Women 50–65 years of age have the lowest cervical cancer screening rate among those 21–65 years of age, as reported in three national surveillance databases: Behavioral Risk Factor Surveillance System (BRFSS), Health Information National Trends Survey (HINTS), and Health Center Patient Survey (HCPS) (Harper et al., 2020). Likewise, women 50–65 years of age also have the lowest colorectal cancer (CRC) screening rates among those 50–75 years of age (American Cancer Society, 2020). Only half of the women in this age group are up to date for both screens, while 25% have cervical only, 12% CRC only, and 12% have neither screen (Harper et al., 2021a). As we have previously reported in the evaluation of women in southeast Michigan, those more likely to be up to date for only cervical cancer screening compared to both CRC and cervical cancer screens are younger women and women of Middle East and North African (MENA) ethnicity (Harper et al., 2021a).

MENA women in southeastern Michigan have become an at-risk hidden population for health care as there is no US Census category that represents their ethnicity on national surveillance health surveys. The Arab immigration to the Detroit area (known as the ‘Arab capital of North America’ [Crowder, 2015] happened over the past century in four waves [Semaan, 2015]) in part due to homeland wars and economic poverty, with an opportunity to relocate for better employment opportunities in the auto-industry in southeastern Michigan. Early Arab immigrants were Christian and primarily from Lebanon, Israel, and Syria (Cumoletti and Batalova, 2018) with later increased immigration by Muslim Arabs from primarily Palestine, Iraq, and Yemen. While Arab immigration to the United States has been increasing year over year since the 1950s, health care indicators such as cervical cancer screening, incidence, or mortality have only been reported for Arab Americans after the September 11, 2001, attacks when an Arab American identity was forged (Seeff and McKenna, 2003; Schwartz et al., 2004).

Over the past two decades, cervical cancer screening rates have improved among MENA women who were significantly less likely to ever receive cervical cancer screening in their lifetime than White women (Dallo and Kindratt, 2015; Yassine et al., 2010) to the most recent report showing near equivalency with White women (Harper et al., 2021a; Harper et al., 2021b). However, while the cervical cancer screening prevalence for MENA women is similar to White women, participation in both CRC and cervical cancer screening differs for MENA women. Instead of half obtaining both cancer screenings, only 18% of MENA women are up to date for both, 50% have cervical cancer screening only, 7% CRC screening alone, and 20% report no screening at all (Harper et al., 2021a).

Personal risk perceptions, and cancer perceptions and knowledge as well as physician communication behaviors, are powerful influencers of screening uptake. In particular, fatalism about cancer leads to less participation in cancer screening programs among White, African American, and Hispanic race/ethnicities (Niederdeppe and Levy, 2007; Chavez et al., 1997). Greater perceptions of self-cancer risk relative to other people have been linked with an increased uptake of CRC screening (Zhao and Nan, 2016; Blalock et al., 1990, Atkinson et al., 2015).

In addition, physician communication behaviors may be a key modifiable determinate of cancer screening behaviors (Peterson et al., 2016) so much so that increasing communication behavior is included as a major objective in the Healthy People 2030 guidelines (HP 2030 Guidelines, 2020). Simple physician recommendations for a prevention intervention have been successful in increasing human papillomavirus (HPV) vaccine uptake (Kempe et al., 2019), CRC screening (Hudson et al., 2012; Atkinson et al., 2015), and cervical cancer screening (Luque et al., 2018). But more specific communication patterns that examine involvement in health care decisions and dealing with women’s feelings of uncertainty might better deconstruct the association with the cancer type and its related screening behaviors.

The primary aim of our study was to determine if CRC and/or cervical cancer screening uptake among the multiethnic sample of White, Black, and MENA women 50–65 years of age from southeast Michigan was associated with personal risk perceptions, cancer risk perceptions, and physician communication behavior.

There were 394 women, average age of 57.7 years (SD 4.5), who completed the CRC and cervical cancer screening questions (Table 2). Women declared their race/ethnicity as 69% White, 19% Black, 9% MENA, and 3% others including Asian/Pacific islander, Hispanic, American Indian, and multi-race. This distribution is very similar to the population distribution of southeastern Michigan, with some over-representation of MENA women (Detroit-Warren-Dearborn MI Census Reporter, 2019). The majority of the study population were Christian, had a college education, were married, had a chronic disease, and had an income between $50,000 and $99,999 also consistent with the median income for southeast Michigan (Detroit-Warren-Dearborn MI Census Reporter, 2019).

Religious affiliation among White women was 65% Christian (including Chaldean, Catholic, Assyrian, Coptic, and Jehovah Witness), 1% Muslim, 14% Jewish, and 29% no religion/no belief in god. Among Black women only two religions were reported, 77% Christian, and 23% no religion/no belief in god. Among MENA women 34% reported being Christian and 66% reported being Muslim.

Among all women, those declaring Muslim religion participated significantly less often in dual cervical cancer and CRC screening than women of other religions (p<0.05, Supplementary file 1 – 'Screening outcomes by total population religion and by MENA ethnicity'). However, among MENA women, neither Muslim nor Christian religions were associated with preferential cervical cancer or CRC screening, with both religions having the greatest percentages in the cervical cancer-only screening group.

Moreover, women of different religions had significantly different proportions of agreement for the cancer risk perceptions and the physician communication behaviors, where Muslim women among all religions had the lowest agreement that she was involved with her physician in decisions about her health care as much as she wanted (Supplementary file 2 – 'Agreement with cancer risk perceptions and physician communication behaviors by self-declared religion'). Supplementary file 3 – 'Cancer screenings by religion and race/ethnicity' shows that MENA ethnicity, not a religious affiliation, is significantly associated with cervical cancer and/or CRC screening patterns.

There are significant gaps in the screening rates for both cervical cancer and CRC. We focused on understanding the many combinations of screening uptake that occur and found different predictors for dual or single CRC and cervical cancer screening among women in southeast Michigan. In prior work, having a chronic disease increased CRC or cervical cancer screening rates compared to no screen (Harper et al., 2021a; Cofie et al., 2018; Borrayo and O'Lawrence, 2016) and other studies have shown that cancer fatalism is a major barrier to screening uptake (Clarke et al., 2021; Jun and Oh, 2013). In this work, neither having chronic diseases nor cancer risk perceptions, such as cancer fatalism, had an influence on any cervical cancer or CRC screening behavior pattern. We did however find that positive PCP communication including the woman in her health care as much as she wants (PCP-patient dyad decision-making) was associated with completing both CRC and cervical cancer screening compared to no screen, but even more importantly also compared to only cervical cancer screening – the first new insight from this work.

When one screen alone was completed, women indicated no associated involvement by the PCP in their health care decisions, whereas if there is significant PCP-patient dyad decision-making, there is a higher likelihood that both screens are completed. This creates a hypothesis that comprehensive cancer screening may best be accomplished through a PCP-patient relationship and not through targeted single cancer site screenings. To date, in the United States, specific organ cancer screenings are directed by the respective specialties. For instance, gynecologists dominate the screening method and frequency recommendations for cervical cancer screening just as gastroenterologists dominate for CRC screening. Even the USPSTF guidelines, based in primary care, consider single cancer screenings alone, without the possibility of synergistic multi-organ screenings. In addition, single cancer screenings have been the mainstay of US population programs to date with some success (Wong and Miller, 2019; Pollack et al., 2020). But our results may indicate that a single cancer screen when done outside the PCP-patient relationship is perceived more as a test to be done rather than part of general wellbeing. We hypothesize a solution of home-based or self-screening options to target dual cervical cancer (primary HPV testing) and CRC (fecal immunochemical testing with DNA) screening to be used in the PCP-patient dyad decision-making process (El Khoury et al., 2021; Gorin et al., 2021). The self-screening option could also allow the general internist who does not provide gynecologic exams the ability to be effective in this PCP-patient dyad. Moreover, we hypothesize that the PCP-patient dyad relationship may further enhance follow-up after any abnormal screenings (Tsui et al., 2019; Peterson et al., 2016).

The second new insight from this work is that age continues to be an important predictor of these two screens, but in opposite directions. Within the 50–65 years’ age range, younger women participate more in cervical cancer screening and older women participate more in CRC screening. We hypothesize a two-level system solution: one patient-centric and one physician-centric. The patient-centric phenomenon is based in the woman’s choice of her PCP. Women who choose a gynecologist as the PCP have less opportunity for dual cancer screening options, as the physician relationship is likely to be focused on the reproductive years and end at the time of menopause in her fifties, and certainly by 65 when there are no further routine reasons for gynecologic care. Likewise, we hypothesize that women who choose a general internist as the PCP are more likely to focus on other medical issues as most general internists do not provide gynecologic exams. Furthermore, we hypothesize that women who have a family physician as a PCP are the group most likely to have both screens completed as both cancer preventions are part of the foundational PCP-patient relationship of family medicine care. While it is patient-centric to choose the PCP, it is physician-centric for test ordering. We hypothesize for future work that family medicine physicians order dual screening more often than gynecologists or general internists.

The third new insight is the documentation of the disparities in cancer screening among MENA women which are not well reported due to US Census race/ethnicity categories. Currently race/ethnicity must be indicated by having the respondent write in their MENA heritage rather than having it as a separate preidentified racial/ethnic category. We have shown in this work that MENA women are rarely screened for CRC, be it alone or in addition to cervical cancer screening. Past work also shows MENA women have little CRC screening (Harper et al., 2021a). In addition, we have shown that it is not religion itself, but rather the cultural ethnicity of MENA that is associated with the behaviors. We hypothesize that both physician and patient education in the MENA community about patient involvement in decision-making and the screens themselves will improve both cervical cancer and CRC screening.

Finally, we are the first to show for Black women in southeast Michigan that there are significant strong associations between the positive PCP-patient dyad in decision-making and the completion of both CRC and cervical cancer screening compared to cervical cancer screening alone even after adjustment for age. We hypothesize that the PCP-patient dyad for Black women occurs in patient-centered medical homes as the health care structure in which they seek care leading to dual screening.

In summary, this work shows that race/ethnicity, age, and physician communication behavior are three independent influencers associated with completing both CRC and cervical cancer screening compared to cervical cancer screening alone. This work provides a baseline for several future studies.

The complete raw data-set collected in the study including the participants' data set, syntax file and log files for analysis has been uploaded to https://www.openicpsr.org/openicpsr/project/148081/version/V1/view.

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Author details

1. Diane M Harper

   1. Department of Family Medicine, University of Michigan School of Medicine, Ann Arbor, United States
   2. Department of Obstetrics & Gynecology, University of Michigan School of Medicine, Ann Arbor, United States
   3. Department of Women’s Studies, University of Michigan, College of Literature, Science and the Arts, Ann Arbor, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Writing - original draft, Writing - review and editing

   For correspondence

   harperdi@med.umich.edu

   Competing interests

   Senior editor, eLife

   "This ORCID iD identifies the author of this article:" 0000-0001-7648-883X

2. Madiha Tariq

   Arab Community Center for Economic and Social Services (ACCESS), Dearborn, United States

   Contribution

   Project administration, Writing - review and editing

   Competing interests

   No competing interests declared

3. Asraa Alhawli

   Arab Community Center for Economic and Social Services (ACCESS), Dearborn, United States

   Contribution

   Project administration, Writing - review and editing

   Competing interests

   No competing interests declared

4. Nadia Syed

   Arab Community Center for Economic and Social Services (ACCESS), Dearborn, United States

   Contribution

   Project administration, Writing - review and editing

   Competing interests

   No competing interests declared

5. Minal Patel

   1. Department of Health Behavior & Health Education, University of Michigan School of Public, Ann Arbor, United States
   2. Outreach and Health Disparities Research, University of Michigan Rogel Cancer Center, Ann Arbor, United States

   Contribution

   Conceptualization, Funding acquisition, Investigation, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

6. Ken Resnicow

   1. Outreach and Health Disparities Research, University of Michigan Rogel Cancer Center, Ann Arbor, United States
   2. Center for Health Communications Research, University of Michigan, School of Public Health, Ann Arbor, United States

   Contribution

   Conceptualization, Data curation, Funding acquisition, Investigation, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

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