Prevalence of systemic sclerosis and atherosclerosis: A systemic review and meta-analysis

Paper Details

Research Paper 01/03/2022
Views (348) Download (32)

Prevalence of systemic sclerosis and atherosclerosis: A systemic review and meta-analysis

Hayaa M Alhuthali, Saeedah H Aljadani, Hind Ali Alzahrani, Saba Beigh
Int. J. Biosci.20( 3), 232-249, March 2022.
Certificate: IJB 2022 [Generate Certificate]


Systemic sclerosis (SSc) and atherosclerosis-related diseases are among the most diagnosed diseases persisting globally. In agreement with earlier publications, we wanted to determine the prevalence of SSc and atherosclerosis. Thorough systematic searches of published studies across various countries in Embase, Medline, Web of Science, Scopus, and PubMed were performed to update our systemic review from January 1990 to December 2020. The author/s, year of publication, sampling size, Mortality, Study design, the prevalence of a particular Sex in that study, mean age, follow up years, limited cutaneous systemic sclerosis (LcSSc) patients, disease duration, body mass index, the prevalence for various symptoms of SSc and NOS of the selected study were explored in this study. The search yielded 1191 articles among which 81 articles were finally encompassed in this study. Among these selected 81 articles, 63 were related to Atherosclerosis among which 29 and 34 articles were prospective and retrospective studies respectively. The studies related to atherosclerosis involved a total of 43, 60,282 participants with their average age of mortality as 54.68 patients per 1000 individuals among the prevalent persons of the disease. However, 18 articles were related to Systemic Sclerosis involving 5821 patients with mean age 53.79 years. This study revealed that the SSc and atherosclerosis symptoms correlate with each other and SSc increases the prevalence of atherosclerosis. SSc patients are at higher risk of having atherosclerotic diseases especially cardiovascular diseases and on the diagnosis of SSc in the patients. As a result, preventative actions for atherosclerotic disorders must be adopted.


Abola MT, Bhatt DL, Duval S, Cacoub PP, Baumgartner I, Keo H, Creager MA, Brennan DM, Steg G, Hirsch AT. 2012. Fate of individuals with ischemic amputations in the REACH Registry: three-year cardiovascular and limb-related outcomes. Atherosclerosis 221(2), 527e35.

Abularrage CJ, Conrad MF, Hackney LA, Paruchuri V, Crawford RS, Kwolek CJ, LaMuraglia GMCambria RP. 2010. Long-term outcomes of diabetic patients undergoing endovascular infrainguinal interventions. Journal Vascular Surgery. 52 (2), 314–322.

Abu-Shakra M. and Lee P. 1995. Mortality in systemic sclerosis: a comparison with the general population. The Journal of rheumatology 22, 2100-2102.

Afifi L, Sanchez IM, Wallacemm. 2018. Diagnosis and management of peristomal pyoderma gangrenosum: A systematic review. Journal of the American Academy of Dermatology 78, 1195-1196.

Agu K, Nzegwu M, Obi E. 2014. Prevalence, morbidity, and mortality patterns of typhoid ileal perforation as seen at the University of Nigeria Teaching Hospital Enugu Nigeria: an 8-year review. World Journal of Surgery 38, 2514-2518.

Akbaricm, Pomposelli FB, Gibbons GW, Campbell DR, Pullingmc, Mydlarz D, LoGerfo FW. 2000. Lower extremity revascularization in diabetes: late observations. Archeol Surgery 135, 452-456.

Ali H, Kiat RNg, Low HL. 2015. A qualitative systematic review of the prevalence of coronary artery disease in systemic sclerosis. International Journal of Rheumatic Diseases 18, 276-286.

Allanore Y, Meune C, Kahan A. 2008. Systemic sclerosis and cardiac dysfunction: evolving concepts and diagnostic methodologies. Current Opinion in Rheumatology 20, 697-702.

Arias-Nuñezmc, Llorca J, Vazquez-Rodriguez TR, Gomez-Acebo I, Miranda-Filloy JA, Martin J, Gonzalez-Juanatey C, Gonzalez-Gay MA. 2008. Systemic sclerosis in northwestern Spain: a 19-year epidemiologic study. Medicine 87, 272-280.

Ashida R, Ihn H, Mimura Y, Jinnin M, Asano Y, Kubo M, Tamaki M. 2009. Clinical and laboratory features of Japanese patients with scleroderma and telangiectasia. Clinical and Experimental Dermatology: Clinical dermatology 34, 781-783.

Aviña-Zubieta JA, Man A, Yurkovich M, Huang K, Sayre EC, Choi HK. 2016. Early cardiovascular disease after the diagnosis of systemic sclerosis. American Journal Medicine 129, 324-31.

Bellando-Randone S, Guiducci S, Matucci-Cerinic M. 2012. Very early diagnosis of systemic sclerosis. Polish Archives of Internal Medicine 122, 18-23.

Brevetti G, Martone VD, Perna S, Cacciatore F, Corrado S, Di Donato A, Iorio AD. 1998. Intermittent claudication and risk of cardiovascular events. Angiology 49(10), 843e8.

Burke AP, Farb A, Malcom G, Virmani R. 2001. Effect of menopause on plaque morphologic characteristics in coronary atheroma esclerosis. American Heart Journal 141, (suppl) S58-62.

Butt SA, Jeppesen JL, Torp Pedersen C, Sam F, Gislason GHJacobsen S, Andersson C. 2019. Cardiovascular manifestations of systemic sclerosis: a Danish Nationwide Cohort Study. Journal American Heart Association 8, e13405.

Caro J, Migliaccio-Walle K, Ishak KJ, Proskorovsky I. 2005. The morbidity and mortality following a diagnosis of peripheral arterial disease: long-term follow up of a large database. BMC Cardiovascular Disorder 5, 14-44.

Cen X, Feng S, Wei S, Yan L, Sun L. 2020. Systemic sclerosis and risk of cardiovascular disease: a PRISMA-compliant systemic review and meta-analysis of cohort studies. Medicine 99, 47. (e23009)

Cheng SW, Ting AC, Lau H, Wong J. 2000. Survival in patients with chronic lower extremity ischemia: a risk factor analysis. Annals Vascular Surgery 14, 158-165.

Chiang CH, Liu CJ, Huang CC, Chan WL, Huang PH, Chen TJ, Chungcm, Lin SJ, Chen JW, Leu HB. 2012. Systemic sclerosis and risk of ischaemic stroke: a nationwide cohort study. Rheumatology 52, 161-5.

Chu S, Chen Y, Liu C, Tseng WC, MW, Hwang CY, Chen CC, Lee DD, Chen TJ, Chang YT, Wang WJ, Liu HN. 2013. Increased risk of acute myocardial infarction in systemic sclerosis: a nationwide population-based study. American Journal Medicine 126, 982-8.

Chu SY, Chen YJ, Liu CJ, Tseng WC, Lin MW, Hwang CY, Chen CC, Lee DD, Chen TJ, Chang YT, Wang WJ. 2013. Increased risk of acute myocardial infarction in systemic sclerosis: a nationwide population-based study. The American journal of medicine 126, 982-988.

Chung L, Denton CP, Distler O, Furst DE, Khanna D, Merkel PA. 2012. Clinical trial design in scleroderma: where are we and where do we go next?” The Scleroderma Clinical Trials Consortium, Clinical Experimental Rheumatology 30, S97-102.

Clarke R, Du H, Kurmi O, Parish S, Yang M, Arnold M, Yu Guo Y, Bian Z, Wang L, Chen Y, Meijer R, Sansome S, mcDonnell J, Collins R, Li L, Chen Z. 2017. Burden of carotid artery atherosclerosis in Chinese adults: implications for future risk of cardiovascular diseases. European Journal of Preventive Cardiology 24(6), 647-656.

Collins TC, Beyth RJ, Nelson DB, Petersen NJ, Suarez-Almazor ME, Bush RL, Hirsch AT, Ashtoncm. 2007. Process of care and outcomes in patients with peripheral arterial disease. Journal General Internal Medicine 22, 942-948.

Criqui MH, Langer RD, Fronek A, Feigelson HS, Klauber MR, mcCann TJ, Browner D. 1992. Mortality over a period of 10 years in patients with peripheral arterial disease. New England Journal Medicine 326, 381e6.

D’Angelo WA, Fries JF, Masi AT, Shulman LE. 1969. Pathologic observations in systemic sclerosis (scleroderma) -A study of fifty-eight autopsy cases and fifty-eight matched controls. American Journal Medicine 46(3), 428-440.

Dawson I, van Bockel JH, Brand R. 1993. Late nonfatal and fatal cardiac events after infrainguinal bypass for femoropopliteal occlusive disease during a thirty-one-year period. Journal Vascular Surgery 18, 249-260.

Denton CP, Khanna D. 2017. Systemic sclerosis. Lancet 390, 1685-1699.

Dick F, Diehm N, Galimanis A, Husmann M, Schmidli J, Baumgartner I. 2007. Surgical or endovascular revascularization in patients with critical limb ischemia: influence of diabetes mellitus on clinical outcome. Journal Vascular Surgery 45, 751-761.

Diehm C, Allenberg JR, Pittrow D, Mahn M, Tepohl G, Haberl RL, Darius H, Burghaus ITrampisch HJ, 2009. Mortality and vascular morbidity in older adults with asymptomatic versus symptomatic peripheral artery disease. Circulation 120(21), 2053e61.

Dimitroulas T, Baniotopoulos P, Pagkopoulou E, Soulaidopoulos S, Nightingale P, Sandoo A, Karagiannis A, Douglas K, Sachinidis A, Garyfallos A, Kitas G. 2020. Subclinical atherosclerosis in systemic sclerosis and rheumatoid arthritis: a comparative matched-cohort study. Rheumatology International 40(12), 1997-2004.

Dormandy JA, Murray GD. 1991. The fate of the claudicantea prospective study of 1969 claudicants. European journal of Vascular Surgery 5(2), 131e3.

Dumoitier N, Lofek S, Mouthon L. 2014. Pathophysiology of systemic sclerosis: state of the art in 2014, La Presse Médicale 43, e267-78, 2014.

Elhai M, Avouac J, Kahan A, Allanore Y. 2015. Systemic sclerosis: recent insights. Joint Bone Spine 82, 148-153.

Elhai M, Meune C, Avouac R, Kahan K, Allanore Y. 2012. Trends in mortality in patients with systemic sclerosis over 40 years: a systematic review and meta-analysis of cohort studies. Rheumatology 51, 1017-1026.

Faglia E, Clerici G, Clerissi J, Gabrielli L, Losa S, Mantero M, Caminiti M, Curci V, Lupattelli T, A Morabito A. 2006. Early and five-year amputation and survival rate of diabetic patients with critical limb ischemia: data of a cohort study of 564 patients. European Journal Vascular Endovascular Surgery 32(5), 484e90.

Feringa HH, van Waning VH, Bax JJ, Elhendy A, Boersma E, Schouten O. 2006. Cardioprotective medication is associated with improved survival in patiets with peripheral arterial disease. Journal American Coll Cardiology 47(6), 1182e7.

Ferri C, Valentini G, Cozzi F, Sebastiani M, Michelassi C, La Montagna G, Bullo A, Cazzato M, Tirri E, Storino F, Giuggioli D. 2002. Systemic sclerosis: demographic, clinical, and serologic features and survival in 1,012 Italian patients. Medicine 81,139-153.

Fiotti N, Altamura N, Cappelli C, Schillan M, Guarnieri G, Giansante C. 2003. Long term prognosis in patients with peripheral arterial disease treated with antiplatelet agents. Eur J Vasc Endovascular Surgery 26(4), 374e80.

Frech T, Walker AE, Barrett-O’Keefe Z, Hopkins PN, Richardson RS, Wray DW, Donato AJ. 2015. Systemic sclerosis induces pronounced peripheral vascular dysfunction characterized by blunted peripheral vasoreactivity and endothelial dysfunction. Clinical rheumatology 34, 905-913.

Frerix M, Stegbauer J, Kreuter A, Weiner SM. 2014. Atherosclerotic plaques occur in absence of intima-media thickening in both systemic sclerosis and systemic lupus erythematosus: a duplexsonography study of carotid and femoral arteries and follow-up for cardiovascular events. Arthritis research & therapy 16(1), 54.

Gabrielli A, Avvedimento EV, Krieg T. 2009. Scleroderma. New England Journal Medicine 360, 1989-2003.

Garg PK, Tian L, Criqui MH, Liu K, Ferrucci L, Guralnik JM, Tan J,mcDermott MM. 2006. Physical activity during daily life and mortality in patients with peripheral arterial disease. Circulation 114, 242-248.

Geirsson ÁJ, Wollheim FA, Åkesson A. 2001. Disease severity of 100 patients with systemic sclerosis over a period of 14 years: using a modified Medsger scale. Annals of the Rheumatic Diseases 60, 1117-1122.

Golledge J, Quigley F, Velu R. 2014. Association of impaired fasting glucose, diabetes and their management with the presentation and outcome of peripheral artery disease: a cohort study. Cardiovascular Diabetol 13, 147.

Goodney PP, Nolan BW, Schanzer A, Eldrup-Jorgensen J, Stanley AC, Stone DH, Likosky DS, Cronenwett JL. 2010. Factors associated with death 1 year after lower extremity bypass in Northern New England. Journal Vascular Surgery 51, 71-78.

Hachulla E, Carpentier P, Gressin V, Diot E, Allanore Y, Sibilia Y, Launay D, Mouthon L, Jego P, Cabane J, De Groote P. 2009. Risk factors for death and the 3-year survival of patients with systemic sclerosis: the French ItinerAIR-Sclerodermie study. Rheumatology 48, 304-308.

Hansson, GK. 2005. Inflammation, atherosclerosis, and coronary artery disease. New England Journal of Medicine 352, 1685-1695.

Heron E, Hernigou A, Chatellier G, Fornes P, Emmerich J, Fiessinger JN. 1999. Intracerebral calcification in systemic sclerosis. Stroke 30, 2183-2185.

Hesselvig J, Kofoed K, Wu J. 2018. Localized scleroderma, systemic sclerosis and cardiovascular risk: a Danish Nationwide Cohort Study. Acta Dermato-Venereologica 98, 361-5.

Hesselvig JH, Ahlehoff O, Dreyer L, Gislason G, Kofoed K. 2016. Cutaneous lupus erythematosus and systemic lupus erythematosus are associated with clinically significant cardiovascular risk: a Danish nationwide cohort study. Lupus 26, 48-53.

Hong YM. 2010. Atherosclerotic cardiovascular disease beginning in childhood, ”Korean Circulation Journal 40, 1-9.

Hooi JD, Kester AD, Stoffers HE, Rinkens PE, Knottnerus JA, van Ree JW. 2004. Asymptomatic peripheral arterial occlusive disease predicted cardiovascular morbidity and mortality in a 7-year follow up study. Journal Clinical Epidemiology 57(3), 294e300.

Hu S, Hou Y, Wang Q, Li M, Xu D, Zeng X. 2018. Prognostic profile of systemic sclerosis: analysis of the clinical EUSTAR cohort in China. Arthritis research and therapy 20, 235.

Jacobsen S, Halberg P, Ullman S. 1998. Mortality and causes of death of 344 Danish patients with systemic sclerosis (scleroderma). British journal of rheumatology 37, 750-755.

Jager A, Kostense PJ, Ruhe HG, Heine RJ, Nijpels G, Dekker JM. 1999. Microalbuminuria and peripheral arterial disease are independent predictors of cardiovascular and all-cause mortality, especially among hypertensive subjects: five-year follow up of the Hoorn Study. Arteriosclerosis Thrombomocyte Vascular Biology 19(3), 617e24.

Jonsson B, Skau T. 2002. Ankle brachial index and mortality in a cohort of questionnaire recorded leg pain on walking. European Journal Vascular Endovascular Surgery 24(5), 405e10.

Jude EB, Oyibo SO, Chalmers N, Boulton AJ. 2001. Peripheral arterial disease in diabetic and nondiabetic patients: a comparison of severity and outcome. Diabetes Care 24(8), 1433e7.

Kalman PG, Johnston KW. 1997. Predictors of long-term patient survival after in situ vein leg bypass. Journal Vascular Surgery 25, 899-904.

Karacagil S, Almgren B, Bowald S. 1995. Comparative analysis of patency, limb salvage and survival in diabetic and non-diabetic patients undergoing infrainguinal bypass surgery. Diabetics Medicine 12, 537-541.

Kardys I, Vliegenthart R, Oudkerk M, Hofman A, Witteman JC. 2007. The female advantage in cardiovascular disease: do vascular beds contribute equally? American Journal Epidemiology 166, 403-12.

Khanna D, Furst DE, Allanore Y, Bae S, Bodukam V, Clements PJ, Cutolo M, Czirjak L, Denton CP, Distler O, Walker UA. 2015. Twenty-two points to consider for clinical trials in systemic sclerosis, based on EULAR standards. Rheumatology 54, 144-151.

Khurma V, Meyer C, Park GS, mcMahon M, Lin J, Singh RR, Khanna D. 2008. “A pilot study of subclinical coronary atherosclerosis in systemic sclerosis: coronary artery calcification in cases and controls. Arthritis Care and Research 59, 591-597.

Kim H, Kim S, Han S, Rane PP, Fox KM, Qian Y, Suh HS. 2019. Prevalence and incidence of atherosclerotic cardiovascular disease and its risk factors in Korea: a nationwide population-based study. BMC Public Health 19, 1112.

Kobayashi M, Shindo S, Kubota K, Kojima A, Ishimoto T, Iyori K. 2000. Causes of late mortality in patients with disabling intermittent claudication. Japanese Circulation Journal 64, 925e7.

Komócsi A, Pintér T, Faludi R, Magyari B, Bozó J, Kumánovics G, Minier T, Radics J, Czirjak L. 2010. Overlap of coronary disease and pulmonary arterial hypertension in systemic sclerosis. Annals of the rheumatic diseases 69, 202-205.

Kurmann RD, Sandhu AS, Crowson CS, Matteson EL, Osborn TG, Warrington KJ, Mankad R, Makol A. 2019. Cardiovascular Risk Factors and Atherosclerotic Cardiovascular Events Among Incident Cases of Systemic Sclerosis: Results from a Population-Based Cohort (1980-2016),” In Mayo Clinic Proceedings 95, 1369-1378.

Lee AJ, Price JF, Russell MJ, Smith FB, van Wijkmc, Fowkes FG. 2004. Improved prediction of fatal myocardial infarction using the ankle brachial index in addition to conventional risk factors: the Edinburgh Artery Study. Circulation 110, 3075e80.

Leibson CL, Ransom JE, Olson W. 2004. Peripheral arterial disease, diabetes, and mortality. Diabetes Care 27, 2843-2849.

Leng GC, Fowkes FG, Lee AJ, Dunbar J, Housley E, Ruckley CV. 1996. Use of ankle brachial pressure index to predict cardiovascular events and death: a cohort study. BMJ 313 (7070), 1440e4.

Li X, Luo Y, Xu Y, Li J, Hu D. 2010. Relationship of ankle brachial index with all-cause mortality and cardiovascular mortality after a 3 year follow up: the China ankle brachial index cohort study. Journal Hum Hypertension 24,111e6.

Luther M, Lepäntalo M. 1997. Femorotibial reconstructions for chronic critical leg ischemia: influence on outcome by diabetes, gender and age. European Journal Vascular Endovasculare Surgery 13, 569-577.

Malmstedt J, Leander K, Wahlberg E. 2008. Outcome after leg bypass surgery for critical limb ischemia is poor in patients with diabetes: a population-based cohort study. Diabetes Care 31, 887-892.

Man A, Zhu Y, Zhang Y, Dubreuil M, Rho YH, Peloquin C, Simms RW, Choi HK. 2013. The risk of cardiovascular disease in systemic sclerosis: a population-based cohort study. Annals of the rheumatic diseases 72, 1188-1193.

McDermottmm, Feinglass J, Slavensky R, Pearce WH. 1994. The ankle brachial index as a predictor of survival in patients with peripheral vascular disease. Journal General Internal Medicine 9(8), 445e9.

McGill HC, mcMahan CA, Herderick EE, Malcom GT, Tracy RE, Strong JP. 2000. Origin of atherosclerosis in childhood and adolescence.The American Journal of Clinical Nutrition 72, 1307-15, 2000.

McKenna M, Wolfson S, Kuller L. 1991. The ratio of ankle and arm arterial pressure as an independent predictor of mortality. Atherosclerosis 87(2e3), 119e28.

McMahon M, Grossman J, FitzGerald J, DahlinLee E, Wallace DJ, Thong BY, Badsha H, Kalunian K, Charles C, Navab, Fogelman AM. 2006. Proinflammatory high‐density lipoprotein as a biomarker for atherosclerosis in patients with systemic lupus erythematosus and rheumatoid arthritis. Arthritis and Rheumatology 54, 2541-2549.

Meune C, Vignaux O, Kahan A, Allanore Y. 2010. “Heart involvement in systemic sclerosis: evolving concept and diagnostic methodologies. Archives of Cardiovascular Diseases 103, 46-52.

Missouris CG, Kalaitzidis RG, Kerry SM. 2004. Predictors of mortality in patients with peripheral vascular disease: a prospective follow-up study. British Journal Diabetes Vascular Disease 4, 196-200.

Miura T, Soga Y, Miyashita Y. 2014. Five-year prognosis after endovascular therapy in claudicant patients with iliofemoral artery disease. Journal Endovascular Therary 21, 381-388.

Moher D, Liberati A, Tetzlaff J, Altman DG. 2009. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Annals of Internal Medicine 151, 264-69.

Mok MY, Chiu SS, Lo Y. 2009. Coronary atherosclerosis using computed tomography coronary angiographyin patients with systemic sclerosis. Scandinavian Journal of Rheumatology 38, 381-385.

Mok MY, Lau CS, Chiu SSH, Tso AWK, Lo Y, Law LSC, Mak KF, Wong WS, Khong PL, Lam KSL. 2011. Systemic sclerosis is an independent risk factor for increased coronary artery calcium deposition. Arthritis and Rheumatism 63, 1387-1395.

Mueller T, Hinterreiter F, Luft C, Poelz W, Haltmayer M, Dieplinger B. 2014. Mortality rates and mortality predictors in patients with symptomatic peripheral artery disease stratified according to age and diabetes. Journal Vascular Surgery 59(5), 1291e9.

Muluk SC, Muluk VS, Kelley ME, Whittle JC, Tierney JA, Webster MW. 2001. Outcome events in patients with claudication: a 15 year study in 2777 patients. Journal Vascular Surgery 33(2), 251e7. discussion 7e8.

Murabito JM, Evans JC, Larsonmg, Nieto K, Levy D, Wilson PW. 2003. The ankle brachial index in the elderly and risk of stroke, coronary disease, and death: the Framingham Study. Archives Internal Medicine 163(16), 1939e42.

Neill SGO, Giles I, Lambrianides A, Manson J, D’Cruz D, Schrieber L, March LM, Latchman DS, Isenberg DA, Rahman A. 2010. Antibodies to apolipoprotein A‐I, high‐density lipoprotein, and C‐reactive protein are associated with disease activity in patients with systemic lupus erythematosus. Arthritis and Rheumatism 62, 845-854.

Ngian GS, Sahhar J, Proudman SM, Stevens W, Wicks IP and Van Doornum S. 2012. Prevalence of coronary heart disease and cardiovascular risk factors in a national cross-sectional cohort study of systemic sclerosis. Annals of the rheumatic diseases 71, 980-1983.

Nihtyanova SI, Tang EC, Coghlan JG, Wells AU, Black,cm, Denton CP. 2010. Improved survival in systemic sclerosis is associated with better ascertainment of internal organ disease: a retrospective cohort study,” An International Journal of Medicine 103, 109-115.

Nikpour M, Stevens WM, Herrick AL, Proudman SM. 2010. Epidemiology of systemic sclerosis,” Best Practice and Research Clinical Rheumatology 24, 857-869.

Nordin A, Jensen-Urstad K, Björnådal L, Pettersson S, Larsson A, Svenungsson E. 2013. Ischemic arterial events and atherosclerosis in patients with systemic sclerosis: a population-based case-control study. Arthritis research and therapy 15(4), R87.

Nussinovitch U, Shoenfeld Y. 2011. Atherosclerosis and macrovascular involvement in systemic sclerosis: Myth or reality, Autoimmunity Reviews 10 (5), 259-266.

O’Hare AM, Katz R, Shlipakmg, Cushman M, Newman AB. 2006. Mortality and cardiovascular risk across the ankle-arm index spectrum: results from the Cardiovascular Health Study. Circulation 113(3), 388e93.

Denton P. 2010. Advances in pathogenesis and treatment of systemic sclerosis. Clinical Medicine 15, s58-63.

Panopoulos S, Tektonidou M, Drosos, AA, Liossis SN, Dimitroulas T, Garyfallos A, Sakkas L, Boumpas D, Voulgari PV, Daoussis D, Thomas K. 2018. Prevalence of comorbidities in systemic sclerosis versus rheumatoid arthritis: a comparative, multicenter, matched-cohort study. Arthritis research and therapy 20,1-6.

Panopoulos ST, Bournia VK, Trakada G, Giavri I, Kostopoulos C, Sfikakis PP. 2013. “Mycophenolate versus cyclophosphamide for a progressive interstitial lung disease associated with systemic sclerosis: a 2-year case-control study,” Lung 191, 483-89.

Pasqualini L, Schillaci G, Pirro M, Vaudo G, Leli C, Colella R. 2012. Prognostic value of low and high ankle-brachial index in hospitalized medical patients. European Journal Internal Medicine 23(3), 240e4.

Pasqualini L, Schillaci G, Vaudo G, Innocente S, Ciuffetti G, Mannarino E. 2001. Predictors of overall and cardiovascular mortality in peripheral arterial disease. American Journal Cardiology 88(9), 1057e60.

Piper MK, Raza K, Nuttall SL, Stevens R, Toescu V, Heaton S, Gardner-Medwin J, Hiller L, Martin U, Townend J, Bacon PA. 2007. Impaired endothelial function in systemic lupus erythematosus. Lupus 16, 84-88

Resnick HE, Lindsay RS, mcDermottmm, Devereux RB, Jones KL, Fabsitz RR. 2004. Relationship of high and low ankle brachial index to all cause and cardiovascular disease mortality: the Strong Heart Study. Circulation 109(6), 733e9.

Rho YH, Chung CP, Oeser A, Solus J, Asanuma Y, Sokka T, Pincus T, Raggi P, Gebretsadik T, Shintani, Steincm A. 2009. Inflammatory mediators and premature coronary atherosclerosis in rheumatoid arthritis. Arthritis Care and Research 61, 1580-1585.

Rodríguez-Saldaña J, Rodriguez-Flores M, Cantú-Brito C, Aguirre-Garcia J. 2014. A Pathological Study of the Epidemiology of Atherosclerosis in Mexico City. Cardiology Research and Practice 264205.

Sangiorgi G, Roversi S, Biondi Zoccai G. 2013. Sex-related differences in carotid plaque features and inflammation. Journal Vascular Surgery 57, 338-44.

Sciarra I, Vasile M, Carboni A, Stefanantoni A, Iannace N, Angelelli C, Scarno AG, Valesini G, Riccieri V. 2020. Subclinical atherosclerosis in systemic sclerosis: Different risk profiles among patients according to clinical manifestations. International Journal of Rheumatic Diseases 24(4), 502-509.

Scussel-Lonzetti L, Joyal F, Raynauld JP, Roussin A, Rich E, Goulet JR, Raymond Y, Senecal JL. 2002. Predicting mortality in systemic sclerosis: analysis of a cohort of 309 French Canadian patients with emphasis on features at diagnosis as predictive factors for survival. Medicine-Baltimore 81, 154-167.

Sikkink CJ, van Asten WN, van’t Hof MA, van Langen H, van der Vliet JA. 1997. Decreased ankle/brachial indices in relation to morbidity and mortality in patients with peripheral arterial disease. Vasc Med (London, England) 2(3), 169e73.

Simeón CP, Armadans L, Fonollosa V, Solans R, Selva A, Villar M, Lima J, Vaque J, Vilardell M. 2003. Mortality and prognostic factors in Spanish patients with systemic sclerosis. Rheumatology 42, 71-75.

Solomon DH, Karlson EW, Rimm EB, Cannuscio CC, Mandl LA, Manson JE, Stampfer MJ, Curhan GC. 2003. Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation 107, 1303-1307.

Song P, Fang Z, Wang H, Cai Y, Rahimi K, Zhu Y, Fowkes FGR, Fowkes FJI, Rudan I. 2020. Global and regional prevalence, burden, and risk factors for carotid atherosclerosis: a systematic review, meta-analysis, and modelling study. Lancet Global Health 8, e721-29.

Song P, Xia W, Zhu Y. 2018. Prevalence of carotid atherosclerosis and carotid plaque in Chinese adults: a systematic review and metaregression analysis. Atherosclerosis 276, 67-73.

Sprengers RW, Janssen KJ, Moll FL, Verhaarmc, van der Graaf Y. 2009. Prediction rule for cardiovascular events and mortality in peripheral arterial disease patients: data from the prospective second manifestations of ARTerial disease (SMART) cohort study. Journal Vascular Surgery 50(6), 1369e76.

Steg PG, Bhatt DL, Wilson PW, D’Agostino Sr R, Ohman EM, Rother J. 2007. One-year cardiovascular event rates in outpatients with atherothrombosis. Jama 297(11), 1197e206.

Suominen V, Uurto I, Saarinen J, Venermo M, Salenius J. 2010. PAD as a risk factor for mortality among patients with elevated ABIea clinical study. Europen Journal Vascular Endovascular Surgery 39(3), 316e22.

Surinach JM, Alvarez LR, Coll R, Carmona JA, Sanclemente C, Aguilar E. 2009. Differences in cardiovascular mortality in smokers, past-smokers and non-smokers: findings from the FRENA registry. European Journal Internal Medicine 20(5), 522e6.

Sutton-Tyrrell K, Venkitachalam L, Kanaya AM, Boudreau R, Harris T, Thompson T. 2008. Relationship of ankle blood pressures to cardiovascular events in older adults. Stroke 39(3), 863e9.

Suzuki K, Iida O, Yamauchi Y, Nakano M, Soga Y, Kawasaki D, Tazaki J, Yamaoka T, Suematsu N, Shintani Y, Miyashita Y, Inoue N, Meguro T, 2013. Impact of diabetes mellitus on critical limb ischemia with below the knee disease: Japan below-the knee artery treatment subanalysis. Angiology 71(5), 444-451.

Tarek el G, Yasser AE, Gheita T. 2006. Coronary angiographic findings in asymptomatic systemic sclerosis. Clinical Rheumatol 25, 487-490.

Taute BM, Thommes S, Taute R, Rapmund I, Lindner K, Podhaisky H. 2009. Long-term outcome of patients with mild intermittent claudication under secondary prevention. Vasa 38(4), 346e55.

Tyndall J, Bannert B, Vonk M, Airò P, Cozzi F, Carreira PE, Bancel DF, Allanore Y, Müller-Ladner UO, Distler O, Iannone F. 2010. Causes and risk factors for death in systemic sclerosis: a study from the EULAR Scleroderma Trials and Research (EUSTAR) database,” Annals of the rheumatic diseases 69,1809-1815.

Ungprasert P, Charoenpong P, Ratanasrimetha P. 2014. Risk of coronary artery disease in patients with systemic sclerosis: a systematic review and meta-analysis. Clinical Rheumatology 33, 1099-104.

Vaartjes I, de Borst GJ, Reitsma JB, de Bruin A, Moll FL, Grobbee DE. 2009. Long-term survival after initial hospital admission for peripheral arterial disease in the lower extremities. BMC Cardiovascular Disorder 9, 43.

Vickrey BG, Rector TS, Wickstrom SL, Guzy PM, Sloss EM, Gorelick PB, Garber S, mcCaffrey DF, Dake MD, Levin RA. 2002. Occurrence of secondary ischemic events among persons with atherosclerotic vascular disease. Stroke 33(4), 901-6.

Vrsalović M, Vucur K. 2016. Diabetes and critical limb ischemia: the deadly duo in patients with symptomatic peripheral artery disease. Acta Clinica Croatica 55, 240-246.

Wölfle KD, Bruijnen H, Loeprecht H, Rümenapf GSchweiger H, Grabitz K, Sandmann W, Lauterjung L, Largiader J, Erasmi H, Kasprzak PM, Raithel D, Allenberg JR, Lauber A, Berlakovich GM, Kretschmer G, Hepp W, Becker HM, Schulz A. 2003. Graft patency and clinical outcome of femorodistal arterial reconstruction in diabetic and nondiabetic patients: results of a multicenter comparative analysis. European Journal Vascular Endovascular Surgery 25, 229-234.

Ying D, Gianfrancesco MA, Trupin L, Yazdany J, Greidinger EL, Schmajuk G. 2020. Increased risk of ischemic stroke in systemic sclerosis: a national cohort study of US veterans. Journal Rheumatology 47, 82-8.

Youssef P, Brama T, Englert H, Bertouch J. 1995. Limited scleroderma is associated with increased prevalence of macrovascular disease. The Journal of Rheumatology 22, 469-472.