Expanding colorectal cancer screening among minority women

Expanding Colorectal Cancer ScreeningAmong Minority WomenMoshe Shike, MD1; Mark Schattner, MD1; Alvaro Genao, MD2; Winsome Grant, PhD, NP3; Margaret Burke, MBA4;

Ann Zauber, PhD5; Lianne Russo, MS1; and Valerie Cuyjet, NP6

BACKGROUND: Colorectal cancer screening (CRCS) in the United States is inadequate in minority communities and

particularly among those who lack insurance. Finding ways to increase screenings in these minorities presents a

healthcare challenge. The authors sought to determine whether offering CRCS at the time of mammography is an

effective way to increase CRCS among minority women. METHODS: This study was offered to women attending the

Breast Examination Center of Harlem (BECH), a community outreach program of Memorial Sloan-Kettering serving

the primarily black and Hispanic Harlem Community. Screening was explained, medical fitness was determined, and

colonoscopies were performed. Barriers to screening and ways to overcome them were ascertained. Participants had

to be at least 50 years of age without a history of colorectal cancer or screening within the last 10 years. RESULTS:

There were 2616 women eligible for CRCS, of these women 2005 (77%) refused to participate in the study, and 611

(23%) women were enrolled. There was a high interest in CRCS including among those who declined to participate in

the study. The major barrier was lack of medical insurance, which was partially overcome by alternative funding. Of

the 611 women enrolled, 337 (55%) went on to have screening colonoscopy. Forty-nine (15%) women had adenoma-

tous polyps. CONCLUSIONS: Offering CRCS to minority women at the time of mammography and without a physi-

cian’s referral is an effective way to expand screening. Screening colonoscopy findings are similar to those in the

general population. Alternatives to traditional medical insurance are needed for the uninsured. Cancer 2011;117:70–6.

VC 2010 American Cancer Society.

KEYWORDS: colorectal cancer screening, colonoscopy, underserved population, uninsured.

Colorectal cancer (CRC) is the second leading cause of cancer mortality in the United States, with an estimated148,810 new diagnoses and 49,960 deaths in 2008.1 CRC screening (CRCS) by fecal occult-blood testing has been shownto reduce mortality. Although randomized studies of colonoscopy have not been performed, indications are that colono-scopy is particularly effective for CRCS.2-4 All colorectal cancer screening strategies cost less than $20,000 (US dollars)per life-year saved.5 This is comparable to the cost effectiveness of mammography.5

Despite the proven efficacy of CRCS, no more than 50% of the US population undergo screening,6 in contrast toscreenings for breast and cervical cancer, which are used by a high percentage of women.7-8 Inadequate screening for coloncancer is even more pronounced in minority communities such as Harlem, New York, where the 5-year survival rate ofCRC patients is 20%9 compared with the national average10 of 47%-62%. The decline in CRC mortality seen in whitemales and females has not occurred among African Americans. Increasing CRCS, particularly in minority communities, isa major healthcare concern.

Certain obstacles particular to medically underserved communities prevent minorities from obtaining adequatehealthcare and appropriate cancer screening. Those obstacles include lack of medical insurance, under-representation inthe healthcare field, distrust of or poor satisfaction with the healthcare system, and inadequate infrastructure. For His-panics who speak primarily Spanish, poor communication is another factor in making healthcare inaccessible.

DOI: 10.1002/cncr.25566, Received: March 5, 2010; Revised: April 26, 2010; Accepted: June 29, 2010, Published online October 25, 2010 in Wiley Online Library

(wileyonlinelibrary.com)

Corresponding author: Moshe Shike, MD, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10065; Fax: (212) 717-3113; Shikem@mskcc.

org

1Department of Medicine, Memorial Sloan-Kettering Cancer Center. New York, New York; 2Department of Medicine, North General Hospital, New York, New York;3Department of Nursing, Memorial Sloan-Kettering Cancer Center, New York, New York; 4Hospital Administration, Memorial Sloan-Kettering Cancer Center, New

York, New York; 5Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, New York; 6Ralph Lauren Center for Cancer

Care and Prevention, New York, New York

The authors wish to thank Carol Pearce, MFA, writer/editor with the MSKCC Department of Medicine, for editorial assistance.

70 Cancer January 1, 2011

Original Article

Although women in general are more likely to par-ticipate in preventive healthcare, CRCS is still suboptimalin this group and far below the screening rates for cervicaland breast cancer. More than 90% of American womenhave had a Papanicolaou (Pap) test, and 85% of womenaged�40 years have had a mammogram.7 A random sur-vey of New York’s Harlem households from 1992-1994showed that 80% of women aged 50 to 65 years havehad a mammogram.8 Despite the lack of adequate pri-mary care and medical insurance, minority women go toscreening mammography centers, driven by word-of-mouth recommendations or promotions through mediaannouncements. In some of these centers, mammographyis offered without charge.

This study examined the feasibility of offeringCRCS to women at the time of mammography, thuseliminating the need for referral by a clinic or a physician,and thereby removing a major barrier to CRCS. In thisway, we hoped to identify the barriers to screening and theways to overcome them and also to determine the preva-lence, stage, and pathology of lesions found during screen-ing. We hypothesized that mammography centers offereda unique opportunity to introduce the concept of colo-rectal cancer screening at the time of mammography orPap smear. The women being tested would already be fa-miliar with the concept of cancer screening, and wehypothesized that a substantial proportion would undergocolorectal cancer screening if they were made aware of itsimportance and if a mechanism existed to facilitate it.

A recent meta-analysis11 of interventions to promotescreening mammography in populations with historicallylow rates of screening demonstrates that individualized,directed strategies (ie, one-on-one counseling) in a health-care setting resulted in a significant increase in use. Similarfindings were reported in CRCS.12

MATERIALS AND METHODS

Patients

The study was offered to women attending the Breast Ex-amination Center of Harlem (BECH). This clinic, partof a community outreach program of Memorial Sloan-Kettering Cancer Center, offers free screening for breastand cervical cancer to women from the Harlem Commu-nity in New York City. A program to facilitate CRCS wasimplemented at BECH 2 years before the beginning ofthis study. Participation in our study was offered to all eli-gible women seen during the study period from July 2003through October 2005.

Eligibility

To be eligible, participants had to be �50 years of agewith no history of colorectal cancer or CRCS. History ofCRCS was defined as fecal occult-blood testing annuallyfor at least the last 3 years or colonoscopy within the last10 years. Women with a serious illness that precluded acolonoscopy (severe heart or pulmonary disease, uncon-trolled diabetes, or uncontrolled hypertension) wereexcluded from the study. Because the study participantsrequired a telephone contact, those without such a contactwere excluded. Telephone contact could be either througha participant’s own telephone, a work telephone, or a closeneighbor or relative.

Eligible women were given an initial explanation ofthe rationale for CRCS by a trained bilingual (Englishand Spanish) study assistant. Further explanation andconsent were done by a nurse practitioner after the screen-ing breast examination.

When an eligible woman chose not to participate inthe study, the reasons for refusal were recorded anony-mously. The study was approved by the Memorial Sloan-Kettering Cancer Center Institutional Review Board andNorth General Hospital Privacy Board.

Precolonoscopy Evaluation

When a woman chose to participate in the study, a full ex-planation of the study was provided by a research assistantand a nurse, and the woman was asked to sign a consentform. Explanation was given in Spanish when necessary,and the consent form was also available in Spanish. Thosewho signed the consent completed a questionnaire (bythemselves or with the assistance of a study assistant) toassess their attitudes, beliefs, and barriers toward colono-scopy screening. Then, an appointment was scheduled witha CRCS nurse practitioner (NP) for a precolonoscopy med-ical evaluation and a general physical examination. At thatsame appointment, a detailed explanation covered the colo-noscopy, preparation for the procedure, potential complica-tions, and what to expect during and after the colonoscopy.Participants were also asked about family history of coloncancer. Blood was drawn for complete blood count (CBC),prothrombin time (PT), partial thromboplastin time(PTT) , and creatinine unless results were available from 30days before the appointment. Participants who were foundto have active medical problems, such as angina, heart fail-ure, severe pulmonary problems, uncontrolled diabetes, orhypertension, were referred to a medical clinic or to theirprimary physician and asked to return after treatment of themedical condition. An appointment for colonoscopy was

Colon Cancer Screening in Minority Women/Shike et al

Cancer January 1, 2011 71

made for those participants who successfully completedprecolonoscopy evaluation.

Colonoscopy

Colonoscopy was performed in a Harlem communityhospital (North General Hospital) by 1 of 3 gastroenterol-ogists. The gastroenterologist recorded the colonoscopyfindings, early or late procedure-related complications,and the pathology findings, when applicable.

After their recovery from sedation, participants wereinformed of their colonoscopy findings by the gastroen-terologist as is routine in clinical practice. Information onfollow-up treatment (if necessary) or screening and resultsof pathologic examination of lesions found during colo-noscopy were provided to participants by the CRCS nursepractitioner or gastroenterologist.

A telephone call was made to the participants within6 weeks after colonoscopy. They were asked about anylate procedure-related complications and questionedabout their satisfaction with the colonoscopy experience.

The reasons for noncompliance with the appoint-ment for precolonoscopy medical evaluation or for colo-noscopy were recorded through a telephone contact,when applicable.

Pathology

Pathology slides were initially reviewed by pathologists atthe community hospital and subsequently by a specialistin gastrointestinal (GI) pathology. The GI pathologist

was unaware of the initial pathology diagnosis. This wasdeemed necessary because of discrepancies that have beenreported between community pathologists and GI pathol-ogists in diagnosis of polyps.13

Statistical Analysis

Statistical analyses included descriptive statistics, groupmeans, and medians.

RESULTSA total of 2616 women were eligible, and of these, 611(23%) consented to participate, whereas 2005 (77%)declined (Fig. 1).

Figure 1. Number of participants in the study is shown.

Table 1. Reasons for Refusing to Participate in the Study(n¼2005)

Reasons for Refusala No. ofWomen (%)a

Wants to discuss with primary physician 576 (29)

Wants CRCS but not part of a study 437 (22)

Lack of insurance 379 (19)

Needs time to think about it 197 (10)

Already has CRCS appointment 158 (8)

Fear of CRCS 150 (7)

No interest in CRCS 107 (5)

No time for CRCS 100 (5)

Insurance not accepted at community hospital 90 (4)

Lack of adequate knowledge 21 (1)

Miscellaneous 262 (13)

CRCS indicates colorectal cancer screening.aWomen could indicate multiple reasons for refusal.

Original Article


Refusers

Because of limitations imposed by the Health InsurancePortability and Accountability Act (HIPPA), only age andreasons for refusal were collected anonymously for the2005 women who declined to participate in the study. Themean age was 58 years (range, 44-91 years). Reasons for re-fusal (Table 1) included wanting to discuss CRCS withtheir primary physician (29%), wanting to have CRCSwithout participating in a study (22%), and lack of insur-ance (19%). Among all eligible women, only 5% cited lackof interest in CRCS, 7% cited fear, and 1% cited lack ofadequate knowledge as reasons for not wanting CRCS.

Study Participants

The mean age of the 611 women who enrolled in the studywas 56 years (range, 47-84 years); 77% were <60 years ofage. The racial composition was: 49% black non-Hispanic,34% white Hispanic, 9% black Hispanic, and 8% others(Table 2). Two hundred thirty-three (38%) of the womenspoke only Spanish, and 378 (62%) spoke English.

Of the 611 women who initially joined the study,397 (65%) attended the precolonoscopy medical evalua-tion appointment; 337 (85%) of these women went on tohave screening colonoscopy and 60 (15%) did not. Rea-sons for failure to have a colonoscopy among the 60women were medical issues/illness, 13; financial/insur-ance issues, 12; moved/traveling, 9; had it done elsewhere,9; lost to follow-up, 9; and fear of the procedure, 8.

Findings From Precolonoscopy MedicalEvaluation

During precolonoscopy evaluations, nurses found thefollowing gastrointestinal symptoms in 60 (15%)women: constipation, 33; rectal bleeding, 34; change inconsistency of bowel movements, 6; abdominal pain/per-sistent bloating for past 3 months, 10; diarrhea, 3; recentunintentional weight loss, 1. Eleven women were referredto primary care physicians by a nurse practitioner

because of medical issues that needed to be resolvedbefore CRCS. These included 6 women with uncon-trolled hypertension and 5 with a variety of problems.Six of these women did not return for CRCS. Fivewomen had their medical issue resolved and went on tohave CRCS without complications.

Family History

Of the 397 women who attended precolonoscopy evalua-tion, 365 (92%) reported no family history of colon can-cer, 30 (8%) reported a family history, and 2 (1%)women did not know their family history (Table 3). Table3 also correlates colonoscopy compliance and noncompli-ance in relation to family history.

Medical Insurance

Insurance status of the women who entered the studycan be found in Table 4. Almost half of the study partici-pants had some form of health insurance. At the start ofthe study, there were no grants to pay for screening thosewho were uninsured. These women were still offeredCRCS when they were willing to pay $50 for the preco-lonoscopy evaluation and $300 for a colonoscopy. Atotal of 29 women paid $350 out of pocket for CRCS.As previously noted (Table 1), 379 women who wereuninsured refused to participate in the study. Later in thestudy, grants were available from the American CancerSociety and philanthropic sources, and CRCS withoutcharge was offered to 223 uninsured women, of whom151 (68%) then had CRCS. Overall, grants accountedfor 45% of the payments for CRCS of women who ini-tially refused colonoscopy because of lack of insurance.

Colonoscopy Examination and Findings

In the 337 participants who had colonoscopy, the cecumwas reached in 301 (89%) and the colon cleared in 294(87%).

The colon was not cleared in 43 (13%) participants.Endoscopists recorded multiple reasons: 17 presented

Table 2. Characteristics of Study Participants (N¼611) According to Colonoscopy Versus NoColonoscopy

Characteristics Total onStudy N5611

UnderwentColonoscopy n5337

NoColonoscopy n5274

Mean age, y [range] 56 [47-84] 56 [50-84] 56 [47-82]

Race, no. (%)Black, Non-Hispanic 301 (49) 162 (48) 139 (51)

White Hispanic 208 (34) 115 (34) 93 (34)

Black Hispanic 53 (9) 27 (8) 26 (9)

Other 49 (8) 33 (10) 16 (6)



with poor bowel preparation, 30 were ascribed to techni-cal difficulties, and 3 participants experienced discomfort.Subsequently, 6 patients were instructed to have a repeatcolonoscopy and 37 a barium enema. At 2 years, only 2 ofthese participants had a repeat colonoscopy; 19 had a bar-ium enema. None of these tests detected polyps or cancer.

There were no complications during colonoscopy.Of the 337 participants who had colonoscopy, 101 (30%)patients were found to have a total of 149 polyps. Pathol-ogy findings are presented in Table 5. The polyps werehistologically classified by general pathologists and by aGI pathology specialist. The GI pathologist classifiedmore polyps as adenomas compared with the generalpathologists, but within the adenomas, the GI pathologistwas less likely to classify the adenoma pathology asadvanced compared with the community hospital generalpathologists.

Patients Satisfaction With Colonoscopy

Information on patient experience and satisfaction withthe CRCS was obtained from 313 of 337 women. On thebasis of their experience, 88% of the women reported that

they would have a colonoscopy again if necessary, 95%would recommend it to family and/or friends, and 95%consider colonoscopy a good test to have.

DISCUSSIONThis study demonstrated the usefulness of introducingcolonoscopy screening within the context of an active, on-going, mammography-screening program. The usefulnessof this approach is evident from the interest in CRCS itgenerated and the participation rate in colonoscopy. Toour knowledge, this is the largest study to date withscreening colonoscopy findings in minority women.

Of the 611 women who participated in this study,92% were black or Hispanic. Many of these women wereunlikely to undergo CRCS, given that most of themlacked medical insurance and access to routine medicalcare. Introducing them to CRCS through the mammog-raphy center and without a physician’s referral was effec-tive. This approach is viable for similar women in thegeneral population because many women undergo mam-mography even without regular medical insurance.14 It isclear from these data that after a simple, short explanationof screening colonoscopy given by a nonprofessional (inthis case a study assistant), women became interested inthe procedure even in the absence of a physician’s referral.

Although only 611 (23%) of the 2616 women whowere eligible consented to participate in the study, theoverwhelming majority of women were interested inCRCS as shown in Table 1. Only 150 (7%) women citedlack of interest as a reason for declining CRCS. These dataindicate that once the women’s attention was capturedand an adequate explanation was given (facilitated byexplaining in Spanish to those who did not speak Eng-lish), the overwhelming majority were interested inCRCS. Thus, offering CRCS at the time of

Table 4. Insurance Status and Payments for StudyColonoscopy (n¼337)

Payment Type No. (%)

Insured, total

157 (47)

Commercial insurance 68 (20)

Medicaid/medicaid HMO 55 (16)

Medicare/medicare HMO 19 (6)

Union insurance 15 (4)

Uninsured, total 180 (53)

Philanthropic grant 151 (45)

Self-pay 29 (9)

Table 3. Family History of Colorectal Cancer in Study Participants Related to Study Colonoscopy

Study Colonoscopy

Compliancen5337 No. (%)

Noncompliancen560 No. (%)

Family history n=397 No. (%)No family history of CRC 365 (92) 309 (92) 56 (93)

Unknown 2 (<1) 1 (<1) 1 (2)

Family history of CRC 30 (8) 27 (8) 3 (5)

First-degree relative 21 (5) 19 (6) 2 (3)

Second-degree relative 17 (4) 16 (5) 1 (2)

CRC indicates colorectal cancer.

Original Article


mammography is an effective way of generating interestand initiating the process.

An important component of the program was thescheduling of subsequent appointments. Once a womanwas interested in participating in the study and in having ascreening colonoscopy, an appointment was made for herto see a nurse practitioner for a precolonoscopy medicalevaluation. This ensured that the next step in the processwould be taken, limiting the potential for dropout. It alsoallowed the office assistant to follow up with the womenwho did not come to their appointment. This navigatorassistant helped women overcome barriers to schedulingand facilitated the process. A similar approach was usedby Chen et al12 However, in Chen’s study, women werereferred from primary care clinics, and it is not reported

what percentage of those approached actually participatedin CRCS. All patients in that report had medical insur-ance and, therefore, comprised a different populationthan ours, with only 47% having any insurance and, thus,less likely to undergo CRCS.

The medical clearance by a nurse practitioner waseffective in identifying those who were not qualified forcolonoscopy because of medical reasons. The lack of sig-nificant medical complications during colonoscopy indi-cates that a preprocedure medical evaluation by a nursepractitioner may be adequate, although our sample size issmall. The only time women encountered a physician inthis CRCS study was at the time of colonoscopy. Adaptingthis model may facilitate CRCS among low socioeco-nomic groups, considering that theymight not have a fam-ily physician or their physician may be too busy to dealwith preventivemedicine.

The most important barrier to CRCS by colono-scopy was lack of insurance. Of the 337 women whounderwent colonoscopy, 57% lacked insurance. It is re-markable that 29 (9%) women paid the $350 out ofpocket. The remaining 48% were able to have the proce-dure paid for by grants from the American Cancer Societyand other philanthropic sources. This group of women,with keen interest in CRCS, could possibly have under-gone cheaper methods of CRCS but were unlikely to havea colonoscopy outside of this study. This highlights theneed to find alternative funding sources from governmentor private institutions. Such funding is common in breastcancer screening.14 Considering that the cost effectivenessof breast and colon cancer screening is comparable, for-mulating a funding strategy for CRCS for the uninsuredsimilar to that used for breast cancer screening couldimprove CRCS in minority populations.

This study is unique in that it included only women,92% of whom were either black or Hispanic. Thirty per-cent of the women had polyps; 15% had adenomas. Thesenumbers are comparable to the findings of Schoenfeld etal15 who found adenomatous polyps in 20% of women,although in that group, only 14% were black or Hispanic.Advanced adenomas were found in 7% of women in ourstudy, again similar to Schoenfeld’s findings.15

Attempts to enhance colorectal cancer screeningin this population by media campaigns, provision offecal occult-blood test (FOBT) cards and other meth-ods have usually not met with much success.16-17 Itappears that a comprehensive program is needed inmedically underserved areas. Such a program needsto include not only the initial contact but also

Table 5. Comparison of Colonoscopy Polyps as Determinedby GI and General Pathologists (n¼101)

Polypsa GI Pathologist,No.

GeneralPathologist,No.

Total no. polyps 149 149

Adenoma 66 57

LocationRight-sidedb 37 34

‡1.0 cm 7 7

Advanced 10 15

Left-sidedc 29 23

‡1.0 cm 7 7

Advanced 8 13

Size �1.0 cm 14 14

Size (range) (0.1-5.0) (0.1-5.0)

Advancedd 18 28

Pathologye

Tubular 53 29

Tubular-villous 12 27

Tubular-villous and

high-grade dysplasia

1 1

NonadenomaTotal 79 88

Total non-neoplastic/

nonhyperplastic

25 16

Total hyperplastic 54 72

‡1.0 cm 2 3

Right-sided 13 17

‡1.0 cm right-sided 1 2

Size (range) (0.2-1.5) (0.2-1.5)

GI indicates gastrointestinal.a Left-sided defined as splenic flexure, descending colon, sigmoid colon,

rectum.b Advanced defined as �1.0 cm or tubular-villous.c No villous pathology found.d Total number of lost polyps was 4.e Right-sided defined as cecum, ascending colon, hepatic flexure, trans-

verse colon.



assistance in navigating through the various stages ofthe screening process.

CONFLICT OF INTEREST DISCLOSURESThis work was supported by a National Cancer Institute (NCIgrant R21 CA100587) and the American Cancer Society (Clini-calTrials.Gov Identifier: NCT00613873). The funding sourcesdid not have any role in the study except to provide thefunding.

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Original Article


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Expanding colorectal cancer screening among minority women