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Genetic and Environmental Effects on the Abdominal Aortic Diameter Development

Abstract

Background:

Configuration of the abdominal aorta is related to healthy aging and a variety of disorders.

Objectives:

We aimed to assess heritable and environmental effects on the abdominal aortic diameter.

Methods:

114 adult (69 monozygotic, 45 same-sex dizygotic) twin pairs (mean age 43.6 ± 16.3 years) underwent abdominal ultrasound with Esaote MyLab 70X ultrasound machine to visualize the abdominal aorta below the level of the origin of the renal arteries and 1-3 cm above the bifurcation.

Results:

Age- and sex-adjusted heritability of the abdominal aortic diameter below the level of the origin of the renal arteries was 40% [95% confidence interval (CI), 14 to 67%] and 55% above the aortic bifurcation (95% CI, 45 to 70%). None of the aortic diameters showed common environmental effects, but unshared environmental effects were responsible for 60% and 45% of the traits, respectively.

Conclusions:

Our analysis documents the moderate heritability and its segment-specific difference of the abdominal aortic diameter. The moderate part of variance was explained by unshared environmental components, emphasizing the importance of lifestyle factors in primary prevention. Further studies in this field may guide future gene-mapping efforts and investigate specific lifestyle factors to prevent abdominal aortic dilatation and its complications.

Keywords:
Aorta, Abdominal / genetics; Heredity; Atherosclerosis; Risk Factors

Resumo

Fundamento:

A configuração da aorta abdominal relaciona-se com o envelhecimento saudável e uma série de distúrbios.

Objetivos:

Avaliar efeitos herdáveis e ambientais no diâmetro da aorta abdominal.

Métodos:

114 pares de gêmeos adultos (69 monozigóticos e 45 dizigóticos do mesmo sexo), com idade média de 43,6 ± 16,3 anos, foram submetidos a ultrassonografia abdominal com o aparelho Esaote MyLab 70X para visualização da aorta abdominal abaixo da origem das artérias renais e 1-3 cm acima da bifurcação aórtica.

Resultados:

A herdabilidade ajustada para idade e sexo do diâmetro da aorta abdominal abaixo da origem das artérias renais foi 40% [intervalo de confiança (IC) 95%, 14 – 67%] e acima da bifurcação, 55% (IC 95%, 45 – 70%). Nenhum dos diâmetros aórticos apresentou efeitos ambientais comuns, mas os efeitos ambientais não compartilhados foram responsáveis por 60% e 45% dos traços, respectivamente.

Conclusões:

Nossa análise mostrou herdabilidade moderada e diferença do diâmetro da aorta abdominal com especificidade de segmento. A parte moderada da variância foi explicada pelo componente ambiental não compartilhado, enfatizando a importância do estilo de vida na prevenção primária. Estudos adicionais nesse campo poderão guiar futuros esforços de mapeamento genético e investigar fatores específicos de estilo de vida para prevenir dilatação da aorta abdominal e suas complicações.

Palavras-chave:
Aorta Abdominal / genética; Hereditariedade; Aterosclerose; Fatores de Risco

Introduction

The size of the aorta decreases with distance from the aortic valve in a tapering fashion, the normal diameter of the descending aorta being defined as < 1.6 cm/m2, and that of the abdominal aorta, less than 3.0 cm.11 Erbel R, Alfonso F, Boileau C, Dirsch O, Eber B, Haverich A, et al; Task Force on Aortic Dissection, European Society of Cardiology. Diagnosis and management of aortic dissection. Eur Heart J. 2001;22(18):1642-81.,22 Erbel R, Eggebrecht H. Aortic dimensions and the risk of dissection. Heart. 2006;92(1):137-42. Configuration of the abdominal aorta can be related to healthy ageing, exercise, and/or a variety of disorders, such as hypertension, aneurysm, dissection or rupture.11 Erbel R, Alfonso F, Boileau C, Dirsch O, Eber B, Haverich A, et al; Task Force on Aortic Dissection, European Society of Cardiology. Diagnosis and management of aortic dissection. Eur Heart J. 2001;22(18):1642-81.,22 Erbel R, Eggebrecht H. Aortic dimensions and the risk of dissection. Heart. 2006;92(1):137-42. The increase of the aortic size is continous during life, the normal expansion rate is about 1-;2 mm/year and involves all segments.33 Roman MJ, Devereux RB, Kramer-Fox R, O'Loughlin J. Two-dimensional echocardiographic aortic root dimensions in normal children and adults. Am J Cardiol. 1989;64(8):507-12. The ageing of the aorta is accompanied by a loss of compliance and an increase of wall stiffness caused by structural changes, including an increase in the collagen content, formation of intimal atherosclerosis with calcium deposits, smooth muscle activation, matrix degradation, cystic media necrosis, upregulation of proteolytic pathways and oxidative stress.11 Erbel R, Alfonso F, Boileau C, Dirsch O, Eber B, Haverich A, et al; Task Force on Aortic Dissection, European Society of Cardiology. Diagnosis and management of aortic dissection. Eur Heart J. 2001;22(18):1642-81.,22 Erbel R, Eggebrecht H. Aortic dimensions and the risk of dissection. Heart. 2006;92(1):137-42.,44 Nordon IM, Hinchliffe RJ, Loftus IM, Thompson MM. Pathophysiology and epidemiology of abdominal aortic aneurysms. Nat Rev Cardiol. 2011;8(2):92-102. It is also known that certain genetic diseases, such as abdominal aortic aneurysm formation, are associated with aortic geometry.44 Nordon IM, Hinchliffe RJ, Loftus IM, Thompson MM. Pathophysiology and epidemiology of abdominal aortic aneurysms. Nat Rev Cardiol. 2011;8(2):92-102.,55 Kuivaniemi H, Shibamura H, Arthur C, Berguer R, Cole CW, Juvonen T, et al. Familial abdominal aortic aneurysms: collection of 233 multiplex families. J Vasc Surg. 2003;37(2):340-5. The relationship between the increasing aortic size and the risk of spontaneous rupture or dissection has been well documented.66 Rider OJ, Petersen SE, Francis JM, Ali MK, Hudsmith LE, Robinson MR, et al. Ventricular hypertrophy and cavity dilatation in relation to body mass index in women with uncomplicated obesity. Heart. 2011;97(3):203-8. Although familiar accumulation of these abdominal aortic aneurysms has been reported by several studies, the extent of genetic determination over the abdominal aortic geometry is still scarce. Although the prevalence of the diseases related to the abdominal aortic diameter (e.g., atherosclerosis, aortic aneurysm) has increased in the past decades due to lifestyle changes and various risk factors, no study has investigated whether the variation of the abdominal aortic diameter is due to genetic or environmental differences. If heritable effects are important, studies are necessary to identify specific genetic markers that determine abdominal aortic size. On contrary, if environment plays a greater role, an emphasis should be put on lifestyle interventions in order to influence the development of the abdominal-aortic-diameter-related diseases. Accordingly, the objective of this study was to assess the extent of genetic and environmental effects on the abdominal aortic diameter.

Methods

Participants and study design

From the Hungarian Twin Registry, 114 healthy Caucasian twin pairs [69 monozygotic (MZ), 45 same-sex dizygotic (DZ) twin pairs] above 18 years of age (mean age 43.6 ± 16.3 years) were selected and recruited for an abdominal ultrasound in the Department of Radiology and Oncotherapy of the Semmelweis University in 2009 and 201077 Littvay L, Metneki J, Tarnoki AD, Tarnoki DL. The Hungarian Twin Registry. Twin Res Hum Genet. 2013;16(1):185-9.. We excluded opposite-sex DZ twin pairs to avoid bias of the heritability estimates in the presence of gender-specific or X-chromosome effects. Pregnant subjects were excluded from the study. Patients with atherosclerotic disease or other causes of aortic stenosis were not excluded from the analysis. Instead of genotyping for zygosity classification, we used a multiple­choice self­reported seven-part questionnaire.88 Heath AC, Nyholt DR, Neuman R, Madden PA, Bucholz KK, Todd RD, et al. Zygosity diagnosis in the absence of genotypic data: an approach using latent class analysis. Twin Res. 2003;6(1):22-6. Risk factors, history of cardiovascular diseases and smoking habits were recorded on a questionnaire. All participants gave informed consent. This study was approved by the Ethical Committee of the Semmelweis University and was conducted in full compliance with regulations of the Declaration of Helsinki.

Limited abdominal ultrasonography

A limited abdominal ultrasonography was performed using B-mode and Doppler ultrasound in order to visualize the abdominal aorta below the level of the origin of the renal arteries and 1-3 cm above the bifurcation, equipped with a curved array transducer (1-;8 MHz, CA431, Esaote MyLab 70X Vision, Esaote, Genova, Italy). Standardized digital images of the aorta were recorded in supine position, and transversal plane images were applied for axial views. The gray-scale amplification gain, the time-gain compensation curve, and focus number were adjusted to acquire the best images of the aorta. The examinations were performed by the same radiologist. Trackball was used in order to set the best image of the aorta in systole, and the largest aortic diameter was measured in the transverse plane by electronic calipers at the time of scanning.

Statistical analysis

The SPSS Statistics 17 (SPSS Inc., Chicago, IL, USA) was used for descriptive analysis and comparison of MZ and DZ subsamples by independent samples t-test. Pearson correlations were calculated between aortic diameters and continuous variables. Aortic diameter parameters showed a normal distribution.

A descriptive estimate of the genetic influence in MZ and DZ pairs was calculated using the within-pair co-twin correlations corrected for the twins' age and gender. In twin analysis, substantially higher MZ co-twin correlation (compared to DZ correlations) suggests heritability, while similar co-twin correlations imply that shared environmental components drive the variance more strongly. Higher DZ similarities compared to MZ twins suggest that unshared (unique) environmental factors are responsible for the trait. Based on similarities between MZ and DZ twins, structural equation modeling (A-C-E model) was carried out with Mplus Version 6.1 (Muthén & Muthén, Los Angeles, CA, USA)99 Muthen LK, Muthen BO. Mplus: statistical analysis with latent variables. User's guide. 6th ed. Los Angeles: Muthen & Muthen; 1998-2010. in order to decompose the variance into additive genetic effects (A), and common (or shared) environmental (C) and unique (or unshared) environmental (E) effects.1010 Neale MC, Maes HH, Cardon LR. Methodology for genetic studies of twins and families. Dordrecht (The Netherlands): Kluwer Academic Publishers BV; 1992. Empirical confidence intervals were calculated with a Bollen-Stine Bootstrap.1111 Bollen KA, Stine RA. Bootstrapping goodness-of-fit measures in structural equation models. Sociological Methods Research. 1992;21(2):205-29. All inferential statistics was estimated using full information maximum likelihood. Nested models were compared using likelihood-ratio and χ2 tests, and Akaike Information Criteria model selection was performed according to the principle of parsimony. P value < 0.05 was considered significant.

Results

Descriptive analysis

There were no significant differences between MZ and DZ twins in risk factors, history of diseases and clinical characteristics. Thirty-nine percent of the study sample was comprised of males. The MZ and DZ groups were formed by 32 males and 106 females, and 30 males and 60 females, respectively. Hypertension, hypercholesterolemia and diabetes were present in 32%, 22% and 6%. Active individuals represented 17% of the sample, and ex-smokers, 14%. The mean aortic diameters below the origin of the renal arteries and above the level of the aortic bifurcation were 1.5 ± 0.2 cm and 1.4 ±0.2 cm, respectively. There was no significant difference between MZ and DZ twins regarding the aortic diameter below the level of the origin of the renal arteries, but DZ twins had significantly smaller aortic diameter above the bifurcation (1.4 ± 0.2 vs. 1.3 ± 0.2 cm, p < 0.005). There was no abdominal aortic aneurysm among the subjects. There was no significant correlation between the aortic diameters and body mass index, weekly alcohol intake, cigarette smoking, diabetes and hypercholesterolemia. Hypertensive subjects had significantly larger aortic diameter below the level of the renal artery origin (1.6 ± 0.2 vs. 1.5 ± 0.2, p < 0.05), but there was no similar relationship above the level of the aortic bifurcation.

Univariate analysis

Monozygotic co-twin correlations were higher than DZ ones, indicating that age- and sex-adjusted heritability of the abdominal aortic diameter below the level of the origin of the renal arteries was 40% [95% confidence interval (CI), 14 to 67%], and that above the aortic bifurcation was 55% (95% CI, 45 to 70%) (Table 1). None of the aortic diameters showed common environmental effects, but unshared environmental effects were responsible for 60% and 45% of the traits, respectively.

Table 1
Parameter estimates for additive hereditary (A), common environmental (C) and unique environmental (E) influences on aortic diameter by structural equation modeling

Discussion

To our knowledge, our results demonstrate first the genetic effects on the abdominal aortic diameters in a healthy sample. This heritability was moderate, and a similarly moderate extent of variance was explained by unshared environmental components.

Only Cecelja et al1212 Cecelja M, Jiang B, McNeill K, Kato B, Ritter J, Spector T, et al. Increased wave reflection rather than central arterial stiffness is the main determinant of raised pulse pressure in women and relates to mismatch in arterial dimensions: a twin study. J Am Coll Cardiol. 2009;54(8):695-703. have investigated the aortic dimensions in twins so far, and have reported that the highly heritable augmentation pressure in women is associated with the ratio of distal to proximal arterial diameters, but no heritability assessment of aortic diameters has been performed. The Strong Heart Study1313 Bella JN, MacCluer JW, Roman MJ, Almasy L, North KE, Welty TK, et al. Genetic influences on aortic root size in American Indians: the Strong Heart Study. Arterioscler Thromb Vasc Biol. 2002;22(6):1008-11. has investigated the heritability of echocardiographically derived aortic root diameters in the American Indian participants, and has reported an additive genetic contribution of 51%, which is comparable to our findings. However, the diameter of the abdominal aorta has never been assessed. Our findings underscore that there is a moderate role of genetic effects in the aortic diameter development, which may predispose to aortic dilatation. These findings indicate that, in half, genetic effects drive the ageing of the abdominal aorta, but in the other half of the variance it can be influenced by the lifestyle. This is a very important point because the loss of compliance, atherosclerosis and increase of aortic stiffness, which are related to aortic geometry and in which age-related increases in collagen synthesis potentially lead to dilatation, could be prevented with a healthy lifestyle.1414 Schlatmann TJ, Becker AE. Histologic changes in the normal aging aorta: implications for dissecting aortic aneurysm. Am J Cardiol. 1977;39(1):13-20. In addition, it has never been demonstrated that there is a segment-specific difference in the heritability: the aortic diameter above the level of bifurcation is more heritable than that below the level of the origin of renal arteries. We might speculate whether this finding could explain why atherosclerosis is more common before the bifurcation. It is known that hemodynamic disturbances, such as turbulent flow or low shear stress, associated with branching or high curvature, contribute to some of the localization of atherosclerosis.1515 Norman PE, Powell JT. Site specificity of aneurysmal disease. Circulation. 2010;121(4):560-8.

16 VanderLaan PA, Reardon CA, Getz GS. Site specificity of atherosclerosis: site-selective responses to atherosclerotic modulators. Arterioscler Thromb Vasc Biol. 2004;24(1):12-22.

17 Boussel L, Rayz V, McCulloch C, Martin A, Acevedo-Bolton G, Lawton M, et al. Aneurysm growth occurs at region of low wall shear stress: patient-specific correlation of hemodynamics and growth in a longitudinal study. Stroke. 2008;39(11):2997-3002.
-1818 Lee K, Sung J, Lee SC, Park SW, Kim YS, Lee JY, et al. Segment-specific carotid intima-media thickness and cardiovascular risk factors in Koreans: the Healthy Twin Study. Eur J Prev Cardiol. 2012;19(5):1161-72. Segment-specific differences in heritability have been shown in case of carotid arteries indicating that inherited effects made a heterogeneous contribution to intima-media thickness by segment.1818 Lee K, Sung J, Lee SC, Park SW, Kim YS, Lee JY, et al. Segment-specific carotid intima-media thickness and cardiovascular risk factors in Koreans: the Healthy Twin Study. Eur J Prev Cardiol. 2012;19(5):1161-72.

In addition to the genetic mechanism, we reported that unique environmental factors, such as lifestyle, play a moderate role in determining aortic diameters. These risk and lifestyle factors have been extensively studied (smoking, hypertension, diabetes, obesity, etc.). According to some researchers, the programming of this mechanism begins already in foetal life and depends on mother's exposure to risk factors as well as via epigenetic modulation.1919 Alkemade FE, Gittenberger-de Groot AC, Schiel AE, VanMunsteren JC, Hogers B, van Vliet LS, et al. Intrauterine exposure of maternal atherosclerotic risk factors increases the susceptibility to atherosclerosis in adult life. Arterioscler Thromb Vasc Biol. 2007;27(10):2228-35. Identification of risk factors, which have a 45-60% influence, rather proximally under the level of origin of renal arteries, would make the diagnosis more effective allowing possibility of detection of diseases in early stages and their prevention with lifestyle habit changing. The disease is believed to be connected with the lifestyle associated with high levels of oxidative stress and highly processed food.2020 Mikolajczyk-Stecyna J, Korcz A, Gabriel M, Pawlaczyk K, Oszkinis G, Slomski R. Risk factors in abdominal aortic aneurysm and in Polish population aortoiliac occlusive disease and differences between them. Sci Rep. 2013;3:3528. Erratum in: Sci Rep. 2014;4:3771.

A long-term goal of the present study is to detect and map new polymorphic genes that influence variation in abdominal aortic size and thereby contribute to the development of asymptomatic subclinical aortic dilatation and dissection or rupture. In recent years, several (relatively few) genes related to abdominal aortic aneurysm formation have been reported. Susceptibility genes, rather than causal gene mutations, were suspected in aneurysms, particularly abdominal aortic aneurysms, which are genetically complex.2121 Kuivaneimi H, Platsoucas CD, Tilson MD 3rd. Aortic aneurysms: an immune disease with a strong genetic component. Circulation. 2008;117(2):242-52. A genome­wide study with infrarenal aorta diameter ≥ 30 mm or ruptured abdominal aortic aneurysm demonstrated that LDLR rs6511720 is associated with abdominal aortic aneurysm.2222 Bradley DT, Hughes AE, Badger SA, Jones GT, Harrison SC, Wright BJ, et al. A variant in LDLR is associated with abdominal aortic aneurysm. Circ Cardiovasc Genet. 2013;6(5):498-504. A recent report showed that rs10757278 and rs1333049 on chromosome 9p21.3 are significantly associated with increased risk of abdominal aortic aneurysm in the Chinese population.2323 Wei Y, Xiong J, Zuo S, Chen F, Chen D, Wu T, et al. Association of polymorphisms on chromosome 9p21.3 region with increased susceptibility of abdominal aortic aneurysm in a Chinese Han population. J Vasc Surg. 2014;59(4):879-85. However, genetic studies in healthy individuals are necessary and other population-based studies on genetic factors influencing abdominal aortic size need to be performed to identify specific genetic markers that determine abdominal aortic size. This information may lead to improvement in diagnostic and therapeutic strategies in the prevention of abdominal aortic dilatation and its complications.

Limitations of our study must be noted. No ECG gating was applied in our study, but systolic dilatation of the aorta was well identifiable in all cases. Second, aortic size measurements performed provide only a single static evaluation at one point in time. Older patients might demonstrate a more significant influence of environmental factors on aortic size, and alter the analysis of this study. Also, the relationship of genetic and environmental influence on aortic growth over time would be significantly more important than the influence over size at one point in time. In addition, ultrasonography has a weakness of inter-observer variability and limited visibility of aorta due to bowel gases and obesity, but in this study all participants were evaluated by the same radiologist and the aorta was well visible in all cases. Ultrasound was found to be relatively equal in the imaging of abdominal aorta compared to computed tomography.2424 Sprouse LR 2nd, Meier GH 3rd, Parent FN, DeMasi RJ, Glickman MH, Barber GA. Is ultrasound more accurate than axial computed tomography for determination of maximal abdominal aortic aneurysm diameter? Eur J Vasc Endovasc Surg. 2004;28(1):28-35. Additional limitation includes the relatively small number of participating DZ twins compared to usual twin studies, which may lead to statistical errors in the A-C-E model analysis by increasing the E variance.

Conclusions

In summary, moderate heritability and its segment-specific difference of abdominal aortic diameter were shown in a healthy sample, which will guide future gene-mapping efforts. Unshared environmental factors were responsible for the other, moderate portion of the variance.

  • Sources of Funding
    There were no external funding sources for this study.
  • Study Association
    This study is not associated with any thesis or dissertation work.

References

  • 1
    Erbel R, Alfonso F, Boileau C, Dirsch O, Eber B, Haverich A, et al; Task Force on Aortic Dissection, European Society of Cardiology. Diagnosis and management of aortic dissection. Eur Heart J. 2001;22(18):1642-81.
  • 2
    Erbel R, Eggebrecht H. Aortic dimensions and the risk of dissection. Heart. 2006;92(1):137-42.
  • 3
    Roman MJ, Devereux RB, Kramer-Fox R, O'Loughlin J. Two-dimensional echocardiographic aortic root dimensions in normal children and adults. Am J Cardiol. 1989;64(8):507-12.
  • 4
    Nordon IM, Hinchliffe RJ, Loftus IM, Thompson MM. Pathophysiology and epidemiology of abdominal aortic aneurysms. Nat Rev Cardiol. 2011;8(2):92-102.
  • 5
    Kuivaniemi H, Shibamura H, Arthur C, Berguer R, Cole CW, Juvonen T, et al. Familial abdominal aortic aneurysms: collection of 233 multiplex families. J Vasc Surg. 2003;37(2):340-5.
  • 6
    Rider OJ, Petersen SE, Francis JM, Ali MK, Hudsmith LE, Robinson MR, et al. Ventricular hypertrophy and cavity dilatation in relation to body mass index in women with uncomplicated obesity. Heart. 2011;97(3):203-8.
  • 7
    Littvay L, Metneki J, Tarnoki AD, Tarnoki DL. The Hungarian Twin Registry. Twin Res Hum Genet. 2013;16(1):185-9.
  • 8
    Heath AC, Nyholt DR, Neuman R, Madden PA, Bucholz KK, Todd RD, et al. Zygosity diagnosis in the absence of genotypic data: an approach using latent class analysis. Twin Res. 2003;6(1):22-6.
  • 9
    Muthen LK, Muthen BO. Mplus: statistical analysis with latent variables. User's guide. 6th ed. Los Angeles: Muthen & Muthen; 1998-2010.
  • 10
    Neale MC, Maes HH, Cardon LR. Methodology for genetic studies of twins and families. Dordrecht (The Netherlands): Kluwer Academic Publishers BV; 1992.
  • 11
    Bollen KA, Stine RA. Bootstrapping goodness-of-fit measures in structural equation models. Sociological Methods Research. 1992;21(2):205-29.
  • 12
    Cecelja M, Jiang B, McNeill K, Kato B, Ritter J, Spector T, et al. Increased wave reflection rather than central arterial stiffness is the main determinant of raised pulse pressure in women and relates to mismatch in arterial dimensions: a twin study. J Am Coll Cardiol. 2009;54(8):695-703.
  • 13
    Bella JN, MacCluer JW, Roman MJ, Almasy L, North KE, Welty TK, et al. Genetic influences on aortic root size in American Indians: the Strong Heart Study. Arterioscler Thromb Vasc Biol. 2002;22(6):1008-11.
  • 14
    Schlatmann TJ, Becker AE. Histologic changes in the normal aging aorta: implications for dissecting aortic aneurysm. Am J Cardiol. 1977;39(1):13-20.
  • 15
    Norman PE, Powell JT. Site specificity of aneurysmal disease. Circulation. 2010;121(4):560-8.
  • 16
    VanderLaan PA, Reardon CA, Getz GS. Site specificity of atherosclerosis: site-selective responses to atherosclerotic modulators. Arterioscler Thromb Vasc Biol. 2004;24(1):12-22.
  • 17
    Boussel L, Rayz V, McCulloch C, Martin A, Acevedo-Bolton G, Lawton M, et al. Aneurysm growth occurs at region of low wall shear stress: patient-specific correlation of hemodynamics and growth in a longitudinal study. Stroke. 2008;39(11):2997-3002.
  • 18
    Lee K, Sung J, Lee SC, Park SW, Kim YS, Lee JY, et al. Segment-specific carotid intima-media thickness and cardiovascular risk factors in Koreans: the Healthy Twin Study. Eur J Prev Cardiol. 2012;19(5):1161-72.
  • 19
    Alkemade FE, Gittenberger-de Groot AC, Schiel AE, VanMunsteren JC, Hogers B, van Vliet LS, et al. Intrauterine exposure of maternal atherosclerotic risk factors increases the susceptibility to atherosclerosis in adult life. Arterioscler Thromb Vasc Biol. 2007;27(10):2228-35.
  • 20
    Mikolajczyk-Stecyna J, Korcz A, Gabriel M, Pawlaczyk K, Oszkinis G, Slomski R. Risk factors in abdominal aortic aneurysm and in Polish population aortoiliac occlusive disease and differences between them. Sci Rep. 2013;3:3528. Erratum in: Sci Rep. 2014;4:3771.
  • 21
    Kuivaneimi H, Platsoucas CD, Tilson MD 3rd. Aortic aneurysms: an immune disease with a strong genetic component. Circulation. 2008;117(2):242-52.
  • 22
    Bradley DT, Hughes AE, Badger SA, Jones GT, Harrison SC, Wright BJ, et al. A variant in LDLR is associated with abdominal aortic aneurysm. Circ Cardiovasc Genet. 2013;6(5):498-504.
  • 23
    Wei Y, Xiong J, Zuo S, Chen F, Chen D, Wu T, et al. Association of polymorphisms on chromosome 9p21.3 region with increased susceptibility of abdominal aortic aneurysm in a Chinese Han population. J Vasc Surg. 2014;59(4):879-85.
  • 24
    Sprouse LR 2nd, Meier GH 3rd, Parent FN, DeMasi RJ, Glickman MH, Barber GA. Is ultrasound more accurate than axial computed tomography for determination of maximal abdominal aortic aneurysm diameter? Eur J Vasc Endovasc Surg. 2004;28(1):28-35.

Publication Dates

  • Publication in this collection
    10 Nov 2015
  • Date of issue
    Jan 2016

History

  • Received
    22 Feb 2015
  • Accepted
    02 Sept 2015
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