Primary Human Papillomavirus Screening: Women’s Perceptions of New Cervical Cancer Screening Recommendations

Abstract

Background:

Current clinical guidelines recommended primary human papillomavirus (HPV) screening for cervical cancer testing. Previous studies reported patient-level barriers (e.g., limited knowledge and attachment to Pap test) that may hinder wide adoption of primary HPV screening. We assessed these women-level factors following the implementation of primary HPV screening (July 2020) at Kaiser Permanente Southern California (KPSC).

Methods:

We administered a patient survey (mail and on-line) to female KPSC members aged 30–65 years who received primary HPV screening between October and December 2020. Those who preferred English vs. Spanish language were sampled separately. The survey included domains on knowledge about HPV and HPV screening, awareness of screening guidelines, and attitudes about HPV testing. Demographic data were collected using electronic health records. We used weighted multivariable logistic and modified Poisson regressions for associations between language preference and survey responses.

Results:

In total, 3,009 surveys were returned (38.0% response rate). Few women (7.0%) found HPV testing as an acceptable screening method. The majority of women (92.2%) remained unaware that HPV testing can replace Pap test for screening. The Pap test was the most preferred screening approach for 33.2% Spanish-speaking women vs. 19.9% English-speaking women. Only 20.6% knew that women aged 30–65 years can be screened every 5 years with cotest or primary HPV screening. Most women (96.4%) did not perceive stigma about taking the HPV test.

Conclusion:

Proactive patient education will help improve women’s knowledge about primary HPV screening, which may facilitate its implementation in additional health care settings.

Introduction

In 2018, the U.S. Preventive Service Task Force recommended primary human papillomavirus (HPV) screening as an effective screening strategy for women aged 30–65 years.¹ Primary HPV screening uses HPV test as the initial screening test, and depending on the HPV test result, a Pap test may be used as a reflex test to determine follow-up. Primary HPV screening is more sensitive^2

–7 and reliable^7
–9 for detection of severe precancerous lesions than Pap testing, and is as effective as Pap and HPV cotesting.^1,10

–13 Similar to cotesting, primary HPV screening safely prolongs screening intervals to screening every 5 years.^1,14

Despite strong evidence and endorsement by multiple national guideline organizations, uptake of primary HPV screening has been limited in the United States.¹⁵ The slow adoption of primary HPV screening in the United States could be owing to multilevel barriers at the health system, provider, and patient levels. Patient-level implementation barriers for primary HPV screening include low levels of awareness of primary HPV screening¹⁶ concern regarding the extended screening interval (5-year interval),^17

–20 stigma associated with a positive HPV test,^21,22 attachment to Pap test,^23,24 and viewing the transition from cotesting to primary HPV screening as a means to save cost²⁴ resulting in concerns regarding quality of care.²³ In addition, limited health literacy can also be a barrier for women to understand the relationship between HPV and cervical cancer.^25,26 Therefore, a multitude of patient-level barriers may have a negative impact on the implementation of primary HPV screening.

Recent studies highlighted women’s lack of understanding of primary HPV screening, despite being screened with this approach. Findings from two qualitative British interview studies and a cross-sectional survey of Canadian women indicated a need for more information on the association between HPV and cervical cancer; the purpose of HPV testing in cervical cancer screening (CCS); implications of a positive HPV test; and patient education regarding the longer screening interval and effectiveness.^22,27,28 Another study done in England suggested that women who undergo primary HPV screening might experience anxiety and distress because they do not understand the implications of a positive HPV test result.

Although previous studies offer important insights on educational strategies to facilitate acceptance and improve patient experience of primary HPV screening, study populations from England and Canada may not be readily generalizable to the US population. In California, for example, a considerable proportion (26.9%) are primary Spanish speakers.^29,30 Spanish speakers have been shown to have lower knowledge and awareness about the association between HPV and cervical cancer, HPV vaccine, and the importance of screening compared to English-speaking women.³⁰ In addition, lower level of general health literacy among minority women may also post a potential barrier for acceptance of new screening approach such as primary HPV screening. Previous studies have found that fundamental literacy is low among Spanish speakers about words commonly used in cervical cancer screenings (CCSs), such as pap smear.³¹ When compared to Spanish-speaking women with adequate health literacy, Spanish-speaking women with low health literacy were less likely to get a Pap smear.³² Past studies highlight a need for large scale studies among diverse US women who received primary HPV screening to assess women’s knowledge and perception related to this new screening approach.

In July 2020, Kaiser Permanente Southern California (KPSC) implemented primary HPV screening for routine CCS for women aged 30–65 years. We conducted a survey among women who received primary HPV screening at KPSC to measure patient knowledge, awareness, attitudes, and perceptions associated with primary HPV screening. Here we report findings from this survey to inform US women’s potential educational needs to enhance acceptance and care experience of primary HPV screening.

Methods

Study setting and study population

This study was conducted at KPSC, a large integrated health care delivery system in Southern California. KPSC provides care to 4.7 million members who are racially and socioeconomically diverse and broadly representative of Southern California residents.³³ The study population consisted of female KPSC members aged 30–65 years who received a recent (within the past 30 days before recruitment) primary HPV screening for their routine CCS from their primary care or obstetrics and gynecology provider and had a negative test result. We only included women with negative test result since their knowledge level would reflect the average women who have undergone a routine primary HPV screening visit, whereas women who tested HPV-positive may seek additional self-education or receive more education from clinicians to explain the positive result. Two different sampling methods were used for English and Spanish language preferred women. Simple random sampling was used to identify potential study participants whose preferred written language was English. For Spanish language preferred women, everyone who received primary HPV screening in the study window were included (since there were much fewer Spanish-preferred women than English-preferred women). Although data from the administrative database on “preferred spoken language” was available, we chose preferred written language since we used a self-administered survey that was available in English and Spanish. Hereafter, women who preferred English written language will be referred to as “English speakers” and Spanish written preferred as “Spanish speakers.” Women were excluded if their preferred written language was other than English or Spanish since surveys in other languages were unavailable. This study was approved by the KPSC Institutional Review Board (IRB).

Survey development & outcome measures

The survey included the following domains: “Awareness and knowledge about Human Papillomavirus (HPV),” “Awareness and Attitude about Cervical Cancer Screening”, and “Shame and Stigma” in taking an HPV test and receiving a positive test result (see Supplementary Appendix S1). These domains were identified by patient stakeholders involved in study decision-making as important patient-centered outcomes for successful transition to primary HPV screening. All patient stakeholders were invited by email to attend a focus group to discuss patient survey questions. All invited patient stakeholders (three KPSC members and one non-KPSC member) attended the focus group to review patient-level barriers for the implementation of primary HPV screening for routine CCS. The list was based on a comprehensive literature review. After identifying the relevant domains, we conducted a literature review to identify validated survey questions. For the survey, we adopted validated or published survey questions when possible.^21,34

–37 The patient survey included a combination of Likert scale and multiple-choice questions (see Supplementary Appendix S1). We also included a question about source of information, “Where would you go if you would like to learn about cervical cancer screening tests and/or protocol?” and preferred communication regarding changes to care, “When changes are made to my preventive care, including changes to cervical cancer screening, I would like the change to be communicated via. . . . .” We also asked respondents to provide their highest education level and current marital status.

The final survey was reviewed by patient stakeholders for readability and face validity. The survey was translated into Spanish by a certified language translation vendor. Both the English and the Spanish surveys were piloted with two to three bilingual research staff and cross-checked for consistency between those two languages.

Electronic health record data

We identified eligible female members for the survey using KPSC’s electronic health records. Information of the women’s age, race/ethnicity, preferred written language, preferred spoken language, email address, home address, length of KPSC membership, and insurance type was obtained from the membership file. Women’s CCS history was obtained from utilization files using CPT procedure codes. The 2020 US Census data was used to obtain information on neighborhood income level.

Survey administration

We administered the survey between October and December 2020. Survey invitations were sent by mail and email with up to five reminders. Individuals were given the option to complete an online survey or hard-copy (enclosed with the recruitment letter). For the online survey, we used the Research Electronic Data Capture (RedCap) platform which is a secure web application for the development and management of online surveys.³⁸ Individuals who completed the survey received a $20 gift card.

Statistical analysis

We described the socio-demographic characteristics of the study respondents overall and by written language preference (English or Spanish). We also compared the socio-demographic characteristics of respondents and non-respondents (see Supplementary Appendix S2). The descriptive analyses for the patient characteristics, survey responses, and regression models were conducted using both unweighted and weighted approaches based on the survey response weight. Survey response weight was derived from a logistic regression including race/ethnicity, age, length of KP membership and insurance type. The weighted analysis was intended to reflect the population of interest—Kaiser Permanente health plan members who received primary HPV screening, aged 30–65 years old.

To inform the planned analyses, we examined weighted survey responses for all women, and for the following three subgroups: English speakers (non-Hispanic women), English speakers (Hispanic women), and Spanish speakers (Hispanic women) to evaluate whether it was necessary to account for Hispanic ethnicity beyond language preference for capturing meaningful variations in survey responses. With the exception of one question, “Which of the following cervical cancer screening options is acceptable to you?” (see Supplementary Appendix S3), the survey responses were mostly similar between English speaker non-Hispanic women and English speaker Hispanic women. Because of the similarity in their survey responses, we did not separate English speaker women who were of Hispanic ethnicity vs. those who were not of Hispanic ethnicity in the final analyses. The distributions of survey responses were then calculated by language preference and compared between the English and Spanish speaking women using chi-square tests.

We examined the outcomes of interest for the three domains, “Awareness and Knowledge about Human Papillomavirus,” “Awareness and Attitude about Cervical Cancer Screening,” “Perception (Shame and Stigma).” The responses to Likert questions (e.g., “How familiar are you with cervical cancer screening guidelines”) were combined to create two response categories (very familiar/familiar/somewhat familiar vs. not familiar). Other Likert questions were also combined when the response categories were qualitatively similar (i.e., “strongly disagree/disagree” and “strongly agree/agree”). The responses from the “perception” domain were combined to create dichotomized categories (i.e., agree vs. disagree or familiar vs. not familiar). Questions about “awareness and knowledge about HPV,” “don’t know” was combined with the incorrect answers (correct vs. incorrect/don’t know).

We used modified Poisson regression model to evaluate the adjusted associations between language preference and survey responses. In this model, responses were recategorized to compare responses of interest (i.e., Pap test vs. others). For the HPV knowledge score, the response options were recoded as correct or incorrect (including “don’t know”). The HPV knowledge score was obtained by converting Q2–Q9 responses into a score (correct responses were summed for a score) (see Supplementary Appendix S4). Data from incomplete surveys were excluded from analysis. There was minimal missing data.

As all of the outcomes of interest are common (>10%), we used the weighted Poisson regression model with robust standard errors to estimate the associations. Covariates included in the Poisson regression model were age, income, marital status, length of KP membership, and insurance type. We also used logistic regression on the HPV and cervical cancer knowledge score (dichotomized) which included the same covariates used in the Poisson regression model. Key outcomes from each of the three domains were examined in the Poisson regression model.

Results

Socio-demographic characteristics

The demographic characteristics between the nonrespondents and respondents were similar (see Supplementary Appendix S3). The overall response rate was 38% (32% Spanish and 42% English). The analytic sample consisted of 2,617 English and 392 Spanish speaking women. Compared to English speakers, Spanish speakers were on average, older, less educated, married, and had a shorter number of years as a Kaiser Permanente member. Also, compared to English speakers, Spanish speakers reported lower annual income. Spanish speakers were twice as likely to report having Medicaid compared to their English-speaking counterparts (12.9% vs. 6.7%) (see Table 1).

Table 1.

Demographic Characteristics of English and Spanish Speakers (N = 3009)^a

Variable	Total	English Speakers Weighted	Spanish Speakers Weighted	p-value
	3,009	2,617	392
Race/Ethnicity				<0.0001
Hispanic	1,375 (45.7%)	983 (37.6%)	392 (100%)
Non-Hispanic White	884 (29.4%)	884 (33.8%)	0 (0%)
Other	751 (24.9%)	751 (28.7%)	0 (0%)
Age				<0.0001
30–39	1,014 (33.7%)	980 (37.4%)	34 (8.6%)
40–49	734 (24.4%)	622 (23.8%)	112 (28.6%)
50–59	853 (28.3%)	679 (25.9%)	174 (44.4%)
60–69	409 (13.6%)	336 (12.9%)	72 (18.4%)
Age (Mean in Years, SD)	46.2 (10.65)	45.4 (13.20)	51.4 (4.56)	<0.0001
Neighborhood Income Level^b				<0.0001
<$25,000	9 (0.3%)	7 (0.3%)	2 (0.4%)
$25,000–$49,999	361 (12%)	302 (11.5%)	108 (27.6%)
$50,000–$74,999	515 (17.1%)	715 (27.3%)	165 (42.1%)
$75,000–$99,999	1,169 (38.9%)	771 (29.4%)	87 (22.2%)
>$100,000	954 (31.7%)	819 (31.3%)	30 (7.7%)
Educational Attainment (% With Bachelor’s Degree or Higher)	30.6 (18.51)	32.3 (22.86)	18.8 (7.07)	<0.0001
Marital Status				<0.0001
Single	673 (22.4%)	634 (24.2%)	39 (9.9%)
Married	1,894 (62.9%)	1,596 (61%)	298 (76.1%)
Divorced	298 (9.9%)	270 (10.3%)	27 (6.9%)
Widowed	49 (1.6%)	33 (1.3%)	16 (4.2%)
Other/Prefer not to answer	95 (3.2%)	84 (3.2%)	11 (2.9%)
Length of KP Membership (Mean in Years)	5.2 (3.84)	5.3 (4.71)	4.7 (2.14)	0.040
Insurance Type				0.000
Commercial Insurance	2,704 (89.9%)	2,376 (90.8%)	329 (83.9%)
Medicaid	227 (7.5%)	177 (6.7%)	50 (12.9%)
Medicare	75 (2.5%)	63 (2.4%)	13 (3.3%)
Other	2 (0.1%)	2 (0.1%)	0 (0%)

Analyses were limited to women aged 30–65 years old who received a primary HPV screening exam within the past 30 days. Percentages were weighted to match the 2020 KPSC female members for race/ethnicity, age, education, marital status, length of membership, and insurance.

2020 US Census Data.

HPV, human papillomavirus.

Awareness and knowledge about HPV

Overall, 32.3% of women did not know that an HPV infection can cause an abnormal Pap test: 31.2% of English speakers and 40% of Spanish speakers (p = 0.002, Table 2). Most women (92.2%) were also unaware that primary HPV testing can replace the Pap test: English speakers 93.2% and 85.3% of Spanish speakers (p < 0.0001). Over a third of the women (34.3%) thought that HPV testing was done only to diagnose sexually transmitted disease. More Spanish speakers believed this to be true compared to English speakers (51.7% vs. 31.8%, p < 0.0001). A third (28.5%) of women also thought HPV was rare: 38.6% of Spanish speakers and 27.1% English speakers (p < 0.001). Over half (55.3%) of the respondents did not know there were “many types of HPV” with Spanish speakers having less awareness compared to English speakers (67.2% vs. 53.6%, p < 0.0001). Over half of all women (53.5%) correctly answered 3–5 questions on HPV awareness and knowledge. Less than a quarter of all women answered 6–8 questions correctly. English speakers (25.1%) answered 6–8 questions correctly compared to the Spanish preferred (16.2%) (see Supplementary Appendix S4), (p = 0.005). However, language was not a statistically significant predictor in the multivariable logistic regression for HPV knowledge score.

Table 2.

Awareness and Knowledge about Human Papillomavirus (HPV)^a

Questions	Total Weighted	English Speakers Weighted n(%)	Spanish Speakers Weighted n(%)	p-value
	3,009	2,617	392
1. Have you heard of human papillomavirus (HPV)?				0.205
Yes	2,670 (89.1%)	2,331 (89.4%)	339 (87.2%)
No/Don’t Know	326 (10.9%)	276 (10.6%)	50 (12.8%)
2. Do you think HPV causes cervical cancer?				0.697
Yes	2,016 (67.6%)	1,763 (67.6%)	253 (67.1%)
No/Don’t Know	968 (32.4%)	844 (32.4%)	124 (32.9%)
3. Can HPV infections cause an abnormal Pap test?				0.002
Yes	2,004 (67.7%)	1,780 (68.8%)	224 (60%)
No/Don’t Know	955 (32.3%)	806 (31.2%)	149 (40%)
4. If an HPV test shows that a woman does not have HPV, her risk of cervical cancer is low	0.05			0.050
True	985 (33.1%)	844 (32.5%)	141 (36.8%)
False/Don’t Know	1,993 (66.9%)	1,751 (67.5%)	242 (63.2%)
	<0.00
5. Testing for HPV can replace the Pap test to screen for cervical cancer	232 (7.8%)			<0.0001
True	232 (7.8%)	176 (6.8%)	56 (14.7%)
False/Don’t Know	2,754 (92.2%)	2,430 (93.2%)	325 (85.3%)
6. Testing for HPV is only for diagnosing sexually transmitted diseases				<0.0001
True/Don’t Know	1,023 (34.3%)	826 (31.8%)	197 (51.7%)
False	1,956 (65.7%)	1,773 (68.2%)	184 (48.3%)
7. HPV is very rare				<0.0001
True/Don’t Know	849 (28.5%)	703 (27.1%)	146 (38.6%)	849 (28.5%)
False	2,127 (71.5%)	1,895 (72.9%)	232 (61.4%)	2,127 (71.5%)
8. There are many types of HPV				<0.0001
True	1,326 (44.7%)	1,205 (46.4%)	121 (32.8%)	1,326 (44.7%)
False/Don’t Know	1,641 (55.3%)	1,392 (53.6%)	249 (67.2%)	1,641 (55.3%)
9. Most sexually active people will get HPV at some point in their lives				0.821
True	958 (32.2%)	833 (32.1%)	125 (32.9%)	958 (32.2%)
False/Don’t Know	2,019 (67.8%)	1,764 (67.9%)	256 (67.1%)	2,019 (67.8%)

Analyses were limited to women aged 30–65 years old who received a primary HPV screening exam within the past 30 days. Percentages were weighted to match the 2020 KPSC female members.

Awareness and attitude about cervical cancer screening

Women were also largely unaware about the recommended CCS interval for 30–65 years old; only 20.6% knew that 30- to 65-year-old women are supposed to be screened every 5-years with cotest or primary HPV screening (see Table 3). There was a large discrepancy between English and Spanish speaking women regarding CCS intervals: 12.2% of Spanish speakers chose “every 5 years” compared to 21.8% of the English speakers (p < 0.0001). Over half of women (58.9%) thought they had received a Pap test at their recent CCS exam. When asked “which cervical cancer screening option is acceptable to you,” only 6.9% chose “HPV test alone”: 2.5% of Spanish speakers and 7.5% English speakers (p < 0.0001). Among Spanish speakers, the Pap test was the most acceptable (33.2%) compared to 19.9% of English speakers (p < 0.0001) (Table 3). Most Spanish speakers (61.1%) also preferred the Pap test even if their provider recommend a “better test,” compared to 32.3% of English speakers (p < 0.0001). Most women (76.7%) trusted their provider for recommending the “best test” for CCS. However, Spanish speakers were less likely to trust their provider’s recommendation compared to the English speakers (65.5% vs. 78.2%, p < 0.0001). More Spanish speaking women also felt “nervous” about changes to CCS tests compared to the English-speaking women (49.9% vs. 34.2%, p < 0.0001). A majority of women (77.3%) felt “confident” that changes to CCS were made by the health care organization to improve patient care.

Table 3.

Awareness and Attitude about Cervical Cancer Screening^a

Questions	Total Weighted	English Speakers Weighted n(%)	Spanish Speakers Weighted n(%)	p-value
	3009	2617	392
10. How familiar are you with cervical cancer screening guidelines?				0.916
Not familiar	891 (30%)	771 (29.7%)	120 (32.2%)
Very familiar/Familiar/Somewhat Familiar	2,075 (70%)	1,823 (70.3%)	253 (67.8%)
11. Do you know how often you are supposed to get screened for cervical cancer?				<0.0001
Every year	652 (22%)	503 (19.5%)	149 (39.1%)
Every 2 years	548 (18.5%)	474 (18.4%)	74 (19.2%)
Every 3 years	555 (18.7%)	505 (19.5%)	51 (13.2%)
Every 5 years	610 (20.6%)	564 (21.8%)	47 (12.2%)
I don’t know	599 (20.2%)	537 (20.8%)	62 (16.2%)
12. Do you know which test was performed for the cervical cancer screening at your recent visit?				<0.0001
Pap test	1,742 (58.9%)	1,460 (56.6%)	281 (74.1%)
human papillomavirus (HPV) test	147 (5%)	139 (5.4%)	8 (2.2%)
Pap test and HPV test at the same time (co-test)	663 (22.4%)	617 (23.9%)	46 (12.1%)
None of these	16 (0.5%)	10 (0.4%)	6 (1.6%)
I don’t know	390 (13.2%)	352 (13.7%)	38 (10.1%)
13. Which of the following cervical cancer screening options is acceptable to you?				<0.0001
Pap test alone	651 (21.6%)	521 (19.9%)	130 (33.2%)
HPV test alone	206 (6.9%)	197 (7.5%)	10 (2.5%)
Pap test followed by HPV test if Pap result is not normal	1,157 (38.5%)	1,053 (40.2%)	104 (26.6%)
Pap test and HPV test at the same time	1,035 (34.4%)	943 (36%)	92 (23.4%)
None of these	46 (1.5%)	44 (1.7%)	3 (0.6%)
I don’t know	415 (13.8%)	351 (13.4%)	64 (16.4%)
14. I trust that my provider has recommended the best test to screen for cervical cancer.				<0.0001
Strongly Disagree/Disagree	244 (8.2%)	193 (7.5%)	51 (13.5%)
Strongly Agree/Agree	2,279 (76.7%)	2,031 (78.2%)	248 (65.5%)
Uncertain	451 (15.2%)	371 (14.3%)	80 (21%)
15. I would feel better having a Pap test, even if my doctor told me that some other test was better for cervical cancer screening.				<0.0001
Strongly Disagree/Disagree	889 (30.1%)	807 (31.3%)	82 (22%)
Strongly Agree/Agree	1,061 (35.9%)	831 (32.3%)	229 (61.1%)
Uncertain	1,004 (34%)	940 (36.5%)	63 (16.9%)
16. I get nervous when there are changes to the way my care is provided, including changes to cervical cancer screening tests.				<0.0001
Strongly Disagree/Disagree	1,262 (42.6%)	1,139 (43.9%)	123 (33.5%)
Strongly Agree/Agree	1,072 (36.2%)	888 (34.2%)	184 (49.9)
Uncertain	627 (21.2%)	565 (21.8%)	62 (16.7%)
17. I am confident that changes made to my preventive care by Kaiser Permanente, including changes to cervical cancer screening, are made to achieve better patient care.				<0.0001
Strongly Disagree/Disagree	175 (6.0%)	133 (5.2%)	41 (11.2%)
Strongly Agree/Agree	2,275 (77.3%)	1,978 (76.8%)	296 (80.2%)
Uncertain	493 (16.8%)	462 (17.9%)	32 (8.6%)

Analyses were limited to women aged 30–65 years old who received a primary HPV screening exam within the past 30 days. Percentages were weighted to match the 2020 KPSC female members.

In the multivariable models evaluating the adjusted relationship between language preference and measures of awareness and attitude about CCS, all differences described above remained statistically significant, except for the question about the acceptable option for CCS (Table 4).

Table 4.

Associations Between Language and Cervical Cancer Screening Survey Questions.

Survey questions (n = 1157)	Adjusted weighted robust Poisson rate ratio	p-value
Awareness and Attitude about Cervical Cancer Screening
11. Do you know how often you are supposed to get screened for cervical cancer? (n = 1102)Every 5 years (correct answer) vs. Every year/Every 2 years/Every 3 years/I don’t know	0.64 (0.46, 0.88)	0.007
13. Which of the following cervical cancer screening options is acceptable to you? (n = 836)human papillomavirus (HPV) test/Pap test followed by HPV/Pap test and HPV test at same time vs. Pap test/None of these/I don’t know	1.27 (0.92, 1.76)	0.145
14. I trust that my provider has recommended the best test to screen for cervical cancer. (n = 1101)Disagree/Strongly disagree/Uncertain vs. Agree/Strongly agree	0.57 (0.46, 0.72)	<0.0001
15. I would feel better having a Pap test, even if my doctor told me that some other test was better for cervical cancer screening. (n = 1094)Disagree/Strongly disagree/Uncertain vs. Agree/Strongly agree	2.04 (1.61, 2.57)	<0.0001
16. I get nervous when there are changes to the way my care is provided, including changes to cervical cancer screening tests. Disagree/Strongly disagree/Uncertain vs. Agree/Strongly agree	1.45 (1.13, 1.87)	0.004
Perception
18. If I take the HPV test, people would think poorly of me. (n = 793)Disagree/Strongly disagree vs. Agree/Strongly agree	1.86 (1.17, 2.94)	0.008
20. If I test positive for HPV, people would think poorly of me. (n = 785)Disagree/Strongly disagree vs. Agree/Strongly agree	1.22 (0.85, 1.75)	0.287
22. If you take the HPV test, how embarrassed would you feel? (n = 1000)Not at all vs. Somewhat/Quite/Very	0.82 (0.63, 1.06)	0.131
23. If you test positive for HPV, how embarrassed would you feel? (n = 951)Not at all vs. Somewhat/Quite/Very	0.66 (0.51, 0.86)	0.002

Results are based on Poisson regression model using data on English speakers as the reference groupa

Analyses were limited to women aged 30–65 years old who received a primary HPV screening exam within the past 30 days.

With regards to the preferred channels for learning about changes made to preventive care, “verbal communication from the provider at the office visit” was the most common choice: Spanish 56.1% and English 58.2%. Among Spanish speakers the second most common was “KPSC Newsletter in the mail” (41.4%). English speakers second choice was “email from doctors office” (56.3%). Women also reported that physician was their top choice for learning about CCS tests: Spanish 87.2% and 80.8% English. Spanish and English speakers second most common choice was their KP.org account.

Perception (shame and stigma)

Women’s emotional reaction toward taking an HPV test and/or receiving a positive test result were mixed depending on language preference. Overall most women (96.4%) did not think that people perceive them poorly if they took an HPV test; 87.5% did not think people would think poorly of them if they tested HPV positive; and 64.1% did not would feel embarrassed to take an HPV test (see Table 5). Approximately, 54.5% of women would feel “embarrassed” for testing HPV positive. However, English and Spanish speakers had differences in their responses regarding their perception of shame and stigma in taking an HPV test and/or receiving a positive HPV test result. As compared to English speakers, more Spanish speakers thought other people would think “poorly” of them if they “took the HPV test” (2.6% vs. 8.7%, p < 0.001). Also compared to English speakers more Spanish speakers thought their “spouse or partner would get angry by taking an HPV test” (2.1% vs. 4.5%, p = 0.004). When asked about feeling “embarrassed” for taking an HPV test, there were more English speakers who would feel embarrassed (37.1% vs. 27.8%, p = 0.029). English speakers were also more likely to feel embarrassed if they received a positive HPV test result compared to Spanish speakers (57.2% vs. 36%, p < 0.0001).

Table 5.

Perception^a

Questions	Total	English Speakers Weighted n(%)	Spanish Speakers Weighted n(%)	p-value
	3,009	2,617	392
18. If I take the human papillomavirus (HPV) test, people would think poorly of me				<0.0001
Strongly Disagree/Disagree	1,909 (96.4%)	1,609 (97.4%)	299 (91.3%)
Strongly Agree/Agree	72 (3.6%)	43 (2.6%)	29 (8.7%)
Not applicable	0 (0.0%)	0 (0.0%)	0 (0.0%)
19. If I take the HPV test, my spouse or partner would get angry at me				0.004
Strongly Disagree/Disagree	1,855 (91.3%)	1,554 (92.1%)	301 (79.7%)
Strongly Agree/Agree	51 (2.5%)	35 (2.1%)	15 (4.5%)
Not applicable	125 (6.2%)	98 (5.8%)	27 (7.9%)
20. If I test positive for HPV, people would think poorly of me				<0.0001
Strongly Disagree/Disagree	1,716 (87.5%)	1,438 (87.9%)	277 (85.6%)
Strongly Agree/Agree	246 (12.5%)	199 (12.2%)	1,146 (14.3%)
Not applicable	0 (0.0%)	0 (0.0%)	0 (0.0%)
21. If I test positive for HPV, my spouse or partner would get angry at me				0.050
Strongly Disagree/Disagree	2,305 (82.1%)	2,064 (82.5%)	241 (79.7%)
Strongly Agree/Agree	256 (9.1%)	225 (8.9%)	31 (10.2%)
Not applicable	244 (8.7%)	213 (8.5%)	31 (10.1%)
22. If you take the HPV test, how embarrassed would you feel?				0.029
Not at all	1,725 (64.1%)	1,474 (62.9%)	316 (91.2%)
Somewhat/Quite/Very	968 (35.9%)	872 (37.1%)	30 (8.8%)
Not applicable	0 (0.0%)	0 (0.0%)	0 (0.0%)
23. If you test positive for HPV, how embarrassed would you feel?				<0.0001
Not at all	1,166 (45.5%)	958 (42.8%)	207 (64%)
Somewhat/Quite/Very	1,395 (54.5%)	1,279 (57.2%)	117 (36%)
Not applicable	0 (0.0%)	0 (0.0%)	0 (0.0%)

Analyses were limited to women aged 30–65 years old who received a primary HPV screening exam within the past 30 days. Percentages were weighted to match the 2020 KPSC female members.

In the adjusted Poisson regression model (see Table 4), Spanish speakers were 1.86 times more likely to believe “people would think poorly” of them by taking the HPV test (Adj RR = 1.86, 95% CI = 1.17–2.94, p = 0.008). Conversely, Spanish speakers were less likely to feel “embarrassed” if they tested positive for HPV (Adj RR = 0.66, 95% CI = 0.51–0.86, p = 0.002).

Discussion

In light of the recent changes in the US CCS guidelines and recent implementation of primary HPV screening in some health systems, this study surveyed women who recently received primary HPV screening. We found that only a minority of women (∼7%) found primary HPV screening to be an acceptable method. A high proportion of women did not understand the role of HPV testing in CCS, and had outdated understanding of CCS guidelines. We also learned that most women in hypothetical situations would not feel shame or embarrassment for taking the HPV test, although a considerable proportion of women reported the feeling of embarrassment if they were to test positive for HPV, indicating an area that could benefit from intervention. In the adjusted analysis, Spanish language preference was a significant predictor for less awareness of screening guideline, more attachment to Pap test, less trust in providers, and more stigma associated with HPV testing. Taken together, these findings highlight the need for patient education around HPV and its role in CCS, including cultural sensitivity and language appropriate patient education during the implementation phase of primary HPV screening to optimize patient experience, address potential concerns, and mitigate patient resistance.

Our findings highlight a knowledge gap among women regarding HPV and cervical cancer, despite public health efforts to increase this awareness and knowledge. These findings are similar to those from previous studies^16,27 suggesting no significant improvement in women’s knowledge over the years. Our study again demonstrates the need to provide education on HPV, HPV-related cancers, screening with HPV test, and HPV vaccination. In a study of English women who had received primary HPV screening, most women, regardless of education level, reported poor knowledge of HPV, HPV testing, and the meaning of their test results.²⁸ In fact, 40% of women with a negative test result wanted more information regarding HPV testing and how it fits with primary HPV screening²⁸ and many women in the study were uninformed and unaware they had received primary HPV screening. Similarly, more than 50% of women in our study mistakenly thought they had received the Pap test alone when they had received primary HPV screening. The limited knowledge about HPV, HPV testing, and primary HPV screening suggests that providers and health care organizations should prioritize educating women during the initial stages of implementation. Improving health literacy should also be prioritized since studies have shown there is a positive association between HPV knowledge/awareness and acceptance of primary HPV screening.³⁹ Higher levels of health literacy (specifically regarding HPV), therefore, may alleviate patient anxiety, reduce patient confusion, and the inquiries that providers receive about the HPV test result.

Our findings are consistent with previous studies on women’s perception of primary HPV screening. In Saraiya et al, primary HPV screening was the least accepted option for CCS (13.5%) among women who responded to the 2015 HealthStyles Fall Survey (an annual survey which explores the health behaviors and attitudes of American adults).¹⁶ A survey study conducted between 2014 and 2016 on CCS preference among women attending health clinics in San Francisco, California also found that only 5.3% of the study respondents chose HPV testing.⁴⁰ Both studies suggest that women’s perception of primary HPV testing has not changed much since 2014. However women’s willingness to accept primary HPV screening can be as high as 55% if they are provided with information comparing HPV based CCS to the Pap test.⁴¹ At this time, however, low levels of awareness about primary HPV screening continue to exist. Our survey findings are similar to findings from earlier studies where a majority of women were unaware of primary HPV screening and the 5-year screening interval.^{16,17,19,20,42} These data suggest that educational information to help women understand the benefits of primary HPV (i.e., efficacy and longer screening intervals) may facilitate overcoming this low level of acceptance.^43,44 A previous study demonstrated that presenting women with an educational video and exercises thinking about the different CCSs could help them understand that annual screenings are unnecessary.⁴⁰ Similar interventions may be helpful in improving knowledge and acceptance of primary HPV screening, potentially focusing on its sensitivity to identify the main cause of cervical cancer (HPV 16/18) and women at highest risk. Helping women understand the role of reflex Pap test in the primary HPV screening algorithm may also help with women’s acceptance give women’s attachment to Pap test, which may be particularly helpful to the Spanish-preferred women.

Providers are crucial in helping patients accept primary HPV screening. Patients are more willing to accept longer screening intervals if recommended by their provider^16,20,41 and provider-focused educational interventions have been found to be effective in aligning recommendations with updated guidelines.⁴⁵ In our study, we learned that most women preferred learning about changes to CCSs from their providers. To this end, a previous study found that three-quarters of the women surveyed reported that having a provider recommendation would facilitate their decision to have HPV-based CCS over the Pap test.⁴¹ Therefore, providers should be given adequate education about primary HPV screening before the implementation effort, as well as training or support to enable providers to address patient questions/concerns (such as synchronous patient–provider communication)²⁵ regarding the change from cytology to HPV-based screening effectively and efficiently. Synchronous patient-provider communication will allow patients to ask questions and providers to asses patient understanding of the screening test.²⁵ In addition, newsletters or individualized letters from provider’s office or patient education materials presented at the clinic may also be useful methods for delivering patient education without taking time away from the clinic visit.

Spanish speakers reported lower levels of provider trust compared to English speakers. Provider distrust among Spanish speakers maybe owing to language barriers and lack of cultural understanding by the providers. As Spanish speakers in our study had higher levels of being “nervous” regarding changes to CCS tests compared to their English-speaking counterparts, provider-level interventions such as providing culturally sensitive care could be considered to improve provider–patient communication and cultural understanding to facilitate trust.^46,47

Our study findings showed that most women would not feel shame or experience stigma for taking an HPV test or receiving an HPV positive test result. We noted that more Spanish speakers perceived HPV testing to be stigmatizing. One explanation is that more Spanish speakers may believe that HPV tests are “only” for diagnosing STD (as demonstrated in this study) and thus associate HPV test to be stigmatizing. Women may also fear that a positive HPV test could lead to accusations of infidelity and abandonment by their spouse or partner. As literature suggest that culture and gender roles make it difficult for some Spanish speaking women to attend gynecological exams,^46,48 cervical cancer exams based on an HPV test could further exacerbate this problem. However, an unexpected finding was that Spanish speakers (36%) were less likely to feel embarrassed compared to English speakers (57.2%) if they tested positive for HPV. This is contrary to previous literature which suggests that shame is identified among non-white ethnic women who test positive for HPV.²² Educational interventions to inform women on what it means to have a positive test result and provider-patient discussions to de-stigmatize primary HPV screening should be encouraged.

Our study is one of the first in the US to examine awareness, attitude, knowledge and perception among women who received primary HPV screening. However, our study has several limitations that should be considered when interpreting our results. First, as in any survey, there may be survey participation bias. However, to this end, we have performed response weighted analysis to help mitigate this concern. Our survey invitation sample focused on those who attended CCS. Our findings may not be generalizable to women who do not regularly attend CCS. Furthermore, our study included women who had a negative test result only which limits our findings and generalizability to women who tested HPV positive. However, as women may receive more education about HPV and HPV screening after testing HPV positive, our study population of women who tested HPV negative may better represent the level of knowledge and perception among average women. The study finding also may not be generalizable to regions outside of Southern California, or to those who are uninsured.

Conclusion

The study highlights the need for continued patient education to improve women’s HPV knowledge, guideline awareness, and perception toward primary HPV screening to facilitate acceptance and adoption of primary HPV screening in the United States. Provider–patient communication and patient education may help reduce concerns and resistance to primary HPV screening. For Spanish speakers who are known to encounter a complex set of barriers (limited language ability, acculturation, beliefs about HPV and CCSs), culturally sensitive, and language appropriate interventions may help to improve awareness and knowledge of primary HPV screening.

Footnotes

Acknowledgments

The authors thank the study participants for their contribution to the knowledge and insights gained. The authors also thank Bhanuja Dub, Talar S. Habeshian, Alejandra E. Montano, Visanee V. Musigdilok, and Justin Tayag from Kaiser Permanente Southern California (KPSC) for assisting with survey data collection.

Authors’ Contributions

N.T.C.: Project administration, resources, writing (original, review/editing); B.S.M.: Methodology, investigation, writing (review/editing); E.E.H.: Methodology, investigation, writing (review/editing); Q.N.M.: Methodology, investigation, writing (review/editing); M.K.G.: Methodology, writing (review/editing); C.H.: Project administration, resources, writing (review/editing); E.S.: Methodology, writing (review/editing); D.T.: Conceptualization, investigation, supervision, funding acquisition, writing (review/editing); C.R.C.: Conceptualization, methodology, investigation, visualization, supervision, funding acquisition, writing (review/editing).

Data Availability Statement

There are no data associated with this article. This study is registered on clinicaltrial.gov.

Author Disclosure Statement

The authors declare no competing interests.

Funding Information

This research was funded through a Patient-Centered Outcomes Research Institute (PCORI) Award (CDR-2018C1-10987).

Supplementary Material

Supplementary Appendix S1

Supplementary Appendix S2

Supplementary Appendix S3

Supplementary Appendix S4

References

Curry

, Krist

, Owens

, et al. Screening for cervical cancer: US preventive services task force recommendation statement. JAMA, 2018; 320(7):674–686; doi: 10.1001/jama.2018.10897

Ronco

, Giorgi-Rossi

, Carozzi

, et al. Efficacy of human papillomavirus testing for the detection of invasive cervical cancers and cervical intraepithelial neoplasia: A randomised controlled trial. Lancet Oncol, 2010; 11(3):249–257; doi: 10.1016/s1470-2045(09)70360-2

Rijkaart

, Berkhof

, Rozendaal

, et al. Human papillomavirus testing for the detection of high-grade cervical intraepithelial neoplasia and cancer: Final results of the POBASCAM randomised controlled trial. Lancet Oncol, 2012; 13(1):78–88; doi: 10.1016/s1470-2045(11)70296-0

Naucler

, Ryd

, Törnberg

, et al. Human papillomavirus and Papanicolaou tests to screen for cervical cancer. N Engl J Med, 2007; 357(16):1589–1597; doi: 10.1056/NEJMoa073204

Mayrand

, Duarte-Franco

, Rodrigues

, et al. Human papillomavirus DNA versus Papanicolaou screening tests for cervical cancer. N Engl J Med, 2007; 357(16):1579–1588; doi: 10.1056/NEJMoa071430

Cuzick

, Clavel

, Petry

, et al. Overview of the European and North American studies on HPV testing in primary cervical cancer screening. Int J Cancer, 2006; 119(5):1095–1101; doi: 10.1002/ijc.21955

Castle

, Stoler

, Wright

Jr , et al. Performance of carcinogenic Human Papillomavirus (HPV) testing and HPV16 or HPV18 genotyping for cervical cancer screening of women aged 25 years and older: A Subanalysis Of the ATHENA Study. Lancet Oncol, 2011; 12(9):880–890; doi: 10.1016/s1470-2045(11)70188-7

Stoler

, Schiffman

, Atypical Squamous Cells of Undetermined Significance-Low-grade Squamous Intraepithelial Lesion Triage Study (ALTS) Group . Interobserver reproducibility of cervical cytologic and histologic interpretations: Realistic Estimates from the ASCUS-LSIL Triage Study. JAMA, 2001; 285(11):1500–1505; doi: 10.1001/jama.285.11.1500

Carozzi

, Del Mistro

, Confortini

, et al. Reproducibility of HPV DNA testing by hybrid capture 2 in a screening setting. Am J Clin Pathol, 2005; 124(5):716–721; doi: 10.1309/84e5-whjq-hk83-bgqd

10.

Saslow

, Solomon

, Lawson

, et al. American cancer society, American society for colposcopy and cervical pathology, and American society for clinical pathology screening guidelines for the prevention and early detection of cervical cancer. CA Cancer J Clin, 2012; 62(3):147–172; doi: 10.3322/caac.21139

11.

Massad

, Einstein

, Huh

, et al. 2012 updated consensus guidelines for the management of abnormal cervical cancer screening tests and cancer precursors. Obstet Gynecol, 2013; 121(4):829–846; doi: 10.1097/AOG.0b013e3182883a34

12.

Chrysostomou

, Stylianou

, Constantinidou

, et al. Cervical cancer screening programs in Europe: The transition towards HPV vaccination and population-based HPV testing. Viruses, 2018; 10(12); doi: 10.3390/v10120729

13.

Austin

, Onisko

, Zhao

. Enhanced detection of cervical cancer and precancer through use of imaged liquid-based cytology in routine cytology and HPV cotesting. Am J Clin Pathol, 2018; 150(5):385–392; doi: 10.1093/ajcp/aqy114

14.

Fontham

ETH

, Wolf

AMD

, Church

, et al. Cervical cancer screening for individuals at average risk: 2020 guideline update from the American Cancer Society. CA Cancer J Clin, 2020; 70(5):321–346; doi: 10.3322/caac.21628

15.

Nayar

. Cervical cancer prevention in the United States-where we’ve been and where we’re going: The American Cancer Society Primary HPV Screening Initiative. Cancer Cytopathol, 2023; 131(12):747–750; doi: 10.1002/cncy.22733

16.

Saraiya

, Kwan

, Cooper

. Primary HPV testing: U.S. women’s awareness and acceptance of an emerging screening modality. Prev Med, 2018; 108:111–114; doi: 10.1016/j.ypmed.2017.12.007

17.

Silver

, Rositch

, Burke

, et al. Patient concerns about human papillomavirus testing and 5-year intervals in routine cervical cancer screening. Obstet Gynecol, 2015; 125(2):317–329; doi: 10.1097/aog.0000000000000638

18.

Nothacker

, Nury

, Roebl Mathieu

, et al. Women’s attitudes towards a human papillomavirus-based cervical cancer screening strategy: A systematic review. BMJ Sex Reprod Health, 2022; 48(4):295–306; doi: 10.1136/bmjsrh-2022-201515

19.

Ogilvie

, Smith

, van Niekerk

, et al. Correlates of women’s intentions to be screened for human papillomavirus for cervical cancer screening with an extended interval. BMC Public Health, 2016; 16:213; doi: 10.1186/s12889-016-2865-8

20.

Ogden

, Glanz

, Schapira

, et al. Patient perspectives on primary HPV testing for routine cervical cancer screening. J Gen Intern Med, 2020; 35(3):956–958; doi: 10.1007/s11606-019-05175-4

21.

Waller

, Marlow

, Wardle

. The association between knowledge of HPV and feelings of stigma, shame and anxiety. Sex Transm Infect, 2007; 83(2):155–159; doi: 10.1136/sti.2006.023333

22.

McBride

, Tatar

, Rosberger

, et al. Emotional response to testing positive for human papillomavirus at cervical cancer screening: A mixed method systematic review with meta-analysis. Health Psychol Rev, 2021; 15(3):395–429; doi: 10.1080/17437199.2020.1762106

23.

Hahn

, Munoz-Plaza

, Altman

, et al. De-implementation and substitution of clinical care processes: Stakeholder perspectives on the transition to primary Human Papillomavirus (HPV) testing for cervical cancer screening. Implement Sci Commun, 2021; 2(1):108; doi: 10.1186/s43058-021-00211-z

24.

Franco

, American Cancer Society’s Primary HPV Screening Initiative . The time has come to implement primary human papillomavirus screening for cervical cancer in the United States. Cancer, 2023; 129(18):2765–2768; doi: 10.1002/cncr.34899

25.

Head

, Johnson

, Scott

, et al. Communicating cervical cancer screening results in light of new guidelines: Clinical practices at federally qualified health centers. Health Commun, 2020; 35(7):815–821; doi: 10.1080/10410236.2019.1593079

26.

Head

, Imburgia

, Zimet

, et al. Women’s understanding of their Pap and HPV test results: Implications for patient–provider communication. J Com Healthcare, 2017; 10(1):37–46; doi: 10.1080/17538068.2017.1282085

27.

Smith

, Racey

, Gondara

, et al. Women’s acceptability of and experience with primary human papillomavirus testing for cervix screening: HPV FOCAL trial cross-sectional online survey results. BMJ Open, 2021; 11(10):e052084; doi: 10.1136/bmjopen-2021-052084

28.

Marlow

, Forster

, McBride

, et al. Information needs among women taking part in primary HPV screening in England: A content analysis. BMJ Open, 2020; 10(12):e044630; doi: 10.1136/bmjopen-2020-044630

29.

US Census Demographic Profile. Available from: https://www.census.gov/

30.

Escobar

, Amboree

, Sonawane

, et al. Human papillomavirus awareness among foreign- and US-born Hispanics, United States, 2017–2018. Prev Med Rep, 2021; 22:101379; doi: 10.1016/j.pmedr.2021.101379

31.

Flores

, Acton

, Arevalo-Flechas

, et al. Health literacy and cervical cancer screening among Mexican-American women. Health Lit Res Pract, 2019; 3(1):e1–e8; doi: 10.3928/24748307-20181127-01

32.

Garbers

, Chiasson

. Inadequate functional health literacy in Spanish as a barrier to cervical cancer screening among immigrant Latinas in New York City. Prev Chronic Dis, 2004; 1(4):A07.

33.

Koebnick

, Langer-Gould

, Gould

, et al. Sociodemographic characteristics of members of a large, integrated health care system: Comparison with US Census Bureau data. Perm J. Summer, 2012; 16(3):37–41.

34.

Cabana

, Rand

, Powe

, et al. Why don’t physicians follow clinical practice guidelines? A framework for improvement. JAMA, 1999; 282(15):1458–1465; doi: 10.1001/jama.282.15.1458

35.

, He

. Knowledge of HPV and acceptability of HPV vaccine among women in western China: A cross-sectional survey. BMC Womens Health, 2018; 18(1):130; doi: 10.1186/s12905-018-0619-8

36.

Dodd

, McCaffery

, Marlow

, et al. Knowledge of Human Papillomavirus (HPV) testing in the USA, the UK and Australia: An international survey. Sex Transm Infect, 2014; 90(3):201–207; doi: 10.1136/sextrans-2013-051402

37.

Thayaparan

, Mahdi

. The Patient Satisfaction Questionnaire short form (PSQ-18) as an adaptable, reliable, and validated tool for use in various settings. Med Educ Online, 2013; 18:21747; doi: 10.3402/meo.v18i0.21747

38.

Capture RED. REDCap Platform. Vanderbilt University Available from: https://projectredcap.org/about/ [Last accessed: December 20, 2023 ].

39.

Kitur

, Horowitz

, Beck

, et al. HPV knowledge, vaccine status, and health literacy among university students. J Cancer Educ, 2022; 37(6):1606–1613; doi: 10.1007/s13187-021-01997-1

40.

Schrier

, Holt

, Kuppermann

, et al. Changing preferences for a cervical cancer screening strategy: Moving away from annual testing. Womens Health Rep (New Rochelle), 2022; 3(1):709–717; doi: 10.1089/whr.2022.0007

41.

Thompson

, Galvin

, Daley

, et al. Recent changes in cervical cancer screening guidelines: U.S. women’s willingness for HPV testing instead of Pap testing. Prev Med, 2020; 130:105928; doi: 10.1016/j.ypmed.2019.105928

42.

Johnson

, Head

, Scott

, et al. Persistent disparities in cervical cancer screening uptake: Knowledge and sociodemographic determinants of papanicolaou and human papillomavirus testing among women in the United States. Public Health Rep, 2020; 135(4):483–491; doi: 10.1177/0033354920925094

43.

Obermair

, Dodd

, Bonner

, et al. ‘It has saved thousands of lives, so why change it?’ Content analysis of objections to cervical screening programme changes in Australia. BMJ Open, 2018; 8(2):e019171; doi: 10.1136/bmjopen-2017-019171

44.

Arbyn

, Gultekin

, Morice

, et al. The European response to the WHO call to eliminate cervical cancer as a public health problem. Int J Cancer, 2021; 148(2):277–284; doi: 10.1002/ijc.33189

45.

van Bodegom-Vos

, Davidoff

, Marang-van de Mheen

. Implementation and de-implementation: Two sides of the same coin? BMJ Qual Saf, 2017; 26(6):495–501; doi: 10.1136/bmjqs-2016-005473

46.

Fleming

, Simmons

, Christy

, et al. Educating hispanic women about cervical cancer prevention: Feasibility of a Promotora-Led Charla intervention in a farmworker community. Ethn Dis, 2018; 28(3):169–176; doi: 10.18865/ed.28.3.169

47.

Bhatia

, Lega

, Wu

, et al. Breast, cervical and colorectal cancer screening in adults with diabetes: A systematic review and meta-analysis. Diabetologia, 2020; 63(1):34–48; doi: 10.1007/s00125-019-04995-7

48.

Knoff

, Harlow

, Yassine

, et al. Cervical cancer screening practice and knowledge among Hispanic migrant and seasonal farmworkers of Michigan. J Prim Care Com Health, 2013; 4(3):209–215; doi: 10.1177/2150131913476303

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.48 MB

0.63 MB

0.44 MB

0.29 MB