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. Author manuscript; available in PMC: 2012 Jul 1.
Published in final edited form as: Biol Blood Marrow Transplant. 2010 Dec 8;17(7):995–1003. doi: 10.1016/j.bbmt.2010.10.023

Factors associated with adherence to preventive care practices among hematopoietic cell transplantation survivors

Nandita Khera 1, Eric J Chow 1, Wendy M Leisenring 1, Karen L Syrjala 1, K Scott Baker 1, Mary ED Flowers 1, Paul J Martin 1, Stephanie J Lee 1
PMCID: PMC3062948  NIHMSID: NIHMS248782  PMID: 21145404

Abstract

Preventive care guidelines are available for hematopoietic cell transplantation (HCT) survivors. We assessed adherence to these guidelines and examined factors associated with lower adherence. A questionnaire was mailed to adult HCT survivors to collect information regarding survivor health, adherence to recommended guidelines and financial concerns. Multivariable models identified patient and transplant characteristics associated with lower adherence. Of 3066 survivors more than 2 years after HCT, 1549 (51%) responded. Median age of respondents was 54.5 years, and the median adherence to recommended preventive care based on age and gender-specific recommendations was 75%. Lower adherence was associated with autologous HCT, concerns about medical costs, non-white race, male gender, lower physical functioning, no chronic graft vs. host disease (cGVHD), longer time since HCT, and lack of knowledge about recommended tests. Although 98% of respondents had medical insurance, 26% endorsed concern about medical costs and reported efforts to limit medical costs. Concern about medical costs was associated with female gender, age younger than 65 years, no cGVHD and low physical and mental functional status. Future efforts to improve adherence should address concern about medical costs and lack of knowledge as they emerged as major modifiable predictors of lower adherence to preventive care practices in HCT survivors.

INTRODUCTION

Hematopoietic cell transplantation (HCT) is used to treat many malignant and non-malignant conditions. Improved supportive care strategies and transplantation techniques have led to an increasing population of HCT survivors, drawing greater attention to their unique problems and challenges. Observational studies show that HCT survivors have higher risks for chronic diseases and secondary cancers than the general population.112

One approach to improving the health and health related quality of life (HRQOL) of HCT survivors is to enhance early detection and management of complications through better preventive care. Specific recommendations for screening and preventive care practices for HCT survivors have been developed based on review of the literature and consensus.13 In addition, the US Preventive Services Task Force14 recommendations for preventive care for the general population, are also applicable to HCT survivors.

A few cross-sectional studies have described health behaviors or health care utilization patterns and adherence to survivorship recommendations in HCT survivors.1517 The goal of our cross-sectional study was to assess the adherence rates to recommended preventive care guidelines and to examine previously unstudied factors that may be associated with adherence. We hypothesized that adherence would be high in HCT survivors but that certain potentially modifiable characteristics would predict lower adherence to recommended screening tests.

PATIENTS AND METHODS

Patients

The research was approved by the Institutional Review Board at the Fred Hutchinson Cancer Research Center (FHCRC). Survivors from the FHCRC database who met the following criteria were considered eligible for the study: age over 18 at the time of survey, prior transplantation at FHCRC, current mailing address available, and survived at least 2 years after HCT irrespective of current disease status. We could not locate approximately 5% of survivors who were two or more years after their transplant. Eligible patients were mailed a self-administered survey that asked about current health status and included specific questions pertaining to preventive care and financial concerns.

Questionnaire

A 45 item module was developed to collect information regarding adherence to preventive care guidelines and financial concerns. The survey was designed based on literature review and piloted on a small group of volunteer patients similar to the target population prior to distribution. Feedback was collected from the pilot group regarding clarity of the questions and time taken to complete the module.

Participants reported whether they had preventive health testing such as medical exams including dental, eye, and gynecologic. Specific exams assessed included blood pressure, stool occult blood, sigmoidoscopy or colonoscopy, and clinical breast exam, Pap smear and mammogram (women), and digital rectal exam for prostate cancer screening (men). Information about blood testing including thyroid function, lipids, and prostate specific antigen (men) was also collected. For each preventive measure, the time interval since last testing was collected (less than 1 year ago, 1–2 years ago, 3–4 years ago or more than 5 years ago). Additional questions asked about participants' level of interest in receiving health maintenance reminders, self-perceived knowledge about recommended testing for transplant survivors and willingness to participate in a health maintenance study for transplant survivors. The questionnaire did not ask for information about annual household income, educational status and type of provider seen.

The financial section asked about availability of medical insurance coverage, worry about lifetime caps, and bankruptcy due to medical expenses. This section also asked whether concerns regarding the cost of medical care led to one of five avoidance behaviors (cut back on prescribed medications, not purchased a prescription medication, avoided making appointments to see the doctor, not used a medically related service such as physical therapy, or did not have a medical test performed).

The supplementary module was added to a battery of 236 questions that are mailed to survivors annually along with general follow-up recommendations. Standard questions asked about number of hospitalizations and outpatient visits, presence of chronic GVHD or other specific complications, and current medications. Physical and mental functioning were assessed by self-reported performance status and activity level, measured by the Medical Outcomes Study Short Form 12 (SF12).18 Age, sex, race and ethnicity, and information about the HCT were available from the clinical research database. The survey was mailed once to each survivor along with a stamped, self addressed return envelope. No reminders were sent to non-respondents as is the routine policy followed by the Long Term Follow-up program's for these questionnaires. Data were collected between July 2008 and July 2009.

Statistical Analysis

Current employment status was categorized hierarchically in the following order since participants may be engaged in several activities: full time work outside the home, full time school, part time work outside the home, part time school, work at home, retired, none of these. Concern about medical costs was considered present if any of the five avoidance behaviors to limit costs was endorsed. Lack of knowledge about recommended tests was determined based on the answer to “Do you know what tests are recommended for transplant survivors?” Groups were compared with Wilcoxon rank sum tests or Chi-Square tests as appropriate.

Recommended screening tests were determined from the literature based on the current age and sex of the respondent.13, 14, 19 Though we used the guidelines from 2006 to 2009 as our source, not many of them are new and should be familiar to the health care providers in the community. We used the recommendations for adults and not children4 because only 8.7% of the respondents (n=135) were children at the time of HCT. Respondents were considered adherent with screening recommendations if they reported having the screening test within an appropriate time interval plus a 1 year margin. For example, since annual mammograms are recommended for women over age 40 years13, respondents age 40 or older were considered compliant with the recommendation if they reported having a mammogram within the past 2 years.

Multivariable logistic regression models were constructed for binary outcomes of “concerns about medical costs” and “lack of knowledge about recommended tests for survivors” considering sex, race, age, graft source (bone marrow vs. blood), conditioning regimen (myeloablative vs. not myeloablative), type of transplant (autologous vs. allogeneic), presence of chronic graft-versus-host disease (cGVHD), interval since HCT, and physical and mental functioning (high vs. low) as candidate covariates. Proportional odds regression models were constructed for the adherence variable to evaluate associations between the ordinal variable of >50% compliance and > 75% compliance using the same covariates listed above as well as “concerns about medical costs” and “lack of knowledge”. One factor, current age, did not satisfy the proportional odds assumption and for this covariate, the model was relaxed to allow different odds ratios for each cut-point.20 Factors were included in final multivariable models if their associated p-value was <0.1 or if their exclusion markedly changed parameter values for other factors in the model (>10% change). All reported p-values are two-sided.

RESULTS

Of the 3066 survivors who were sent the questionnaire, 51% responded which is typical for the annual survey. Table 1 summarizes the demographic and disease related characteristics of the respondents vs. non respondents. Participants had a median current age of 54.5 years and median interval time of 11.0 years since HCT. The median time since the most recent evaluation at the transplant center was 8.0 years. Participants were 51% male and 95% White. The non-respondents were more likely to be younger, male, Hispanic/Latino, and non-White, and to have received bone marrow, myeloablative conditioning and allogeneic HCT, have lower disease risk, with a longer time interval since HCT as well as since the most recent evaluation at the transplant center. There were no significant differences in relapse status and presence of chronic GVHD between the two groups.

Table 1.

Respondent and Non-Respondent characteristics

Respondents Non-respondents P-value

Number, % 1549 (51) 1517 (49)

Current age, median years (range) 54.5 (18.2–81.8) 47.4 (18.0–82.3) <0.001

Age at transplant, median years (range) 42.2 (0.9–73.8) 32.6 (1.2–71.2) <0.001

White, n (%) 1379 (95) 1275 (93) 0.01
 Missing or unknown 95 139

Hispanic or Latino, n (%) 35 (2) 87 (6) <0.001
 Missing or unknown 47 54

Male, n (%) 796 (51) 876 (58) <0.001

Transplant type, n (%) 0.001
 Autologous 415 (27) 343 (23)
 Related 748 (48) 837 (55)
 Unrelated 386 (25) 337 (22)

Diagnosis, n (%) <0.001
 Chronic leukemia 429 (28) 422 (28)
 Acute leukemia 352 (23) 453 (30)
 Lymphoma 282 (18) 239 (16)
 Multiple myeloma 121 (8) 66 (4)
 Myelodysplastic syndrome 170 (11) 109 (7)
 Aplastic anemia 92 (6) 118 (8)
 Solid tumor 53 (4) 54 (4)
 Other heme 19 (1) 33 (2)
 Other 14 (1) 8 (1)
 Missing 17 15

Post transplant relapse, n (%) 181 (12) 157 (10) 0.24

Disease risk, n (%) 0.005
 Low 599 (40) 664 (45)
 Intermediate 604 (40) 514 (35)
 High 308 (20) 284 (19)
 Missing 38 55

Graft source, n (%) <0.001
 Peripheral blood 682 (44) 536 (35)
 Bone marrow 866 (56) 975 (64)
 Umbilical cord blood 1 (<1) 6 (<1)

Myeloablative conditioning, n (%) 1424 (92) 1449 (96) <0.001
 Missing 1 7

Time since transplant, median years (range) 11.0 (2.6–38.0) 13.1 (2.5–36.7) <0.001

Time since last seen at FHCRC, median years (range) 8.0 (0–37.0) 10.4 (0–35.3) <0.001

Chronic GVHD, among allogeneic patients, n (%) 748 (66) 731 (62) 0.064

Two-sided p-values from Wilcoxon rank sum tests for continuous variables and from Chi-square tests for categorical variables.

Eighty-five percent of respondents perceived their general health as good to excellent. Forty-four percent worked full time outside the home or went to school full time, and 56% were able to do their usual activities without any limitation. Seventy-six percent reported seeing their doctor within the past 3 months (Table 2). Median physical and mental component score, as derived from SF-12, were 51.0 [Interquartile range (IQR) 38.9–55.8] and 55.9 (IQR 49.9–58.7) respectively.

Table 2.

Current health status

Characteristics n (%)

General health
 Excellent 288 (19)
 Very good 547 (36)
 Good 477 (31)
 Fair 188 (12)
 Poor 29 (2)
 Missing 20

Karnofsky performance status(self-reported)
 100% 753 (49)
 90% 436 (28)
 80% 152 (10)
 ≤ 70% 192 (13)
 Missing 16

Work status
 Full time work outside the home 627 (41)
 Full time school 43 (3)
 Part time work outside the home 192 (12)
 Part time school 14 (1)
 Work at home 125 (8)
 Retired 421 (27)
 None of these 117 (8)
 Missing 10

Ability to do usual job, housework or school work
 Yes, doing this without limitation 851 (56)
 Yes, but limited a little 415 (27)
 Yes, but limited a lot 167 (11)
 No, unable to do these things 84 (6)
 Missing 32

Number of physician appointments during the last 3 months
 None 367 (24)
  1 522 (34)
  2 256 (17)
  3 or more 381 (25)

Current chronic GVHD1
 No 815 (72)
 Yes 245 (22)
 Don't know 66 (6)

GVHD medications currently taken (allogeneic only)
 None 932 (83)
 At least one of the following: 202 (17)
  Corticosteroids 106 (10)
  Cyclosporine or tacrolimus 84 (7)
  Mycophenolate mofetil 31 (3)
  Sirolimus 24 (2)
1

GVHD = graft-vs.-host disease

Adherence to preventive care guidelines

Overall median adherence to recommended preventive care guidelines was 75% after making appropriate age and gender-specific adjustments. No specific screening tests accounted for lower adherence rates (data not shown). Adherence to preventive care that relies on physical exam ranged from 61% for a skin exam to 92% for breast examination. Laboratory testing ranged from 50% for thyroid function tests to 91% for cholesterol testing. Specialized testing rates were high, including 82% of colonoscopy or sigmoidoscopy, 84% for Pap smear and 90% for mammogram. (Table 3)

Table 3.

Adherence to recommended preventive care. Shaded boxes indicate compliance with recommended guidelines

Time since last tested, n (%)
Asymptomatic target population and Recommended frequency or testing N eligible Less than 1 year 1–2 years 3+ years Never Do not recall Missing
Recommended preventive care used to determine adherence rate
Tooth cleaning and dental exam All, annually1 1549 1229 (81) 164 (11) 114 (7) 7 (1) 11 (1) 24
Thyroid blood test All, annually1 1549 578 (39) 160 (11) 122 (8) 187 (12) 452 (30) 50
Blood pressure test All, every clinic visit, at least every 2 years1,2 1549 1401 (92) 61 (4) 15 (1) 17 (1) 29 (2) 26
Cholesterol test Women older than 45 and men older than 35, every 5 years1,2 1287 918 (73) 170 (13) 64 (5) 25 (2) 85 (7) 25
Stool occult blood test All greater than 50 years, annually1,2,3 997 235 (25) 162 (17) 219 (23) 119 (13) 212 (22) 50
Colonoscopy or sigmoidoscopy All greater than 50 years, every 5 years for sig or 10 years for colo1,2,3 997 201 (21) 202 (21) 383 (40) 122 (13) 58 (6) 31
Skin exam by professional All, annually3 1549 705 (47) 205 (14) 237 (16) 188 (12) 174 (12) 40
Skin exam by patient or family All, annually3 1549 883 (59) 83 (6) 72 (5) 287 (19) 168 (11) 56
Gynecologic exam Women greater than 21, annually1,3 or least every 3 years2 753 488 (66) 150 (20) 73 (10) 7 (1) 22 (3) 13
Pap smear Women greater than 21, annually1,3 or least every 3 years2 753 472 (64) 151 (20) 88 (12) 12 (2) 18 (2) 12
Breast examination Women 20–40 every 3 years; women over 40, annually3 753 558 (76) 120 (16) 41 (6) 8 (1) 12 (2) 14
Mammogram Women over 40, annually2,3 641 457 (73) 107 (17) 39 (6) 13 (2) 7 (1) 18
Additional preventive care testing not considered in adherence rate
Eye exam All, 1 year post-transplant1 1549 897 (59) 401 (26) 198 (13) 15 (1) 14 (1) 24
Bone density test – women All women and those who received steroids or calcineurin inhibitors, 1 year post-transplant; and women after age 602 753 257 (35) 211 (29) 159 (22) 54 (7) 48 (7) 24
Bone density test – men All women and those who received steroids or calcineurin inhibitors, 1 year post-transplant; and women after age 602 796 118 (15) 115 (15) 198 (26) 195 (25) 140 (18) 30
Prostate specific antigen No recommendation,2,3 796 309 (39) 112 (14) 60 (8) 137 (17) 169 (21) 9
Digital rectal exam No recommendation,2,3 796 242 (31) 144 (19) 155 (20) 142 (18) 89 (12) 24

Source:

1

Rizzo JD et al, BBMT 2006; 12: 138–151

2

Agency for Healthcare Research and Quality, US Preventive Services Task Force (USPSTF). http://www.ahrq.gov/clinic/uspstfix.htm

3

Smith RA et al, CA Cancer J Clin. 2008: 58: 161–179

Patient participation in preventive health care

Most (87%) patients were interested in some form of assistance from the transplant center in health maintenance, primarily in the form of mailed information. A minority (27%) reported they felt knowledgeable about recommended tests for transplant survivors, while 46% of respondents indicated that they “did not know but would like to” and 26% indicated that they “did not know and relied on the doctor to know”. (Table 4)

Table 4.

Patient participation in preventive health care

Characteristics n (%)

Interest in health maintenance programs
 None 199 (13)
 At least one of the following: 1313 (87)
  Annual one day clinic visit to prevent health problems  364 (24)
  Mailed information annually about recommended tests  965 (64)
  Yearly telephone call to discuss recommended tests  408 (27)
  Mailed reminders when you are due for recommended tests  683 (45)
 Missing 37

Keeps records of medical tests and results 930 (61)
 Missing 30

Knowledge of recommended tests for transplant survivors
 Yes 418 (27)
 No, but would like to know 702 (46)
 No, rely on doctor to know 401(26)
 Missing 28

Willingness to participate in a study to determine the best ways to help survivors maintain their health
 Yes, definitely 652 (43)
 Yes, probably 591 (39)
 No 268 (18)
 Missing 38

Breast self examination – optional for women over 203 (n=805)
 Regularly (once a month) 232 (31)
 Occasionally 360 (49)
 Rarely or never 146 (20)
 Missing 15

Testicular self examination – annually for men3; not recommended by USPSTF2 (n=869)
 Regularly (once a month) 140 (19)
 Occasionally 259 (35)
 Rarely or never 343 (46)
 Missing 54
1

Rizzo JD et al, BBMT 2006; 12: 138–151

2

Agency for Healthcare Research and Quality, US Preventive Services Task Force (USPSTF). http://www.ahrq.gov/clinic/uspstfix.htm

3

Smith RA et al, CA Cancer J Clin. 2008; 58: 161–179

Influence of financial factors on health behaviors

Ninety-eight percent of the respondents had medical insurance coverage but 26% reported attempts to limit medical costs by engaging in one or more potentially deleterious health behaviors. Twenty-six percent worried that medical expenses would reach their lifetime limit, 1% reported that they had already reached their limit, and 3% reported filing for bankruptcy due to medical expenses. (Table 5)

Table 5.

Insurance status and concern about medical costs

Characteristics n (%)

Medical insurance*
 Medical insurance 1153 (74)
 Medicare/Medicaid 457 (30)
 VA 75 (5)
 Other 152 (10)
 None 24 (2)

Denied coverage because of cancer or cancer treatment 154 (11)
 Missing 163

Availability of employee group medical coverage is an important reason why work at current job 471 (37)
 Missing 274

Cost of medical care has caused
No change in use of medical care 1121 (74)
At least one of the following: 392 (26)
 Cut back on the prescribed medications taken  158 (10)
 Not purchased a prescription medication  166 (11)
 Avoided making appointments to see physician  226 (15)
 Not used a medically related service such as physical therapy  193 (13)
 Not had a medical test performed  187 (12)
Missing 37–4

Worried that expenses will reach the limit and the insurance company will stop paying 368 (25)
 Missing 57

Insurance company has already stopped paying because cap exceeded 19 (1)
 Missing 69

Filed bankruptcy because of medical expenses 40 (3)
 Missing 46
*

may have multiple insurance types, sum > 100%

Regression models

An ordinal regression analysis showed that lower adherence rates were associated with autologous HCT, concerns about medical costs, interval time greater than 15 years since HCT, non- white race, male gender, lower physical functioning, not having chronic GVHD, younger current age (<40 years old) and self-reported lack of knowledge about the recommended tests (Table 6). Association with Hispanic ethnicity could not be tested because of the small number of Hispanic/Latino respondents (n=35, 2.3%). Multivariable logistic regression models showed that concerns about medical costs were associated with lower physical and mental functioning, age less than 65 years and being female and marginally, not having chronic GVHD. Lack of knowledge about recommended tests for survivors was more common among males, those who received autologous transplants, those who did not develop chronic GVHD, non-white subjects, those older than 65 years of age, and those who were more than 15 years post-HCT (Table 7).

Table 6.

Multivariable proportional odds regression models for ordinal categories of adherence to recommended preventive care, two cutpoints used: <50%*:

Common OR (95% CI) p-value
Male 2.81 (2.27, 3.49) <0.001
Autologous transplant 1.69 (1.30, 2.19) 0.001
Concerns about medical costs 1.48 (1.15, 1.89) 0.002
Time since transplant
 <5 years 1.0 - - -
 5–9.9 years 0.88 (0.63, 1.22) 0.44
 10–14.9 years 1.08 (0.71, 1.64) 0.58
 15 years or more 1.42 (1.03, 1.94) 0.02
Non-White 1.90 (1.21, 3.00) 0.006
Physical Function < −1 STD 1.43 (1.11, 1.85) 0.006
No CGVHD 1.80 (1.29, 2.50) <0.001
Lack of Knowledge 2.00 (1.57, 2.56) <0.001
<75% Compliance <50% Compliance
OR (95% CI) p-value OR (95% CI) p-value
Current Age
 ≥65 years 1.0 - - - 1.0 - - -
 55–64.9 years 0.98 (0.71, 1.36) 0.92 1.08 (0.72, 1.63) 0.69
 40–54.9 years 0.47 (0.32, 0.69) <0.001 1.25 (0.78, 2.00) 0.36
 <40 years 1.08 (0.71, 1.64) 0.71 2.14 (1.32, 3.47) 0.002

Abbreviations: STD = standard deviation, GVHD = graft versus host disease, OR = Odds Ratio, CI = Confidence Interval.

Table 7.

Multivariable logistic regressions for concern about medical costs and lack of knowledge about recommended tests

Dependent variable Covariates OR (95% CI) p-valuea p-valueb
Concern about medical cost Physical functioning
 < −1 STD 2.68 (2.03, 3.53) <0.001
Mental functioning
 < −1 STD 2.32 (1.65, 3.27) <0.001
Age
 65 or older 1.0 - - <0.001
 50–64.9 2.42 (1.57, 3.74) <0.001
 40–49.9 3.98 (2.50, 6.36) <0.001
 <40 3.10 (1.88, 5.14) <0.001
Male 0.64 (0.50, 0.82) <0.001
No chronic GVHD 1.40 (0.98, 2.00) 0.06

Lack of knowledge about recommended tests for survivors Male 1.44 (1.13, 1.83) 0.003
No chronic GVHD 1.46 (1.05, 2.03) 0.03
Autologous transplant 1.54 (1.13, 2.11) 0.007
Time since Transplant
 <5 years 1.0 - - <0.001
 5–9.9 years 0.92 (0.64, 1.32) 0.65
 10–14.9 years 0.79 (0.54, 1.14) 0.20
 15 years or more 1.62 (1.12, 2.34) 0.010
Non-white 1.90 (1.02, 3.54) 0.042
Age 65 or older 1.41 (1.01, 1.97) 0.043

Abbreviations: STD = standard deviation, GVHD = graft versus host disease, OR = Odds Ratio, CI = Confidence Interval.

a

Category specific p-value from Wald test shown where different from overall variable level p-value.

b

Global p-value for covariate.

DISCUSSION

HCT survivors have a higher risk of developing adverse medical conditions and new malignancies compared to the general population. Our study showed high rates of self-reported adherence to screening practices among the respondents. These rates are higher than those reported for the general population in 2008 by the National Center for Health Statistics. For instance, 90% of females older than 40 years in our study had a mammogram in the past 2 years as compared to 68% of the general population.21 Likewise, 82% of our HCT survivors over age 50 reported having had a colonoscopy/sigmoidoscopy compared to 61.8% of the general population.22

In general, the high preventive screening rates reported by our HCT survivors have been reported in some, but not all studies in cancer survivors. Mayer et al23 reported screening adherence rates in cancer survivors exceeding American Cancer Society recommendations, national prevalence data and Healthy people 2010 goals for individual tests. Trask et al24 reported similar findings and also noted variation in adherence rates by the type of screening test. A study by Earle et al25 reported increased use of preventive services by elderly breast cancer survivors compared to controls. Within the HCT survivor population, Shankar et al17 reported increased frequency of physical exams and general medical contact compared to sibling controls. These high screening rates may indicate increased survivor awareness and attention to preventive care, the so-called “teachable moment” effect,26 where survivors, having survived one life-threatening disease, are more motivated to try to prevent additional illness.

In contrast, other studies have shown lower rates of preventive care in cancer survivors than in the general population. The Childhood Cancer Survivor study showed suboptimal adherence to recommended guidelines among survivors of childhood cancers.27, 28 In another study by Earle and Neville,29 colorectal carcinoma survivors had lower rates of adherence to recommended screening practices than controls. Compared to healthy controls, the HCT survivor group in Bishop's study had similar rates of breast and colorectal cancer screening but lower rates of pap smears.15 Prasad et al16 compared non Hispanic and Hispanic HCT survivors and reported lack of insurance, absence of English proficiency and lack of concern for future health as factors associated with lower health care utilization in the Hispanic cohort.

Lower adherence to preventive care recommendations could be explained by problems related to the patient, physician or health care delivery. For example, patients who have survived one cancer may avoid cancer screening because of increased anxiety about discovering a second malignancy. Poor mental and physical functioning due to cancer or treatment-related complications might decrease the ability to maintain a healthy lifestyle and/or obtain aggressive preventive care. Prescribing physicians may be more familiar with USPTF guidelines and less aware of specific screening guidelines for HCT patients. A pediatric study showed that many pediatric oncologists who care for long term cancer survivors are not familiar with available guidelines for surveillance of late effects.30 This could account for younger age being associated with lower adherence as most USPTF guidelines apply to older people and therefore are most applicable to an the older age group. A collaborative study by the NCI and the American Cancer Society is comparing the perceived roles, knowledge, and practices of primary care physicians and oncologists with regard to follow-up survivorship care with results expected by the end of 2010.

Not having a regular source of health care and access to health insurance has also been cited as a risk factor for suboptimal utilization of health care services, not only in cancer survivors but also in the general population.31,32 Although a number of studies have examined the clinical consequences of being uninsured,3336 very few studies have investigated the health consequences of financial barriers to medical care for the so-called “under insured” population, especially in the HCT setting. A recent study looking at health care disparities in cancer survivors reported that the prevalence of forgoing one or more medical service due to cost was about 17.6% in cancer survivors.37 In the general population, 3–4 % of insured men and 5–8% of insured women reported not having received needed prescription medications or medical care due to cost concerns.38 Our study documented a much higher rate of medical cost concern than the general population as well as cancer survivors, since 26% of patients in our respondent group admitted to potentially risky avoidance behaviors related to concerns about medical costs, even though nearly all respondents (98%) had insurance coverage.

In addition to cost concerns, lower adherence was predicted by male gender and non-white race, factors that have been identified in other studies to be associated with adverse health behaviors and decreased health utilization.1517,39 Interestingly, lack of chronic GVHD also emerged as a predictor for lack of knowledge and thereby lower adherence. This could be explained by the fact that cGVHD patients would have more frequent follow-up with the transplant center and reinforcement of knowledge about preventive care recommendations with each visit. Similarly, the lack of follow-up with the transplant center after an autologous transplant due to lower need for continued specialized post-transplant therapy could explain our finding of lower adherence and higher likelihood of lack of knowledge in autologous transplant survivors. Another contributing factor would be the perception of treating physicians about the intensity of their prior treatment and susceptibility to complications as lower than that of allogeneic transplant survivors. This result is in contrast to the study by Bishop et al15, where autologous HCT survivors were more likely to report breast or cervical cancer screening, and there was no significant difference among the rates of all suggested cancer screenings between allogeneic and autologous groups. One possible explanation for the discrepancy is that compared to our study, Bishop's study included a higher percentage of patients with autologous transplants for breast cancer, a situation where breast and cervical cancer screening might be emphasized. Our multivariable analysis also identified longer time since transplant as a risk factor for lower adherence, similar to that reported by the Childhood Cancer Survivor study.39 This finding may be due to lack of understanding of late effects of therapy if patients and physicians believe that the risk declines with time.

Our study has some limitations. Approximately half of the eligible survivors did not return the survey. The non-respondents were more likely to have characteristics associated with lower adherence, suggesting that our results may be an overestimation of the population adherence rates and therefore represent the `best case scenario'. Despite this, our analyses are valid for the half of patients who did respond to the survey (n=1549), reflecting a large number of survivors for whom preventive care adherence is good but could still be improved hopefully minimizing long term complications. We also acknowledge that this was a single center study from the USA and results might vary depending on the follow-up practices and resources to disseminate information about these guidelines at other transplant centers across the world. In addition, adherence rates were calculated on the basis of self-report and were not validated by review of patient records from treating physicians. This could lead to overestimation of adherence rates since self-reported data about health behaviors may be affected by a social desirability bias.4042 It also gives rise to the possibility of participant bias since participants who return health surveys are usually more driven to maintain optimal health by utilization of health services and adoption of healthy lifestyle behaviors. Another limitation of our study stems from the possibility of lack of awareness of guidelines for long term follow-up of HCT survivors among non-transplant physicians. Because we did not collect information on the type of provider following the patient, we cannot comment on whether this factor is associated with lower adherence. Another important limitation of our study is that we did not ask the survivors questions regarding their lifestyle practices. For certain cancers that are not amenable to easy screening procedures, it might be more important to maintain a healthy lifestyle than to adhere to medical testing alone. In the case of skin cancer, where prevention by avoidance of unprotected UV exposure may be of comparable benefit to regular skin exams, it would have been interesting to know whether a low adherence to recommended screening was also associated with non-adherence to preventive behaviors such as use of sunscreens. Finally, in examining financial concerns, we did not specifically assess whether the perceived cost burden was due to high out-of-pocket costs, low lifetime caps or lack of catastrophic provisions.

Our results suggest that future attempts to improve survivors' adherence to preventive practices would benefit from attention focused on patients' financial concerns and lack of knowledge, as both are potentially modifiable factors and may have emerged as even stronger predictors if our non-respondent group was included in the analysis. For example, better communication with the patient about the reasons for screening recommendations and frank discussion about the financial implications for the patient along with approaches to mitigate personal costs may improve adherence. Given the high rate of financial concerns related to medical care in our population, national policies that ensure the affordability of health insurance coverage would help alleviate those stresses. The Affordable Care Act is a step in the right direction since it aims to make wellness and preventive services affordable and accessible by requiring health plans to cover these services and by eliminating cost-sharing. Our study also highlights the need for redesigning of health insurance benefits packages to include incentives for adoption of healthy lifestyle practices. Another important intervention to improve patient and physician knowledge may be the provision of comprehensive survivorship care plans43 by the transplant centers, similar to those that have been developed for breast and colon cancer survivors by ASCO.44 Although there is a paucity of data regarding the effectiveness of these plans in improving patient knowledge and adherence to preventive practices, one can assume that providing a diagnostic and treatment summary along with follow-up recommendations that identify the physician who will implement them will improve coordination of care.45 A recent study reported that a survivorship care discussion between patients and physicians may have positive effects on some aspects of follow-up care.46 Finally, efforts to provide community outreach education and support programs to exploit the `teachable moment'26 provided by the transplant process itself may encourage healthy behaviors. These strategies should be tested in future studies to see if they will result in improved adherence to preventive guidelines, and ultimately lead to improved HRQOL and decreased morbidity and mortality.

Acknowledgements of research support

Grant support: CA18029, CA112631 and HL36444 from the National Institutes of Health

Footnotes

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Financial disclosure statement: The authors declare no competing financial interests

REFERENCES

  • 1.Baker K, Ness K, Steinberger J, et al. Diabetes, hypertension, and cardiovascular events in survivors of hematopoietic cell transplantation: a report from the bone marrow transplantation survivor study. Blood. 2007;109:1765–1772. doi: 10.1182/blood-2006-05-022335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Bhatia S, Francisco L, Carter A, et al. Late mortality after allogeneic hematopoietic cell transplantation and functional status of long-term survivors: report from the Bone Marrow Transplant Survivor Study. Blood. 2007;110:3784–3792. doi: 10.1182/blood-2007-03-082933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Friedman D, Rovo A, Leisenring W, et al. Increased risk of breast cancer among survivors of allogeneic hematopoietic cell transplantation: a report from the FHCRC and the EBMT-Late Effect Working Party. Blood. 2008;111:939–944. doi: 10.1182/blood-2007-07-099283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Landier W, Bhatia S, Eshelman D, et al. Development of risk-based guidelines for pediatric cancer survivors: the Children's Oncology Group Long-Term Follow-Up Guidelines from the Children's Oncology Group Late Effects Committee and Nursing Discipline. J Clin Oncol. 2004;22:4979–4990. doi: 10.1200/JCO.2004.11.032. [DOI] [PubMed] [Google Scholar]
  • 5.Leisenring W, Friedman D, Flowers M, Schwartz J, Deeg H. Nonmelanoma skin and mucosal cancers after hematopoietic cell transplantation. J Clin Oncol. 2006;24:1119–1126. doi: 10.1200/JCO.2005.02.7052. [DOI] [PubMed] [Google Scholar]
  • 6.Leung W, Ahn H, Rose S, et al. A prospective cohort study of late sequelae of pediatric allogeneic hematopoietic stem cell transplantation. Medicine (Baltimore) 2007;86:215–224. doi: 10.1097/MD.0b013e31812f864d. [DOI] [PubMed] [Google Scholar]
  • 7.Martin P, Counts GJ, Appelbaum F, et al. Life expectancy in patients surviving more than 5 years after hematopoietic cell transplantation. J Clin Oncol. 2010;28:1011–1016. doi: 10.1200/JCO.2009.25.6693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Rizzo J, Curtis R, Socié G, et al. Solid cancers after allogeneic hematopoietic cell transplantation. Blood. 2009;113:1175–1183. doi: 10.1182/blood-2008-05-158782. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Savani B, Stratton P, Shenoy A, Kozanas E, Goodman S, Barrett A. Increased risk of cervical dysplasia in long-term survivors of allogeneic stem cell transplantation--implications for screening and HPV vaccination. Biol Blood Marrow Transplant. 2008;14:1072–1075. doi: 10.1016/j.bbmt.2008.07.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Socié G, Cahn J, Carmelo J, et al. Avascular necrosis of bone after allogeneic bone marrow transplantation: analysis of risk factors for 4388 patients by the Société Française de Greffe de Moëlle (SFGM) Br J Haematol. 1997;97:865–870. doi: 10.1046/j.1365-2141.1997.1262940.x. [DOI] [PubMed] [Google Scholar]
  • 11.Socié G, Salooja N, Cohen A, et al. Nonmalignant late effects after allogeneic stem cell transplantation. Blood. 2003;101:3373–3385. doi: 10.1182/blood-2002-07-2231. [DOI] [PubMed] [Google Scholar]
  • 12.Tichelli A, Bucher C, Rovó A, et al. Premature cardiovascular disease after allogeneic hematopoietic stem-cell transplantation. Blood. 2007;110:3463–3471. doi: 10.1182/blood-2006-10-054080. [DOI] [PubMed] [Google Scholar]
  • 13.Rizzo JD, Wingard JR, Tichelli A, et al. Recommended screening and preventive practices for long-term survivors after hematopoietic cell transplantation: joint recommendations of the European Group for Blood and Marrow Transplantation, the Center for International Blood and Marrow Transplant Research, and the American Society of Blood and Marrow Transplantation. Biol Blood Marrow Transplant. 2006;12:138–151. doi: 10.1016/j.bbmt.2005.09.012. [DOI] [PubMed] [Google Scholar]
  • 14.Guide to Clinical Preventive Services [[Accessed July 17,2009]];Agency for Healthcare Research and Quality: U.S. Preventive Services Task Force (USPSTF) http://www.ahrq.gov/clinic/uspstfix.htm.
  • 15.Bishop MM, Lee SJ, Beaumont JL, et al. The preventive health behaviors of long-term survivors of cancer and hematopoietic stem cell transplantation compared with matched controls. Biol Blood Marrow Transplant. 2010;16:207–214. doi: 10.1016/j.bbmt.2009.09.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Prasad PK, Sun CL, Baker KS, et al. Health care utilization by adult Hispanic long-term survivors of hematopoietic stem cell transplantation: report from the Bone Marrow Transplant Survivor Study. Cancer. 2008;113:2724–2733. doi: 10.1002/cncr.23917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Shankar SM, Carter A, Sun CL, et al. Health care utilization by adult long-term survivors of hematopoietic cell transplant: report from the Bone Marrow Transplant Survivor Study. Cancer Epidemiol Biomarkers Prev. 2007;16:834–839. doi: 10.1158/1055-9965.EPI-06-0714. [DOI] [PubMed] [Google Scholar]
  • 18.Ware J, Jr., Kosinski M, Keller SD. A 12-Item Short-Form Health Survey: construction of scales and preliminary tests of reliability and validity. Med Care. 1996;34:220–233. doi: 10.1097/00005650-199603000-00003. [DOI] [PubMed] [Google Scholar]
  • 19.Smith RA, Cokkinides V, Brawley OW. Cancer screening in the United States, 2008: a review of current American Cancer Society guidelines and cancer screening issues. CA Cancer J Clin. 2008;58:161–179. doi: 10.3322/CA.2007.0017. [DOI] [PubMed] [Google Scholar]
  • 20.Williams R. Generalized ordered logit/partial proportional odds models for ordinal dependent variables. The STATA Journal. 2006;6:58–82. [Google Scholar]
  • 21.National Center for Health Statistics. Health, United States, 2009: With Special Feature on Medical Technology. Hyattsville, MD: 2010. [PubMed] [Google Scholar]
  • 22.BRFSS Prevalence and Trends Data. Colorectal Cancer Screening/Sigmoidoscopy Nationwide (States and DC and territories); 2008. [Accessed January 21, 2010]. http://apps.nccd.cdc.gov/brfss/display.asp. [Google Scholar]
  • 23.Mayer DK, Terrin NC, Menon U, et al. Screening practices in cancer survivors. J Cancer Surviv. 2007;1:17–26. doi: 10.1007/s11764-007-0007-0. [DOI] [PubMed] [Google Scholar]
  • 24.Trask PC, Rabin C, Rogers ML, et al. Cancer screening practices among cancer survivors. Am J Prev Med. 2005;28:351–356. doi: 10.1016/j.amepre.2005.01.005. [DOI] [PubMed] [Google Scholar]
  • 25.Earle CC, Burstein HJ, Winer EP, Weeks JC. Quality of non-breast cancer health maintenance among elderly breast cancer survivors. J Clin Oncol. 2003;21:1447–1451. doi: 10.1200/JCO.2003.03.060. [DOI] [PubMed] [Google Scholar]
  • 26.Ganz PA. A teachable moment for oncologists: cancer survivors, 10 million strong and growing! J Clin Oncol. 2005;23:5458–5460. doi: 10.1200/JCO.2005.04.916. [DOI] [PubMed] [Google Scholar]
  • 27.Nathan PC, Greenberg ML, Ness KK, et al. Medical care in long-term survivors of childhood cancer: a report from the childhood cancer survivor study. J Clin Oncol. 2008;26:4401–4409. doi: 10.1200/JCO.2008.16.9607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Yeazel MW, Oeffinger KC, Gurney JG, et al. The cancer screening practices of adult survivors of childhood cancer: a report from the Childhood Cancer Survivor Study. Cancer. 2004;100:631–640. doi: 10.1002/cncr.20008. [DOI] [PubMed] [Google Scholar]
  • 29.Earle CC, Neville BA. Under use of necessary care among cancer survivors. Cancer. 2004;101:1712–1719. doi: 10.1002/cncr.20560. [DOI] [PubMed] [Google Scholar]
  • 30.Henderson TO, Hlubocky FJ, Wroblewski KE, Diller L, Daugherty CK. Physician preferences and knowledge gaps regarding the care of childhood cancer survivors: a mailed survey of pediatric oncologists. J Clin Oncol. 2010;28:878–883. doi: 10.1200/JCO.2009.25.6107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Buchmueller TC, Grumbach K, Kronick R, Kahn JG. The effect of health insurance on medical care utilization and implications for insurance expansion: a review of the literature. Med Care Res Rev. 2005;62:3–30. doi: 10.1177/1077558704271718. [DOI] [PubMed] [Google Scholar]
  • 32.Weissman JS, Epstein AM. The insurance gap: does it make a difference? Annu Rev Public Health. 1993;14:243–270. doi: 10.1146/annurev.pu.14.050193.001331. [DOI] [PubMed] [Google Scholar]
  • 33.Braveman P, Schaaf VM, Egerter S, Bennett T, Schecter W. Insurance-related differences in the risk of ruptured appendix. N Engl J Med. 1994;331:444–449. doi: 10.1056/NEJM199408183310706. [DOI] [PubMed] [Google Scholar]
  • 34.American College of Physicians . White Paper. American College of Physicians; Philadelphia: 2000. No Health Insurance? It’s Enough to Make You Sick—Scientific Research Linking the Lack of Health Coverage to Poor Health. [Google Scholar]
  • 35.Institute of Medicine . Care without Coverage; Too Little, Too Late. National Academy Press; Washington, D.C.: 2002. [PubMed] [Google Scholar]
  • 36.Rahimi AR, Spertus JA, Reid KJ, Bernheim SM, Krumholz HM. Financial barriers to health care and outcomes after acute myocardial infarction. JAMA. 2007;297:1063–1072. doi: 10.1001/jama.297.10.1063. [DOI] [PubMed] [Google Scholar]
  • 37.Weaver K, Rowland J, Bellizzi K, Aziz N. Forgoing medical care because of cost: assessing disparities in healthcare access among cancer survivors living in the United States. Cancer. 2010;116:3493–3504. doi: 10.1002/cncr.25209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.National Center for Health Statistics Health, United States, 2008 With Chartbook. Hyattsville, MD: 2009. p. 100. [Google Scholar]
  • 39.Oeffinger K, Mertens A, Hudson M, et al. Health care of young adult survivors of childhood cancer: a report from the Childhood Cancer Survivor Study. Ann Fam Med. 2004;2:61–70. doi: 10.1370/afm.26. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Crowne D, Marlowe D. A new scale of social desirability independent of psychopathology. J Consult Psychol. 1960;24:349–354. doi: 10.1037/h0047358. [DOI] [PubMed] [Google Scholar]
  • 41.Kristiansen C, Harding C. The social desirability of preventive health behavior. Public Health Rep. 1984;99:384–388. [PMC free article] [PubMed] [Google Scholar]
  • 42.Toobert D, Hampson S, Glasgow R. The summary of diabetes self-care activities measure: results from 7 studies and a revised scale. Diabetes Care. 2000;23:943–950. doi: 10.2337/diacare.23.7.943. [DOI] [PubMed] [Google Scholar]
  • 43.Hoffman B, Stovall E. Survivorship perspectives and advocacy. J Clin Oncol. 2006;24:5154–5159. doi: 10.1200/JCO.2006.06.5300. [DOI] [PubMed] [Google Scholar]
  • 44.American Society of Clinical Oncology [Accessed on May 30,2010];ASCO Chemotherapy Treatment Plan and Summary. http://www.asco.org/treatmentsummary.
  • 45.Lin J, Donehower R. Make quality cancer survivorship care possible in the era of workforce shortage. J Oncol Pract. 2010;6:52–53. doi: 10.1200/JOP.091056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Cheung W, Neville B, Earle C. Associations among cancer survivorship discussions, patient and physician expectations, and receipt of follow-up care. J Clin Oncol. 2010;28:2577–2583. doi: 10.1200/JCO.2009.26.4549. [DOI] [PubMed] [Google Scholar]

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