Cervical cancer risk and screening among women seeking assistance with basic needs

Abstract

Background:

In the United States more than half of cervical cancers occur in women who are inadequately screened. Interventions to improve access to cervical cancer preventive care is critical to reduce health inequities.

Objective:

We aimed to evaluate need for cervical cancer screening among women seeking assistance with basic needs and to assess best approaches to facilitate Papanicolaou (Pap) referral.

Study Design:

This is a secondary analysis of a randomized controlled trial of low-income female callers to Missouri 2–1–1, a helpline for local health/social services. Need for cervical cancer screening was assessed. Callers were randomized to one of three arms, each providing a Pap referral: verbal referral only, verbal referral+ tailored print reminder, or verbal referral+navigator. Primary outcome was contacting a Pap referral one month post-intervention. Student’s t-tests or Mann-Whitney U tests were used to analyze significant differences in continuous variables, while Fisher’s Exact or χ² tests were used for categorical variables. We stratified by number of unmet basic needs (0–1 vs. ≥2) and compared success of contacting a Pap referral between study groups (verbal referral vs. tailored reminder vs. navigator) using Fisher’s exact test and χ² test, respectively. Multivariate logistic regression was used to assess risk factors for non-adherence for Pap at baseline and 1-month follow-up, adjusting for race/ethnicity, age, insurance status, self-rated health, smoking, and study group.

Results:

Among 932 female callers, 26.8% needed cervical screening. Frequency of unmet basic needs was high, the most common being lack of money for unexpected expenses (91.2%) and necessities like food, shelter and clothing (73.2%). Among those needing a Pap, 211 received screening referrals. Women in the navigator group (11/73, 15.1%) reported higher rates of contacting a Pap referral than those exposed to verbal referral only (9/67, 13.4%) or verbal referral+tailored print reminder (21/71, 29.6%), p = 0.03. Among 176 women with ≥ 2 unmet needs who received a Pap referral, provision of a navigator remained associated with contacting the referral (33.9% vs. verbal referral 17.2% vs. tailored reminder 10.2%, p=0.005). Assignment to navigator group [adjusted odds ratio (aOR) 3.4, 95% CI 1.4–8.5] and non-white race (aOR 2.0 (95% CI 1.5–2.8) were independent predictors of contacting a Pap referral.

Conclusions:

Low-income women seeking assistance with basic needs often lack cervical cancer screening. Health navigators double the likelihood that women will make contact with Pap services, but most 2–1–1 callers still fail to schedule Pap testing despite assistance from navigators. Interventions beyond health navigators are needed to reduce cervical cancer disparities.

INTRODUCTION

For decades, Papanicolaou (Pap) testing has been the successful core of cervical cancer prevention efforts.¹ However, Pap testing requires presentation to a clinician for a somewhat invasive screening examination. Suboptimal adherence to recommended screening schedules has been strongly correlated with the development of cervical cancer, and in the United States more than half of cervical cancers occur in women who are inadequately screened.^2,3

Reasons for inadequate screening are many^4–11 and often deeply rooted to social and structural determinants of health that drive health inequities. Fundamentally, screening requires that women at risk prioritize future health over immediate life challenges, allocating time and effort to navigating health systems so they can obtain care. This may be especially difficult for indigent women, and lower socioeconomic status is a risk factor for the development of cervical cancer.^12–14

Unmet basic needs may be more specific than socioeconomic status as a measure of life stressors that pose obstacles to screening. Basic needs encompass adequate housing, food security, personal and neighborhood safety, and ability to pay bills and secure essential goods. After controlling for income, education, and other demographic characteristics, having more unmet basic needs has been linked to worse health and greater mortality.^15–18 Individuals whose basic needs are met are more likely to engage in health-promoting behaviors.^16,19–22 Public health approaches that consider physical, social, cultural, community or policy context within which people live have the greatest potential benefit.^23,24 As such, community health workers and patient navigators play pivotal roles in reducing health inequities by increasing access to cancer preventive care for medically underserved populations.²⁵ To further this campaign, we aimed to fill a gap in the literature regarding the impact of unmet basic needs on cervical cancer screening by conducting a secondary analysis of a larger study of low-income callers to a Missouri helpline. Our analysis addressed the following research questions: 1) What are the characteristics, including the prevalence of unmet basic needs, of female callers to a helpline who need cervical cancer screening? 2) What sociodemographic factors, including basic needs, are related to contacting a referral for Pap testing? 3) Is the association between basic needs and contacting a referral for Pap testing different by intervention group?

MATERIALS AND METHODS

The Institutional Review Board at Washington University in St. Louis approved this study. This secondary analysis was part of a larger trial,²⁰ registered in Clinicaltrials.gov (#NCT01027741), studying the impact of unmet needs on health interventions.

Study setting

Participants were recruited from June 2010 to June 2012, from among callers to United Way 2–1–1 Missouri, a telephone information and referral helpline that continues to expand based on growing demand. 2–1–1 Missouri received 160,000 calls in 2013 and in 2019, 184,000 calls and 237,000 service requests. 2–1–1 is a federally designated dialing code that provides callers with contact information for specific community resources, including health and social services.²⁶ Most callers seek help with such basic needs as meals and utility payments. Although few callers contact 2–1–1 for health-related services (<4% in 2019), studies show that the health needs of 2–1–1 callers are significantly greater than those in the general population.^20,27,28

Study sample and recruitment

After receiving standard 2–1–1 service(s), a random sample of callers was selected to complete a brief health risk assessment. Eligible participants in the randomized controlled trial included Missouri residents age ≥18 years of age who spoke English, were willing to provide their date of birth and sex, and were calling with a service request for themselves, but were not in immediate crisis. A schema of patient recruitment for the sample used in the current analyses is depicted in Figure 1.

Figure 1.

Participants were recruited from June 2010 to June 2012 from among callers to United Way 2–1–1 Missouri, a telephone information and referral helpline that continues to expand based on growing demand.

Need for Pap was self-reported using items from the 2008 Behavioral Risk Factor Surveillance System (BRFSS),²⁹a branch of the Centers for Disease Control and Prevention, which is a data collection program designed to measure behavioral risk factors for adults aged 18 years or older living in households. Up to three referrals were given. However, if a caller had more than three cancer prevention needs, a computer algorithm identified and prioritized their prevention needs in descending order: colonoscopy, mammography, human papillomavirus vaccine for self or girl in home, Pap test, smoking cessation, and smoke free home policy. Based on this algorithm, 211 women who needed a Pap (84%) received a referral to a provider who performs cervical cancer screening and make up the current analytic sample.

Interventions

The original trial was designed such that participants were randomized to one of three interventions to connect them with needed cancer prevention services: verbal referral only (verbal referral group, n = 321 women), verbal referral and a tailored print reminder (tailored reminder group, n = 314 women), or verbal referral and a navigator (navigator group, n = 297 women).

Verbal referral.

Those in the verbal referral only group received from 2–1–1 information specialists a scripted referral consisting of three parts: risk feedback³⁰ confirming no cervical cancer screening within two years, a recommendation³¹ for Pap testing and mention of its importance in cervical cancer prevention, and an offer of referral³² to a free or low-cost service, often the Show Me Healthy Women program, the Missouri branch of the Breast and Cervical Cancer Program of the Centers for Disease Control and Prevention. The verbal referral included the referral telephone number and/or address, information about hours of operation, and information about documentation that might be required to obtain services.

Tailored print reminder

Women in the verbal referral + tailored print reminder group received verbal referral and were mailed a print reminder consisting of a short personal story tailored to cervical cancer screening; an accompanying photo matched to the participant’s age, race, and gender; action details summarizing information needed to access Pap testing, and motivation and preparation information describing why Pap testing is important and suggesting questions to ask when contacting the provider. All print materials were written at a Flesch-Kincaid 4^th grade level.

Navigator/health coach

Women randomized to the navigator arm received the verbal referral and were assigned a telephone health coach who explained Pap testing and its importance, answered participants’ questions, and elicited and addressed barriers to screening including arranging transportation, making appointments, and providing reminders. Two women similar in age to the average 2–1–1 caller were trained by a psychologist and a social worker who had previously worked as a health navigator. The first navigator call was placed within one working day of the baseline assessment and verbal referral. The navigator re-contacted participants to follow up on issues that developed since initial contact and maintained this relationship and support for up to four months. Study health coaches and navigators were not affiliated with a particular health care system or clinic.

Measures

Sociodemographic characteristics were solicited from each study participant at baseline. The primary outcome for the current analysis was making contact for the Pap referral one month after intervention. At one-month follow-up, participants completed a phone interview administered by the research team and were asked if they remembered receiving a health referral (yes/no/don’t remember). Those who remembered were asked if they had made contact for Pap testing. Those who did not recall receiving a health referral were considered to have not made contact.

Reasons for calling 2–1–1.

Every call received by 2–1–1 was coded into mutually exclusive categories (bills/employment/home and family/health/housing/other). Although 2–1–1 does not limit the number of services a caller requests, for purposes of this research, up to three service requests were coded for each participant.

Unmet basic needs

Basic needs were assessed using a screener developed by the study team and drawing upon Segal’s Personal Empowerment scale³³ and items developed by Blazer.¹⁵ It assessed participants’ perceived likelihood that their safety, housing, food, and financial needs would be met in the next month. Five questions beginning with: “How likely is it that…” included a) “… someone will threaten to hurt you physically in the next month?” b) “… you will have a place to stay all of next month”, c) “…you and others in your home will get enough to eat in the next month”; d) “…you will have enough money in the next month for necessities like food, shelter and clothing?”; e) “…you will have enough money in the next month to deal with unexpected expenses?” Answer choices for each of these five questions included: very likely, likely, unlikely, and very unlikely. Needs were considered unmet if reported as unlikely or very unlikely to be resolved in the next month. The basic needs assessment also included a self-assessment of the safety of their neighborhood (very safe, safe, unsafe, very unsafe) and the amount of space in their home given the number of people living there (more than enough, about the right amount, not enough living space). For these specific questions, living in an “unsafe” or “very unsafe” neighborhood and/or reporting “not enough living space” were also considered an unmet basic need. Prevalence of each type of unmet basic need was reported using descriptive statistics. Number of unmet basic needs was captured as a discrete variable (range 0–7) and dichotomized as low (0–1) vs. high (≥2).

Data analysis

Student’s t-tests or Mann-Whitney U tests were used to analyze significant differences in continuous variables, while Fisher’s Exact or χ₂ tests were used for categorical variables. We stratified by number of unmet basic needs (0–1 vs. ≥2) and compared success of contacting a Pap referral between study groups (verbal referral vs. tailored reminder vs. navigator) using Fisher’s exact test and χ² test, respectively. Multivariate logistic regression was used to assess risk factors for non-adherence for Pap at baseline and 1-month follow-up, adjusting for race/ethnicity, age, insurance status, self-rated health, smoking, and study group. A p-value <0.05 was considered statistically significant. All statistical analyses were performed using SAS version 9.4 (SAS Institute, Cary, NC).

RESULTS

Among 932 female callers to 2–1–1 included in this study, 250 (26.8%) needed Pap testing. Sociodemographic characteristics of the participants are presented in Table 1. Patients in need of screening had multiple cervical cancer risk factors. These women had a mean age of 48.2 years, were predominantly non-white, poor and unemployed, unmarried, and actively smoking. The proportion of white women who needed a Pap was higher than that of their non-white counterparts (36.8 % vs. 22.6%, p<0.01). Compared to women who were up to date with cervical cancer screening, those in need of a Pap were more likely to be older (p<0.01), uninsured (43.6% vs. 35.9%, p=0.03), have children living at home (57.6% vs. 40.9%, p<0.01), and rate their health as poor or fair (23.6% vs. 15.2%, p<0.01), but fewer were current cigarette smokers (52.0% vs. 62.0%, p=0.01). After adjusting for age, insurance status, self-rated health, and smoking status, non-white race remained a significant risk factor for needing cervical cancer screening at baseline [adjusted odds ratio (aOR) = 2.1, 95% confidence interval (CI) 1.5–2.9].

Table 1.

Characteristics of participants based on need for Pap testing (N = 932)

Characteristic	Needed Pap (N=250)	Did not need Pap (N=682)	Pa
Age (mean yrs; SD)	48.2 ± 13.7	41.7 ± 12.5	<0.01
Race/ethnicity			<0.01
White	101 (40.4)	173 (25.3)
Other	149 (59.6)	509 (74.6)
Income <$10,000	102 (40.8)	316 (46.3)	0.13
Education			0.51
Less than high school degree	71 (28.4)	204 (29.9)
High school graduate	72 (28.8)	214 (31.3)
Some college or beyond	107 (42.8)	263 (38.6)
Married	35 (14.0)	83 (12.1)	0.46
Employed	45 (18.0)	142 (20.8)	0.34
Children <18 yrs who are still living at home	144 (57.6)	279 (40.9)	<0.01
Uninsured	109 (43.6)	245 (35.9)	0.03
Self-rated general health			<0.01
Good-excellent	191 (76.4)	578 (84.8)
Poor or fair	59 (23.6)	104 (15.2)
Current smoker	130 (52.0)	423 (62.0)	0.01
Service request from 2–1–1
Bills	168 (67.2)	515 (75.5)	0.01
Home and family	111 (44.4)	274 (40.2)	0.25
Health	24 (9.6)	62 (9.1)	0.87
Employment	17 (6.8)	63 (9.2)	0.24
Housing	13 (5.2)	35 (5.1)	0.97
Other	35 (14.0)	77 (11.3)	0.26
Median number of unmet basic needs (range: 0-7)a	2 (2, 3)	2 (2, 3)	0.94
Total # of basic needs			0.51
0-1 unmet basic need	45 (18.0)	136 (19.9)
≥ 2 unmet basic need	205 (82.0)	546 (80.1)
Basic needs items
Not enough money for unexpected expensesb	228 (91.2)	610 (89.4)	0.43
Not enough money for necessitiesb	183 (73.2)	471 (69.1)	0.22
Not enough to eatb	42 (16.8)	107 (15.7)	0.68
Likely to have no place to stayb	44 (17.6)	100 (14.7)	0.27
Not enough living space in home	66 (26.4)	191 (28.0)	0.63
Living in unsafe neighborhoodc	39 (15.6)	165 (24.2)	0.01
Likely to be threatened physicallyd	12 (5.8)	30 (4.4)	0.79

Data are mean ± SD, n (%), or median (interquartile range).

^aStudent’s/-tests or Mann-Whitney U tests for continuous variables; Fisher’s Exact or χ² tests for categorical variables.

^bPercent “unlikely” + “very unlikely”

^cPercent “unsafe” + “very unsafe”

^dPercent “very likely” + “somewhat likely”

Reasons for calling 2–1–1 were similar between the two groups with the exception of assistance with paying bills. In descending order, these requested 2–1–1 services included bills, home and family, other, health, employment, and housing. Women who were up to date with their Pap requested assistance with bills more often than women in need of a Pap (75.5% vs. 67.2%, p=0.01).

Nearly all (94.7%) female callers, regardless of their adherence to Pap testing, had at least one unmet basic need, with callers reporting an average of two unmet needs. Table 1 shows the distribution of these unmet needs for women who did and did not need Pap testing. The most common need was money for unexpected expenses.

Based on the prioritization algorithm, 211 of the 250 women who needed a Pap test received a Pap referral. Few women (41/211, 19.4%) had contacted the Pap referral at one month follow-up. Table 2 shows results of a logistic regression analysis of factors potentially correlated with making contact for Pap testing. A greater number of unmet basic needs was not associated with making contact for Pap referral, although this assessment was limited by the self-selection of our study group with almost all having unmet basic needs. Nonwhite women were twice as likely to contact the Pap referral than their white counterparts (aOR 2.04 95% CI 0.9–1.0). The only modifiable factor associated with contacting a Pap referral was provision of a navigator—contact was reported by only 11/73 (15.1%) in the verbal referral group, 9/67 (13.4%) in the tailored reminder group, but 21/71 (29.6%) in the navigator group (p = 0.03). After adjusting for potential confounders, provision of a navigator increased the likelihood of contacting a Pap referral by 3-fold (aOR 3.4 95% CI 1.4–8.5) compared to the verbal referral only.

Table 2.

Logistic regression model assessing correlates for contacting a Pap referral prior to one month of follow-up (N=211)

Risk Factors	Crude OR (95% CI)	Adjusted ORa (95% CI)
Study group
Referral only	Reference	Reference
Tailored reminder	0.9 (0.3-2.3)	1.1 (0.4-3.2)
Navigator	2.4 (1.0-5.4)	3.4 (1.4-8.5)
Age	1.0 (0.9-1.0)	1.0 (0.9-1.0)
Race
White	Reference	Reference
Other	2.0 (1.5-2.7)	2.04 (1.5-2.8)
Income <$10,000	1.8 (0.9-3.7)	1.7 (0.8-3.5)
Education < high school	1.1 (0.8-1.5)	0.96 (0.7-1.3)
Unemployed	2.2 (0.7-6.5)	3.3 (1.0-11.4)
Uninsured	1.7 (0.9-3.4)	1.8 (0.9-3.8)
Self rated general health:
Good-Excellent	Reference	Reference
Poor or fair	1.2 (0.6-2.7)	1.7 (0.7-3.9)
Basic needs
0-1	Reference	Reference
≥ 2	0.88 (0.6-1.3)	0.98 (0.7-1.5)

^aA binary logistic regression model was used for multivariate analysis, adjusting for race/ethnicity, age, insurance status, self-rated health, smoking, and study group.

Lastly, we stratified by number of unmet basic needs to determine its effect on contacting the Pap referral. Among 176 women with ≥ 2 unmet needs who received a Pap referral, provision of a navigator remained associated with contacting the referral (33.9% vs. verbal referral 17.2% vs. tailored reminder 10.2%, p=0.005, Figure 2).

Figure 2.

Receipt of Pap referral was based on individual prioritized cancer prevention need(s). χ² was performed to calculate P-value.

COMMENT

Principal findings

Calling a 2–1–1 helpline identified women with multiple cervical cancer risk factors who often needed cervical cancer screening services. In our sample, 27% of women were inadequately screened based on their self-reported date of last Pap. Despite multiple interventions, including verbal referral and provision of a tailored print reminder or a navigator, less than a third of these high-risk, high needs women made contact for Pap testing. However, provision of a navigator doubled the probability that women would make contact for screening; this remained true even among women with multiple unmet needs. Passive interventions (provision of a tailored, written reminder delivered by mail) failed to improve cervical cancer screening behavior over that achieved with verbal referral alone.

Results of the study in the context of existing literature

Adhering to recommended cervical cancer screening and follow-up of precursor lesions requires patients to prioritize their future health over more immediate concerns such as unmet basic needs. This may be especially difficult for low-income women and may, in part, explain why low income patients are 2-fold more likely than higher income patients to develop cervical cancer^13,34 and even after adjusting for stage, are 2-fold more likely to die of their disease.³⁵ Prior studies aimed at improving adherence to cervical cancer prevention strategies have mainly focused on patient education and counseling, patient reminder systems, and financial incentives including transportation vouchers.³⁶ However, given the known impact of lower socio-economic status on suboptimal cervical cancer screening,^8–11,13,14 self-identification as needing help through 2–1–1 calls appears to identify women at even higher risk who lack access to care. Thus, this is an important group for targeting with interventions to minimize cervical cancer disparities.

Clinical implications

Among 2–1–1 callers, the number of unmet basic needs did not appear to impact the likelihood that women would obtain appointments for screening within a month. This may be because most 2–1–1 callers have such profound needs for economic and social resources that differences in the level of need are relatively unimportant. Resolving these needs may be a pre-requisite to freeing time and attention to accomplish screening and cancer precursor treatment. However, doing so may require interventions at multiple levels, including assisting women with transportation and childcare, redesigning health systems, and influencing social policy to provide women at risk for cervical cancer with secure homes free of hunger. We are conducting further research exploring the prospective value of navigators specifically trained to help women meet their basic needs as a means to facilitate follow-through for abnormal cervical screening results. Other future directions include testing effective screening tools (eg, Segal Personal Empowerment scale), that may be used by health services to predict patient adherence; and investigating differences in adherence based on cervical cancer screening strategy—cytology only, cotesting, versus primary human papillomavirus (HPV) testing.

Strengths and limitations

Some limitations may impact the generalizability of our study. Our data were derived from a secondary analysis of a trial originally designed to evaluate the effectiveness of reminder interventions encouraging men and women to contact a cancer prevention referral. Thus, we were limited by the type and number of variables previously collected, including the primary outcome. We acknowledge the potential for interview bias and that contacting a cancer prevention referral as opposed to arriving at an appointment may overestimate the proportion of women actually screened and treated for identified cancer precursors. Furthermore, our study involved self-selected women who had unmet basic needs, but were motivated enough to call 2–1–1. The probability of making contact for Pap referral and the impact of a navigator may be different for women with no unmet needs and for women with unmet needs who do not contact 2–1–1. We also encountered sample size limitations, especially when women were grouped by number of basic needs. Prioritization of Pap referral in the study algorithm after colonoscopy, mammography, and HPV vaccine reduced the number of women needing Pap testing who were referred. Furthermore, criteria for determining which women needed a Pap referral relied on self-report which fundamentally, requires knowledge of what a Pap test is and what samples examiners collect. Prior studies have shown that as many as two-thirds of women cannot differentiate a pelvic exam from a Pap test.³⁷ Hence, our results may underestimate the need for screening among 2–1–1 callers. Nevertheless, our study fills a gap in the literature and to our knowledge, is the first to report on cervical cancer risk and screening among 2–1–1 callers seeking assistance with basic needs.

Conclusions

In summary, women contacting 2–1–1 are likely to have health needs that greatly exceed those of the general population^20,27,28 in addition to lacking financial resources and social support required for obtaining Pap testing. Health navigators double the likelihood that women will make contact with Pap services, but most 2–1–1 callers still fail to schedule Pap testing despite this assistance. These women may require more tailored interventions. Further research is needed to understand how unmet basic needs pose barriers to cervical screening and how effective interventions to meet basic needs may lead to better cancer prevention behavior. Continuing this line of research is critical to improve outcomes for low-income, medically-underserved populations. No woman should die from a preventable cancer.

AJOG at a Glance:

Why was the study conducted?

• Little is known about the impact of unmet basic needs on adherence to cervical cancer screening.

• Improved access to cancer preventive care is critical to reduce health inequities.

What are the key findings?

• 2–1–1 callers seeking assistance with unmet basic needs often lack cervical cancer screening.

• Women in the navigator group reported higher rates of contacting a Pap referral than those exposed to verbal referral only or verbal referral+tailored print reminder.

What does the study add to what is already known?

• Health navigators double the likelihood that women will make contact with Pap, but most 2–1–1 callers still fail to schedule Pap testing despite navigator assistance.