack knowledge of the HPV vaccine and recommendations for vaccination.23 In one study,

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providers reported a lack of knowledge about the relationship between HPV and urogenital or oral cancers.37 Additionally, HCPs reported recommending the vaccine only to select populations rather than all 11- and 12-year-olds, especially populations providers perceive as high risk (often lowincome and/or patients of color), while others reported only vaccinating older teens or females, but not males.37 Evidence also demonstrates that HCPs have not adhered to recommended screening guidelines.45 System-level barriers include limited opportunities during a provider visit to offer HPV vaccine and a lack of flexible tracking and reminder capabilities for completion of the vaccine series. 23 Another system barrier is cost to patients and to providers. HCPs consistently mentioned poor insurance coverage or reimbursement and the costs to purchase37 and store the vaccine as barriers.37,44 For school nurses, system barriers included lack of managerial support, poor staffing, time constraints, and strained relationships between the nurses and educational institutions.46 Pap Test Screening The literature provides data about barriers to Pap testing. According to the World Health Organization, women lack awareness of cervical cancer.6 Additionally, attitudes toward sexual health, open discussion of sexual behaviors, and individual beliefs are barriers to cervical cancer screening. Lack of knowledge for cervical cancer screening has been reported in the literature,47-49 while some women reported not being aware of the benefits of early detection.50 Socioeconomic barriers exist as well; these barriers include poverty, lack of transportation, and immigration status.51 Data from the 2005 Health Information National Trends Survey demonstrated that current smokers are significantly less likely to have regular Pap tests.52 Obesity, another risk factor for cervical cancer, was strongly associated with not maintaining regular screening practices.52 Perceived barriers to the actual Pap test have been reported. Women reported not looking forward to the perceived invasiveness of the Pap test,47,53 low comfort associated with the test,53-55 anxiety about the possible results of the test, and reluctance to screen after a bad experience54 as reasons for not obtaining screenings. Individual barriers to lack of testing are important, but also understanding why current screening guidelines are not followed by providers is important. Evidence demonstrates that HCPs have begun

screening women before recommendations and continued to screen when guidelines recommend that screening is not needed.56

ROLE OF HEALTH CARE PROFESSIONALS Methods to Promote Vaccination Understanding the barriers to HPV vaccination and providing education to overcome these barriers is essential. As part of regular primary prevention strategies, vaccination for HPV must be recommended to all parents of 11- and 12-year-olds and before these children become sexually active. Parents consistently identify HCPs as a key influencing factor in their decision to vaccinate their children.37,42 Teaching about the risk of HPV infection to parents and young adults is important, as well as equating the vaccine as part of the social norm of health care.42,57 System barriers must be addressed. Creating communication systems to support initiation of the vaccine series are important, but there is also a need to create system strategies for adolescents and young adults to complete the vaccination series.58 Innovative communication reminders such as text messaging may lead to increased series completion.37 HCPs must take advantage of missed opportunities to vaccinate when adolescents are seeking care within health care systems, such as getting physical exams for athletics.37 Because there are costs associated with purchasing and storing the vaccines, systems must be developed to help HCPs manage the additional costs.58 Health care systems should also initiate community education for schools and universities.59 Using media to get the message out about HPV vaccination and the consequences of not being vaccinated are essential. Mass media campaigns should be targeted at the end of summer and when school begins in the fall.58 This timing coordinates with parents bringing their children in for well child and school health visits. Health education on college campuses may lead to increased awareness and uptake of the vaccine for those not vaccinated previously.58 Emphasizing the severity of HPV-related disease is central to increasing regret if one does not get vaccinated and has increased intention to seek vaccination.60 Because college males have been shown to be less knowledgeable about the existence of the HPV vaccine, educational campaigns on college campuses should increase awareness about the vaccine41,61 and target males in particular.

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Methods to Promote Screening HCPs must receive continued updates on cervical cancer screening guidelines. While professional organizations support current recommended screening guidelines, professional organizations must continue to focus on getting the word out to HCPs. Health care systems can play an important role in promoting adherence to guidelines as well.17 Guidelines can be communicated through system messaging to HCPs and the public. Using medical record reminders can be another effective tool in reminding HCPs about inappropriate cervical cancer screening practices62 and what practices are supported by professional organizations. One key to promoting screening is to increase patient-provider communication.50 Open communication is necessary for patients to learn about the benefit of early detection. Educational sessions can also increase knowledge of cervical cancer screening guidelines along with the need to complete recommended Pap tests.51 In one study, community health workers who provided education for Hispanic women resulted in increased knowledge and report of having a Pap test.51 Education messages about HPV infection and vaccination should vary somewhat for females and males.58 Females need to learn about the risks of having sex at an early age, having multiple sex partners, having a partner who has had many partners, and having sex with uncircumcised males.8 Additionally, data has suggested females have reported more concerns about the safety or effectiveness of HPV vaccines; therefore, education should focus on reducing these barriers.43 Males must learn about the risks for an HPV infection with multiple sex partners and how to use latex condoms the correct way every time they have sex.58 The cost of getting an HPV vaccination is a greater barrier for males.43 Therefore, educational messages should identify convenient times to receive the vaccine or direct patients to a clinic that offers the vaccine at a reduced rate.39

IMPLICATIONS FOR NURSING PRACTICE Nurses must be aware of effective models to promote health behaviors. Using models to increase screening and vaccination practices has been described in the literature. Various health behavior models that predict behavior change may be categorized broadly as intrapersonal and interpersonal approaches. Intrapersonal models include the Health Belief Model and the Transtheoretical Model (TTM), while interpersonal models often include

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use of the Social Cognitive Theory.63 What these models share in common is that knowledge is necessary but not sufficient to produce behavior change. A premise of the Health Belief Model and the TTM is the need to use education as an initial intervention. The Health Belief Model has been used to address cervical cancer screening knowledge and behaviors. Studies have demonstrated that knowledge was related to increased cervical screening behaviors.47,48,64 The model can also guide health behavior interventions to address cultural specific beliefs, attitudes, and behaviors.51 The TTM has been used to explain health behavior change through a series of stages.65 However, studies found inconsistent findings on whether the TTM increases screening behaviors.66,67 Within the Social Cognitive Theory, self-efficacy is a belief that one can overcome barriers and execute behaviors or high-risk situations successfully,68 supporting the notion that more than knowledge is needed to make a behavior change. Women with increased selfefficacy demonstrated increased cervical screening behaviors.47,69-71 Nurses and other HCPs should use these models, by supporting increased knowledge and self-efficacy, to address behavior change and support an increase in cervical cancer vaccination and screening. HPV Education Nurses and other HCPs should provide clear and accessible educational information and emphasize that HPV vaccination is safe, prevents cancer, and co-administer it with tetanus, diphtheria, acellular pertussis vaccine, and quadrivalent meningococcal conjugate vaccine.23 All educational campaigns must provide knowledge but also address the fact that the vaccine is safe, effective, and well tolerated in an attempt to promote selfefficacy. Overall educational campaigns must include not only the need to receive the initial vaccine but to return for the remaining dosages. Once vaccination begins, nurses should initiate reminder/ recall strategies for parents to bring their children back to the HCP for all dosages,72 such as reminder phone calls or text messaging. School nurses can be instrumental in developing educational campaigns for students. School nurses should focus on all 11- and 12-year-old students and provide education on HPV infections and the effectiveness of vaccination. Even use of simple educational pamphlets about HPV and HPV vaccination can influence acceptance rates and are cost effective.73 These pamphlets must be made available in the school

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nurse’s office and can be sent home to all 11- and 12year-old students during the school year. Acquiring tailored educational materials for specific populations is important, such as using educational materials in Spanish language for students to take home in Spanish-speaking households.73 College health nurses must address the educational needs of young adults as well. Because there is a significant gap in the number of young adults who have received the HPV vaccinations, providing educational sessions may lead to increased awareness and uptake of the vaccine for those not vaccinated previously. Educational messages must focus on the importance of receiving the vaccine to prevent cancer and sexually transmitted infections. While listening to professional lectures or receiving fact sheets for young adults has shown mixed results in the literature,74,75 these strategies should be continued as a part of health education on college campuses. Screening Education Educational programs can be an effective method of helping some women learn about cervical health, and can create an expectation of success or selfefficacy with Pap test screening. Evidence indicates that knowledge of HPV infection and current cervical cancer screening guidelines can increase a woman’s likelihood of maintaining screening behaviors.47,52 However, even though women may know about cervical health and screening behaviors, not all women follow screening guidelines. Knowledge alone does not promote behavior change. Rather, women need to believe they can execute screening behaviors successfully. Nurses can be instrumental in sharing experiences and verbal persuasion to increase a woman’s belief that she can be successful and receive the Pap test.47

FUTURE DIRECTIONS IN CANCER SCREENING AND IMPLICATIONS FOR NURSING PRACTICE It is anticipated that future guidelines may include more sophisticated targeting of women at highest and lowest risk for cervical cancer.17 Sawaya and colleagues suggested the age for initiating screening may increase, as well as the interval for screening, as the use of HPV vaccinations increase.17 Any new screening must be accessible, affordable, and allow for timely treatment when positive results are found.17

There is ongoing research into more specific screening tests for cervical cancer. Testing for E6 and E7 oncoproteins is yielding promising results. The oncoproteins have been linked to cellular transformations in cervical cancer and may lead to cotests for women who are HPV-positive.76 Another new idea is the development of low-cost, rapid home screening for HPV. This type of testing may lead to more women completing screening for HPV.10 A cobas (Roche Molecular Systems, Inc., Pleasanton, CA, USA) HPV DNA test was approved by the FDA in 2014.77 The test is a qualitative multiplex assay that can be used alone to detect a total of 14 high-risk HPV types, including HPV 16 and 18. The assay is automated on the cobas 4800 System and provides real-time polymerase chain reaction technology for amplification and detection.77 The FDA approved its use in women aged 25 and older to determine if there is a need for additional testing for HPV types.28 A study completed by Stoler and colleagues found that one in seven women with normal Pap test cytology was positive for HPV 16 and had CIN2 or cells indicating moderate dysplagia.78 The researchers also found that HPV testing alone was better than Pap test cytology in determining severe cervical cell carcinoma.78

CONCLUSION Nurses must be advocates for increasing knowledge of cervical cancer and its prevention. Education is an essential initial step in the arsenal for cervical cancer prevention. Providing clear messages about best actions for vaccination and screening behaviors are critical. It is necessary that individuals reduce risk and prevent the development of precancer, and it is necessary to find and treat precancer before it becomes cancer. Primary prevention strategies about HPV, its risks, and the need for vaccination are essential in the form of sustained educational campaigns for parents, young adults, and HCPs. Special attention should be provided to the social determinants of seeking vaccinations and the system-level barriers that exist within the health care system. Encouraging women to follow cervical screening guidelines is also important. Helping women to overcome barriers associated with obtaining a Pap test are needed. Using models for behavior change are effective approaches to promote prevention strategies. Nurses are on the front lines of providing education and strategies to overcome barriers to vaccination and screening behaviors in women and men.

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