The Open Public Health Journal




ISSN: 1874-9445 ― Volume 12, 2019
RESEARCH ARTICLE

Preventive Services Utilization Among Cancer Survivors Compared to Cancer-free Controls



Annemarie Uhlig1, *, Johannes Uhlig2, 3, Arne Strauss1, Lutz Trojan1, Joachim Lotz2, 4, Ali Seif Amir Hosseini2
1 Department of Urology, University Medical Center, University of Göttingen, Göttingen, Germany
2 Department of Interventional and Diagnostic Radiology, University Medical Center, University of Göttingen, Göttingen, Germany
3 Division of Interventional Radiology, Department of Radiology and Biomedical Imaging, Yale School of Medicine, New Haven, CT, United States of America
4 German CT for Cardiovascular Research, Partnersite Goettingen, Goettingen, Germany

Abstract

Purpose:

To summarize the current evidence on preventive services utilization in cancer survivors.

Methods:

A systematic literature review and meta-analysis was conducted in February 2016. Studies were included if they compared the utilization of influenza vaccination, cholesterol/lipid testing, bone densitometry, or blood pressure measurement among survivors of adulthood cancer to cancer-free controls. Random effects meta-analyses were conducted to pool estimates.

Results:

Literature search identified 3740 studies of which 10 fulfilled the inclusion criteria. Cancer survivors were significantly more likely to utilize bone densitometry (OR=1.226, 95% CI: 1.114 – 1.350, p<0.001) and influenza vaccination (OR=1.565, 95% CI: 1.176 – 2.082, p=0.002) than cancer-free controls. No statistically significant differences were detected for blood pressure measurement and cholesterol/lipid testing (OR=1.322, 95% CI: 0.812 – 2.151, p=0.261; OR=1.046, 95% CI: 0.96 – 1.139, p=0.304).

Conclusions:

Cancer survivors were more likely to receive influenza vaccinations and bone densitometry. Future studies should evaluate underlying mechanisms and whether the utilization of preventive services translates into prolonged survival of cancer survivors.

Implications for Cancer Survivors:

Our meta-analysis demonstrated cancer survivors to be more likely to receive the preventive services such as influenza vaccination and bone densitometry than cancer free controls. Still, these results should be interpreted in the context of suboptimal utilization of preventive services in general, and for cancer survivors in specific. Future research should evaluate the underlying mechanisms and whether utilization of preventive services is associated with overall survival in cancer survivors.

Keywords: Preventive services, Meta-analysis, Cancer survivors, Lipid testing, Influenza vaccination, Bone densitometry.


Article Information


Identifiers and Pagination:

Year: 2018
Volume: 11
First Page: 122
Last Page: 133
Publisher Id: TOPHJ-11-122
DOI: 10.2174/1874944501811010122

Article History:

Received Date: 28/12/2017
Revision Received Date: 09/03/2018
Acceptance Date: 12/03/2018
Electronic publication date: 30/03/2018
Collection year: 2018

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© 2018 Uhlig et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence this author at the Department of Urology, University Medical Center, University of Goettingen, Robert-Koch-Strasse 40, 37075 Goettingen, Germany; Tel:0049-551-39-65891; Email: annemarie.uhlig@med.uni-goettingen.de




1. INTRODUCTION

Over the last decades, the number of patients surviving cancer, commonly referred to as cancer survivors, has increased rapidly, reaching approximately 11.9 million US survivors in 2008 [1Parry C, Kent EE, Mariotto AB, Alfano CM, Rowland JH. Cancer survivors: A booming population. Cancer Epidemiol Biomarkers Prev 2011; 20(10): 1996-2005.[http://dx.doi.org/10.1158/1055-9965.EPI-11-0729] [PMID: 21980007] ]. A high prevalence of both acute and chronic medical comorbidities, such as influenza infections, hypertension, or metabolic syndrome, are observed in cancer survivors and may be attributable to treatment side effects and a detrimental lifestyle [2Jørgensen TL, Hallas J, Friis S, Herrstedt J. Comorbidity in elderly cancer patients in relation to overall and cancer-specific mortality. Br J Cancer 2012; 106(7): 1353-60.[http://dx.doi.org/10.1038/bjc.2012.46] [PMID: 22353805] , 3Mohile SG, Xian Y, Dale W, et al. Association of a cancer diagnosis with vulnerability and frailty in older Medicare beneficiaries. J Natl Cancer Inst 2009; 101(17): 1206-15.[http://dx.doi.org/10.1093/jnci/djp239] [PMID: 19638506] ]. A recent literature review has shown that these conditions negatively influence survival of cancer patients [4Sarfati D, Koczwara B, Jackson C. The impact of comorbidity on cancer and its treatment. CA Cancer J Clin 2016; 66(4): 337-50.[http://dx.doi.org/10.3322/caac.21342] [PMID: 26891458] ].

In light of the crucial role of comorbidities in the growing number of cancer survivors, several publications analyzed the utilization of preventive services, such as influenza vaccination, or bone densitometry for early detection of osteoporosis, showing contradicting results: both increased and decreased utilization of preventive services were reported [5Duffy CM, Clark MA, Allsworth JE. Health maintenance and screening in breast cancer survivors in the United States. Cancer Detect Prev 2006; 30(1): 52-7.[http://dx.doi.org/10.1016/j.cdp.2005.06.012] [PMID: 16455209] , 6Khan NF, Carpenter L, Watson E, Rose PW. Cancer screening and preventative care among long-term cancer survivors in the United Kingdom. Br J Cancer 2010; 102(7): 1085-90.[http://dx.doi.org/10.1038/sj.bjc.6605609] [PMID: 20234361] ].

So far, two systematic reviews examined the utilization of screening services among cancer survivors to detect cancer recurrence or secondary malignancies. A systematic review by Wilkins et al. [7Wilkins KL, Woodgate RL. Preventing second cancers in cancer survivors. Oncol Nurs Forum 2008; 35(2): E12-22.[http://dx.doi.org/10.1188/08.ONF.E12-E22] [PMID: 18321824] ] concluded that cancer survivors were less likely to adopt cancer screening than cancer-free controls. Conversely, a systematic review and meta-analysis by Corkum et al. [8Corkum M, Hayden JA, Kephart G, Urquhart R, Schlievert C, Porter G. Screening for new primary cancers in cancer survivors compared to non-cancer controls: A systematic review and meta-analysis. J Cancer Surviv 2013; 7(3): 455-63.[http://dx.doi.org/10.1007/s11764-013-0278-6] [PMID: 23645522] ] reported that cancer survivors were screened more frequently for new primary breast, cervical, and colorectal cancers compared to cancer-free controls. However, so far no review has focused on the utilization of preventive services other than cancer screening.

Therefore, the aim of this study was to summarize the evidence on utilization of preventive services in cancer survivors compared to cancer-free controls.

2. METHODS

2.1. Literature Search

In February 2016, a systematic literature search without date and language restrictions was conducted using Medical Subject Heading (MeSH) terms and title/abstract keywords related to preventive services, cancer, and cancer survivorship. The full search algorithm is provided in the Appendix.

The electronic database MEDLINE (PubMed) was searched for peer-reviewed observational epidemiological studies. The EMBASE electronic database was searched with according search terms via the DIMDI portal (Deutsches Institut für Medizinische Dokumentation und Information). To identify additional studies and gray literature, conference proceedings were screened and public health professionals at the Harvard TH Chan School of Public Health contacted.

2.2. Study Selection

For inclusion in this review, the following criteria had to be fulfilled: Observational study design, adult cancer survivors (of any cancer type), cancer-free controls (defined as adults without any history of cancer, except for non-melanoma skin cancer). We considered studies for inclusion reporting on at least one of the following outcomes: Blood pressure measurement, cholesterol/lipid testing, bone densitometry, or immunization vaccines.

Studies of childhood cancer survivors, secondary survivors such as family members of cancer survivors and those with no cancer-free control group or controls matched on screening services were excluded. In addition, review articles, commentaries, and editorials were excluded from this review.

Two authors independently reviewed each study for inclusion by first assessing titles and abstracts, and then the full text. Disagreements in study selection were resolved by consensus. Reasons for exclusion were documented.

2.3. Data Extraction

A standardized form was utilized to extract data. Information on each study included authors, publication year, study design, data source, cancer and preventive service ascertainment, inclusion and exclusion criteria, country of study population, type of cancer included, time under observation, total sample size, sample size for cases and controls, population characteristics such as age, gender, race, ethnicity, insurance, and socioeconomic status, preventive services, and statistical analyses used.

For specific preventive services, the following data was extracted: Definition of preventive service completion including time frame, eligibility criteria for preventive service, total number among cancer survivors and controls, Odds Ratios (ORs) and 95% Confidence Intervals (CIs) comparing cancer survivors to cancer-free controls, as well as confounders considered in the analyses.

At least two authors independently extracted data using the standardized data extraction form and compared their results. Discrepancies were resolved by consensus.

2.4. Assessment of Study Quality

Two independent authors performed a quality assessment of each eligible study using the Newcastle-Ottawa quality assessment Scale (NOS) [9Wells GASB, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses 2000. [cited 2016 08.20.2016]. Available from: http://www.medicine.mcgill.ca/rtamblyn/Readings/The%20Newcastle%20-%20Scale%20for%20assessing%20the%20quality%20of%20nonrandomised%20studies%20in%20meta-analyses.pdf]. The scale includes 8 questions, grouped under 3 broader categories: Group selection, comparability of groups, and outcome ascertainment. A single point is awarded for each question, and a maximum of two points may be awarded for comparability of groups. Study quality is reported on a scale from 0 points (greatest bias) to 9 points (least bias). The NOS is widely applied for study quality assessment because of its easy implementation and recommendation by the Cochrane Collaboration Handbook [10Higgins J, Green S. 2011. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0, 2011. The Cochrane Collaboration. Available from www.handbook.cochrane.org].

2.5. Statistical Analyses

Meta-analyses were calculated for influenza vaccination, cholesterol/lipid testing, bone densitometry and blood pressure measurement using STATA, version 13, (StataCorp LP, College Station, TX, USA). Meta-regressions, influence meta-analyses and other sensitivity analyses, as well as tests of publication bias were conducted separately for each preventive service.

All ORs and 95% CIs compared utilization of preventive services among cancer survivors versus cancer-free controls. For studies reporting crude numbers or percentages, crude ORs and 95% CIs were calculated from raw data. All ORs and CIs extracted from original studies were log transformed before analysis. The 95% CIs were used to calculate the natural logarithm of the standard error as ln(SE) = [ln (upper 95% CI) - ln(lower 95% CI)]/3.92.

A random effects model using the DerSimonian-Laird method was chosen due to heterogeneity among study designs and populations, as well as potential variability in definitions of cancer survivorship and preventive service utilization [11DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986; 7(3): 177-88.[http://dx.doi.org/10.1016/0197-2456(86)90046-2] [PMID: 3802833] ]. For one study reporting separate ORs for cancer subgroups, a random effects model was used to provide one study-wide pooled estimate of comparison.

To assess between-study heterogeneity in each analysis, forest plots were assessed for overlapping confidence intervals. In addition, heterogeneity was evaluated utilizing the I-squared statistic and associated p-value from a χ2 test [12Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002; 21(11): 1539-58.[http://dx.doi.org/10.1002/sim.1186] [PMID: 12111919] ]. Subgroup analyses were computed to identify potential sources of heterogeneity based on study characteristics. Subgroups were defined a priori and included study design (matched case-control vs. cross-sectional), study quality (NOS>=7 vs. <7), cancer type (breast cancer vs. all cancer types), preventive service ascertainment (self-reported vs. medical records/insurance claims data) and matching procedure (comorbidity matched controls vs. non-comorbidity matched controls).

Sensitivity analyses were conducted based on the inclusion of one study by Snyder et al. [13Snyder CF, Frick KD, Peairs KS, et al. Comparing care for breast cancer survivors to non-cancer controls: A five-year longitudinal study. J Gen Intern Med 2009; 24(4): 469-74.[http://dx.doi.org/10.1007/s11606-009-0903-2] [PMID: 19156470] ]. This study had been primarily excluded due to matching on mammography.

To assess the influence of individual studies on the overall effect size, a meta-influence plot was calculated. For these influence analyses, one study at a time was left out to assess to which extend the overall pooled estimate changed. This method allows to assess, whether the overall results are merely driven by one study.

For assessment of potential publication bias, Egger´s tests were conducted and funnel plots of the log OR vs. its standard error were visually inspected [14Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315(7109): 629-34.[http://dx.doi.org/10.1136/bmj.315.7109.629] [PMID: 9310563] ].

All p-values provided are two-sided. An alpha level of 0.05 was chosen for statistical significance.

3. RESULT

3.1. Study Selection and Study Characteristics

PubMed and EMBASE database searches yielded 3740 publications after removal of duplicates. 541 publications were identified after screening of titles and abstracts. Of these, 10 studies fulfilled the prespecified inclusion criteria. A total of 71.564 cancer survivors and 241.683 cancer-free controls were included. One study by McBean et al. [15McBean AM, Yu X, Virnig BA. The use of preventive health services among elderly uterine cancer survivors. Am J Obstet Gynecol 2008; 198(1): 86.e1-8.[http://dx.doi.org/10.1016/j.ajog.2007.05.036] [PMID: 18166316] ] reported no differences in utilization of influenza vaccination and bone density testing, but failed to provide multivariable adjusted odds ratios and was therefore excluded from further analyses. Fig. (1) shows the record flow chart of this review.

Fig. (1)
Record flow chart for publications comparing preventive services utilization in cancer-survivors compared to non-cancer controls.


Table 1 details study characteristics. Of 10 included studies, 2 were cross sectional [16Fairley TL, Hawk H, Pierre S. Health behaviors and quality of life of cancer survivors in Massachusetts, 2006: data use for comprehensive cancer control. Prev Chronic Dis 2010; 7(1): A09.[PMID: 20040224] , 17Lowenstein LM, Ouellet JA, Dale W, Fan L, Gupta Mohile S. Preventive care in older cancer survivors. J Geriatr Oncol 2015; 6(2): 85-92.[http://dx.doi.org/10.1016/j.jgo.2014.12.003] [PMID: 25547206] ], and 8 were matched case control studies [18Earle CC, Burstein HJ, Winer EP, Weeks JC. Quality of non-breast cancer health maintenance among elderly breast cancer survivors. J Clin Oncol 2003; 21(8): 1447-51.[http://dx.doi.org/10.1200/JCO.2003.03.060] [PMID: 12697865] , 19Earle CC, Neville BA. Under use of necessary care among cancer survivors. Cancer 2004; 101(8): 1712-9.[http://dx.doi.org/10.1002/cncr.20560] [PMID: 15386307] , 5Duffy CM, Clark MA, Allsworth JE. Health maintenance and screening in breast cancer survivors in the United States. Cancer Detect Prev 2006; 30(1): 52-7.[http://dx.doi.org/10.1016/j.cdp.2005.06.012] [PMID: 16455209] , 6Khan NF, Carpenter L, Watson E, Rose PW. Cancer screening and preventative care among long-term cancer survivors in the United Kingdom. Br J Cancer 2010; 102(7): 1085-90.[http://dx.doi.org/10.1038/sj.bjc.6605609] [PMID: 20234361] , 20Bishop 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(2): 207-14.[http://dx.doi.org/10.1016/j.bbmt.2009.09.015] [PMID: 19781657] -23Snyder CF, Frick KD, Kantsiper ME, et al. Prevention, screening, and surveillance care for breast cancer survivors compared with controls: Changes from 1998 to 2002. J Clin Oncol 2009; 27(7): 1054-61.[http://dx.doi.org/10.1200/JCO.2008.18.0950] [PMID: 19164212] ] Among the latter, 2 matched on comorbidities (scale from 0-2) as one of the matching factors [22Snyder CF, Frick KD, Herbert RJ, et al. Preventive care in prostate cancer patients: following diagnosis and for five-year survivors. J Cancer Surviv 2011; 5(3): 283-91.[http://dx.doi.org/10.1007/s11764-011-0181-y] [PMID: 21553320] , 23Snyder CF, Frick KD, Kantsiper ME, et al. Prevention, screening, and surveillance care for breast cancer survivors compared with controls: Changes from 1998 to 2002. J Clin Oncol 2009; 27(7): 1054-61.[http://dx.doi.org/10.1200/JCO.2008.18.0950] [PMID: 19164212] ].

Four studies ascertained the utilization of preventive services using self-reported data such as questionnaires or interviews [5Duffy CM, Clark MA, Allsworth JE. Health maintenance and screening in breast cancer survivors in the United States. Cancer Detect Prev 2006; 30(1): 52-7.[http://dx.doi.org/10.1016/j.cdp.2005.06.012] [PMID: 16455209] , 16Fairley TL, Hawk H, Pierre S. Health behaviors and quality of life of cancer survivors in Massachusetts, 2006: data use for comprehensive cancer control. Prev Chronic Dis 2010; 7(1): A09.[PMID: 20040224] , 7Wilkins KL, Woodgate RL. Preventing second cancers in cancer survivors. Oncol Nurs Forum 2008; 35(2): E12-22.[http://dx.doi.org/10.1188/08.ONF.E12-E22] [PMID: 18321824] , 20Bishop 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(2): 207-14.[http://dx.doi.org/10.1016/j.bbmt.2009.09.015] [PMID: 19781657] ], 5 used insurance claims data [18Earle CC, Burstein HJ, Winer EP, Weeks JC. Quality of non-breast cancer health maintenance among elderly breast cancer survivors. J Clin Oncol 2003; 21(8): 1447-51.[http://dx.doi.org/10.1200/JCO.2003.03.060] [PMID: 12697865] , 19Earle CC, Neville BA. Under use of necessary care among cancer survivors. Cancer 2004; 101(8): 1712-9.[http://dx.doi.org/10.1002/cncr.20560] [PMID: 15386307] , 21Lafata JE, Salloum RG, Fishman PA, Ritzwoller DP, O’Keeffe-Rosetti MC, Hornbrook MC. Preventive care receipt and office visit use among breast and colorectal cancer survivors relative to age- and gender-matched cancer-free controls. J Cancer Surviv 2015; 9(2): 201-7.[http://dx.doi.org/10.1007/s11764-014-0401-3] [PMID: 25252623] -23Snyder CF, Frick KD, Kantsiper ME, et al. Prevention, screening, and surveillance care for breast cancer survivors compared with controls: Changes from 1998 to 2002. J Clin Oncol 2009; 27(7): 1054-61.[http://dx.doi.org/10.1200/JCO.2008.18.0950] [PMID: 19164212] ], and one study utilized medical records [6Khan NF, Carpenter L, Watson E, Rose PW. Cancer screening and preventative care among long-term cancer survivors in the United Kingdom. Br J Cancer 2010; 102(7): 1085-90.[http://dx.doi.org/10.1038/sj.bjc.6605609] [PMID: 20234361] ]. One study was conducted in the United Kingdom [6Khan NF, Carpenter L, Watson E, Rose PW. Cancer screening and preventative care among long-term cancer survivors in the United Kingdom. Br J Cancer 2010; 102(7): 1085-90.[http://dx.doi.org/10.1038/sj.bjc.6605609] [PMID: 20234361] ]; 9 studies were localized in the United States of America.

Table 1
Characteristics of 10 cross-sectional/case-control studies on preventive services utilization comparing cancer survivors and cancer-free controls.


3.2. Preventive Service Utilization

Fig. (2) depicts that, overall, cancer survivors were significantly more likely to utilize preventive services than their cancer-free controls (OR=1.279, 95% CI: 1.145 – 1.430, p<0.001).

Fig. (2)
Subtotal and total random effects pooled estimates for preventive services.


Comparably, in separate analyses of each preventive service, cancer survivors were significantly more likely to utilize bone densitometry (pooled OR=1.226, 95% CI: 1.114 – 1.350, p<0.001) and influenza vaccination (pooled OR=1.565, 95% CI: 1.176 – 2.082, p=0.002) than cancer-free controls. No statistically significant difference between cancer survivors and controls was evident for blood pressure measurement and cholesterol/lipid testing (pooled OR=1.322, 95% CI: 0.812 – 2.151, p=0.261; pooled OR=1.046, 95% CI: 0.96 – 1.139, p=0.304).

3.3. Heterogeneity Assessment and Stratified Analyses

For each preventive service, heterogeneity was analyzed in subgroups by study design, study quality, cancer types included, ascertainment of preventive service utilization, and control matching. Results are separately presented in Tables (2a and 2b).

Table 2a
Heterogeneity (%) across studies for each preventive service and subgroups.


Table 2b
Stratified analysis (OR with 95% CI with p-value for effect measure modification) across studies for each preventive service and subgroups.


There was substantial (50-75%) or considerable (75-100%) between-study heterogeneity for most subgroups, except for breast cancer patients receiving bone densitometry, NOS<7 studies for influenza vaccination and comorbidity matched controls receiving cholesterol/lipid tests (not statistically significant at the chosen alpha-level).

For several subgroups, only one study was available, resulting in non-calculable between-study heterogeneity (NA).

Stratified analyses for each preventive service were calculated for subgroups by study design, study quality, cancer type, ascertainment of preventive service utilization, and control matching. Pooled odds ratios and p-values for subgroup comparisons are depicted in (Tables 2a and 2b). There was no statistically significant effect measure modification in subgroup pooled odds ratios at the chosen alpha level.

3.4. Sensitivity Analyses

For sensitivity analyses, we included one study by Snyder et al. that was primarily excluded due to matching of breast-cancer patients on controls receiving mammography [13Snyder CF, Frick KD, Peairs KS, et al. Comparing care for breast cancer survivors to non-cancer controls: A five-year longitudinal study. J Gen Intern Med 2009; 24(4): 469-74.[http://dx.doi.org/10.1007/s11606-009-0903-2] [PMID: 19156470] ].

Pooled estimates changed to OR=1.32 (95% CI: 0.81-2.15, p=0.261) for blood pressure measurement, OR=1.208 (95% CI: 1.126-1.297, p<0.001) for bone densitometry, OR=1.037 (95% CI: 0.967-1.112, p=0.307) for cholesterol/lipid test, and OR=1.508 (95% CI: 1.201-1.893, p<0.001) for influenza vaccination.

Influence analyses showed substantial changes in the pooled estimate towards smaller odds ratios upon exclusion of Earle at al [18Earle CC, Burstein HJ, Winer EP, Weeks JC. Quality of non-breast cancer health maintenance among elderly breast cancer survivors. J Clin Oncol 2003; 21(8): 1447-51.[http://dx.doi.org/10.1200/JCO.2003.03.060] [PMID: 12697865] ]. for influenza vaccination, Earle at al [19Earle CC, Neville BA. Under use of necessary care among cancer survivors. Cancer 2004; 101(8): 1712-9.[http://dx.doi.org/10.1002/cncr.20560] [PMID: 15386307] ]. for cholesterol/lipid test, and Lowenstein at al [17Lowenstein LM, Ouellet JA, Dale W, Fan L, Gupta Mohile S. Preventive care in older cancer survivors. J Geriatr Oncol 2015; 6(2): 85-92.[http://dx.doi.org/10.1016/j.jgo.2014.12.003] [PMID: 25547206] ]. for blood pressure measurement, as well as towards a larger odds ratio upon exclusion of Snyder at al [13Snyder CF, Frick KD, Peairs KS, et al. Comparing care for breast cancer survivors to non-cancer controls: A five-year longitudinal study. J Gen Intern Med 2009; 24(4): 469-74.[http://dx.doi.org/10.1007/s11606-009-0903-2] [PMID: 19156470] ]. for bone densitometry.

3.5. Publication Bias

Egger’s test suggested no evidence of publication bias for blood pressure measurement (p=0.746), bone densitometry (p=0.404), cholesterol/lipid test (p=0.667) and influenza vaccination (p=0.350). Upon visual inspection, there was no asymmetry in the funnel plots.

4. DISCUSSION

This systematic literature review and meta-analysis demonstrates that cancer survivors are more likely to receive certain preventive services than their cancer-free counterparts: The observed pooled estimates were OR=1.23 (95% CI:1.11-1.35, p<0.001) for bone densitometry and OR=1.57 (95% CI: 1.18-2.08, p=0.002) for influenza vaccination. At the same time, no statistically significant difference was evident for cholesterol/lipid tests (OR=1.05, 95% CI: 0.96-1.14, p=0.261) and blood pressure measurement (OR=1.32, 95% CI: 0.81-2.15, p=0.304).

One study matching breast cancer-survivors to cancer-free controls on receipt of mammography supports the results of our review [13Snyder CF, Frick KD, Peairs KS, et al. Comparing care for breast cancer survivors to non-cancer controls: A five-year longitudinal study. J Gen Intern Med 2009; 24(4): 469-74.[http://dx.doi.org/10.1007/s11606-009-0903-2] [PMID: 19156470] ]. This may indicate that the utilization of preventive services, such as bone densitometry, is independent from screening for primary malignancies. On an individual study level, only Lafata et al. [21Lafata JE, Salloum RG, Fishman PA, Ritzwoller DP, O’Keeffe-Rosetti MC, Hornbrook MC. Preventive care receipt and office visit use among breast and colorectal cancer survivors relative to age- and gender-matched cancer-free controls. J Cancer Surviv 2015; 9(2): 201-7.[http://dx.doi.org/10.1007/s11764-014-0401-3] [PMID: 25252623] ] and Khan et al. [6Khan NF, Carpenter L, Watson E, Rose PW. Cancer screening and preventative care among long-term cancer survivors in the United Kingdom. Br J Cancer 2010; 102(7): 1085-90.[http://dx.doi.org/10.1038/sj.bjc.6605609] [PMID: 20234361] ] reported estimates of less than OR=1 for bone densitometry, blood pressure measurement, and cholesterol/lipid tests. These studies were based on patient populations from the United Kingdom and Non-governmental organization databases, thus indicating that the pooled estimates of this review might not be generalizable to all populations.

For most preventive services, there was considerable to substantial heterogeneity, which was consistently high across subgroups, except for bone densitometry in breast cancer patients.

This heterogeneity is inherent to the outcomes evaluated in the different studies and reflects the inconsistent results reported by earlier reviews on cancer screening services [7Wilkins KL, Woodgate RL. Preventing second cancers in cancer survivors. Oncol Nurs Forum 2008; 35(2): E12-22.[http://dx.doi.org/10.1188/08.ONF.E12-E22] [PMID: 18321824] , 8Corkum M, Hayden JA, Kephart G, Urquhart R, Schlievert C, Porter G. Screening for new primary cancers in cancer survivors compared to non-cancer controls: A systematic review and meta-analysis. J Cancer Surviv 2013; 7(3): 455-63.[http://dx.doi.org/10.1007/s11764-013-0278-6] [PMID: 23645522] ]. In our study, heterogeneity might originate from differing timeframes and definitions of preventive services. Further, differences in the study´s underlying patient populations might explain the observed heterogeneity: For example, Synder et al. exclusively included older male patients with prostate cancer [22Snyder CF, Frick KD, Herbert RJ, et al. Preventive care in prostate cancer patients: following diagnosis and for five-year survivors. J Cancer Surviv 2011; 5(3): 283-91.[http://dx.doi.org/10.1007/s11764-011-0181-y] [PMID: 21553320] ], while Bishop et al. evaluated predominately younger, female patients with breast cancer or leukemia [20Bishop 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(2): 207-14.[http://dx.doi.org/10.1016/j.bbmt.2009.09.015] [PMID: 19781657] ]. On the individual study level, demographics of cancer-survivors and controls were well balanced using matching procedures or multivariable statistical models.

In stratified analyses the pooled estimates showed consistent effects across all subgroups. There was no evidence of effect measure modification, although the tests might be statistically underpowered due to small sample sizes. In sensitivity analyses, the pooled estimates proved robust upon inclusion of one study by Snyder et al. [13Snyder CF, Frick KD, Peairs KS, et al. Comparing care for breast cancer survivors to non-cancer controls: A five-year longitudinal study. J Gen Intern Med 2009; 24(4): 469-74.[http://dx.doi.org/10.1007/s11606-009-0903-2] [PMID: 19156470] ]. There was no evidence for publication bias.

Several explanations for differing utilization of preventive and screening services among cancer survivors and their cancer-free counterparts have been suggested, both on the health care provider and individual patient level.

Providers might realize that cancer survivors are at high risk for comorbidities, leading to an increase in examinations. In addition, cancer patients may frequently interact with the health care system. Thus, they might have a higher awareness and eagerness to utilize preventive services. On the contrary, providers may focus on malignancies, ignoring other potential comorbidities. Cancer-survivors may also suffer from their diagnosis emotionally, discouraging further interaction with the health care system [24Simard S, Thewes B, Humphris G, et al. Fear of cancer recurrence in adult cancer survivors: A systematic review of quantitative studies. J Cancer Surviv 2013; 7(3): 300-22.[http://dx.doi.org/10.1007/s11764-013-0272-z] [PMID: 23475398] ]. Finally, cancer survivors may face financial challenges due to health-care costs related to cancer treatment, deterring them from further examinations.

Throughout the last decade, recommendations for annual influenza vaccinations have changed in the US. As of 2010, the US Advisory Committee on Immunization Practices recommends influenza vaccinations for all ages [25Fiore AE, Uyeki TM, Broder K, Finelli L, Euler GL, Singleton JA, et al. Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP),2010. MMWR Recommendations and reports : Morbidity and mortality weekly report Recommendations and reports. 2010; 59(Rr-8): 1-62.]. Still, older versions recommend influenza vaccinations only for patients older than 50 years [25Fiore AE, Uyeki TM, Broder K, Finelli L, Euler GL, Singleton JA, et al. Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP),2010. MMWR Recommendations and reports : Morbidity and mortality weekly report Recommendations and reports. 2010; 59(Rr-8): 1-62.]. Since many studies were conducted prior to 2010, one might argue that the observed differences in influenza vaccination arise from an elder population of cancer survivors compared to cancer-free controls. Further, racial and ethnic disparities in US influenza vaccination rates have been reported [26Hebert PL, Frick KD, Kane RL, McBean AM. The causes of racial and ethnic differences in influenza vaccination rates among elderly Medicare beneficiaries. Health Serv Res 2005; 40(2): 517-37.[http://dx.doi.org/10.1111/j.1475-6773.2005.0e371.x] [PMID: 15762905] ]. Racial/ethnic population imbalances among included studies might explain the observed differences between cancer survivors and cancer-free controls. However, in most of the included studies, cancer survivors and controls were of comparable age and race/ethnicity [5Duffy CM, Clark MA, Allsworth JE. Health maintenance and screening in breast cancer survivors in the United States. Cancer Detect Prev 2006; 30(1): 52-7.[http://dx.doi.org/10.1016/j.cdp.2005.06.012] [PMID: 16455209] , 6Khan NF, Carpenter L, Watson E, Rose PW. Cancer screening and preventative care among long-term cancer survivors in the United Kingdom. Br J Cancer 2010; 102(7): 1085-90.[http://dx.doi.org/10.1038/sj.bjc.6605609] [PMID: 20234361] , 18Earle CC, Burstein HJ, Winer EP, Weeks JC. Quality of non-breast cancer health maintenance among elderly breast cancer survivors. J Clin Oncol 2003; 21(8): 1447-51.[http://dx.doi.org/10.1200/JCO.2003.03.060] [PMID: 12697865] -23Snyder CF, Frick KD, Kantsiper ME, et al. Prevention, screening, and surveillance care for breast cancer survivors compared with controls: Changes from 1998 to 2002. J Clin Oncol 2009; 27(7): 1054-61.[http://dx.doi.org/10.1200/JCO.2008.18.0950] [PMID: 19164212] ]. Since “cancer survivorship” was consistently defined as living after treatment for cancer, it is unlikely that influenza vaccinations given during cancer treatment have biased our results.

In the general population, bone densitometry is routinely utilized as a screening tool for osteoporosis, while in cancer-survivors bone densitometry can be used to detect cancer-treatment related osteoporosis as well: For women undergoing hormone therapy for breast cancer bone densitometry might be utilized to detect treatment related osteoporosis. Most included studies evaluated bone densitometry from medical claims data without reporting on the indication for this preventive service. Therefore, the difference in bone densitometry utilization between breast cancer survivors and cancer-free controls might be biased by diagnostic rather than preventive use. Still, our findings were not limited to this specific subgroup and therefore indicate more generalizable results.

Blood pressure measurement and cholesterol/lipid testing showed non-significant differences between cancer survivors and cancer free controls. In contrast to bone densitometry and influenza vaccination, these preventive services are highly established in general practice and comparably inexpensive [27Kaczorowski J, Myers MG, Gelfer M, et al. How do family physicians measure blood pressure in routine clinical practice? National survey of Canadian family physicians. Can Fam Physician 2017; 63(3): e193-9.[PMID: 28292817] , 28Dean CA, Arnold LD, Hauptman PJ, Wang J, Elder K. Patient, physician, and practice characteristics associated with cardiovascular disease preventive care for women. J Women Health (2002). 2017.]. Completion rates of these preventive services are probably much higher, although literature search yielded no explicit US/European rates during the last years. Therefore, the absolute difference in utilization between cancer survivors and controls might be lower in the highly prevalent preventive services blood pressure measurement and cholesterol/lipid testing than for less frequently applied bone densitometry and influenza vaccination. This might contribute to the observed lack of statistical significance in our meta-analysis, aggravated by small sample sizes.

The main limitation of this study is a low sample size and considerable heterogeneity of those studies included, although mitigated to a certain degree by implementation of random effects meta-analyses. Included studies evaluated highly divergent populations such as survivors of prostate, breast or colorectal cancer.

Further, timeframes for preventive services were inconsistent across studies, and often failed to follow national guidelines. Only one study was conducted outside the US, and thus our results might not be generalizable to a broader population or different health care systems. In addition, with only 10 studies included, subgroup analyses were potentially underpowered to detect effect measure modification. Moreover, including only 3 studies evaluating blood pressure measurement limits the interpretability of these results.

The random effects models calculated in this review only estimate one parameter for τ2 (between study variability) obtained via the DerSimonian-Laird method. This method neglects potential variability of τ2, and thus might provide pooled estimates with confidence intervals too narrow, and p-values too small. Moreover, with random effects models, small studies yield a relatively high weight when compared to large studies, as opposed to fixed effects models. In this review, sample sizes vary from 425 to 145.000 patients, and thus the relatively homogenous weighting of random effects models might be questioned. Finally, only few studies provided separate measures of preventive service utilization distinguishing follow-up care by primary care physicians and oncologists, and subgroup analyses were not feasible [18Earle CC, Burstein HJ, Winer EP, Weeks JC. Quality of non-breast cancer health maintenance among elderly breast cancer survivors. J Clin Oncol 2003; 21(8): 1447-51.[http://dx.doi.org/10.1200/JCO.2003.03.060] [PMID: 12697865] , 19Earle CC, Neville BA. Under use of necessary care among cancer survivors. Cancer 2004; 101(8): 1712-9.[http://dx.doi.org/10.1002/cncr.20560] [PMID: 15386307] , 21Lafata JE, Salloum RG, Fishman PA, Ritzwoller DP, O’Keeffe-Rosetti MC, Hornbrook MC. Preventive care receipt and office visit use among breast and colorectal cancer survivors relative to age- and gender-matched cancer-free controls. J Cancer Surviv 2015; 9(2): 201-7.[http://dx.doi.org/10.1007/s11764-014-0401-3] [PMID: 25252623] -23Snyder CF, Frick KD, Kantsiper ME, et al. Prevention, screening, and surveillance care for breast cancer survivors compared with controls: Changes from 1998 to 2002. J Clin Oncol 2009; 27(7): 1054-61.[http://dx.doi.org/10.1200/JCO.2008.18.0950] [PMID: 19164212] ]. It remains unclear, whether the higher preventive service utilization for cancer survivors observed in our study is mainly attributable to specialists´ follow-up.

Still, this review has several strengths. A rigid literature search was conducted, identifying 541 potential publications, of which 10 fulfilled the inclusion criteria. Two authors separately screened and extracted data, thereby minimizing errors. Moreover, statistical analyses and subgroups were chosen a priori.

CONCLUSION

In conclusion, this review demonstrates that cancer-survivors are more likely to utilize the preventive services influenza vaccinations and bone densitometry than their cancer-free counterparts. Our findings must be critically viewed in light of suboptimal screening rates in the general US population, and cancer-survivors in particular [29Sabatino SA, White MC, Thompson TD, Klabunde CN. Cancer screening test use - United States, 2013. MMWR Morb Mortal Wkly Rep 2015; 64(17): 464-8.[PMID: 25950253] ]. Future research should evaluate the underlying mechanisms, whether results are generalizable to other populations and if utilization of preventive services is translates into prolonged overall survival.

AUTHORS CONTRIBUTIONS

Annemarie Uhlig, Johannes Uhlig, Arne Strauss, Lutz Trojan, Joachim Lotz and Ali Seif Amir Hosseini contributed to conception, design, data gathering, evaluation and analysis, and promoted the manuscript. The final manuscript was approved by all authors.

FUNDING

None.

ETHICAL APPROVAL AND CONSENT TO PARTICIPATE

Not required (meta-analysis of IRB approved studies).

HUMAN AND ANIMAL RIGHTS

No Animals/Humans were used for studies that are bases of this research.

CONSENT FOR PUBLICATION

Not applicable.

CONFLICTS OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

Declared none.

REFERENCES

[1] Parry C, Kent EE, Mariotto AB, Alfano CM, Rowland JH. Cancer survivors: A booming population. Cancer Epidemiol Biomarkers Prev 2011; 20(10): 1996-2005.[http://dx.doi.org/10.1158/1055-9965.EPI-11-0729] [PMID: 21980007]
[2] Jørgensen TL, Hallas J, Friis S, Herrstedt J. Comorbidity in elderly cancer patients in relation to overall and cancer-specific mortality. Br J Cancer 2012; 106(7): 1353-60.[http://dx.doi.org/10.1038/bjc.2012.46] [PMID: 22353805]
[3] Mohile SG, Xian Y, Dale W, et al. Association of a cancer diagnosis with vulnerability and frailty in older Medicare beneficiaries. J Natl Cancer Inst 2009; 101(17): 1206-15.[http://dx.doi.org/10.1093/jnci/djp239] [PMID: 19638506]
[4] Sarfati D, Koczwara B, Jackson C. The impact of comorbidity on cancer and its treatment. CA Cancer J Clin 2016; 66(4): 337-50.[http://dx.doi.org/10.3322/caac.21342] [PMID: 26891458]
[5] Duffy CM, Clark MA, Allsworth JE. Health maintenance and screening in breast cancer survivors in the United States. Cancer Detect Prev 2006; 30(1): 52-7.[http://dx.doi.org/10.1016/j.cdp.2005.06.012] [PMID: 16455209]
[6] Khan NF, Carpenter L, Watson E, Rose PW. Cancer screening and preventative care among long-term cancer survivors in the United Kingdom. Br J Cancer 2010; 102(7): 1085-90.[http://dx.doi.org/10.1038/sj.bjc.6605609] [PMID: 20234361]
[7] Wilkins KL, Woodgate RL. Preventing second cancers in cancer survivors. Oncol Nurs Forum 2008; 35(2): E12-22.[http://dx.doi.org/10.1188/08.ONF.E12-E22] [PMID: 18321824]
[8] Corkum M, Hayden JA, Kephart G, Urquhart R, Schlievert C, Porter G. Screening for new primary cancers in cancer survivors compared to non-cancer controls: A systematic review and meta-analysis. J Cancer Surviv 2013; 7(3): 455-63.[http://dx.doi.org/10.1007/s11764-013-0278-6] [PMID: 23645522]
[9] Wells GASB, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses 2000. [cited 2016 08.20.2016]. Available from: http://www.medicine.mcgill.ca/rtamblyn/Readings/The%20Newcastle%20-%20Scale%20for%20assessing%20the%20quality%20of%20nonrandomised%20studies%20in%20meta-analyses.pdf
[10] Higgins J, Green S. 2011. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0, 2011. The Cochrane Collaboration. Available from www.handbook.cochrane.org
[11] DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986; 7(3): 177-88.[http://dx.doi.org/10.1016/0197-2456(86)90046-2] [PMID: 3802833]
[12] Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002; 21(11): 1539-58.[http://dx.doi.org/10.1002/sim.1186] [PMID: 12111919]
[13] Snyder CF, Frick KD, Peairs KS, et al. Comparing care for breast cancer survivors to non-cancer controls: A five-year longitudinal study. J Gen Intern Med 2009; 24(4): 469-74.[http://dx.doi.org/10.1007/s11606-009-0903-2] [PMID: 19156470]
[14] Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315(7109): 629-34.[http://dx.doi.org/10.1136/bmj.315.7109.629] [PMID: 9310563]
[15] McBean AM, Yu X, Virnig BA. The use of preventive health services among elderly uterine cancer survivors. Am J Obstet Gynecol 2008; 198(1): 86.e1-8.[http://dx.doi.org/10.1016/j.ajog.2007.05.036] [PMID: 18166316]
[16] Fairley TL, Hawk H, Pierre S. Health behaviors and quality of life of cancer survivors in Massachusetts, 2006: data use for comprehensive cancer control. Prev Chronic Dis 2010; 7(1): A09.[PMID: 20040224]
[17] Lowenstein LM, Ouellet JA, Dale W, Fan L, Gupta Mohile S. Preventive care in older cancer survivors. J Geriatr Oncol 2015; 6(2): 85-92.[http://dx.doi.org/10.1016/j.jgo.2014.12.003] [PMID: 25547206]
[18] 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(8): 1447-51.[http://dx.doi.org/10.1200/JCO.2003.03.060] [PMID: 12697865]
[19] Earle CC, Neville BA. Under use of necessary care among cancer survivors. Cancer 2004; 101(8): 1712-9.[http://dx.doi.org/10.1002/cncr.20560] [PMID: 15386307]
[20] 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(2): 207-14.[http://dx.doi.org/10.1016/j.bbmt.2009.09.015] [PMID: 19781657]
[21] Lafata JE, Salloum RG, Fishman PA, Ritzwoller DP, O’Keeffe-Rosetti MC, Hornbrook MC. Preventive care receipt and office visit use among breast and colorectal cancer survivors relative to age- and gender-matched cancer-free controls. J Cancer Surviv 2015; 9(2): 201-7.[http://dx.doi.org/10.1007/s11764-014-0401-3] [PMID: 25252623]
[22] Snyder CF, Frick KD, Herbert RJ, et al. Preventive care in prostate cancer patients: following diagnosis and for five-year survivors. J Cancer Surviv 2011; 5(3): 283-91.[http://dx.doi.org/10.1007/s11764-011-0181-y] [PMID: 21553320]
[23] Snyder CF, Frick KD, Kantsiper ME, et al. Prevention, screening, and surveillance care for breast cancer survivors compared with controls: Changes from 1998 to 2002. J Clin Oncol 2009; 27(7): 1054-61.[http://dx.doi.org/10.1200/JCO.2008.18.0950] [PMID: 19164212]
[24] Simard S, Thewes B, Humphris G, et al. Fear of cancer recurrence in adult cancer survivors: A systematic review of quantitative studies. J Cancer Surviv 2013; 7(3): 300-22.[http://dx.doi.org/10.1007/s11764-013-0272-z] [PMID: 23475398]
[25] Fiore AE, Uyeki TM, Broder K, Finelli L, Euler GL, Singleton JA, et al. Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP),2010. MMWR Recommendations and reports : Morbidity and mortality weekly report Recommendations and reports. 2010; 59(Rr-8): 1-62.
[26] Hebert PL, Frick KD, Kane RL, McBean AM. The causes of racial and ethnic differences in influenza vaccination rates among elderly Medicare beneficiaries. Health Serv Res 2005; 40(2): 517-37.[http://dx.doi.org/10.1111/j.1475-6773.2005.0e371.x] [PMID: 15762905]
[27] Kaczorowski J, Myers MG, Gelfer M, et al. How do family physicians measure blood pressure in routine clinical practice? National survey of Canadian family physicians. Can Fam Physician 2017; 63(3): e193-9.[PMID: 28292817]
[28] Dean CA, Arnold LD, Hauptman PJ, Wang J, Elder K. Patient, physician, and practice characteristics associated with cardiovascular disease preventive care for women. J Women Health (2002). 2017.
[29] Sabatino SA, White MC, Thompson TD, Klabunde CN. Cancer screening test use - United States, 2013. MMWR Morb Mortal Wkly Rep 2015; 64(17): 464-8.[PMID: 25950253]

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