We assessed the cancer screening and surveillance practices of 8,347 survivors of childhood cancer. Encouragingly, female survivors considered average risk for developing cervical or breast cancer demonstrated acceptable rates of adherence to Papanicolaou smear and mammography recommendations, with adherence rates of 81% and 67% for each test, respectively. This suggests that female childhood cancer survivors are generally health conscious and aware of screening guidelines published for the general population. Survivors of cancer in adulthood have been demonstrated to have better adherence to cancer screening recommendations than that observed in the general population (
41), although actual screening rates are quite variable and often sub-optimal.
Despite the relatively high screening rates for survivors at average risk for another cancer, the rates of cancer surveillance for those at high risk for a therapy-related second malignant neoplasm were alarmingly low. Less than half of the survivors at increased risk of breast, colorectal or skin cancer reported compliance with recommended surveillance. Females who have received radiation therapy to the chest during childhood demonstrate a 13% to 20% cumulative incidence of breast cancer by 40 to 45 years of age (
42), a risk similar to that observed in women with breast cancer susceptibility gene mutations (
43-
45). Several studies have recognized an emerging risk of colorectal cancer in patients who have received abdominal or pelvic radiation as part of their primary therapy, with a 3.9 to 4.7- fold increased risk when compared to the general population (
13,
14,
46). Increased rates of other gastrointestinal malignancies such as gastric cancer have also been observed, suggesting that clinicians need to be aware of new symptoms in survivors who have received radiation to any portion of their gastrointestinal tract. Malignant melanoma occurs with increased frequency in childhood cancer survivors (
5,
14,
15), and the cumulative incidence of non-melanoma skin cancer is almost 7% in 30-year survivors of childhood cancer (
2). Thus, the low surveillance rates observed in our cohort suggest that opportunities to detect secondary breast, colorectal or skin cancers early in their course are being missed, placing some survivors at increased risk for both serious morbidity and mortality.
The dichotomy of low rates of surveillance among the high risk survivors within the setting of high rates of cancer screening among average risk survivors suggests that the problem is not simply a lack of interest or compliance on the part of the survivors. Survivors were more likely to report an indicated mammogram or skin exam if they received their follow-up care at a cancer center or in a long-term follow-up program. However, only a minority of adult survivors (12.4% in this cohort) continues to receive regular care at a cancer center once they reach adulthood (
47). Although many pediatric cancer centers offer specialized care to survivors during childhood and adolescence, few provide access to specialized clinics once survivors reach adulthood (
48). Several adult cancer centers run survivorship clinics although these generally target survivors of adult malignancies such as breast or colon cancer, and are not routinely used by survivors of childhood cancer (
49,
50). These data suggest that interventions to improve adherence to cancer surveillance should be directed at the primary care physicians who care for the majority of long-term childhood cancer survivors, as well as to the survivors themselves. Prior research has suggested that a physician recommendation is a statistically significant determinant of adherence to mammography guidelines (
51). However, since the guidelines for high risk patients recommend that breast and colorectal cancer surveillance commence many years before screening in the general population, many primary care physicians are likely unaware of the surveillance guidelines for these high risk patients (
52). In fact, primary care physicians’ lack of familiarity with the health problems faced by survivors has been identified as a substantial barrier to their provision of adequate survivor care (
52,
53). Targeted education of physicians, open access to guidelines (such as the COG LTFU Guidelines available at
www.survivorshipguidelines.org) and the availability of the pediatric cancer centers as a resource for primary care providers may improve survivor care. Perhaps most importantly, survivors must be provided with the knowledge and tools to advocate for their own care. Survivors are often unaware of the details of their cancer therapy, preventing them from seeking care focused on specific risks (
54). Efforts to empower survivors have included provision of treatment summaries and survivor care plans at the conclusion of cancer therapy. Indeed, in the present study, survivors who had a summary of their cancer treatment were more likely to report a recommended colonoscopy or skin exam. The feasibility of providing survivors with a portable electronic record of their cancer history and recommended care that can be shared with their health care provider is being assessed currently.
Several methodological limitations must be considered when interpreting the results of this study. First, we relied on self report data about the completion of screening tests. Although self report of imaging or diagnostic tests such as mammography or Papanicolaou smear has been demonstrated to be generally reliable (
55), there is no evidence to suggest that patients accurately report skin exams. Second, CCSS participants are a select group of survivors, and their compliance with surveillance recommendations may not be representative of all childhood cancer survivors. Third, this cohort of survivors received their therapy between 1970 and 1986. Caution should be exercised in generalizing these findings to patients treated more recently. It is plausible that patients treated in the current era are better informed about their need for routine surveillance. The CCSS is currently recruiting a cohort of survivors treated between 1987 and 1999 to examine such questions. Finally, assessment of screening compliance among survivors at average risk of developing a second malignant neoplasm focused only on females. There were too few survivors who had reached the age where colorectal cancer screening is recommended to assess compliance with these screening guidelines. Thus, the findings of good compliance among female survivors should not be generalized to male survivors.
In summary, survivors of childhood cancer who are not considered to be at increased risk for developing a second malignant neoplasm demonstrate reasonable adherence to Papanicolaou smear and mammography guidelines. However, survivors at increased risk for developing a new cancer during adulthood demonstrate very poor adherence to recommended surveillance for breast, colorectal and skin cancer. Clinicians who care for survivors of childhood cancers must implement and evaluate methods for ensuring better adherence with recommended cancer surveillance and for improving awareness among both the survivors and the primary care clinicians who provide care for the majority of these survivors as they age. This should include provision of a treatment summary and care plan to all childhood cancer survivors prior to their transition out of a pediatric cancer center.
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