Abstract
Background
Childhood cancer survivors are vulnerable to long-term treatment-related health conditions, which can lead to poor quality of life. Little data exist on the overall health of long-term Australian and New Zealand childhood cancer survivors or on survivors’ motivations for attending survivorship clinics.
Methods
This study administers a cross-sectional questionnaire to long-term survivors ≥5 years from their primary diagnosis. We compared participant-reported number of late effects by a cancer diagnosis, and identified clinical (eg, treatment) and demographic (eg, age) factors that were associated with late effects burden and engagement in cancer survivorship care.
Results
A total of 634 participants completed questionnaires (48% male, mean age = 21.7 years). Most participants (79%) reported at least one cancer-related late effect, most commonly fatigue (40%) and memory/learning difficulties (34%). Brain tumor survivors reported a higher total number of late effects than survivors with other diagnoses (mean = 5.7 vs. 3.2, P < .001). Participants’ most commonly reported motivators for engaging in care were to understand problems that may occur later in life because of their cancer and/or treatment (98.5%) and to get reassurance about one’s health (97.4%). The proportion of survivors endorsing each motivating factor was similar across cancer diagnoses, with the exception of learning more about insurance and pensions (highest in brain tumor survivors = 80%). In multivariable analyses, survivors were more likely to report being engaged in survivorship care if they were younger (P < .001), less time had elapsed since their diagnosis (P < .001), or they reported a higher number of motivating factors (P = .016).
Conclusion
Survivors report a range of health problems decades after treatment completion. Understanding the burden of late effects, and motivators for seeking survivorship care to manage these health problems, is important for ensuring that tailored interventions or services are available to meet the needs of this growing population and to design effective models of survivorship care.
Keywords: late effects, childhood cancer, survivorship care, motivations, follow-up care
Survivors of childhood cancer face unique and complex health problems in adulthood, known as late effects. Understanding survivors’ late effects and factors associated with engaging in survivorship care is critical to ensuring appropriate services are available to meet the needs of the growing survivor population. This study addressed this need.
Implications for Practice.
The present data reveal notable differences in the number/type of late effects across primary cancer diagnoses and factors related to engagement in survivorship care, including demographic (eg, age) and clinical (time since diagnosis, number of motivators). Understanding survivors’ late effects, perceived motivators for engaging in survivorship care, and potentially modifiable factors associated with their engagement is critical to ensuring appropriate services are available to meet the needs of the growing survivor population.
Introduction
Increasing survival rates have revealed the lifelong impact of receiving treatment for childhood cancer. Given the age at which they are treated and the intensity of the treatment that they receive, survivors of childhood cancer face unique and complex health problems in adulthood, known as “late effects.” Late effects include, but are not limited to, second malignancies, late mortality, cardiovascular disease, reproductive, and endocrine problems, which can lead to poor quality of life.1 Childhood cancer survivors report twice as many severe chronic health conditions by age 50 than healthy controls,2 and their mortality is 10 times higher than the general population.3 More intensive cancer treatment, in particular radiotherapy and chemotherapy agents, are associated with an increased risk of health conditions, highlighting the importance of balancing acute treatment needs with potential long-term toxicity as a result of intense therapy. Treatment-related exposure is one factor that directly influences survivors’ risk of adverse health outcomes, while other factors such as genetics, pre-morbid conditions, demographics, and health behaviors may also play a significant role.1
The long-term effects of cancer and its treatment are common, and may vary in severity, with some conditions having a long latent period.1 Some late effects of therapy identified early in follow-up may be managed more easily or resolved without further intervention (eg, growth hormone replacement therapy; or correcting hearing difficulties with hearing aids). However, other conditions may persist well into adulthood, some developing into chronic health problems and influencing the progression of other comorbidities which are typically associated with aging.4 Importantly, survivors who experience physical late effects report substantially poorer mental health or quality of life, than survivors with a lower late effects burden.5 For example, frailty is not uncommon among childhood cancer survivors and increases the risk for chronic disease, mortality, and poor mental health.6 Understanding the incidence of late effects, and survivors’ risk of late effects, is therefore critical for designing effective models of survivorship care, and health and psychological interventions targeted at prevention and management throughout survivorship.7
Multiple single-center and large cohort studies have contributed to our understanding of the long-term health consequences of childhood cancer survivors. Studies in North America have estimated the cumulative incidence of late effects is as high as 95%, 45 years post-diagnosis.8 Survivors frequently suffer more than one late effect, 81% of which are estimated to be severe, life-threatening, disabling, or resulting in death.8 However, studies in the Asia Pacific, including Australia and New Zealand, are generally limited to the investigation of one or a few related late effects (eg, second malignancies, cardiovascular, and endocrine), or are single-center studies, and do not provide a snapshot of the overall health of this high-risk population across these 2 nations.9-11
Most models of survivorship care use a risk-based approach that is driven by survivorship guidelines.12-15 Models of survivorship care are at the intersection of survivor and health system/provider factors, ultimately influencing provider practices and survivor health care use.16 The development of survivorship models of care must therefore be consumer-focused, taking into account the needs and preferences of key stakeholders, including families and healthcare professionals.17 Yet survivors’ motivating factors for seeking care, including their perceived benefits and importance of engaging in survivorship care, are unclear. It also remains unknown what roles the experience of late effects, and survivors’ reported motivating factors, play in their actual engagement in survivorship care. Understanding survivors’ late effects, perceived motivators for engaging in survivorship care, and potentially modifiable factors associated with their engagement is critical to ensuring appropriate services are available to meet the needs of the growing survivor population. In this study, we, therefore, aimed to:
Describe childhood cancer survivors’ reported cancer late effects, categorized by their primary diagnosis.
Evaluate the clinical (eg, treatment intensity and years’ since diagnosis) and demographic (eg, age and rurality) factors associated with the number of reported late effects.
Understand survivors’ motivating factors for engaging in survivorship care, including their perceived benefits or importance (eg, for education and reassurance).
Assess the clinical and demographic factors associated with engagement in survivorship care, including survivors’ reported late effects and motivators for engaging in care.
Methods
We used a cross-sectional observational questionnaire design. This study forms a part of a larger project; the Australian and New Zealand Children’s Haematology/Oncology Group Survivorship Study.17,18 We received ethics approval from the local institutional boards of the 11 Australian and New Zealand recruiting hospitals (Ref:12/POWH/345). We recruited participants from January, 2016 to April, 2018. For this paper, we observed the Strengthening the Reporting of Observational Studies in Epidemiology statement for reporting for observational research.19
Participants
We recruited survivors of childhood cancer if they: Were diagnosed with any cancer type before their 16th birthday, were at least 5 years from diagnosis (ie, were long-term survivors), and had completed cancer treatment and were in remission. Survivors aged over 16 years (“older survivors”) completed their own questionnaire, while parents of survivors younger than 16 years (“younger survivors”) completed the questionnaire on their child’s behalf. We excluded survivors who did not have sufficient English to understand the questionnaire. All participants provided implied consent by returning their completed questionnaire.
Recruitment
We identified participants via participating hospitals’ medical records, with attendance at a survivorship clinic not being a prerequisite. We posted study invitations and questionnaires to survivors, including a postage-paid envelope to return the questionnaire, and a link to complete the questionnaire online if they preferred. For survivors <16 years, we addressed invitations to their parent/guardian.
Measures
We collected survivors’ sex, current age at study participation, and area of residence (coded as 0:“metropolitan” vs. 1:“rural/regional” according to the Accessibility/Remoteness Index of Australia categories). We also collected participants’ (older survivors’ or parents of young survivors’) education level (coded as 0:“high school only” vs 1:“post-school qualifications”), income (coded as 0: “<$60 000 AUD” vs “≥$60 000 AUD”), current marital status, current employment status, and private health insurance status. In addition, participants reported survivors’ relevant clinical information including primary diagnosis, treatment(s) received, and date of diagnosis (used to calculate the time since diagnosis). For analysis, we categorized diagnoses into the following groups (with ≥35 reported cases): Leukaemia, lymphoma, brain tumor, Wilms’ tumor, sarcoma, neuroblastoma, and another category that included all “other” diagnoses. We categorized participants’ treatment intensity according to the Intensity of Treatment Rating Scale version 3 (ITR-3), from least intensive (rating 1) to most intensive (rating 4).20 Participants also reported whether the survivor was currently attending a survivorship clinic for cancer-related follow-up care.
Participants identified late effects that they or their child had experienced from a list of 19 common late effects (Table 1), identified via a literature search of commonly reported late effects. We described each of the late effects listed in lay terms to maximize comprehension (eg, we used the term “hormone issues” rather than “endocrine”). We invited participants to indicate their motivating factors for attending survivorship care on a list of 15 potential factors informed by a literature search and previous research conducted on this topic (Table 1).21 For analysis, we summed the total number of late effects and motivating factors reported by each participant.
Table 1.
List of 19 common late effects, and motivating factors for attending a survivorship clinic, informed by previous research,21 that were provided to participants in the questionnaire.
| Q. Since finishing cancer treatment, have you experienced any of the following: (please select all that apply) |
Q. When thinking about whether or not to attend a long term follow-up clinic, how important is each item below? (response options ranged from 1 = not at all important, 2 = important, 3 = very important) |
|---|---|
| Pain | a. Getting reassurance about my health |
| Thyroid issues | b. Checking that the cancer has not come back |
| Osteoporosis | c. Checking that I have not developed a second cancer |
| Sexual issues | d. Visiting with the people who cared for me when I had cancer |
| Fatigue | e. Receiving care for health problems related to my cancer and/or treatment |
| Heart issues | f. Receiving care for emotional concerns related to my cancer and/or treatment |
| Lymphedema | Learning about: |
| Emotional issues | g. my diagnosis and/or cancer treatment |
| Dental issues | h. health problems that may occur later in life due to my cancer and/or treatment |
| Hormone issues | i. screening and diagnostic tests to maintain my health |
| Vision/hearing | j. how best to care for myself |
| Pregnancy | k. everyday things like insurance, education, employment, pensions, etc. |
| Immunity issues | l. how to communicate with my general practitioner |
| Mobility issues | m genetic information related to my cancer |
| Fertility issues | n. How best to help children with cancer |
| Lung problems | o. How best to help survivors of childhood cancer |
| Memory or learning difficulties | |
| Blood pressure | |
| Gut problems |
Data Analysis
We used SPSS26.0 for all statistical analyses.22 We described participant characteristics and the number of late effects reported using descriptive statistics, including means, standard deviations, and proportions where appropriate. Where relevant we assessed differences between groups using Chi-squared tests, Mann-Whitney U-tests, or one-way ANOVAs (excluding comparisons with <5 cases), with Bonferroni corrections, applied to adjust for multiple comparisons. In univariable and multivariable logistic regression analyses, we identified demographic and clinical factors associated with engagement in survivorship care (indexed by whether the participant indicated that the survivor was currently attending a survivorship clinic). We conducted 2 separate multivariable models, including all relevant clinical and demographic factors in each, respectively. Results were considered statistically significant when P < .05 (2-tailed).
Results
Participant Characteristics
Of 1176 eligible and contactable childhood cancer survivors, we received 634 completed questionnaires (54% response rate), 404 (63.7%) adult survivors of childhood cancer, and 230 (36.3%) parents of young survivors. Survivors were 51.7% female, on average 21.7 years old, and 15.9 years from their primary diagnosis (Table 2). The most common diagnoses were leukemia (44.2%), lymphoma (12.1%), and brain tumor or sarcoma (both 10.7%). The majority of survivors were treated with chemotherapy (93.0%). Most survivors (61.2%) were diagnosed between 2000 and 2010, followed by survivors diagnosed between 1990 and 1999 (22.7%). According to the ITR-3 ratings, survivors most commonly received “very intensive” treatment (rating 3, 38.7%), followed by “moderately intensive” treatment (rating 2, 35.4%). Fifty-five percent of survivors were currently engaged in survivorship care. Participating survivors were more likely to be female (51.7%) compared to non-respondents (43.9%, P = .009), and older (mean age: 21.7 vs. 20.1, t (1150) = −2.827, P = .005).
Table 2.
Participants’ clinical and demographic characteristics, by primary cancer diagnosis.
| Characteristica | All survivors (n = 634) | Leukaemia survivors (n = 278) | Lymphoma survivors (n = 76) |
Brain tumor survivors (n = 67) |
Sarcoma survivors (n = 67) |
Wilms’ tumor survivors (n = 43) |
Neuroblastoma survivors (n = 39) |
Other cancer diagnoses (n = 59)b |
|---|---|---|---|---|---|---|---|---|
| n (%) | n (%) | n (%) | n (%) | n (%) | n (%) | n (%) | n (%) | |
| Male survivors | 305 (48.3) | 136 (48.9) | 37 (48.7) | 32 (48.5) | 27 (40.9) | 20 (46.5) | 15 (60.3) | 35 (60.3) |
| Rural statusc | ||||||||
| Major city | 437 (76.7) | 192 (77.4) | 54 (79.4) | 43 (67.2) | 46 (70.3) | 26 (70.3) | 29 (78.4) | 43 (79.6) |
| Regional/remote | 133 (23.3) | 56 (22.6) | 14 (20.6) | 21 (32.8) | 12 (29.7) | 11 (29.7) | 8 (21.6) | 11 (20.4) |
| Currently married/de facto | 295 (47.0) | 129 (46.7) | 43 (57.3) | 17 (25.4) | 22 (48.8) | 22 (51.2) | 21 (53.8) | 36 (63.2) |
| Education | ||||||||
| High school only | 248 (40.0) | 106 (39.1) | 23 (30.7) | 30 (45.5) | 33 (49.3) | 19 (45.2) | 18 (46.2) | 17 (30.4) |
| Post-school (eg, university) | 372 (60.0) | 165 (60.9) | 52 (69.3) | 36 (54.5) | 34 (50.7) | 23 (54.8) | 21 (53.8) | 39 (69.6) |
| Currently employed | 455 (73.3) | 186 (68.1) | 61 (82.4) | 48 (71.6) | 47 (72.3) | 40 (93.0) | 30 (76.9) | 41 (73.2) |
| Income | ||||||||
| <$60 000 AUD | 260 (48.6) | 113 (49.3) | 30 (46.2) | 33 (58.9) | 30 (50.0) | 18 (47.4) | 15 (42.9) | 20 (40.8) |
| ≥$60 000 AUD | 275 (51.4) | 116 (50.7) | 35 (53.8) | 23 (41.1) | 30 (50.0) | 20 (52.6) | 20 (57.1) | 29 (59.2) |
| Private health insurance | 411 (66.3) | 182 (65.7) | 51 (70.8) | 43 (65.2) | 40 (61.5) | 26 (61.9) | 23 (59.0) | 43 (78.2) |
| Treatment(s) received | ||||||||
| Surgery | 277 (48.6) | 10 (4.3) | 37 (50.7) | 57 (90.5) | 53 (84.1) | 43 (100) | 35 (92.1) | 41 (78.8) |
| Chemotherapy | 575 (93.0) | 274 (98.6) | 69 (93.2) | 50 (82.0) | 61 (93.8) | 42 (97.7) | 33 (84.6) | 44 (80.0) |
| Radiation | 248 (43.6) | 90 (35.4) | 27 (40.3) | 50 (76.9) | 37 (61.7) | 20 (47.6) | 13 (39.4) | 11 (24.4) |
| Bone marrow/stem cell transplant | 110 (20.3) | 60 (25.0) | 12 (17.4) | 8 (15.1) | 7 (12.7) | 3 (7.9) | 17 (47.2) | 3 (6.3) |
| Engaged in survivorship care | 347 (55.2) | 165 (59.8) | 33 (43.4) | 31 (47.0) | 39 (58.2) | 22 (52.4) | 24 (63.2) | 29 (49.2) |
| Treatment intensity (ITR-3)d | ||||||||
| Rating 1 (least intensive) | 25 (5.1) | 0 | 0 | 0 | 3 (5.2) | 15 (48.4) | 0 | 7 (14.9) |
| Rating 2 | 172 (35.4) | 101 (48.3) | 35 (63.6) | 10 (18.9) | 1 (1.7) | 0 | 5 (15.2) | 20 (42.6) |
| Rating 3 | 188 (38.7) | 53 (25.4) | 14 (25.5) | 35 (66.0) | 45 (77.6) | 16 (51.6) | 11 (33.3) | 14 (29.8) |
| Rating 4 (most intensive) | 101 (20.8) | 55 (26.3) | 6 (10.9) | 8 (15.1) | 9 (15.5) | 0 | 17 (51.5) | 6 (12.8) |
| Mean (SD) | Mean (SD) | Mean (SD) | Mean (SD) | Mean (SD) | Mean (SD) | Mean (SD) | Mean (SD) | |
|---|---|---|---|---|---|---|---|---|
| Survivors’ age | 21.7 (8.9) | 21.1 (8.5) | 26.6 (9.8) | 23.6 (7.4) | 22.2 (8.7) | 21.1 (10.6) | 17.4 (7.7) | 18.0 (8.1) |
| Range | 7-61 | 7-48 | 12-61 | 11-53 | 9-45 | 8-56 | 8-37 | 7-49 |
| Years’ since diagnosis | 15.9 (7.9) | 15.9 (7.9) | 16.7 (9.2) | 16.4 (7.0) | 15.3 (7.5) | 18.1 (10.0) | 14.6 (6.4) | 14.6 (7.2) |
| Range | 5-59 | 5-42 | 5-59 | 6-45 | 6-37 | 6-44 | 6-36 | 6-44 |
| Total number of motivators for engaging in survivorship care | 12.5 (2.9) | 12.5 (3.1) | 11.8 (3.0) | 12.6 (2.8) | 12.6 (2.6) | 12.7 (2.2) | 13.4 (2.0) | 12.3 (3.1) |
| Range | 0-15 | 0-15 | 3-15 | 3-15 | 6-15 | 6-15 | 7-15 | 1-15 |
Numbers and percentages may not add up due to missing values and rounding errors. Five survivors did not report their primary cancer diagnosis.
aParent demographic data is reported for young survivors (<16 years); while child survivors’ clinical data is reported (parent proxy).
bOther cancers mostly consisted of hepatoblastoma (n = 14), followed by retinoblastoma (n = 12), and germ cell tumors (n = 6).
cAccording to Area of Remoteness Index Australia (ARIA) classifications. We manually categorized New Zealand postcodes according to the Statistics New Zealand Urban/Rural Profile Classifications.
dTreatment intensity assessed using the Intensity of Treatment Rating ITR-3.20
Abbreviations: ITR-3, intensity of treatment rating version 3; N, number of participants.
Childhood Cancer Survivors’ Reported Cancer Late Effects by Diagnosis
At an average of 15.9 years since their primary diagnosis, participants reported that 79.2% of survivors had experienced at least one late effect related to their cancer/treatment. More than half (52.5%) reported 3 or more late effects. There was a statistically significant difference in late effects burden between diagnostic groups as determined by a one-way ANOVA (F6,622 = 8.270, P < .001; Fig. 1). Post hoc tests revealed that when compared to all other cancer diagnoses, participants reported a higher total number of late effects in brain tumor survivors (mean = 5.7 vs. mean = 3.2, Bonferroni corrected P < .001), and a lower number of late effects in Wilms’ tumor survivors (mean = 1.8 vs. mean = 3.5, Bonferroni corrected P < .001). We did not observe any other significant differences in the number of late effects by a cancer diagnosis in post hoc analyses.
Figure 1.
Total number of reported late effects, by primary cancer diagnosis.
The proportion of late effects reported by participants is categorized by a cancer diagnosis in Fig. 2. Fatigue was the most commonly reported late effect among leukemia (35.2%) and lymphoma (49.3%) survivors, and was among the top 5 reported across all diagnoses. Sarcoma and Wilms’ tumor survivors’ most commonly reported late effect was pain (46.2% and 31.7%, respectively), while brain tumor survivors most commonly reported memory and learning difficulties (63.6%) and neuroblastoma survivors most commonly reported dental problems (55.6%). Emotional problems were the only other late effect among the top 5 reported late effects across all diagnoses (24.4%-43.9%). Dental problems were reported in the top 5 for all diagnosis groups (between 24.4% and 55.6%) except for brain tumor survivors.
Figure 2.
Proportion of participants reporting each cancer-related late effect, by primary cancer diagnosis.
There was evidence of differences between each diagnosis group overall in the proportion of survivors reporting late effects relating to thyroid problems (χ2 = 45.284, Bonferroni corrected P < .001), hormone issues (χ2 = 55.887, P < .001), vision or hearing problems (χ2 = 79.510, P < .001), pregnancy problems (χ2 = 29.491, P < .001), mobility problems (χ2 = 23.880, P = .020), fertility issues (χ2 = 29.503, P < .001), and memory/learning issues (χ2 = 39.767, P < .001). We did not observe any other significant overall differences between the proportions of participants in each cancer diagnosis group reporting any other late effects (all Bonferroni corrected P > .05).
Post hoc analyses revealed that when compared to survivors of all other cancers, participating survivors/parents were less likely to report that leukemia survivors experienced hormone problems (18.1% vs. 28.1%, χ2 = 8.137, P = .02), problems with vision or hearing (15.2% vs. 31.3%, χ2 = 21.32, P < .001), and fertility (9.6% vs. 20.6%, χ2 = 13.586, P < .001).
Participating survivors/parents reported that lymphoma survivors were more likely to experience problems with their immunity than survivors of all other cancers (46.6% vs. 30.3%, χ2 = 7.82, P = .030).
Compared to survivors of all other cancers, participating survivors/parents reported that brain tumor survivors were more likely to experience memory or learning difficulties (63.6% vs. 30.8%, χ2 = 28.106, P < .001), problems with their vision and/or hearing (56.1% vs. 20.2%, χ2 = 41.249, P < .001), hormone issues (54.5% vs. 19.9%, χ2 = 39.212, P < .001), thyroid issues (37.9% vs 11.4%, χ2 = 33.589, P < .001), problems with their mobility (31.8% vs. 13.7%, χ2 = 14.535, P < .001), fertility problems (30.3% vs. 13.9%, χ2 = 11.931, P = .006), and problems in pregnancy (13.6% vs. 2.6%, χ2 = 19.593, P < .001).
Participating survivors/parents reported Wilms’ tumor survivors were less likely to report hormone issues (4.9% vs 25.5%, χ2 = 8.905, P = .018), or problems with their vision and/or hearing (4.9% vs 25.5%, χ2 = 41.249, P < .001), than survivors of all other cancers. No Wilms’ tumor survivors reported problems with their thyroid, compared to 15.3% among other cancer diagnoses (χ2 = 7.156, P = .042).
Compared to survivors of all other cancers, participating survivors/parents reported that neuroblastoma survivors more commonly experienced problems with their vision or hearing (47.2% vs 22.7%, χ2 = 11.146, P < .001).
Clinical and Demographic Factors Associated with the Number of Reported Late Effects
We observed a higher number of reported late effects on average in leukaemia survivors who had been treated with radiotherapy (mean = 3.9 vs 2.7, U = 8481, P = .047), who received the most/very intensive treatment (mean = 3.8 vs 2.8 for those with the least/moderate treatment intensity, U = 6314, P = .047), and survivors with a lower income (mean = 3.5 for <60 000 AUD vs 2.7 for ≥60 000 AUD, U = 5559, P = .045).
Participating survivors/parents reported that lymphoma survivors with a greater number of late effects on average had undergone a bone marrow transplant (mean = 5.3 vs 3.0, U = 497, P = .013), and received the most/very intensive treatment intensity (mean = 4.7 vs 2.4, U = 505, P = .006).
Participating survivors/parents reported that brain tumor survivors experienced a greater number of late effects on average if they had been treated with chemotherapy (mean = 6.5 vs 2.7, U = 863, P = .046), or had undergone a bone marrow transplant (mean = 10.9 vs 5.0, U = 321, P < .001), or received the very/most intensive treatment compared to the least/moderate treatment intensity (mean = 6.5 vs 3.0, U = 325, P = .012). Brain tumor survivors also had the total higher average number of late effects if they were currently unemployed (mean = 7.9 vs 4.9, U = 226, P = .001).
Participating survivors/parents reported that sarcoma survivors who had undergone a bone marrow transplant (mean = 6.1 vs 3.9, U = 246, P = .049) or were currently unemployed (mean = 5.8 vs 3.4, U = 273.5, P = .027) experienced a greater number of late effects on average.
Female Wilms’ tumor survivors were reported to have a higher average number of late effects than male Wilms’ tumor survivors (3.0 vs 1.2, U = 326.5, P = .016), as did Wilms’ tumor survivors living in rural/regional compared to metropolitan areas (3.3 vs 1.5, U = 209, P = .028).
Participating survivors/parents reported that neuroblastoma survivors had experienced a greater number of late effects on average if they had been treated with chemotherapy (4.6 vs 0.8, U = 169, P = .005) or radiotherapy (6.6 vs 2.4, U = 222, P < .001), or had undergone a bone marrow transplant (mean = 6.7 vs 1.8, U = 297.5, P < .001), compared to those who had not received chemotherapy, radiotherapy, or a transplant. Survivors who were currently unemployed also experienced a greater number of late effects on average (mean = 6.3 vs 3.3, U = 76, P = .048).
Besides the factors listed for each diagnosis earlier, we did not observe strong evidence that any other clinical (eg, time since diagnosis) or demographic factors (eg, age and insurance) were associated with the average number of late effects reported in each group.
Motivating Factors for Engaging in Survivorship Care (eg, Education and Reassurance)
All participants endorsed at least one motivating factor for engaging in survivorship care. The average number of motivating factors endorsed by participants was 12.5 (SD = 2.9). Participants’ with 3 most commonly reported motivators for engaging in care were to understand problems that may occur later in life because of their cancer and/or treatment (98.5%, Fig. 3), to receive reassurance about one’s health (97.4%), and to receive education about screening and diagnostic tests to maintain health (96.5%). The 3 least endorsed motivating factors were to learn about “everyday things” such as health insurance or pension (61.0%), to learn about how best to communicate with their general practitioner (GP, 65.5%), and to visit the people who cared for them during their cancer treatment (69.4%).
Figure 3.
Proportion of participants endorsing motivators for engaging in survivorship care.
The average number of motivating factors was similar across survivors with different cancer diagnoses, ranging from 11.8 in lymphoma survivors to 13.4 in neuroblastoma survivors (F6,614 = 11.532, P = .214; Table 2). The proportions of survivors endorsing each of the motivators listed in the questionnaire were similar across cancer diagnoses also, with the exception of “to learn more about everyday things (eg, insurance and pensions)” which appeared lowest in lymphoma survivors (41.3%) and highest in brain tumor survivors (80.3%, P < .001).
Clinical and Demographic Factors Associated with Engagement in Survivorship Care
The results of the univariable and multivariable analyses are presented in Table 3. Among demographic factors evaluated in multivariable analyses, older survivors were less likely to be engaged in survivorship care than younger survivors (odd ratio [OR]; OR = 0.904, 95% CI, 0.879-0.929, P < .001). Among clinical factors evaluated in multivariable analyses, survivors were more likely to be engaged in survivorship care if they reported a higher number of motivators for engaging in survivorship care (OR = 1.101 per motivator, 95% CI, 1.018-1.192, P = .016) or had less time since their cancer diagnosis (OR = 1.098 per year, 95% CI, 1.140-1.057, P < .001). We did not observe any other clinical or demographic factors that were significantly associated with engagement in survivorship care in multivariable analyses.
Table 3.
Factors associated with engagement in survivorship care analyses in univariable and multivariable analyses.
| Univariable | Multivariable | |||||
|---|---|---|---|---|---|---|
| OR | 95% CI | P-value | OR | 95% CI | P-value | |
| Model 1: Demographic characteristics | ||||||
| Male survivors | 0.987 | 0.720, 1.353 | .937 | 1.165 | 0.776, 1.748 | .461 |
| Age | 0.900 | 0.880, 0.921 | <.001 | 0.904 | 0.879, 0.929 | <.001 |
| Currently married/de facto | 1.731 | 1.257, 2.382 | <.001 | 1.366 | 0.837, 2.230 | .212 |
| Area of residence (major city vs regional/rural) | 0.843 | 0.570, 1.245 | .389 | 0.785 | 0.491, 1.256 | .312 |
| Income (<$60 000 AUD vs ≥$60 000 AUD) | 1.540 | 1.091, 2.173 | .014 | 1.117 | 0.686, 1.819 | .658 |
| Private health insurance | 0.733 | 0.522, 1.029 | .073 | 0.847 | 0.546, 1.314 | .458 |
| Post-school education level | 0.827 | 0.597, 1.146 | .253 | 0.857 | 0.547, 1.342 | .499 |
| Currently employed | 0.894 | 0.623, 1.283 | .545 | 0.917 | 0.555, 1.516 | .735 |
| Model 2: Clinical characteristics | ||||||
| Diagnosis | ||||||
| Leukaemia a | ||||||
| Lymphoma | 1.538 | 0.875, 2.704 | .135 | 1.003 | 0.371, 2.714 | .995 |
| Brain tumor | 0.794 | 0.401, 1.572 | .508 | 0.584 | 0.210, 1.627 | .304 |
| Sarcoma | 0.916 | 0.454, 1.851 | .807 | 0.808 | 0.293, 2.226 | .680 |
| Wilms’ tumor | 1.138 | 0.515, 2.512 | .749 | 1.596 | 0.465, 5.485 | .458 |
| Neuroblastoma | 1.441 | 0.712, 2.914 | .309 | 1.215 | 0.445, 3.321 | .704 |
| Other cancers | 1.773 | 0.770, 4.082 | .178 | 1.301 | 0.406, 4.161 | .658 |
| Treatment(s) received | ||||||
| Surgery | 0.608 | 0.435, 0.849 | .003 | 0.660 | 0.311, 1.402 | .280 |
| Chemotherapy | 4.289 | 2.068, 8.892 | <.001 | 3.032 | 0.931, 9.871 | .066 |
| Radiation | 0.896 | 0.642, 1.252 | .521 | 1.201 | 0.684, 2.109 | .523 |
| Bone marrow/stem cell transplant | 1.988 | 1.275, 3.099 | .002 | 1.831 | 0.882, 3.803 | .105 |
| Treatment intensity (ITR-3) | ||||||
| Rating 1 (least intensive) a | ||||||
| Rating 2 | 0.409 | 0.168, 0.997 | .049 | 0.603 | 0.136, 2.667 | .505 |
| Rating 3 | 0.597 | 0.354, 1.005 | .052 | 0.830 | 0.373, 1.844 | .647 |
| Rating 4 (most intensive) | 0.483 | 0.289, 0.805 | .005 | 0.501 | 0.239, 1.047 | .066 |
| Years since diagnosis | 0.893 | 0.869, 0.917 | <.001 | 0.911 | 0.877, 0.946 | <.001 |
| Total number of late effects | 1.008 | 0.963, 1.056 | .720 | 0.979 | 0.910, 1.054 | .576 |
| Total number of motivators for engaging in survivorship care | 1.097 | 1.037, 1.161 | .001 | 1.101 | 1.018, 1.192 | .016 |
aThe reference category.
Bold font indicates significant values (P < .05). Abbreviations: AUD, Australian Dollars; ITR-3, intensity of treatment rating V3; OR, odds ratio.
Discussion
These data provide an understanding of the burden of childhood cancer-related late effects in Australian and New Zealand, motivating factors for engaging in survivorship care, and associated clinical and demographic factors. Participants most commonly reported that survivors had experienced fatigue (40.4%), and memory/learning difficulties (34.3%). Brain tumor survivors reported a higher total number of reported late effects than other diagnoses (mean = 5.7 vs. 3.2). The average number of motivating factors for engaging in survivorship care endorsed by participants was similar across cancer diagnoses, as was the proportion of survivors endorsing each of the listed motivators, with the exception of learning more about insurance and pensions, which was most endorsed for brain tumor survivors. Around half (55%) of survivors were engaged in survivorship care, with engagement being more likely in survivors who were younger, closer in years to their diagnosis, or reported a total higher number of motivating factors. Engagement in survivorship care was not significantly associated with the total number of participants who reported late effects.
The proportion of participants in our study who reported that survivors experienced at least one late effect related to their cancer/treatment (79.2%, on average 16 years from diagnosis) appears to be similar or higher than global reports such as in Norwegian survivors (61.5%, on average 17 years from diagnosis),23 North American survivors (69%, on average 15 years from diagnosis),24 or Korean survivors (73.1%, on average 12 years from diagnosis), although the number/type of late effects assessed generally varied.25 A recent study showed that the self-reported health status of survivors has not improved in recent decades, despite improving cancer survival rates which have instead resulted in a greater number of survivors living with cancer-related health problems who may have died if they were treated earlier decades.26 In our cohort, more than half (52.5%) of participants reported that survivors experienced 3 or more physical and psychological late effects, reflecting the diversity and complexity of the health problems that survivors experience decades post-diagnosis. This highlights the importance of a personalized and multidisciplinary approach to survivorship care, involving primary care physicians, subspecialists, and supportive care clinicians, to achieve optimal management of these health problems from the moment a child or young person is diagnosed with cancer.27,28
Echoing previous studies,23,25 participants in our study most commonly reported fatigue and memory/learning difficulties. Some sub-groups such as Wilms’ tumor survivors, commonly reported long-term pain, consistent with prior literature.29 While these may be considered less severe cancer-related late effects, their significant impact on survivor’s daily lives and quality of life is well-documented.30,31 Despite evidence-based recommendations for the surveillance and management of cancer-related fatigue in young survivors,32 fatigue is not a commonly addressed late effect in Australian survivorship clinics,33 although it is unclear if this is due to low patient reporting or limited screening for fatigue. Our data were collected prior to the global coronavirus pandemic, however, it would be of interest to evaluate whether survivors’ self-report of some late effects (eg, their perceptions regarding immunity problems) have been impacted by COVID-19.34 Unsurprisingly, a higher treatment intensity according to the ITR-3 was a common factor associated with a higher reported number of late effects across several diagnoses in our sample. While we did not collect specific treatment data (eg, site and total dose) to understand the relationship between specific treatment(s) received and symptoms or late effects, further evaluation is needed to understand specific treatment-related toxicities, particularly with the evolution of treatments in recent decades.
Around half (55%) of survivors reported that they were currently attending a survivorship clinic, which was less likely in older survivors. Lower rates of attendance with age may be due to “empty” episodes of care and a resulting decline in survivors’ perceived importance or need to continue attending, despite potentially increased late effects risks with age.17 Alternatively, it may reflect decreasing parental involvement, the better provision of services over time, improved patient education, and/or the increasing involvement of GPs and specialist care as self-management and risk stratification becomes more common elements of long-term survivorship care. In contrast with our findings, Casillas et al. (2015) reported that male survivors with a lower income and education, and with severe/life-threatening conditions, were less likely to be engaged in survivorship care.35 In our sample, we did not observe a relationship between the number of reported late effects and engagement in survivorship care, which could also reflect that survivors with more serious late effects (eg, endocrine or cardiac disease) may have been managed by physicians outside of a survivorship clinic instead. However, few survivors appear to engage with their GP for cancer-related care, warranting efforts to improve GP involvement and training to improve survivor-reported low confidence in their GP’s cancer survivorship knowledge.36
Despite sub-optimal levels of attendance at a survivorship clinic among survivors in our sample, the vast majority appeared to recognize its potential benefits by endorsing multiple motivating factors (mean = 12.9). Two of the most commonly endorsed motivators were seeking education about cancer-related late effects and screening tests needed (both >96%), which appear to be congruent with the top perceived benefits of survivorship care reported by oncology health professionals.37 In a similar US study,21 these same factors appeared comparatively of lower importance to survivors (<51%). It is important to note that even the less commonly endorsed motivating factors in our study, such as learning about “everyday things” such as health insurance or communicating with their GP, was endorsed by a significant proportion of survivors (ie, at least 61% or more). Responses from parents may reflect their, rather than the survivors’, motivating factors for engaging in the survivorship clinic, which may be valuable to evaluate further or compare in future research.
The second highest reported motivator in our study was to receive reassurance about their health, which was significantly associated with actual engagement in survivorship care in regression analyses, despite the fact that the number of late effects that survivors had experienced was not significantly associated. It is possible that the survivors who may be most motivated to attend to gain reassurance about their health (eg, to alleviate a fear of cancer recurrence) may not necessarily be the survivors who have the highest need for the specialized survivorship services available in Australia and New Zealand.38 The relationship between worry about cancer-related health problems and its influence on survivorship care engagement appears to be complex.39,40 Adequately educating survivors about their risk of late effects, and the appropriate level of risk-based surveillance needed (eg, GP-led survivorship care vs specialist-led care), without raising their anxiety remains a significant challenge.40 However, this is important to overcome as risk-stratified models of care become increasingly important to alleviate the pressures of the growing number of survivors on limited services and resources that are available.
Strengths and Limitations
This multi-center study is the largest Australian/New Zealand questionnaire study of childhood cancer survivors’ long-term health. Despite using strategies to maximize our response rate including three follow-up calls per non-respondent and the use of novel video invitations,18 our response rate was modest (54%). Yet, respondents included caregivers and long-term survivors across a wide age range (up to 59 years), representing survivors treated over a number of treatment eras and who were both engaged and disengaged from survivorship care. Although we relied on cross-sectional, self-reported, and parent proxy data to assess the long-term health of survivors, studies suggest that cancer survivors’ reported diagnoses are fairly accurate when compared with medical records.41-43 We asked survivors to specifically indicate cancer-related conditions they were experiencing, although they may have included non-cancer-related health conditions. Given space constraints, our list of late effects was not exhaustive, rather it was focused on commonly occurring late effects and did not capture their severity/magnitude. We did not provide definitions of each of the late effects listed in our survey, using lay terms instead. It is therefore possible that some participants did not select response options if they did not understand them or did not know which health conditions might have been classified within those larger categories. Future studies should collect more longitudinal data, and ideally supplement data with medical records information and data linkage.
Conclusion
This study assessed childhood cancer survivors’ reported late effects by a cancer diagnosis, and their perceptions regarding the importance of engaging in survivorship care, including motivating factors, and clinical/demographic factors associated with their engagement in survivorship care. Survivors experience a range of health problems even decades after treatment completion. Understanding the burden of late effects, and survivors’ motivators for seeking survivorship care to manage these health problems, is important for ensuring tailored interventions and services that are available to meet the needs of this growing population and to design effective models of survivorship care.
Acknowledgments
The authors thank to Joe Alchin (Kids Cancer Centre, Sydney Children’s Hospital; School of Clinical Medicine, Discipline of Paediatrics, UNSW Sydney) for his assistance preparing data for analysis, and Mark Donoghoe (Stats Central, Mark Wainwright Analytical Centre, UNSW Sydney) for his statistical advice. We would also like to thank the families who participated and each of the recruiting sites including: Sydney Children’s Hospital Randwick, the Children’s Hospital at Westmead, John Hunter Children’s Hospital, the Royal Children’s Hospital Melbourne, Monash Children’s Hospital Melbourne, Children’s Hospital Queensland (formerly the Royal Children’s Hospital Brisbane), Perth Children’s Hospital (formerly Princess Margaret Children’s Hospital Perth), Women’s and Children’s Hospital Adelaide, and in New Zealand, Starship Children’s Hospital, Wellington Hospital and Christchurch Hospital. We acknowledge the Department of Health Western Australia and Data Linkage Branch for access to participants’ vital status information.
The members of the ANZCHOG Survivorship Study Group in alphabetical order: Dr. Frank Alvaro, Prof. Richard Cohn, Dr. Rob Corbett, Dr. Peter Downie, Ms. Karen Egan, Ms. Sarah Ellis, Prof. Jon Emery, Dr. Joanna Fardell, Ms. Tali Foreman, Dr. Melissa Gabriel, Prof. Afaf Girgis, Ms. Kerrie Graham, Ms. Karen Johnston, Dr. Janelle Jones, Dr. Liane Lockwood, Dr. Ann Maguire, Dr. Maria McCarthy, Dr. Jordana McLoone, Dr. Francoise Mechinaud, Ms. Sinead Molloy, Ms. Lyndal Moore, Dr. Michael Osborn, Dr. Christina Signorelli, Dr. Jane Skeen, Dr. Heather Tapp, Ms. Tracy Till, Ms. Jo Truscott, Ms. Kate Turpin, Prof. Claire Wakefield, Ms. Jane Williamson, Dr. Thomas Walwyn, and Ms. Kathy Yallop.
Contributor Information
Christina Signorelli, Kids Cancer Centre, Sydney Children’s Hospital, Randwick, NSW, Australia; Discipline of Paediatrics & Child Health, School of Clinical Medicine, UNSW Sydney, NSW, Australia.
Claire E Wakefield, Kids Cancer Centre, Sydney Children’s Hospital, Randwick, NSW, Australia; Discipline of Paediatrics & Child Health, School of Clinical Medicine, UNSW Sydney, NSW, Australia.
Jordana K McLoone, Kids Cancer Centre, Sydney Children’s Hospital, Randwick, NSW, Australia; Discipline of Paediatrics & Child Health, School of Clinical Medicine, UNSW Sydney, NSW, Australia.
Karen A Johnston, Kids Cancer Centre, Sydney Children’s Hospital, Randwick, NSW, Australia; Discipline of Paediatrics & Child Health, School of Clinical Medicine, UNSW Sydney, NSW, Australia.
Ann C Mertens, Department of Pediatrics, Emory University School of Medicine, Atlanta, GA, USA; Aflac Cancer & Blood Disorders Center, Children’s Healthcare of Atlanta, Atlanta, GA, USA; Department of Epidemiology, Emory University Rollins School of Public Health, Atlanta, GA, USA.
Michael Osborn, Youth Cancer Service SA/NT, Royal Adelaide Hospital, Adelaide, Australia.
Richard J Cohn, Kids Cancer Centre, Sydney Children’s Hospital, Randwick, NSW, Australia; Discipline of Paediatrics & Child Health, School of Clinical Medicine, UNSW Sydney, NSW, Australia.
ANZCHOG Survivorship Study Group:
Dr. Frank Alvaro, Prof. Richard Cohn, Dr. Rob Corbett, Dr. Peter Downie, Ms. Karen Egan, Ms. Sarah Ellis, Prof. Jon Emery, Dr. Joanna Fardell, Ms. Tali Foreman, Dr. Melissa Gabriel, Prof. Afaf Girgis, Ms. Kerrie Graham, Ms. Karen Johnston, Dr. Janelle Jones, Dr. Liane Lockwood, Dr. Ann Maguire, Dr. Maria McCarthy, Dr. Jordana McLoone, Dr. Francoise Mechinaud, Ms. Sinead Molloy, Ms. Lyndal Moore, Dr. Michael Osborn, Dr. Christina Signorelli, Dr. Jane Skeen, Dr. Heather Tapp, Ms. Tracy Till, Ms. Jo Truscott, Ms. Kate Turpin, Prof. Claire Wakefield, Ms. Jane Williamson, Dr. Thomas Walwyn, and Ms. Kathy Yallop
Funding
Dr Christina Signorelli is supported by a Cancer Institute NSW Early Career Fellowship (2020/ECF1144). Prof. Claire Wakefield is supported by the National Health and Medical Research Council of Australia (APP2008300). Dr Jordana McLoone is supported by a Medical Research Future Fund grant (MRFBC000002). This study was supported by the Kids Cancer Alliance. The Behavioural Sciences Unit (BSU) is proudly supported by the Kids with Cancer Foundation. The BSU’s survivorship research program is funded by The Kids’ Cancer Project and a Cancer Council NSW Program Grant PG16-02 with the support of the Estate of the Late Harry McPaul. These funding bodies did not have any role in the study, nor did they have a role in the writing of the manuscript or the decision to submit it for publication.
Conflict of Interest
The authors indicated no financial relationships.
Author Contributions
Conception: C.S., C.W., J.M., R.C. Design: All authors. Provision of study material or patients: R.C., K.J. Collection and/or assembly of data: C.S., J.M. Data analysis and interpretation: led by C.S. with support of all co-authors. Manuscript writing: All authors. Final approval of manuscript: All authors.
Data Availability
The data that support the findings of this study are not publicly available due to privacy or ethical restrictions, and the full dataset is not able to be released due to ethical restrictions. Requests may be made to the authors.
Ethics Statement
We received ethics approval from the local institutional boards of the 11 Australian and New Zealand recruiting hospitals (Ref:12/POWH/345). All participants provided implied consent by returning their completed questionnaire.
References
- 1. Signorelli C, Fardell JE, Wakefield CE, Webber K, Cohn RJ.. The cost of cure: chronic conditions in survivors of child, adolescent, and young adult cancers. In: Cancer and Chronic Conditions. Springer; 2016:371-420. [Google Scholar]
- 2. Bhakta N, Liu Q, Ness KK, et al. The cumulative burden of surviving childhood cancer: an initial report from the St Jude Lifetime Cohort Study (SJLIFE). Lancet. 2017;390(10112):2569-2582. https://doi.org/ 10.1016/s0140-6736(17)31610-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. Schindler M, Spycher BD, Ammann RA, et al. Cause-specific long-term mortality in survivors of childhood cancer in Switzerland: a population-based study. Int J Cancer. 2016;139(2):322-333. https://doi.org/ 10.1002/ijc.30080 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4. Council NR. Childhood Cancer Survivorship: Improving Care and Quality of Life. National Academies Press; 2003. [PubMed] [Google Scholar]
- 5. Fardell JE, Wakefield CE, De Abreu Lourenco R, et al. Long-term health-related quality of life in young childhood cancer survivors and their parents. Pediatr Blood Cancer. 2021;68(12):e29398. [DOI] [PubMed] [Google Scholar]
- 6. Henderson TO, Ness KK, Cohen HJ.. Accelerated aging among cancer survivors: from pediatrics to geriatrics. Am Soc Clin Oncol Educ Book. 2014;34(1):e423-ee30. [DOI] [PubMed] [Google Scholar]
- 7. Henderson TO, Oeffinger KC.. Addressing the health burden of childhood cancer survivors—improvements are needed. Nat Rev Clin Oncol. 2018;15(3):137-138. https://doi.org/ 10.1038/nrclinonc.2017.187 [DOI] [PubMed] [Google Scholar]
- 8. Hudson MM, Ness KK, Gurney JG, et al. Clinical ascertainment of health outcomes among adults treated for childhood cancer. JAMA. 2013;309(22):2371-2381. https://doi.org/ 10.1001/jama.2013.6296 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Hsieh SGS, Hibbert S, Shaw P, Ahern V, Arora M.. Association of cyclophosphamide use with dental developmental defects and salivary gland dysfunction in recipients of childhood antineoplastic therapy. Cancer. 2011;117(10):2219-2227. [DOI] [PubMed] [Google Scholar]
- 10. Anazodo AC, Choi S, Signorelli C, et al. Reproductive care of childhood and adolescent cancer survivors: a 12-year evaluation. J Adolesc Young Adult Oncol. 2021;10(2):131-141. https://doi.org/ 10.1089/jayao.2020.0157 [DOI] [PubMed] [Google Scholar]
- 11. Gunn HM, Rinne I, Emilsson H, et al. Primary gonadal insufficiency in male and female childhood cancer survivors in a long-term follow-up clinic. J Adolesc Young Adult Oncol. 2016;5(4):344-350. https://doi.org/ 10.1089/jayao.2016.0007 [DOI] [PubMed] [Google Scholar]
- 12. Kremer LC, Mulder RL, Oeffinger KC, et al. A worldwide collaboration to harmonize guidelines for the long-term follow-up of childhood and young adult cancer survivors: a report from the International Late Effects of Childhood Cancer Guideline Harmonization Group. Pediatr Blood Cancer. 2013;60(4):543-549. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. Frobisher C, Glaser A, Levitt GA, et al. Risk stratification of childhood cancer survivors necessary for evidence-based clinical long-term follow-up. Br J Cancer. 2017;117(11):1723-1731. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Gan H-W, Spoudeas HA.. Long-term follow-up of survivors of childhood cancer (SIGN Clinical Guideline 132). Arch Dis Child Educ Pract. 2014;99(4):138-43. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Tonorezos ES, Barnea D, Cohn RJ, et al. Models of care for survivors of childhood cancer from across the globe: advancing survivorship care in the next decade. J Clin Oncol. 2018;36(21):22232223.-222322230. https://doi.org/ 10.1200/jco.2017.76.5180 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Snyder C, Choi Y, Smith KC, et al. Realist review of care models that include primary care for adult childhood cancer survivors. JNCI Cancer Spectr. 2022;6(2):pkac012. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17. Signorelli C, Wakefield C, McLoone JK, et al. Childhood cancer survivorship: barriers and preferences. BMJ Support Palliat Care. 2019;12(e5):e687-e695. [DOI] [PubMed] [Google Scholar]
- 18. Signorelli C, Wakefield CE, McLoone JK, et al. A cost-effective approach to increasing participation in patient-reported outcomes research in cancer: a randomized trial of video invitations. Int J Cancer 2020;148(4):971-980. [DOI] [PubMed] [Google Scholar]
- 19. Von Elm E, Altman DG, Egger M, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Ann Intern Med. 2007;147(8):573-577. https://doi.org/ 10.7326/0003-4819-147-8-200710160-00010 [DOI] [PubMed] [Google Scholar]
- 20. Kazak AE, Hocking MC, Ittenbach RF, et al. A revision of the intensity of treatment rating scale: classifying the intensity of pediatric cancer treatment. Pediatr Blood Cancer. 2012;59(1):96-99. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. Mertens AC, Liu W, Ness KK, et al. Factors associated with recruiting adult survivors of childhood cancer into clinic-based research. Pediatr Blood Cancer. 2014;61(10):1846-1851. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22. Arbuckle JL. IBM SPSS Amos 20 User’s Guide. Amos Development Corporation, SPSS Inc; 2011. [Google Scholar]
- 23. Mellblom A, Kiserud CE, Rueegg CS, et al. Self-reported late effects and long-term follow-up care among 1889 long-term Norwegian Childhood, Adolescent, and Young Adult Cancer Survivors (the NOR-CAYACS study). Support Care Cancer. 2021;29(6):2947-2957. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24. Oeffinger KC, Eshelman DA, Tomlinson GE, Buchanan GR, Foster BM.. Grading of late effects in young adult survivors of childhood cancer followed in an ambulatory adult setting. Cancer. 2000;88(7):1687-1695. https://doi.org/ 10.1002/(sici)1097-0142(20000401)88:7<1687::aid-cncr24>3.0.co;2-m [DOI] [PubMed] [Google Scholar]
- 25. Yi J, Kim MA, Tian T.. Perceived long-term and physical health problems after cancer: adolescent and young adult survivors of childhood cancer in Korea. Eur J Oncol Nurs. 2014;18(2):145-150. https://doi.org/ 10.1016/j.ejon.2013.11.006. [DOI] [PubMed] [Google Scholar]
- 26. Ness KK, Hudson MM, Jones KE, et al. Effect of temporal changes in therapeutic exposure on self-reported health status in childhood cancer survivors. Ann Intern Med. 2017;166(2):89-98. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27. Alfano CM, Oeffinger K, Sanft T, Tortorella B.. Engaging TEAM medicine in patient care: redefining cancer survivorship from diagnosis. Am Soc Clin Oncol Educ Book. 2022;42(42):1-11. [DOI] [PubMed] [Google Scholar]
- 28. Brinkman TM, Gurney JG.. Early and often: the need for comprehensive discussion of treatment-induced cancer late effects. Pediatrics. 2020;145(5):e20200498. [DOI] [PubMed] [Google Scholar]
- 29. Schulte FS, Patton M, Alberts NM, et al. Pain in long-term survivors of childhood cancer: a systematic review of the current state of knowledge and a call to action from the Children’s Oncology Group. Cancer. 2021;127(1):35-44. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30. Nunes MDR, Jacob E, Lopes-Júnior LC, Leite ACAB, Lima RAGd, Nascimento LC.. Quality of life of cancer children-adolescents with and without fatigue. ACTA Paul Enferm. 2022;35:eAPE0288345. [Google Scholar]
- 31. Langeveld N, Ubbink M, Smets E, Group DLES.. “I don’t have any energy”: the experience of fatigue in young adult survivors of childhood cancer. Eur J Oncol Nurs. 2000;4(1):20-28. [DOI] [PubMed] [Google Scholar]
- 32. Christen S, Roser K, Mulder RL, et al. Recommendations for the surveillance of cancer-related fatigue in childhood, adolescent, and young adult cancer survivors: a report from the International Late Effects of Childhood Cancer Guideline Harmonization Group. J Cancer Surviv. 2020;14(6):923-938. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33. Kelada L, Wakefield C, Heathcote L, et al. Perceived cancer-related pain and fatigue, information needs, and fear of cancer recurrence among adult survivors of childhood cancer. Patient Educ Couns. 2019;102(12):2270-2278. https://doi.org/ 10.1016/j.pec.2019.06.022 [DOI] [PubMed] [Google Scholar]
- 34. Hou SH, Tran A, Cho S, et al. The perceived impact of COVID-19 on the mental health status of adolescent and young adult survivors of childhood cancer and the development of a knowledge translation tool to support their information needs. Front Psychol. 2022;13:867151. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35. Casillas J, Oeffinger KC, Hudson MM, et al. Identifying predictors of longitudinal decline in the level of medical care received by adult survivors of childhood cancer: a report from the childhood cancer survivor study. Health Services Res. 2015;50(4):1021-1042. https://doi.org/ 10.1111/1475-6773.12282 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36. Signorelli C, Wakefield CE, Fardell JE, et al. The role of primary care physicians in childhood cancer survivorship care: multiperspective interviews. Oncologist. 2019;24(5):710-719. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37. Aziz NM, Oeffinger KC, Brooks S, Turoff AJ.. Comprehensive long-term follow-up programs for pediatric cancer survivors. Cancer. 2006;107(4):841-848. https://doi.org/ 10.1002/cncr.22096 [DOI] [PubMed] [Google Scholar]
- 38. Signorelli C, Wakefield CE, McLoone JK, et al. Models of childhood cancer survivorship care in Australia and New Zealand: strengths and challenges. Asia-Pac J Clin Oncol. 2017;13(6):407-415. [DOI] [PubMed] [Google Scholar]
- 39. Signorelli C, Wakefield CE, Fardell JE, et al. Perceptions of future health and cancer risk in adult survivors of childhood cancer: implications for engagement in follow-up care. Cancer. 2019;125(6):1008-1009. https://doi.org/ 10.1002/cncr.31934 [DOI] [PubMed] [Google Scholar]
- 40. Alchin JE, Signorelli C, McLoone JK, et al. Childhood cancer survivors’ adherence to healthcare recommendations made through a distance-delivered survivorship program. J Multidiscip Healthc. 2022;15(eCollection 2022):1719-1734. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41. Layne TM, Ferrucci LM, Jones BA, et al. Concordance of cancer registry and self-reported race, ethnicity, and cancer type: a report from the American Cancer Society’s studies of cancer survivors. Cancer Causes Control. 2019;30(1):21-29. [DOI] [PubMed] [Google Scholar]
- 42. Louie A, Robison L, Bogue M, et al. Validation of self-reported complications by bone marrow transplantation survivors. Bone Marrow Transplant. 2000;25(11):1191-1196. https://doi.org/ 10.1038/sj.bmt.1702419 [DOI] [PubMed] [Google Scholar]
- 43. Okura Y, Urban LH, Mahoney DW, Jacobsen SJ, Rodeheffer RJ.. Agreement between self-report questionnaires and medical record data was substantial for diabetes, hypertension, myocardial infarction and stroke but not for heart failure. J Clin Epidemiol. 2004;57(10):1096-1103. https://doi.org/ 10.1016/j.jclinepi.2004.04.005 [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are not publicly available due to privacy or ethical restrictions, and the full dataset is not able to be released due to ethical restrictions. Requests may be made to the authors.