Diabetes Ther (2018) 9:1335–1345 https://doi.org/10.1007/s13300-018-0444-y ORIGINAL RESEARCH Cardiac Versus Non-Cardiac Related Mortality Following Percutaneous Coronary Intervention in Patients with Insulin-Treated Type 2 Diabetes Mellitus: A Meta-Analysis . . Qiang Wang Hao Liu Jiawang Ding Received: April 26, 2018 / Published online: May 19, 2018 The Author(s) 2018 carried out using RevMan version 5.3 software, ABSTRACT and data were reported with odds ratios (OR) and 95% conﬁdence intervals (CI) as the main Introduction: Cardiovascular mortality is a parameters. major concern for patients with type 2 diabetes Results: A total of 4072 participants with ITDM mellitus (T2DM). Insulin therapy signiﬁcantly were included, of whom 1658 participants and contributes to a high rate of death in these 2414 participants were extracted from random- patients. We have performed a meta-analysis ized controlled trials and observational cohorts, comparing cardiac and non-cardiac-related respectively. Analysis of all data showed that mortality following percutaneous coronary death due to cardiac causes was signiﬁcantly intervention (PCI) in a sample of patients with higher in patients with ITDM (OR 2.16, 95% CI insulin-treated type 2 diabetes mellitus (ITDM). 1.79–2.59; P = 0.00001). At 1 year of follow-up, Methods: Studies were included in the meta- cardiac death was still signiﬁcantly higher analysis if: (1) they were trials or cohort studies compared to non-cardiac death (OR 2.39, 95% involving patients with T2DM post-PCI; (2) the CI 1.47–3.88; P = 0.0004), and this result did outcomes in ITDM were separately reported; not change with a longer follow-up period (3–- and (3) they reported cardiac death and non- 5 years) (OR 2.09, 95% CI 1.70–2.56; cardiac death among their clinical endpoints. P = 0.00001). Death due to cardiac causes was ITDM patients with any degree of coronary still signiﬁcantly higher in the subpopulations artery disease were included. The analysis was of patients with everolimus-eluting stents (OR 2.31, 95% CI 1.26–4.26; P = 0.007), paclitaxel- Enhanced digital features To view enhanced digital eluting stents (OR 2.36, 95% CI 1.63–3.39; features for this article go to https://doi.org/10.6084/ P = 0.00001), sirolimus-eluting stents (OR 2.11, m9.ﬁgshare.6247415. 95% CI 1.67–2.67; P = 0.00001), and zotar- olimus-eluting stents (OR 2.12, 95% CI Q. Wang J. Ding (&) 1.11–4.05; P = 0.02), respectively. Institute of Cardiovascular Diseases, Yichang Central People’s Hospital, Yichang 443000, Hubei, Conclusions: Mortality due to cardiac causes People’s Republic of China was signiﬁcantly higher than that due to non- e-mail: firstname.lastname@example.org cardiac causes in patients with ITDM who had H. Liu undergone PCI. The same conclusion could be Institute of Cardiovascular Diseases, The Second drawn from analyses focused on different fol- Afﬁliated Hospital of Guangxi Medical University, low-up periods, types of coronary stents, and Nanning 530021, Guangxi, People’s Republic of type of study data used. China 1336 Diabetes Ther (2018) 9:1335–1345 words/index terms were used to identify articles Keywords: Cardiovascular disease; Cardiac mortality; Insulin-treated type 2 diabetes of possible interest: – T2DM ? PCI, or mellitus; Non-cardiac mortality; Percutaneous – T2DM ? coronary angioplasty, or coronary intervention – T2DM ? PCI, or – ITDM ? PCI, or INTRODUCTION – Cardiac death ? ITDM ? PCI. In this era of modern medicine, nearly three Inclusion and Exclusion Criteria hundred and ﬁfty million cases of diabetes have been diagnosed to date worldwide . Mortality Studies were included in the meta-analysis is a great concern among this patient popula- review if: (1) they were trials or cohort studies tion, especially in those with type 2 diabetes based on patients with T2DM following PCI; (2) mellitus (T2DM) in co-existence with cardio- they separately reported outcomes in patients vascular disease (CVD). Values calculated by the with ITDM; (3) they reported cardiac death and World Health Organization show that there are non-cardiac death among their endpoints. approximately three million deaths annually Studies were excluded from the systematic due to T2DM and its related complications . review if: (1) they did not involve patients with Cardiovascular mortality, which was evaluated T2DM following PCI; (2) they did not separately in the Second Cardiovascular Outcome Trial report patients with ITDM; (3) they did not report Summit of the Diabetes and Cardiovascular cardiac death among their clinical outcomes; (4) Disease (D&CVD) EASD Study Group , is also they were repeated studies or duplicate studies. a major health risk factor in the population of patients with T2DM. Participants T2DM is an independent cause of mortality. Although data from the Korean National Health All participants in the studies ultimately inclu- Insurance Service–National Sample Cohort ded in our systematic review were patients with showed that 78% of diabetes-related deaths ITDM. However, the extent of the coronary could not be ascribed to diabetes , other artery disease varied among studies and inclu- studies have shown that in T2DM patients with ded ITDM patients with stable coronary artery CVD who were re-vascularized by percutaneous disease, de novo coronary artery disease, acute coronary intervention (PCI), insulin therapy myocardial infarction, single-vessel coronary signiﬁcantly contributed to a high death rate . artery disease, multi-vessel coronary artery dis- We have therefore conducted a meta-analy- ease (Table 1). sis to compare cardiac- versus non-cardiac-re- lated mortalityfollowing PCI in a sample of patients with insulin-treatedtype 2 diabetes Deﬁnition of Endpoints mellitus (ITDM). To date, few studies have sys- tematically assessed cardiac versus non-cardiac In this analysis, cardiac death was compared mortality in such patients following PCI. with non-cardiac death in diabetic patients who received insulin treatment. Therefore, the main focus was on: (1) cardiac mortality: death due to METHODS cardiac causes; (2) non-cardiac mortality: death which was not related to cardiac causes. Searched Databases and Key Words/Index Terms Data Extraction and Review We systematically and thoroughly searched the The following data were extracted by three MEDLINE/PubMed, EMBASE, Cochrane library, reviewers independently of each other: (1) and Google Scholar databases. the following key Diabetes Ther (2018) 9:1335–1345 1337 Table 1 Participants with insulin-treatedtype 2 diabetes mellitus and coronary artery disease participating in the studies included in the systematic review First author/year/reference of studies Coronary artery disease status of study participants Diabetes status of included in the meta-analysis study participants Antoniucci 2004  Acute myocardial infarction ITDM Bangalore 2016  Stable coronary artery disease ITDM Banning 2010  Left main and/or three-vessel coronary artery disease ITDM Dangas 2014  Multiple-vessel coronary artery disease ITDM Jain 2010  Single- or multi-vessel coronary artery disease ITDM Kappetein 2013  Complex coronary artery disease: de novo three-vessel ITDM and/or left main coronary artery disease Kirtane 2008  Single de novo lesion in a native coronary artery ITDM Kirtane 2009  Stable coronary artery disease ITDM Mehran 2004  Multi-vessel coronary artery disease ITDM Nakamura 2010  Coronary artery disease ITDM Simek 2013  All corner patients with coronary artery disease ITDM Tada 2011  Coronary artery disease ITDM ITDM insulin-treated type 2 diabetes mellitus patients with ITDM; (2) the number of events test (the lower the value, the lower the corresponding to cardiac death; (3) the number heterogeneity). of events corresponding to non-cardiac death; A ﬁxed (I \ 50%) effects model or a random (4) baseline features; (5) methodological fea- (I [ 50%) model was used based on the value tures of each study; (5) type of study. of I that was obtained. The methodological qualities for the ran- domized controlled trials were assessed by using Compliance with Ethics Guidelines the guidelines set down in the Cochrane Handbook for Systematic Reviews of Interven- This meta-analysis is based on previously con- tions . The Newcastle–Ottawa Scale (NOS)  ducted studies and does not contain any studies was used to assess the methodological qualities with human participants or animals performed for the observational studies. by any of the authors. Statistical Analysis RESULTS The computer program RevMan version 5.3 Searched Outcomes (The Nordic Cochrane Centre, The Cochrane Collaboration, Copenhagen, Denmark) was used as analytical software. Odds ratios (ORs) We followed the PRISMA guideline for this analysis . with 95% conﬁdence intervals (CIs) were cal- culated. Heterogeneity was assessed by two A total of 1368 publications were identiﬁed from the database search using the chosen key meta-analytical methods: (1) The Cochrane Q statistic test (a P value of B 0.05 indicates a words/index terms. Publications were excluded and eliminated based on the following criteria: statistically signiﬁcant result); (2) the I statistic 1338 Diabetes Ther (2018) 9:1335–1345 – They were not related to the aim of this eluting stents DES, speciﬁcally everolimus-elut- meta-analysis (n = 1282). ing stents (EES), paclitaxel-eluting stents (PES), – They did not report cardiovascular death, sirolimus-eluting stents (SES), and zotarolimus- but instead reported total death among their eluting stents (ZES), as shown in Table 2. clinical outcomes (n = 12). The baseline features of the participants with – They were meta-analyses or review articles ITDM are given in Table 3. Based on the features themselves (n = 5). which are listed, there was no signiﬁcant dif- – They did not separately report patients with ference between those patients who died due to ITDM (n = 21). a cardiac cause and those who died due to a – They were duplicates of the same study non-cardiac cause. (n = 36). The methodological qualities of the studies Ultimately, a total number of 12 articles (6 were also assessed. RCTs were assessed with the randomized controlled trials [RCTs] and 6 recommended features of the Cochrane collab- observational cohorts) [9–20] were included in oration guidelines . Grades were given to this meta-analysis, as shown in Fig. 1. deﬁne the limit of bias (low, low to moderate, moderate, and high). For the observational studies, NOS scores  were given, with a General and Baseline Features maximum number of nine points (a higher of the Participants score indicates better quality study), as shown in Table 4. A total number of 4072 patients with ITDM who participated in 12 observational studies/RCTs Death Due to Cardiac Versus Non-cardiac were included in this meta-analysis. Of these, Causes Following PCI in Patients 1658 participants were extracted from RCTs and with ITDM 2414 participants were extracted from observa- tional studies. Two studies had a follow-up period of \ 1 year, four studies had a follow-up Analysis of the combined data extracted from period of 1 year, and six studies had a follow-up the included RCTs and observational studies period of [ 1 [range 3–5] year). One study revealed that death due to cardiac causes was reported patients who were treated with a bare signiﬁcantly higher in patients with ITDM than metal stent, whereas all of the other studies death due to non-cardiac causes(OR 2.16, 95% involved patients who were treated with drug- Fig. 1 Flow diagram of study selection. ITDM Insulin-treated type 2 diabetes mellitus Diabetes Ther (2018) 9:1335–1345 1339 Table 2 Total number of events and other features of the studies included in the meta-analysis First author/year/ Type of Number of Number of Total Duration Type of stent reference of studies study patients with patients number of of follow- included in the cardiac with non- patients up period meta-analysis death cardiac death Antoniucci 2004  Observational 16 6 84 6 months – Bangalore 2016  RCT 18 8 747 1 year PES, EES Banning 2010  RCT 9 2 88 1 year PES Dangas 2014  RCT 42 20 325 5 years DES (SES and PES) Jain 2010  Observational 29 14 644 1 year ZES Kappetein 2013  RCT 16 5 89 5 years PES Kirtane 2008  RCT 15 13 265 4 years PES, BMS Kirtane 2009  RCT 0 0 144 1 year ZES, PES Mehran 2004  Observational 1 1 81 In-hospital – Nakamura 2010 Observational 13 10 200 3 years SES  Simek 2013  Observational 63 25 489 3 years EES, SES, PES Tada 2011  Observational 149 80 996 3 years SES RCT randomized controlled trials, BMS bare metal stent, SES sirolimus eluting stents, DES drug eluting stents, ZES zotarolimus eluting stents, EES everolimus eluting stents, PES paclitaxel eluting stents CI 1.79–2.59; P = 0.00001; I = 0%) when higher in these patients with ITDM (OR 2.09, (Fig. 2). 95% CI 1.70–2.56; P = 0.00001; I = 15%) However, data from RCTs and observational (Fig. 6). studies were also analyzed separately. When we When the participants were analyzed based considered only data obtained from RCTs in the on the type of stents, death due to cardiac analysis, death from cardiac causes was still causes was still signiﬁcantly higher in those signiﬁcantly higher in patients with ITDM (OR patients having an EES (OR 2.31, 95% CI 2 2 2.20, 95% CI 1.54–3.14; P = 0.0001; I = 14%) 1.26–4.26; P = 0.007, I = 0%) compared to (Fig. 3).Similarly, when we considered only data those a PES (OR 2.36, 95% CI 1.63–3.39; obtained from observational cohorts, death due P = 0.00001; I = 0%), SES (OR 2.11, 95% CI to cardiac causes was signiﬁcantly higher in the 1.67–2.67; P = 0.00001; I = 21%), or ZES (OR ITDM patients (OR 2.14, 95% CI 1.73–2.66; 2.12, 95% CI 1.11–4.05; P = 0.02), as shown in P = 0.00001; I = 0%) (Fig. 4). Fig. 7. When all the studies with a follow-up period of 1 year were analyzed together, cardiac death DISCUSSION was still signiﬁcantly higher in patients with ITDM compared to non-cardiac death (OR 2.39, Cardiovascular death is a major concern among 95% CI 1.47–3.88; P = 0.0004; I = 0%) (Fig. 5). patients with T2DM who are treated by PCI. The When studies with longer follow-up periods results of our meta-analysis show that cardio- were considered (range 3–5 years), mortality vascular death in patients with ITDM who have due to cardiac causes was still signiﬁcantly 1340 Diabetes Ther (2018) 9:1335–1345 Table 3 Baseline features of the participants First author/year/reference Age (years) Males (%) Hypertension Dyslipidemia Current Body mass of studies included in the (%) (%) smoker (%) index (kg/ meta-analysis m ) CD NCD CD NCD CD NCD CD NCD CD NCD CD NCD Antoniucci 2004  69.0 69.0 65.0 65.0 40.0 40.0 30.0 30.0 20.0 20.0 – - Bangalore 2016  58.5 58.5 71.0 71.0 65.6 65.6 76.2/ 76.2 12.3 12.3 26.1 26.1 Banning 2010  65.4 65.4 71.0 71.0 69.9 69.9 81.5 81.5 15.8 15.8 29.5 29.5 Dangas 2014  62.6 62.6 61.3 61.3 87.5 87.5 – - 17.9 17.9 30.5 30.5 Jain 2010  66.6 66.6 62.2 62.2 82.1 82.1 67.9 67.9 13.9 13.9 – - Kappetein 2013  65.4 65.4 71.0 71.0 70.0 70.0 82.0 82.0 16.0 16.0 29.5 29.5 Kirtane 2008  63.0 63.0 64.7 64.7 82.1 82.1 74.0 74.0 18.4 18.4 – - Kirtane 2009  63.3 63.3 71.0 71.0 76.7 76.7 81.4 81.4 64.8 64.8 – - Mehran 2004  63.0 63.0 52.0 52.0 77.0 77.0 71.0 71.0 11.0 11.0 – - Nakamura 2010  66.2 66.2 66.2 66.2 68.1 68.1 58.0 58.0 12.1 12.1 24.0 24.0 Simek 2013  65.1 65.1 69.2 69.2 70.6 70.6 65.5 65.5 32.1 32.1 28.8 28.8 Tada 2011  66.7 66.7 67.0 67.0 76.0 76.0 – - 16.0 16.0 24.1 24.1 CD Cardiac death, NCD non-cardiac death undergone PCI was signiﬁcantly higher that An 11-year retrospective analysis of death death due to non-cardiac causes. This result certiﬁcates in Shanghai also showed an remained consistent even when data from the increasing occurrence of CVD among Chinese RCTs and observational studies were analyzed patients who had previously developed diabetes separately. mellitus , with 29.9% of deaths among To assess the effect of differences in follow- those diabetic patients due to cardiovascular up periods on the cause of death in this patient causes; in comparison, other causes represented group, we also separately analyzed the data only small percentages. However, causes of from all of the studies included in the meta- death based speciﬁcally on patients with ITDM analysis which reported a follow-up period of were not analyzed in that study. 1 year. As reported in the ‘‘Results’’ section, Finally, even though research has shown cardiac death was still signiﬁcantly higher in diabetes mellitus to be independently associ- this subpopulation of patients with ITDM. ated with death due to CVD, other studies have When a longer follow-up period (3–5 years) was shown that insulin therapy also makes a major considered, the major cause of death remained contribution to such an outcome [5, 22]. In cardiovascular. addition, female gender and higher co-mor- We also assessed the impact of coronary bidities have also been suggested to further stents on the results by analyzed the data from contribute to such outcomes . These factors all studies based on the types of coronary stents should further be investigated in future studies. which were implanted (EES, PES, SES, and ZES). There are a few limitations to our analysis. However, cardiovascular cause of death was still First, the total number of patients was relatively signiﬁcantly higher in the patients with ITDM. small, especially for the analysis on impact of Diabetes Ther (2018) 9:1335–1345 1341 Table 4 Assessment of bias risk First author/year/reference of studies included in the meta-analysis Bias risk grade/score Bias status RCTs (Cochrane assessment) Kirtane 2009  B Low to moderate Bangalore 2016  A Low Banning 2010  A Low Dangas 2014  A Low Kirtane 2008  B Low to moderate Kappetein 2013  B Low to moderate Observational studies (NOS assessment) Antoniucci 2004  6 Moderate Jain 2010  8 Low Mehran 2004  6 Moderate Nakamura 2010  6 Moderate Simek 2013  7 Low Tada 2011  6 Moderate NOS Newcastle–Ottawa Scale Fig. 2 Cardiac versus non-cardiac death following percutaneous coronary intervention (PCI) in patients with ITDM. CI Conﬁdence interval, M–H Mantel–Haenszel test types of coronary stents on cause of death in artery disease, left main coronary artery disease, patients with ITDM treated by PCI. Second, data and acute myocardial infarction) were com- from different categories of participants (those bined and analyzed. Third, the anti-platelet with stable coronary artery disease, multi-vessel agents which were used post-PCI were not taken coronary artery disease, single-vessel coronary 1342 Diabetes Ther (2018) 9:1335–1345 Fig. 3 Cardiac versus non-cardiac death following PCI in patients with ITDM based only on data obtained from randomized controlled trials Fig. 4 Cardiac versus non-cardiac death following PCI in ITDM based only on data obtained from observational cohorts Fig. 5 Cardiac versus non-cardiac death following PCI in ITDM during a follow-up period of 1 year Fig. 6 Cardiac versus non-cardiac death following PCI in ITDM during a longer follow-up period (range 3–5 years) Diabetes Ther (2018) 9:1335–1345 1343 Fig. 7 Cardiac versus non-cardiac death following PCI in ITDM according to drug-eluting stents into consideration and this might also have had ACKNOWLEDGEMENTS an impact on the mortality rate. Funding. No funding or sponsorship was CONCLUSIONS received for this study or publication of this article. In patients with ITDM, mortality due to cardiac causes was signiﬁcantly higher than that due to Authorship. All named authors meet the non-cardiac causes following PCI. The same International Committee of Medical Journal conclusion was reached when different lengths Editors (ICMJE) criteria for authorship for this of follow-up periods were assessed, when dif- article, take responsibility for the integrity of ferent data sets were used (total data set, data the work as a whole, and have given their from the observational cohort or RCTs sepa- approval for this version to be published. rately), and when types of coronary stents which were implanted were assessed. 1344 Diabetes Ther (2018) 9:1335–1345 Summit of the Diabetes and Cardiovascular Disease Authorship Contributions. Qiang Wang, (D&CVD) EASD Study Group. Cardiovasc Diabetol. Hao Liu, and Jiawang Ding were responsible for 2017;16(1):35. the conception and design, acquisition of data, analysis and interpretation of data, drafting the 4. Kang YM, Kim YJ, Park JY, Lee WJ, Jung CH. Mor- tality and causes of death in a national sample of initial manuscript, and critical revision of the type 2 diabetic patients in Korea from 2002 to 2013. manuscript for important intellectual content. Cardiovasc Diabetol. 2016;15(1):131. Qiang Wang wrote the manuscript and is the ﬁrst author. 5. Bundhun PK, Li N, Chen MH. Adverse cardiovas- cular outcomes between insulin-treated and non- insulin treated diabetic patients after percutaneous Disclosures. The authors Qiang Wang, Hao coronary intervention: a systematic review and Liu and Jiawang Ding have nothing to disclose. meta-analysis. Cardiovasc Diabetol. 2015;14:135. They do not have any personal, ﬁnancial, commercial, or academic conﬂicts of interest. 6. Higgins JP, Thompson SG, Deeks JJ, et al. Assessing risk of bias in included studies. In: Cochrane handbook for systematic reviews of interventions. Compliance with Ethics Guidelines. This Wiley; 2008. p. 187–241. meta-analysis is based on previously conducted studies and does not contain any studies with 7. Wells GA, Shea B, O’Connell D, et al. The New- human participants or animals performed by castle–Ottawa Scale (NOS) for assessing the quality if nonrandomized studies in meta-analyses. 2009. any of the authors. http://www.ohri.ca/programs/clinical_ epidemiology/oxford.htm. Accessed 19 Oct 2009. Data Availability. All data generated or analyzed during this study are included in this 8. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and published article. meta-analyses of studies that evaluate health- careinterventions: explanation and elaboration. Open Access. 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Published: May 19, 2018