Negative association of diabetes with rupture of abdominal aortic aneurysm

Abstract

Purpose:

To summarize the association of diabetes with abdominal aortic aneurysm rupture, we reviewed currently available studies with a systematic literature search and meta-analytic evaluation.

Methods:

To identify all studies reporting the association of diabetes with abdominal aortic aneurysm rupture, MEDLINE and EMBASE were searched through July 2015. For each study, data regarding diabetes prevalence in both the ruptured and non-ruptured groups were used to generate an unadjusted odds ratio for abdominal aortic aneurysm rupture and 95% confidence intervals. Alternatively, an unadjusted or adjusted odds ratio, or hazard ratio for abdominal aortic aneurysm rupture with 95% confidence interval was directly abstracted (as available) from each individual study.

Results:

Our search identified 11 eligible studies. A primary meta-analysis of nine studies reporting data on ruptured (not including non-ruptured symptomatic) abdominal aortic aneurysm demonstrated that diabetes was associated with significantly lower prevalence/incidence of abdominal aortic aneurysm rupture (odds ratio/hazard ratio, 0.71; 95% confidence interval, 0.56 to 0.89; p = 0.003). A secondary meta-analysis of all 11 studies (adding two studies in which non-ruptured symptomatic abdominal aortic aneurysm was included in the rupture group) also demonstrated that diabetes was associated with significantly lower prevalence/incidence of abdominal aortic aneurysm rupture (odds ratio/hazard ratio, 0.77; 95% confidence interval, 0.63 to 0.95; p = 0.01).

Conclusion:

Diabetes is negatively associated with abdominal aortic aneurysm rupture.

Keywords

Abdominal aortic aneurysm diabetes meta-analysis rupture

Introduction

Coronary artery disease (CAD) and peripheral artery disease (PAD), both representative atherosclerotic diseases, are positively associated with the presence of abdominal aortic aneurysm (AAA).^1,2 Despite the positive associations of CAD and PAD with AAA presence, diabetes (major risk factor of CAD and PAD) is negatively associated with not only presence³ but also growth⁴ of AAA. The negative associations of diabetes with AAA presence and growth support the hypothesis that diabetes may be also negatively associated with AAA rupture. The RESCAN individual patient data meta-analysis⁵ of only two studies^6,7 including a total of 3153 patients with small AAA, however, revealed no association between diabetes and rupture. Whereas, a recent large (including 188 patients with ruptured and 1482 patients with non-ruptured AAA) retrospective study by Theivacumar et al.⁸ suggests that diabetes patients with AAA are significantly less likely to present with rupture or to die from aneurysm rupture when compared to non-diabetes patients with AAA. It is still debated whether diabetes is negatively associated with AAA rupture. To summarize the association of diabetes with AAA rupture, we reviewed currently available studies with a systematic literature search and meta-analytic evaluation in this article.

Methods

All studies reporting the association of diabetes with AAA rupture were identified using a two-level search strategy. First, databases including MEDLINE and EMBASE were searched through July 2015 using Web-based search engines (PubMed and OVID). Second, relevant studies were identified through a manual search of secondary sources including references of initially identified articles and a search of reviews and commentaries. All references were downloaded for consolidation, elimination of duplicates and further analysis. Search terms included ‘rupture’ or ‘ruptured’, ‘abdominal aortic aneurysm/aneurysms’ and ‘diabetes’ or ‘diabetic/diabetics’.

Studies considered for inclusion met the following criteria: the design was a case–control or prospective/retrospective cohort study; the study population was (1) patients with ruptured AAA and those with non-ruptured AAA or (2) patients with diabetes and those without diabetes; and main outcomes included (1) diabetes prevalence or (2) AAA-rupture incidence. Two authors (H.T. and T.U.) reviewed the eligible studies and determined whether the studies met the selection criteria. For each study, data regarding diabetes prevalence in both the ruptured and non-ruptured groups were used to generate an unadjusted odds ratio (OR) for AAA rupture and 95% confidence intervals (CIs). Alternatively, an unadjusted or adjusted OR or hazard ratio (HR) for AAA rupture with 95% CI was directly abstracted (as available) from each individual study. Data were extracted in duplicate by two investigators (H.T. and T.U.), and disagreements were resolved by consensus.

Study-specific estimates (preferentially adjusted estimates) were combined using inverse variance-weighted averages of logarithmic ORs/HRs in both fixed-effect and random-effects models. Between-study heterogeneity was analysed by means of standard χ² tests. Where no statistically significant heterogeneity was identified, the fixed-effect estimate was used preferentially as the summary measure. Sensitivity analyses were performed to assess the contribution of each study to the pooled estimate by excluding individual studies one at a time and recalculating the pooled OR/HR estimates for the remaining studies. Publication bias was assessed graphically using a funnel plot and mathematically using an adjusted rank-correlation test⁹ and a linear regression test.¹⁰ All analyses were conducted using Review Manager version 5.3 (available from http://tech.cochrane.org/revman) and Comprehensive Meta-Analysis version 3 (Biostat, Englewood, NJ).

Results

Of 100 potentially relevant articles screened initially, nine eligible studies^8,11–18 were identified. Furthermore, two relevant studies^6,7 were added through a manual search. In total, our meta-analysis included 11 studies.^{6–8,11–18} Study design (Table 1), patient characteristics (Table 1; online Appendices 1 and 2), diabetes prevalence, rupture incidence and relative risk of rupture are summarized in Table 2. In a case–control study by Buijs et al.,¹¹ non-ruptured symptomatic AAA and ruptured AAA were combined and labelled as non-elective AAA. In the rupture group of another case–control study by Fillinger et al.,¹³ emergency AAA repair was performed because of rupture or acute severe pain. As a primary meta-analysis, thus, we combined the remaining nine studies^{6–8,12,14–18} reporting data on ruptured (not including non-ruptured symptomatic) AAA. Additionally, all of the 11 studies were combined as a secondary meta-analysis.

Table 1.

Study design and patient characteristics.

Study	Design	Definition of rupture	Patient number		Aneurysm diameter (mm)			Age (year)			Men (%)
		Definition of rupture	Rupture	Non-rupture	Rupture	Non-rupture	p value	Rupture	Non-rupture	p value	Rupture	Non-rupture	p value
Case–control study
Buijs et al.¹¹	Case–control	Non-elective^a	91	230	77 ± 20	62 ± 12	<0.001	72 ± 8.2	70 ± 7.7	0.25	92	93	0.96
Da Silva et al.¹²	Case–control	NR	88	570	Median, 76.5 (range, 40–135)	Median, 60.2 (range, 30–130)	0.0001	Median, 71.5 (range, 51–91)	Median, 70.6 (range, 50–98)	0.359	87.5	80.5	0.156
Fillinger et al.¹³	Case–control (matched for diameter, gender and age)	Emergency^b	100	100	60 ± 10	60 ± 10	0.8	72 ± 8	73 ± 9	0.5	77	77	0.9
Gokani et al.¹⁴	Case–control	NR	315	668	Mean, 78	Mean, 67	<0.05	Median, 77.6	Median, 73.0	<0.05	75.6	90.6	<0.05
Lo et al.¹⁵	Case–control	CT/angiographic evidence or found at exploration	440	3605	Men/women, 78 ± 19/71 ± 21	Men/women, 59 ± 12/57 ± 11	NR	Men/women, 72 ± 9/78 ± 7	Men/women, 72 ± 9/74 ± 8	NR	80.9	77.2	NR
Sterpetti et al.¹⁶	Case–control	Autopsy	77	220	80 ± 23	51 ± 17	<0.01	74 ± 9	70 ± 10	NS	85.7	78.2	NS
Theivacumar et al.⁸	Case–control	ICD-10 code, I173	188	1482	Diabetes/non-diabetes, 57/58; p = 0.21			Median, 74 (range, 68–86) for diabetes; median, 74 (range, 44–96) for non-diabetes	Median, 74 (range, 53–89) for diabetes; median, 75 (range, 44–96) for non-diabetes	NR	83.3 for diabetes, 83.5 for non-diabetes	82.6 for diabetes, 84.9 for non-diabetes	NR
Study	Design	Definition of diabetes	Patient number		Initial aneurysm diameter (mm)			Baseline age (year)			Men (%)
			Diabetes	Non-diabetes	Diabetes	Non-diabetes	p value	Diabetes	Non-diabetes	p value	Diabetes	Non-diabetes	p value
Cohort study
Brady et al.⁶ (UKSAT)^c	Prospective small-AAA-patient cohort	NR	145	781	43 ± 7			Mean, 71.6			93.1
Powell et al.¹⁷ (EVAR 2)	Prospective large-AAA-patient cohort	NR	59	341	Median, 67 (IQR, 60–74) for rupture; median, 64 (IQR, 60–73) for non-rupture			76.6 ± 6.0 for rupture; 76.8 ± 6.6 for non-rupture			85.9
Tsai et al.¹⁸	Retrospective population-based cohort	Type 2 (ICD-9 code, 250)	160,391	646,710	NR			70.5 ± 8.62	69.9 ± 8.90	<0.0001	46.5	46.5	0.87
Vega de Céniga et al.^{7 c}	Prospective small-AAA-patient cohort	NR	96	2058	36.2 ± 5.61^d			Mean, 69.4			78.4

AAA: abdominal aortic aneurysm; CT: computed tomography; CTA: CT angiography; EVAR: endovascular aneurysm repair; ICD: International Classification of Diseases; IQR: interquartile range; NR: not reported; NS: not significant; UKSAT: UK Small Aneurysm Trial.

Combining symptomatic (having lower back pain, tenderness of the abdomen or a pulsating abdominal mass that was painful on palpation, without signs of rupture) and ruptured (having acute signs of rupture, such as hypotension and retroperitoneal haemorrhage on either CTA or during surgery).

Rupture or acute, severe pain.

Individual patient data provided by the RESCAN collaborators.⁵

Data in the original study.

Table 2.

Diabetes prevalence, rupture incidence and relative risk of rupture.

Study	Diabetes
	Definition		Prevalence (%)		Relative risk [95% CI] of rupture
			Rupture	Non-rupture	Univariate unadjusted	Multivariate adjusted
Case–control study
Buijs et al.¹¹	Type 1 or 2		21	16	OR, 1.38 [0.74–2.55]^a	Analysis, performed; OR, NR
Da Silva et al.¹²	NR		14.8	15.4	OR, 0.95 [0.51–1.78]^a	Analysis, performed; non-significant OR, NR
Fillinger et al.¹³	NR		13	15	OR, 0.85 [0.38–1.89]^a	Analysis, performed; diabetes, not entered
Gokani et al.¹⁴	NR		5.1	9.7	OR, 0.50 [0.28–0.87]^a	OR, 0.86 [0.49–1.76]
Lo et al.¹⁵	NR		14	18	OR, 0.78 [0.59–1.04]^a	OR for men/women, 0.7 [0.5–1.1]/0.9 [0.4–2.1]
Sterpetti et al.¹⁶	NR		1.3	12.8	OR, 0.09 [0.01–0.67]^a	Analysis, performed; diabetes, not entered
Theivacumar et al.⁸	ICD-10 codes, E100–E149		6.4	11.9	OR, 0.48 [0.26–0.88]	Analysis, not performed
Study	Rupture
	Follow-up (year)	Definition	Incidence (%)		Relative risk [95% CI] of rupture
			Diabetes	Non-diabetes	Univariate unadjusted	Multivariate adjusted
Cohort study
Brady et al.⁶ (UKSAT)^b	Mean, 3.85	Pragmatic, based on local reporting	0.65		HR, 1.20 [0.38–3.81]^c	Analysis, not performed
Powell et al.¹⁷ (EVAR 2)	Median, 1.1 (IQR, 0.4–1.9) for rupture; median, 0.3 (IQR, 0.1–1.6) for non-rupture	Determined by contrast-enhanced CT imaging, surgical findings and by information from the death certificate (including autopsies) provided by the Office for National Statistics	5.1	13.8	HR, 0.40 [0.125–1.30]	HR, 0.45 [0.13–1.50]
Tsai et al.¹⁸	12	ICD-9 code, 441.3	0.019	0.026	OR, 0.72 [0.49–1.07]^a	HR of advanced diabetes (ICD-9 codes 250.4–250.9), 0.57 [0.30–1.09])
Vega de Céniga et al.^{7 c}	Mean, 2.44	Pragmatic, based on local reporting	2.7		HR, 1.52 [0.17–13.67]^c	Analysis, not performed

CI: confidence interval; EVAR: endovascular aneurysm repair; CT: computed tomography; OR: odds ratio; HR: hazard ratio; ICD: International Classification of Diseases; IQR: interquartile range; NR: not reported; UKSAT: UK Small Aneurysm Trial.

Calculated by us.

Individual patient data provided by the RESCAN collaborators.⁵

Adjusted for aneurysm diameter.

Multivariate-adjusted ORs/HRs were available in four studies,^14,15,17,18 whereas univariate-unadjusted ORs/HRs only in seven studies.^{6–8,11–13,16} Two^8,16 of these seven studies provided significantly lower diabetes prevalence in AAA rupture (i.e. significantly lower AAA-rupture prevalence in diabetes), which was sequentially eliminated in sensitivity analyses to assess their impact on the pooled effect estimate. The primary meta-analysis of the nine studies^{6–8,12,14–18} demonstrated that diabetes was associated with significantly lower prevalence/incidence of AAA rupture (i.e. significantly and negatively associated with AAA rupture) (fixed-effects OR/HR, 0.71; 95% CI, 0.56 to 0.89; p = 0.003; Figure 1). There was no between-study heterogeneity of results (p = 0.40) and accordingly little difference in the pooled result from random-effects modelling (random-effects OR/HR, 0.71; 95% CI, 0.56 to 0.90; p = 0.004.)

Figure 1.

Primary meta-analysis of odds/hazard ratios for abdominal aortic aneurysm (AAA) rupture from nine studies reporting a relative risk of exclusive ruptured (not including non-ruptured symptomatic) AAA. CI: confidence interval; EVAR: endovascular aneurysm repair; IV: inverse variance; UKSAT: UK Small Aneurysm Trial.

To assess the impact of qualitative heterogeneity in study design and patient selection on the pooled effect estimate, we performed several sensitivity analyses. First, we excluded a study by Lo et al.¹⁵ with the greatest weight (30.4% and 7.8% for men and women, respectively). Without it, there was still a statistically significant benefit for diabetes (p for heterogeneity = 0.26; fixed-effect OR/HR, 0.67; 95% CI, 0.50 to 0.90; p for effect = 0.007; random-effects OR/HR, 0.67; 95% CI, 0.47 to 0.94; p for effect = 0.02). Second, we excluded both study by Theivacumar et al.⁸ and that by Sterpetti et al.,¹⁶ which reported the significantly lower unadjusted prevalence of AAA rupture in diabetes. Combining the remaining seven studies generated an attenuated but still statistically significant result favouring diabetes (fixed-effect and random-effects OR/HR, 0.78; 95% CI, 0.61 to 0.99; p for effect = 0.04; p for heterogeneity = 0.86). In general, exclusion of any single study from the analysis did not substantively alter the overall result of our analysis (online Appendix 3). Furthermore, the secondary meta-analysis of all the 11 studies (adding two studies^11,13 in which non-ruptured symptomatic AAA was included in the rupture group) also demonstrated that diabetes was associated with significantly lower prevalence/incidence of AAA rupture (p for heterogeneity = 0.26; fixed-effect OR/HR, 0.77; 95% CI, 0.63 to 0.95; p for effect = 0.01; random-effects OR/HR, 0.77; 95% CI, 0.61 to 0.98; p for effect = 0.03). To assess publication bias in the primary meta-analysis, we generated a funnel plot of the logarithm of effect size (OR/HR) versus the precision (reciprocal of standard error (SE)) for each study (online Appendix 4). There was no evidence of significant publication bias (two-tailed p with continuity correction = 1.00 by the adjusted rank-correlation test;⁹ two-tailed p = 0.60 by the linear regression test¹⁰).

Discussion

The results of our analysis suggest the negative association of diabetes with AAA rupture as well as presence³ and growth,⁴ which was robust in sensitivity analyses. Only two studies were able to demonstrate a statistically significant benefit to diabetes, likely due to systematic under-powering (as reflected in the wide CIs and lack of statistical significance) of studies in the design phase and primarily due to the small number of events (ruptures).

Diabetes is negatively associated with AAA presence.^3,19 In a recent meta-analysis by De Rango et al.¹⁹ of 17 large population prevalence studies, preferring to use data adjusted for local confounders at each study level and combining the adjusted data, there was a significant inverse association between diabetes and AAA (OR, 0.80; 95% CI, 0.70 to 0.90; p = 0.0009). Another recent meta-analysis³ of adjusted estimates from 13 studies also demonstrated that diabetes was significantly associated with lower prevalence of AAA (OR, 0.59; 95% CI, 0.52 to 0.67; p < 0.00001). Furthermore, diabetes is also negatively associated with AAA growth.^4,5 The RESCAN meta-analysis⁵ of 6268 individual patient data from 10 studies demonstrated that diabetics had growth rates that were on average 0.51 ± 0.10 (SE) mm/year slower than those of non-diabetics after adjustment for all demographics, medical history and drug history. A recent meta-analysis⁴ of 19 studies also demonstrated a statistically significant slower growth rates in diabetic patients than in non-diabetic patients (unadjusted standardized mean difference (SMD), −0.32; 95% CI, −0.40 to −0.24; p < 0.00001; adjusted SMD, −0.29; 95% CI, −0.41 to −0.18; p < 0.00001).

Although diabetes is negatively associated with all of AAA presence,³ growth⁴ and rupture (as demonstrated in the present analysis), discrepancy between the association of comorbidity with AAA presence and that of the same comorbidity with AAA growth could be identified. Although CAD is positively associated with AAA presence,^1,2 it is negatively associated with AAA growth.²⁰ A previous meta-analysis by Cornuz et al.¹ of six population-based risk factor studies of AAA showed that a history of myocardial infarction was a major risk factor or risk indicator for screening-detected AAA (OR, 2.30; 95% CI, 1.92 to 2.75). A recent meta-analysis by Li et al.² of 10 epidemiological studies also showed that CAD was a risk factor for AAA (OR, 1.82; 95% CI, 1.65 to 2.00). Another recent meta-analysis²⁰ of 20 studies, however, demonstrated a statistically significant association of CAD with slower AAA growth rates (SMD, −0.06; 95% CI, −0.12 to −0.0027; p = 0.04).

Although PAD is also positively associated with AAA presence,^1,2 it is negatively associated with AAA growth.²¹ The meta-analysis by Cornuz et al.¹ of eight population-based risk factor studies of AAA showed that a history of PAD was a major risk factor or risk indicator for screening-detected AAA (OR, 2.48; 95% CI, 2.10 to 2.92). The meta-analysis by Li et al.² of three epidemiological studies also showed that claudication was a risk factor for AAA (OR, 3.00; 95% CI, 1.74 to 5.19). A recent meta-analysis of 11 studeis,²¹ however, demonstrated a statistically significant association of PAD with lower AAA growth rates (SMD, −0.17; 95% CI, −0.25 to −0.09; p < 0.0001).

Although chronic obstructive pulmonary disease (COPD) is also positively associated with AAA presence,²² it is not associated with AAA growth.²³ A recent meta-analysis²² of seven case–control and four population-based AAA-screening studies demonstrated a statistically significant 1.78-fold (OR, 1.78; 95% CI, 1.38 to 2.30; p < 0.00001) increased prevalence/incidence of COPD in patients with AAA relative to subjects without AAA (i.e. a statistically significant 1.78-fold increased prevalence/incidence of AAA in patients with COPD relative to subjects without COPD). Another recent meta-analysis²³ of 10 studies, however, demonstrated that COPD was not associated with AAA growth rates (SMD, 0.04; 95% CI, −0.07 to 0.15; p = 0.50).

The above-mentioned findings (the same comorbidity is positively associated with AAA presence but not or even negatively associated with AAA growth) suggest that accelerated mechanisms regarding expansion of an existing AAA may be different from those regarding initial formation of an AAA. Regrettably, there has been little knowledge regarding an association of CAD, PAD or COPD with AAA rupture. Whereas, the negative associations of diabetes with all of AAA presence,¹ growth² and rupture (as demonstrated in the present analysis) suggest that decelerated mechanisms regarding expansion and exploding of an existing AAA may be the same as those regarding initial formation of an AAA. Although primary abdominal wall hernia²⁴ and simple renal cyst²⁵ are also positively associated with AAA presence, there has been no knowledge regarding an association of these comorbidities with AAA growth or rupture.

Conclusion

Diabetes is negatively associated with rupture as well as presence and growth of AAA. Although diabetes is a major risk factor of CAD and PAD, both CAD and PAD are positively associated with AAA presence. Further investigations would be required to understand precise mechanisms regarding the negative association of diabetes with AAA.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship and/or publication of this article.

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