Abstract
Background
There are conflicting results as to the association between pre-existing diabetes and the risk of mortality in patients with prostate cancer. The purpose of this study is to estimate the influence of pre-existing diabetes on prostate cancer-specific mortality and all-cause mortality.
Methods
We searched PubMed and Embase to identify studies that investigated the association between pre-existing diabetes and risk of death among men with prostate cancer. Pooled risk estimates and 95 % confidence intervals were calculated using fixed-effects models or random-effects models. Heterogeneity tests were conducted between studies. Publication bias was analyzed by using the Egger’s test, Begg’s test, and the trim and fill method.
Results
Of the 733 articles identified, 17 cohort studies that had 274,677 male patients were included in this meta-analysis. Pre-existing diabetes was associated with a 29 % increase in prostate cancer-specific mortality [relative risk (RR) 1.29, 95 % CI 1.22–1.38, I2 = 66.68 %], and with a 37 % increase in all-cause mortality (RR 1.37, 95 % CI 1.29–1.45, p < 0.01, I2 = 90.26 %). Additionally, in a subgroup analysis that was a type specific analysis focusing on type 2 diabetes and was conducted only with three cohort studies, pre-existing type 2 diabetes was associated with all-cause mortality (RR 2.01, 95 % CI 1.37–2.96, I2 = 95.55 %) and no significant association with prostate cancer-specific mortality was detected (RR 1.17, 95 % CI 0.96–1.42, I2 = 75.59 %). There was significant heterogeneity between studies and no publication bias was found.
Conclusions
This meta-analysis suggests diabetes may result in a worse prognosis for men with prostate cancer. Considering heterogeneity between studies, additional studies should be conducted to confirm these findings, and to allow generalization regarding the influence that each type of diabetes has on prostate cancer mortality.
Similar content being viewed by others
Background
Prostate cancer is the second leading cause of cancer death among men in the United States (Siegel et al. 2014). In 2015, the American Cancer Society reported that 1 in 7 men will be diagnosed with prostate cancer during his lifetime (Jemal et al. 2011). The known risk factors for prostate cancer include age, ethnicity, and family history (Jemal et al. 2011). Diabetes mellitus influences the risk of various cancers, including colon, pancreas, and thyroid cancer (Giovannucci et al. 2007; Karlin et al. 2012; Kasper et al. 2009). Prostate cancer appears to be an exception, whereby a diagnosis of diabetes is associated with a reduced incidence in most studies. However, whether a previous history of diabetes influences the prognosis of prostate cancer is not clear (Batty et al. 2011; Bensimon et al. 2014; Fleming et al. 2003; Froehner et al. 2003; Smith et al. 2008; Yeh et al. 2012).
Diabetes is primarily divided into type 1 and type 2 diabetes. Recently, the prevalence of type 2 diabetes has rapidly escalated owing to the increase in obesity, which also increases the risk of various cancers (Baba et al. 2011). Although hyperinsulinemia was hypothesized as the link between type 2 diabetes and the risk of various cancers (Barone et al. 2008), the influence of diabetes on the risk and prognosis of prostate cancer is complex because of the testosterone fluctuations often observed among patients with diabetes, and these fluctuations also influence the development of prostate tumors (Baradaran et al. 2009).
Pre-existing diabetes is defined as having a diagnosis of diabetes before the prostate cancer was diagnosed. Some prospective cohort studies reported that pre-existing diabetes was associated with 32 % increased risk of mortality among prostate cancer patients (Liu et al. 2012), while other studies reported that pre-existing diabetes was not associated with the prognosis of prostate cancer (Chiou et al. 2012). Since here is a controversy whether pre-existing diabetes would affect prognosis of prostate cancer, a meta-analysis would be necessary. There was two prior meta-analyses have studied association between pre-existing diabetes and prognosis of prostate cancer. These two studies indicated that pre-existing diabetes was associated with increased risk of prostate cancer death (Cai et al. 2015; Snyder et al. 2010). However, the meta-analysis by Snyder et al. only included four cohort studies (Snyder et al. 2010), while Cai et al. included 11 cohort studies (Cai et al. 2015). Since these meta-analyses, there are six additional cohort studies, which further examine the association between pre-existing diabetes and prognosis of prostate cancer. By including more studies, it is now possible to further examine subgroup analyses such as types of diabetes, level of adiposity and country where study was conducted. Therefore, we have included 17 cohort studies, which met our inclusion criteria to examine association between pre-existing diabetes and prognosis of prostate cancer.
Methods
Data sources and searches
This meta-analysis study followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. The analysis used the MEDLINE and EMBASE databases to identify applicable studies that were published between January 1970 and August 2016. The studies selected for inclusion needed to evaluate the effects of diabetes mellitus on the risk of death in patients with prostate cancer and they should have been published in the English language and in peer-reviewed journals. The search terms used in this study were “diabetes mellitus”, “prostate cancer”, “survival”, “prognosis”, “death”, and “mortality”. After a study was considered relevant on the basis of the search terms, its references were manually examined to find additional relevant studies. This study selected articles that reported finding in two categories: (1) the association of diabetes with prostate cancer-specific mortality in prostate cancer patients, and (2) the association of diabetes with all-cause mortality in prostate cancer patients. We then separately pooled the results from these two categories, to determine the relationship between type 2 diabetes and both prostate cancer-specific mortality and all-cause mortality, exclusively among prostate cancer patients. Pre-existing diabetes is defined as having a diagnosis of diabetes before the prostate cancer was diagnosed.
Eligibility criteria
Two authors (JL and JYJ) independently reviewed the articles in a standardized manner. Any disagreements in the eligibility for study selection were discussed by all three authors (JL, JYJ, and EG) to obtain a consensus. To be included in this study, each study had to meet three criteria: (1) evaluate prostate cancer, (2) indicate ascertainments of diabetes, including self-report, medication use, and blood test, and (3) report the hazard ratio or relative risk using standard error or a 95 % confidence interval (CI). In cases of publications that were duplicated or originated from the same study population, only the most recent study with the longest follow-up duration was included.
Data extraction and quality assessment
Two authors (JL and JYJ) evaluated the selected articles by following the guidelines of the Meta-analysis of Observational Studies in Epidemiology (MOOSE). In case of discrepancies, all three authors (JL, JYJ, and EG) conducted further discussions to obtain a consensus. The following data elements were extracted for this meta-analysis study: last name of the first author, publication year, country where the study was performed, number of deaths, sample size, description of the method used to diagnose diabetes, outcome determination, age at baseline, adjustment factors, follow-up duration, criteria of the cause of death, and the relative risk or hazard ratio that corresponded to a 95 % CI.
The authors evaluated the quality of the selected studies using the Newcastle-Ottawa Scale for the following factors: clarification as to diabetes status, adjustment for intermediate factors (e.g., age, disease stage, and tumor differentiation), study endpoints for prostate cancer-specific mortality and all-cause mortality, duration of follow-up, representativeness of the exposed cohort, and adequacy of the follow-up of cohorts (Table 1).
Statistical analysis
This meta-analysis study combined the risk estimates with CI or SE to estimate prostate cancer-specific mortality and all-cause mortality. The statistical heterogeneity between studies was estimated using Q statistic, and inconsistency was quantified using the I 2 statistic (Borenstein et al. 2005). Fixed-effect models with forest plots were used to pool the results of homogeneous studies whereas random-effect models with forest plots were used for heterogeneous studies.
Publication bias was evaluated using the Egger test (Egger et al. 1997) and Begg’s test (Begg and Mazumdar 1994). To further assess the potential effects of publication bias, the Duval and Tweedie nonparametric trim and fill method was used (Duval and Tweedie 2000). This method considers the possibility of hypothetically missing studies, imputes their RRs, and then recalculates a pooled estimate (Borenstein et al. 2010). Statistical significance was estimated using a p value of <0.05. All statistical analyses were performed using the Comprehensive Meta-Analysis software version 1.25 (Biostatic, Inc., Englewood, NJ, USA).
Results
Literature search
This meta-analysis study followed the selection processes shown in Fig. 1, by using the above-discussed exclusion and inclusion criteria. Of the 733 searched studies initially identified, 677 were excluded for the following reasons: presented duplicate information, did not report prostate cancer-specific mortality or all-cause mortality, were reviews or meta-analyses, or did not evaluate diabetes mellitus. An additional 39 studies were excluded from this analysis, because they were not mortality studies that evaluated diabetes. After applying the selection criteria, only 17 studies were included (Table 1). The total number of patients with prostate cancer was 274,677. The follow-up periods ranged between 3 and 17 years. This meta-analysis pooled directly the relative risk of prostate cancer-specific mortality and all-cause mortality from the 17 selected studies and then calculated the overall prostate cancer-specific and all-cause mortality, respectively. This study included only prior studies that had prospective and retrospective cohort designs, in order to understand the association between pre-existing diabetes and the prospect of prostate cancer mortality.
Study characteristics
A summary of the descriptive data is presented in Table 1. The majority of the studies selected for this meta-analysis were conducted in the United States (Best et al. 2015; Chamie et al. 2012; D’Amico et al. 2010; Karlin et al. 2012; Merrick et al. 2007; Shetti et al. 2012; Smith et al. 2008; Yeh et al. 2012). The remaining studies were conducted in the Republic of Korea (Park et al. 2006), Sweden (Liu et al. 2012), Netherlands (van de Poll-Franse et al. 2007), United Kingdom (Batty et al. 2011; Bensimon et al. 2014; Currie et al. 2012), Italy (Polesel et al. 2016) and Taiwan (Chiou et al. 2012; Tseng 2011). All 17 studies were published within the last 10 years.
In the studies selected, the prevalence of pre-existing diabetes ranged between 18 and 24 %. The average age of the participants was 58 years. The methods used for determining the existence of diabetes were: (1) medical records; (2) documented use of diabetes medicine; (3) the International Classification of Diseases (ninth revision) diagnosis codes for surveillance, epidemiology, and end results (Medicare); or (4) fasting glucose level. Most studies used in the meta-analysis adjusted for age and for other factors, including disease stage, alcohol use, smoking history, and physical activity (Table 1).
Association between diabetes and mortality
Seventeen studies examined the association between pre-existing diabetes, prostate cancer-specific mortality, and all-cause mortality in patients with prostate cancer (Fig. 2). The association between pre-existing diabetes and the risk of prostate cancer-specific mortality indicated that pre-existing diabetes was significantly associated with a 30 % increase in the risk of prostate cancer-specific mortality (RR 1.29, 95 % CI 1.22–1.38, I2 = 66.68 %, p < 0.01) and with a 65 % increase in the risk of all-cause mortality (RR 1.37, 95 % CI 1.29–1.45, p < 0.01, I2 = 90.26 %, p < 0.01). There was significant heterogeneity between studies. There was no evidence of publication bias on the basis of analyses using the Egger test and Begg’s test. In addition, there was no influence of unpublished data in any analysis using the trim and fill method.
Association between type 2 diabetes and mortality in a subgroup analysis
To further examine whether pre-existing type 2 diabetes, separately from type 1 diabetes, was associated with the prognosis of prostate cancer, five studies, which evaluated only type 2 diabetes, were included in this ancillary analysis (Fig. 3). This analysis showed that pre-existing type 2 diabetes was significantly associated with all-cause mortality (RR 2.01; 95 % CI, 1.37–2.96, I2 = 75.59 %, p < 0.01) whereas no association was found between pre-existing type 2 diabetes and prostate cancer-specific mortality. Significant heterogeneity was found between studies. In addition, there was no evidence of publication bias using the Egger test and Begg’s test and unpublished data were not found in any analysis using the trim and fill method.
Discussion
This meta-analysis study evaluated the association of pre-existing diabetes on prostate cancer-specific mortality and all-cause mortality. A main finding of this meta-analysis was that prostate cancer patients with pre-existing diabetes had an approximately 29 % higher prostate cancer-specific mortality and approximately 37 % higher all-cause mortality. In our ancillary analysis, which only included results from patients with pre-existing type 2 diabetes, we found that patients with prostate cancer with type 2 diabetes had a doubling in all-cause mortality. Although we are cautious in asserting that pre-existing diabetes is a key causal factor for worse prognosis of prostate cancer, taking preventative measures towards precluding diabetes is appropriate for patients with prostate cancer.
This meta-analysis included 17 studies. Of these, 11 studies addressed prostate cancer-specific mortality and 10 addressed all-cause mortality. Two previous meta-analyses reported the association between pre-existing diabetes and prognosis of prostate cancer (Begg and Mazumdar 1994; Liu et al. 2012). The meta-analysis by Snyder et al. (2010) of four cohort studies indicated that patients with prostate cancer with pre-existing diabetes had a 57 % higher all-cause mortality, whereas the meta-analysis by Cai et al. (2015) of 11 studies indicated that patients with prostate cancer with pre-existing diabetes had a 26 % higher prostate cancer-specific mortality and 83 % higher non-prostate cancer mortality. Current meta-analysis found six additional studies that have reported the impact of pre-existing diabetes on prognosis of prostate cancer (Chamie et al. 2012; Chiou et al. 2012; Giovannucci and Chan 2010; Karlin et al. 2012; Liu et al. 2012; Tseng et al. 2012), and the data available in the literature enabled us to perform an ancillary analysis using the studies that evaluated only patients with type 2 diabetes. Our analysis showed that type 2 diabetes increased the all-cause mortality by approximately 100 % when compared to patients with prostate cancer without diabetes. The results from our and other meta-analyses clearly showed that pre-existing diabetes, whether type 2 diabetes alone or both type 1 and 2 diabetes, increased the risk of all-cause mortality in patients with prostate cancer. The association between type 2 diabetes and prostate cancer mortality was not significant compared to the significant association seen for total diabetes mellitus, but it might be related to the sub-group analysis between type 2 diabetes and prostate cancer mortality was conducted only with 3 studies. Also, in assessing the observed positive results from this, there must be an acknowledgement that prostate cancer patients with diabetes have been found not do well with their diabetes treatment/management as well as their anti-cancer treatment/management. Unfortunately, our selected studies did not report the results after an adjustment for diabetes and cancer treatment/management. A further study that would reflect adjustment for this issue could help towards a better understanding of the relationship between diabetes and cancer treatment/management.
There have been controversies about whether pre-existing diabetes is associated with the incidence and prognosis of prostate cancer (Bensimon et al. 2014; D’Amico et al. 2010; Liu et al. 2012; Tseng 2011). Some studies (Batty et al. 2011; Chiou et al. 2012; Smith et al. 2008) suggested an inverse association, but with very wide CI’s. These studies argued that lower androgen levels in patients with type 2 diabetes contributed to the better prognosis of prostate cancer. However, other studies showed significantly worse prognosis in patients with prostate cancer with diabetes. It is not clear as to why some studies found an inverse association whereas others found a direct association between diabetes and prognosis of prostate cancer. Our meta-analyses demonstrated that pre-existing diabetes is associated with worse prognosis of prostate cancer.
Worse prognosis in patients with prostate cancer with diabetes may be related to several mechanisms. First, patients with prostate cancer with diabetes are more likely to have progressive prostate cancer due to the adverse interaction between diabetes mellitus and prostate cancer (Lubik et al. 2011; Ma et al. 2008). Patients with diabetes present with hyperglycemia, and these factors are associated with tumor development and progression (de Beer and Liebenberg 2014; Lai et al. 2014; Venkateswaran et al. 2007). Second, diabetes can diminish the effects of radiotherapy on prostate cancer. Accordingly, patients with prostate cancer with diabetes are more likely to experience a higher failure rate of radiotherapy treatment and worse gastrointestinal and genitourinary complications compared to patients with prostate cancer without diabetes (Chan et al. 2005; Herold et al. 1999). These complications can be explained by possible alterations in insulin-like growth factor 1, which may decrease the effectiveness of the treatments (Casa et al. 2008). Third, changes in certain hormones, including testosterone, sex hormone-binding globulin, and leptin, may affect the risk of prostate cancer (Baradaran et al. 2009). Additionally, previous studies (Basaria et al. 2006; Smith et al. 2006) indicated that low levels of androgens in patients with prostate cancer with diabetes contributed to insulin resistance as well as the risk of prostate cancer death and of non-prostate cancer death. In this respect, long-term androgen deprivation therapy, which is commonly used to treat patients with prostate cancer, increases insulin resistance and hyperglycemia, which in turn induces cardiovascular diseases (Basaria et al. 2006; Smith et al. 2006).
There are several limitations of this study. First, the duration of diabetes in the selected studies was not consistent. The duration of diabetes is crucial because recent findings indicate that longer durations of diabetes were associated with a higher risk of prostate cancer mortality and all-cause mortality (Bensimon et al. 2014). Second, the selected studies used different adjustment factors, such as tumor stage, treatment methods, and varying durations of diabetes, and these different adjustment factors may influence the RRs found in this study. Third, this meta-analysis study did not have adjustment for immortal time bias. This meta-analysis study was unable to address this issue as the prospective studies contained no information regarding follow up status for those men free of diabetes till time of diabetes diagnosis, and then till prostate cancer death occurred. Finally, the selected studies in this meta-analysis did not provide the Gleason scoring content, and therefore, we cannot rule out the possibility that only the high grade tumors are positively associated with diabetes, while the majority of prostate cancer tumors with low histologic grading may not be associated with diabetes co-morbidity.
This study suggested that pre-existing diabetes is clearly associated with total mortality and possibly prostate cancer-specific mortality in men diagnosed with prostate cancer. Future studies are necessary to select adequate treatments for patients with prostate cancer with diabetes in order to improve prognosis and reduce complications. In addition, these studies should examine the differences between type 1 and type 2 diabetes and determine how factors such as the duration of diabetes, radiotherapy treatments, and tumor stages can affect prostate cancer mortality.
References
Baba Y, Nosho K, Shima K, Hayashi M, Meyerhardt JA, Chan AT, Giovannucci E, Fuchs CS, Ogino S (2011) Phosphorylated AKT expression is associated with PIK3CA mutation, low stage, and favorable outcome in 717 colorectal cancers. Cancer 117:1399–1408
Baradaran N, Ahmadi H, Salem S, Lotfi M, Jahani Y, Baradaran N, Mehrsai AR, Pourmand G (2009) The protective effect of diabetes mellitus against prostate cancer: role of sex hormones. Prostate 69:1744–1750
Barone BB, Yeh HC, Snyder CF, Peairs KS, Stein KB, Derr RL, Wolff AC, Brancati FL (2008) Long-term all-cause mortality in cancer patients with preexisting diabetes mellitus: a systematic review and meta-analysis. JAMA 300:2754–2764
Basaria S, Muller DC, Carducci MA, Egan J, Dobs AS (2006) Hyperglycemia and insulin resistance in men with prostate carcinoma who receive androgen-deprivation therapy. Cancer 106:581–588
Batty GD, Kivimaki M, Clarke R, Davey Smith G, Shipley MJ (2011) Modifiable risk factors for prostate cancer mortality in London: forty years of follow-up in the Whitehall study. Cancer Causes Control 22:311–318
Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101
Bensimon L, Yin H, Suissa S, Pollak MN, Azoulay L (2014) Type 2 diabetes and the risk of mortality among patients with prostate cancer. Cancer Causes Control 25:329–338
Best LG, Garcia-Esquinas E, Yeh JL, Yeh F, Zhang Y, Lee ET, Howard BV, Farley JH, Welty TK, Rhoades DA, Rhoades ER, Umans JG, Navas-Acien A (2015) Association of diabetes and cancer mortality in American Indians: the Strong Heart Study. Cancer Causes Control 26:1551–1560
Borenstein M, Hedges L, Higgins J, Rothstein H (2005) Comprehensive meta analysis. Biostat, Englewood
Borenstein M, Hedges LV, Higgins JP, Rothstein HR (2010) A basic introduction to fixed-effect and random-effects models for meta-analysis. Res Synth Methods 1:97–111
Cai H, Xu Z, Xu T, Yu B, Zou Q (2015) Diabetes mellitus is associated with elevated risk of mortality amongst patients with prostate cancer: a meta-analysis of 11 cohort studies. Diabetes Metab Res Rev 31:336–343
Casa AJ, Dearth RK, Litzenburger BC, Lee AV, Cui X (2008) The type I insulin-like growth factor receptor pathway: a key player in cancer therapeutic resistance. Front Biosci 13:3273–3287
Chamie K, Daskivich TJ, Kwan L, Labo J, Dash A, Greenfield S, Litwin MS (2012) Comorbidities, treatment and ensuing survival in men with prostate cancer. J Gen Intern Med 27:492–499
Chan JM, Latini DM, Cowan J, Duchane J, Carroll PR (2005) History of diabetes, clinical features of prostate cancer, and prostate cancer recurrence-data from CaPSURE (United States). Cancer Causes Control 16:789–797
Chiou WK, Hwang JS, Hsu KH, Lin JD (2012) Diabetes mellitus increased mortality rates more in gender-specific than in nongender-specific cancer patients: a retrospective study of 149,491 patients. Exp Diabetes Res 2012:701643
Currie CJ, Poole CD, Jenkins-Jones S, Gale EA, Johnson JA, Morgan CL (2012) Mortality after incident cancer in people with and without type 2 diabetes: impact of metformin on survival. Diabetes Care 35:299–304
D’Amico AV, Braccioforte MH, Moran BJ, Chen MH (2010) Causes of death in men with prevalent diabetes and newly diagnosed high-versus favorable-risk prostate cancer. Int J Radiat Oncol Biol Phys 77:1329–1337
de Beer JC, Liebenberg L (2014) Does cancer risk increase with HbA1c, independent of diabetes? Br J Cancer 110:2361–2368
Duval S, Tweedie R (2000) Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56:455–463
Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634
Fleming ST, Pearce KA, McDavid K, Pavlov D (2003) The development and validation of a comorbidity index for prostate cancer among Black men. J Clin Epidemiol 56:1064–1075
Froehner M, Koch R, Litz R, Oehlschlaeger S, Noack B, Manseck A, Albrecht DM, Wirth MP (2003) Preoperative cardiopulmonary risk assessment as predictor of early noncancer and overall mortality after radical prostatectomy. Urology 61:596–600
Giovannucci E, Chan AT (2010) Role of vitamin and mineral supplementation and aspirin use in cancer survivors. J Clin Oncol 28:4081–4085
Giovannucci E, Liu Y, Platz EA, Stampfer MJ, Willett WC (2007) Risk factors for prostate cancer incidence and progression in the health professionals follow-up study. Int J Cancer 121:1571–1578
Herold DM, Hanlon AL, Hanks GE (1999) Diabetes mellitus: a predictor for late radiation morbidity. Int J Radiat Oncol Biol Phys 43:475–479
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61:69–90
Karlin NJ, Dueck AC, Cook CB (2012) Cancer with diabetes: prevalence, metabolic control, and survival in an academic oncology practice. Endocr Pract 18:898–905
Kasper JS, Liu Y, Giovannucci E (2009) Diabetes mellitus and risk of prostate cancer in the health professionals follow-up study. Int J Cancer 124:1398–1403
Lai GY, Giovannucci EL, Pollak MN, Peskoe SB, Stampfer MJ, Willett WC, Platz EA (2014) Association of C-peptide and leptin with prostate cancer incidence in the Health Professionals Follow-up Study. Cancer Causes Control 25:625–632
Liu X, Ji J, Sundquist K, Sundquist J, Hemminki K (2012) The impact of type 2 diabetes mellitus on cancer-specific survival: a follow-up study in Sweden. Cancer 118:1353–1361
Lubik AA, Gunter JH, Hendy SC, Locke JA, Adomat HH, Thompson V, Herington A, Gleave ME, Pollak M, Nelson CC (2011) Insulin increases de novo steroidogenesis in prostate cancer cells. Cancer Res 71:5754–5764
Ma J, Li H, Giovannucci E, Mucci L, Qiu W, Nguyen PL, Gaziano JM, Pollak M, Stampfer MJ (2008) Prediagnostic body-mass index, plasma C-peptide concentration, and prostate cancer-specific mortality in men with prostate cancer: a long-term survival analysis. Lancet Oncol 9:1039–1047
Merrick GS, Galbreath RW, Butler WM, Waller KE, Allen ZA, Lief J, Adamovich E (2007) Primary Gleason pattern does not impact survival after permanent interstitial brachytherapy for Gleason score 7 prostate cancer. Cancer 110:289–296
Park SM, Lim MK, Shin SA, Yun YH (2006) Impact of prediagnosis smoking, alcohol, obesity, and insulin resistance on survival in male cancer patients: National Health Insurance Corporation Study. J Clin Oncol 24:5017–5024
Polesel J, Gini A, Dal Maso L, Stocco C, Birri S, Taborelli M, Serraino D, Zucchetto A (2016) The impact of diabetes and other metabolic disorders on prostate cancer prognosis. J Diabetes Complications 30:591–596
Shetti MB, Merrick GS, Butler WM, Galbreath R, Torlone A, Lief JH, Adamovich E, Wallner KE (2012) The impact of diabetes mellitus on survival in men with clinically localized prostate cancer treated with permanent interstitial brachytherapy. Am J Clin Oncol 35:572–579
Siegel R, Ma J, Zou Z, Jemal A (2014) Cancer statistics, 2014. CA Cancer J Clin 64:9–29
Smith MR, Lee H, Nathan DM (2006) Insulin sensitivity during combined androgen blockade for prostate cancer. J Clin Endocrinol Metab 91:1305–1308
Smith MR, Bae K, Efstathiou JA, Hanks GE, Pilepich MV, Sandler HM, Shipley WU (2008) Diabetes and mortality in men with locally advanced prostate cancer: RTOG 92-02. J Clin Oncol 26:4333–4339
Snyder CF, Stein KB, Barone BB, Peairs KS, Yeh HC, Derr RL, Wolff AC, Carducci MA, Brancati FL (2010) Does pre-existing diabetes affect prostate cancer prognosis? A systematic review. Prostate Cancer Prostatic Dis 13:58–64
Tseng CH (2011) Prostate cancer mortality in Taiwanese men: increasing age-standardized trend in general population and increased risk in diabetic men. Ann Med 43:142–150
Tseng YY, Su CH, Lui TN, Yeh YS, Yeh SH (2012) Prospective comparison of the therapeutic effect of teriparatide with that of combined vertebroplasty with antiresorptive agents for the treatment of new-onset adjacent vertebral compression fracture after percutaneous vertebroplasty. Osteoporos Int 23:1613–1622
van de Poll-Franse LV, Houterman S, Janssen-Heijnen ML, Dercksen MW, Coebergh JW, Haak HR (2007) Less aggressive treatment and worse overall survival in cancer patients with diabetes: a large population based analysis. Int J Cancer 120:1986–1992
Venkateswaran V, Haddad AQ, Fleshner NE, Fan R, Sugar LM, Nam R, Klotz LH, Pollak M (2007) Association of diet-induced hyperinsulinemia with accelerated growth of prostate cancer (LNCaP) xenografts. J Natl Cancer Inst 99:1793–1800
Yeh HC, Platz EA, Wang NY, Visvanathan K, Helzlsouer KJ, Brancati FL (2012) A prospective study of the associations between treated diabetes and cancer outcomes. Diabetes Care 35:113–118
Authors’ contributions
The authors’ responsibilities were as follows: JL and JYJ contributed to designing the study; JL, JYJ, and EG collected the data; JL wrote the manuscript; and JYJ and EG confirmed the accuracy of the data and the analyses. All authors read and approved the final manuscript.
Acknowledgements
We would like to thank Dr. John Brobst for comments on a previous draft of this manuscript.
Competing interests
The authors declare that they have no competing interests. The authors have full control of all primary data and we agree to allow the journal to review the data if required.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Lee, J., Giovannucci, E. & Jeon, J.Y. Diabetes and mortality in patients with prostate cancer: a meta-analysis. SpringerPlus 5, 1548 (2016). https://doi.org/10.1186/s40064-016-3233-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1186/s40064-016-3233-y