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Colon Cancer Screening Practices After Genetic Counseling and Testing for Hereditary Nonpolyposis Colorectal Cancer

From the Genetic Counseling Research Unit, Medical Genetics Branch, National Human Genome Research Institute, and the Genetics Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health; National Naval Medical Center, Bethesda, MD; and the Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA

Address reprint requests to Donald W. Hadley, MS, CGC, GCRU/MGB/NHGRI/NIH, 10 Center Dr, MSC 1852, Bldg 10/Room 10 C103, Bethesda, MD 20892-1852; e-mail: dhadley{at}nhgri.nih.gov

	ABSTRACT

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PURPOSE: Hereditary nonpolyposis colorectal cancer (HNPCC) is the most common hereditary form of colon cancer. Cancer screening recommendations differ between individuals identified to carry an HNPCC mutation and those who do not carry a known family mutation. We assessed the impact of genetic counseling and testing (GCT) on the use of endoscopic screening procedures and adherence to recommended endoscopic screening guidelines in 56 asymptomatic at-risk individuals from families known to carry an HNPCC mutation.

PATIENTS AND METHODS: We analyzed data on colonoscopy and flexible sigmoidoscopy screenings collected before GCT and 6 months and 12 months post-GCT on 17 mutation-positive and 39 true mutation-negative individuals. Main outcome measures were use of endoscopic screening and adherence to recommended guidelines for the relevant mutation status. Mutation status, age, sex, employment, and income were analyzed as predictor variables.

RESULTS: Among mutation-negative individuals, use of colonoscopy and flexible sigmoidoscopy decreased significantly between pre- and post-GCT (P < .00001 and P < .0003, respectively). Among mutation-positive individuals, a nonsignificant increase (P = .24) in use was noted. Age was also associated with use of endoscopic screening after GCT (P = .03). Mutation status (odds ratio [OR], 7.5; P = .02) and employment (OR, 8.6; P = .025) were associated with nonadherence to endoscopic screening guidelines. More mutation-negative individuals strictly adhered to guidelines than did mutation-positive individuals (87% v 65%).

CONCLUSION: Genetic counseling and testing for HNPCC significantly influences the use of colonic endoscopy and adherence to recommendations for colon cancer screening.

	INTRODUCTION

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Colorectal cancer (CRC) is the third most common cancer and third leading cause of death due to cancer in both men and women in the United States [1,2]. Hereditary nonpolyposis colorectal cancer (HNPCC) accounts for approximately 3% to 5% of all cases of CRC, with lifetime risks for developing CRC exceeding 80% [3,4]. Screening for CRC through colonoscopy and removal of polyps is an effective approach for preventing CRC in HNPCC, with more than a 50% reduction in the risk for CRC, prevention of CRC deaths and a decrease in overall mortality by approximately 65% in HNPCC families [5].

Genetic counseling and testing (GCT) for HNPCC mutations in at-risk asymptomatic individuals is now available. Ideally, knowing one's genetic status for cancer susceptibility genes would allow focused screening and medical management in individuals identified with increased risk because of the presence of a deleterious mutation [6]. Moreover, individuals not carrying deleterious mutations would be able to reduce cancer screening to levels recommended for the general population, thereby preserving resources and, it is hoped, reducing the uncertainty and potential anxiety associated with the at-risk status of the individual before GCT [6,7]. Insight into CRC screening behavior after GCT in individuals identified with HNPCC mutations is beginning to emerge [8-10].

This study evaluates use of endoscopic screening and adherence to recommended screening guidelines in a cohort of at-risk unaffected individuals receiving GCT for HNPCC mutations. Use measures whether an individual has engaged in a screening behavior within a time period of interest. Although use is an important outcome measure, it does not necessarily reflect the individual's execution of prescribed recommendations. In an effort to characterize more clearly CRC screening practices by HNPCC mutation-positive and mutation-negative persons, we assessed participants' precise execution of guidelines for endoscopic screening and use the term adherence to describe completion of the recommended screening tests at the frequency prescribed. In this schema, individuals undergoing screening modalities outside of those recommended or undertaking screening more or less frequently than recommended are considered nonadherent. Thus, individuals exhibiting hypervigilant or hypovigilant screening behaviors, respectively, are identified.

Consideration of adherence to recommended CRC screening guidelines and attempts to identify factors associated with adherence are warranted in these newly identified populations of mutation-positive and mutation-negative individuals, all of whom were previously considered at increased risk because of clinical recognition of HNPCC within their families. A more precise understanding of CRC screening behaviors within this population seems prudent from cognitive and emotional perspectives, as well as from measures of cost effectiveness. The interest in understanding adherence to recommendations grows out of initial concerns regarding the psychological and emotional impact of receiving genetic test results within the context of a family with a hereditary cancer syndrome [6,11,12]. Specifically, there have been concerns that some individuals identified as mutation-negative may not be willing to reduce their cancer screening practices because of family experiences with cancer and the inherent and penetrating worries regarding their risk for cancer [13-15]. Conversely, some mutation-positive individuals might avoid screening, immobilized by the fear of cancer detection [16,17]. In either case, education or counseling approaches could be considered to alleviate the cognitive and/or emotional stressors for the patient while focusing resources in a cost effective manner. However, before implementing new education or counseling approaches, empirical data on the extent to which mutation-negative and mutation-positive individuals adhere to CRC screening guidelines are needed. This report provides the first empirical data on endoscopy use and predictors of adherence to endoscopy screening guidelines after the receipt of positive and true-negative HNPCC mutation results among asymptomatic individuals in families with known HNPCC mutation.

	PATIENTS AND METHODS

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Study Population
A total of 56 adults (age 18 years) with no personal history of cancer, at 50% risk of carrying their families' previously identified deleterious HNPCC mutations, who chose to undergo genetic testing and who completed questionnaires at baseline, 6, and 12 months were used in the current analyses after excluding those simultaneously participating in clinical trials involving colonoscopy (n = 5). These individuals were identified from a previously reported cohort [18] in a study investigating the outcomes of genetic education and counseling with the option of genetic testing for HNPCC. The study was approved by the institutional review boards of the appropriate institutions, and all participants gave their informed consent. Identification and contact of family members at 50% risk was initiated through a first-degree relative identified to carry the family's HNPCC mutation.

The option of genetic testing was considered after a comprehensive, scripted education session that provided basic facts about the incidences of cancer and colon cancer; risk factors for cancer; inheritance of cancer susceptibility in HNPCC families; possible outcomes of genetic testing for HNPCC; potential benefits, limitations, risks associated with genetic susceptibility testing; and a review of cancer surveillance and screening guidelines recommended for HNPCC families. The education session was followed by a client-centered counseling session, which allowed the participant to explore issues related to the option of genetic testing. Those choosing testing had a blood sample collected that was processed in a Clinical Laboratory Improvement Amendments–approved laboratory; results were received in a second counseling session approximately 1 month after sample collection.

Genetic counseling and genetic testing were provided without cost to participants. Verbal and written cancer screening recommendations following published guidelines [19] were provided in both the initial genetic counseling session and the results sessions. Those recommendations included a colonoscopy every 1 to 3 years for mutation-positive persons and general population screening [19] for mutation-negative persons (ie, flexible sigmoidoscopy every 3 to 5 years after the age of 50 years). HNPCC screening recommendations were also included in the clinical summary mailed to the participant after the results session. Data on cancer screening practices (including colonoscopy and flexible sigmoidoscopy) and psychological and social variables were collected at baseline before GCT and at 6 and 12 months post-GCT. Health-related behaviors were assessed by self-report. Self-reported use of colonoscopy has been validated through previous research and has been shown to be highly accurate [20].

Measures
Outcomes variables. Endoscopy screening behavior (ie, colonoscopy and flexible sigmoidoscopy) was assessed at baseline after a brief definition of each procedure by asking, "When was your last colonoscopy (flexible sigmoidoscopy)?" Response categories were never, less than 1 year ago, 1 to 3 years ago, and more than 3 years ago. At the 6- and 12-month interviews, subjects were asked, "Have you had a colonoscopy (flexible sigmoidoscopy) within the last 6 months or since you last completed the questionnaire?" Response categories were yes, no, and unsure. Responses were used to create three different outcome variables: pre-GCT use, post-GCT use, and post-GCT adherence. Use is a dichotomous variable measuring whether or not a participant had at least one colonoscopy (flexible sigmoidoscopy) in a specified time period. Adherence is a dichotomous variable measuring whether or not a participant's behavior was consistent with the actual endoscopic screening recommendation within the 12-month period after GCT. Individuals were categorized as adherent or nonadherent on the basis of their age, mutation status, earliest age at onset of cancer in the family, and length of time since last procedure. Nonadherent individuals were subclassified as hypovigilant if they did not engage in screening when recommended or hypervigilant if they engaged in screening more frequently than recommended.

Predictor variables. Mutation status, age, sex, employment, and annual income (dichotomized as $50,000 or > $50,000) were analyzed to determine if they play a significant role in explaining use and adherence to recommended endoscopic screening. Pre-GCT use was included as a predictor variable when assessing post-GCT use and adherence.

Analyses
The McNemar test was used to test for differences between correlated proportions. When differences in categoric variables between two groups were assessed, Fisher's exact test or ² test was used. Comparisons between groups on continuous variables were performed with the t test. Stepwise logistic regression was performed to identify variables associated with pre-GCT use, post-GCT use, and post-GCT adherence. These analyses used a criterion of 0.10 for entry and exit from the model. Statistical significance was assessed using = .05.

	RESULTS

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Sample Characteristics
Of the 56 individuals, 95% were white, 71% were female, 82% were employed, 95% had health insurance, and the average age was 38.1 years (standard deviation, 13.1 years). Table 1 provides demographic information by mutation status. Mutation testing determined that 39 individuals (70%) were truly negative and 17 individuals (30%) were positive for a deleterious HNPCC mutation. The mutation-positive group was significantly younger than the mutation-negative group, and had a smaller percentage of individuals earning an annual income more than $50,000. The two mutation groups did not significantly differ on the remaining demographic variables.

Post-GCT Use of CRC Endoscopic Screening
Twelve (21%) of 56 individuals had at least one colonoscopy in the 12-month period after GCT. However, there was a significant difference in post-GCT use between mutation-positive and mutation-negative individuals (P = .0004). Specifically, nine (53%) of 17 individuals in the mutation-positive group and three (8%) of 39 individuals in the mutation-negative group had at least one colonoscopy post-GCT. The colonoscopy use rate in the mutation-positive group reflected a slight but nonsignificant increase from the 41% use rate before GCT in this subgroup (P = .24). However, the post-GCT endoscopic screening rates among mutation-negative individuals were significantly less than their pre-GCT rates (colonoscopy pre-GCT, 59% v post-GCT, 8%; P < .00001; flexible sigmoidoscopy pre-GCT, 31% v post-GCT, 0%; P = .0003).

Stepwise logistic regression analysis demonstrated that colonoscopy use after GCT is more likely with a mutation-positive result (OR, 61.6; 95% CI, 5.8 to 652.6; P = .0006) and increasing age (OR, 1.1; 95% CI, 1.008 to 1.2 P = .03). Employment, income, sex, or pre-GCT use did not predict post-GCT use (P > .05).

Together, the pre- and post-GCT use analyses demonstrated that age plays a role in colonoscopy use both before and after GCT. In addition, GCT influences screening behaviors, given that use rates are maintained among individuals receiving a positive mutation result and decrease considerably among individuals receiving a true-negative mutation result.

Post-GCT Adherence to CRC Endoscopic Screening Recommendation
Table 2 lists data on the adherence patterns observed in the sample by mutation status. In the entire sample, 11 (20%) of 56 individuals were classified as nonadherent with recommendations in the 12-month period after GCT. Mutation-positive (OR, 7.5; 95% CI,1.3 to 42.2; P = .02) and unemployed individuals (OR, 8.6; 95% CI,1.3 to 56.6; P = .025) were significantly less likely to adhere to guidelines for endoscopic screening. Age, sex, income, or pre-GCT use was not associated with post-GCT adherence (P > .05).

In the mutation-negative group, five (13%) of 39 individuals did not adhere with recommended screening guidelines after GCT. Among these five individuals, two individuals (40%) exhibited hypovigilance because they did not have the recommended flexible sigmoidoscopy and the remaining three individuals (60%) exhibited hypervigilance. Hence, in the mutation-negative group, nonadherence occurred among individuals for whom endoscopic screening (ie, flexible sigmoidoscopy) was expected as well as among individuals for whom no endoscopic screening was expected. The adherent group was composed completely of individuals for whom no endoscopy was expected during this 12-month time frame.

	DISCUSSION

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The findings from this study demonstrate that GCT for HNPCC significantly influences the use of colonic endoscopy and adherence to recommended endoscopic screening guidelines. This finding deserves consideration because cancer screening recommendations differ between individuals identified to carry an HNPCC mutation and those who do not carry a known family mutation. Furthermore, our findings raise questions regarding factors influencing the overuse and underuse of cancer screening in individuals of known mutation status for cancer susceptibility genes specifically related to age and employment status. Future studies could consider including these variables to assess their potential roles in influencing cancer screening behavior.

Obvious concerns exist for those not undergoing cancer screening at the recommended levels in light of the recognized benefits of periodic screening. Clearly, additional efforts to understand the factors influencing the hypovigilant cancer screening behaviors are of primary importance, particularly in younger mutation-positive persons. Greater inclusion and collaboration with the primary healthcare providers may improve cancer screening adherence through their provision of ongoing support, education, and counseling to high-risk family members. However, studies are needed to elucidate factors influencing cancer screening practices in the younger, high-risk population before attributing hypovigilant screening practices to so-called hedonistic behavior, lower incomes, or absence of adequate coverage by health insurance.

Excessive screening is not typically addressed in screening behavior studies and by default is considered compliant behavior. However, our identification of individuals who are hypervigilant in their cancer screening practices suggests that this subgroup also merits investigation from both psychological and fiscal perspectives. The mutation-positive cohort exhibiting hypervigilance raises concerns regarding the potential of anxiety triggering excessive screening practices although data are lacking to test this hypothesis. Within the mutation-negative hypervigilant cohort, it is possible that individuals who were previously considered to be at high risk are reluctant to immediately stop undergoing colonoscopy. This reluctance may be due to concerns about test reliability or the desire for reassurance within the context of a family with many persons affected with colon cancer. Similarly, mutation-negative persons, age 50 years or older, may lack confidence in sigmoidoscopy to detect colon cancer, given that colonoscopy is defined as the gold standard for families with HNPCC and the more sensitive procedure to identify colon cancer. There is some evidence for this; Bleiker et al [8] recently reported that nearly one third (32%) of participants receiving HNPCC mutation-negative results expressed concerns about foregoing surveillance while expressing relief that they no longer needed to undergo colonoscopy.

Although the limited numbers of nonadherent participants does not allow consideration of statistical significance, our review of participants' reasons why CRC endoscopic screening recommendations were or were not undertaken bears mention. The most common reason given for an individual's decision to screen (or not screen) was that the doctor did (or did not) recommend it (data not shown). These findings are consistent with previously reported data emphasizing the importance of healthcare professionals' endorsement of health screening [3,9-12]. Endorsement by the healthcare professional is dependent on his or her knowledge of current guidelines, as well as an array of other variables, including interpretations of screening effectiveness, inconvenience to patient or provider, patient discomfort, time, cost, and sufficiency of training to perform procedure [21]. In light of the effectiveness of current colon cancer screening modalities, in the general population and in high-risk families, strategies to improve healthcare providers' endorsement of screening recommendations are imperative.

Hereditary breast and ovarian cancer (BRCA1/2) mutation carriers have consistently been found to show higher use of cancer screening (mammography) than noncarriers after GCT [22-24]. However, the greatest change in cancer screening behavior has occurred among noncarriers, with a significant decrease from baseline to 12 months post-GCT [23,24]. In contrast, a nonsignificant increase in screening has been observed in BRCA mutation carriers. Age also has been identified as a significant factor in screening behavior after GCT for BRCA1/2. Studies have shown that younger women in families with BRCA1/2 mutations [23] and more specifically, younger women identified with BRCA1/2 mutations [24], are significantly less likely to undergo screening than older participants. Each of these findings is consistent with our data, and they together suggest that the effect of GCT on cancer screening practices may generalize to a variety of hereditary cancer syndromes. Furthermore, the use of cancer screening by younger high-risk persons in both BRCA and HNPCC populations demonstrates the need for research identifying strategies to increase screening practices in younger high-risk populations.

The participants within this study represent a subset of individuals at risk for HNPCC. Therefore, the findings from this study may not be representative of all HNPCC family members at high risk of developing colon cancer—specifically, those not seeking genetic services. The results suggest that GCT appropriately influences endoscopic screening during the 12 months post-GCT; however, additional studies with larger sample sizes investigating cancer-screening practices after the receipt of genetic services are needed to comprehensively assess use and adherence rates. Furthermore, additional studies are warranted to document CRC screening practices beyond the first year of GCT as well as to determine factors contributing to overuse and underuse of endoscopic screening.

The generalizability of these findings may be somewhat limited because the sample was composed primarily of white individuals with health insurance. The extent to which ethnicity or race and health insurance affect use and adherence to CRC screening recommendations after GCT warrants investigation. Furthermore, the provision of GCT at no charge potentially encourages greater uptake of genetic testing than might be encountered in the general population. However, the costs (insurance or out of pocket) incurred by participants for recommended cancer screening practices were not provided through the study and, therefore, would not be expected to differentially affect cancer screening behavior of participants compared with the general population. It is possible that persons willing to pay for GCT possess greater motivation to adhere to cancer screening recommendations than those receiving GCT at no personal financial cost.

Finally, we emphasize that the goal of genetic counseling is not the unilateral promotion of genetic testing. Rather, it is to facilitate comprehensive consideration of medical, psychological, and social issues inherent in the testing process, inform the patient's decision making, facilitate the adaptation process, and promote behavior consistent with medical recommendations with respect for personal and cultural values and beliefs [25]. In all situations, the consideration of genetic testing as an option should not be rushed. We hypothesize that it is the careful and comprehensive consideration of the individual's personal and family situation through the genetic counseling process that influences in part subsequent adherence to recommended guidelines.

	Authors' Disclosures of Potential Conflicts of Interest

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The authors indicated no potential conflicts of interest.

	Acknowledgment

 
We thank the individuals and families participating in this study for their generous gifts of time, insight, and honesty; without those contributions our knowledge would not advance.

	NOTES

 
Supported by the Medical Genetics Branch of the National Human Genome Research Institute, the Genetics Branch of the Center for Cancer Research within the National Cancer Institute, and by the 2002 Jane Engelberg Memorial Fellowship, an annual grant from the Engelberg Foundation to the National Society of Genetic Counselors Inc.

Authors' disclosures of potential conflicts of interest are found at the end of this article.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
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Submitted June 25, 2003; accepted October 17, 2003.

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