Advertisement
Adult: Aorta| Volume 165, ISSUE 4, P1303-1315.e9, April 2023

Aortic allograft infection risk

      Abstract

      Objective

      Intrinsic risk of infection of cryopreserved allograft aortic root replacements remains poorly understood despite their long history of use. The objective of this study was to determine this intrinsic risk of allograft infection and its risk factors when allografts are implanted for both nonendocarditis indications and infective endocarditis.

      Methods

      From January 1987 to January 2017, 2042 patients received 2110 allograft aortic valves at a quaternary medical center, 1124 (53%) for nonendocarditis indications and 986 (47%) for endocarditis indications (670 [68%] prosthetic valve endocarditis). Staphylococcus aureus caused 193 of 949 cases of endocarditis (20%), 71 (7.3%) in persons who injected drugs. Periodic surveillance and cross-sectional follow-up achieved 85% of possible follow-up time. The primary end point was allograft infection in patients with nonendocarditis and endocarditis indications. Risk factors were identified by hazard function decomposition and machine learning.

      Results

      During follow-up, 30 allografts (26 explanted) became infected in patients in the nonendocarditis group and 49 (41 explanted) in patients with endocarditis. At 20 years, the probability of allograft infection was 5.6% in patients in the nonendocarditis group and 14% in patients with endocarditis. Risk factors for allograft infection in patients in the nonendocarditis group were younger patient age and older donor age. Risk factors for allograft infection in patients with endocarditis were earlier implant year, injection drug use, and younger age. In patients with endocarditis, 18% of allograft infections were caused by the original organism.

      Conclusions

      The low infection rates, both in patients without and with endocarditis, support continued use of allografts in the modern era, in particular for the treatment of invasive endocarditis of the aortic root.

      Graphical abstract

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to The Journal of Thoracic and Cardiovascular Surgery
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Ross D.N.
        Homograft replacement of the aortic valve.
        Lancet. 1962; 2: 487
        • Ross D.
        • Yacoub M.H.
        Homograft replacement of the aortic valve. A critical review.
        Prog Cardiovasc Dis. 1969; 11: 275-293
        • O'Brien M.F.
        • Harrocks S.
        • Stafford E.G.
        • Gardner M.A.
        • Pohlner P.G.
        • Tesar P.J.
        • et al.
        The homograft aortic valve: a 29-year, 99.3% follow up of 1,022 valve replacements.
        J Heart Valve Dis. 2001; 10: 334-344
        • Haydock D.
        • Barratt-Boyes B.
        • Macedo T.
        • Kirklin J.W.
        • Blackstone E.
        Aortic valve replacement for active infectious endocarditis in 108 patients. A comparison of freehand allograft valves with mechanical prostheses and bioprostheses.
        J Thorac Cardiovasc Surg. 1992; 103: 130-139
        • McGiffin D.C.
        • Galbraith A.J.
        • McLachlan G.J.
        • Stower R.E.
        • Wong M.L.
        • Stafford E.G.
        • et al.
        Aortic valve infection. Risk factors for death and recurrent endocarditis after aortic valve replacement.
        J Thorac Cardiovasc Surg. 1992; 104: 511-520
        • Pettersson G.B.
        • Hussain S.T.
        • Shrestha N.K.
        • Gordon S.
        • Fraser T.G.
        • Ibrahim K.S.
        • et al.
        Infective endocarditis: an atlas of disease progression for describing, staging, coding, and understanding the pathology.
        J Thorac Cardiovasc Surg. 2014; 147: 1142-1149
        • Bonn D.
        “Serious concerns” over CryoLife heart valves.
        Lancet Infect Dis. 2002; 2: 587
        • Centers for Disease Control and Prevention (CDC)
        Candida albicans endocarditis associated with a contaminated aortic valve allograft–California, 1996.
        MMWR Morb Mortal Wkly Rep. 1997; 46: 261-263
        • Pettersson G.B.
        • Coselli J.S.
        • Hussain S.T.
        • Griffin B.
        • Blackstone E.H.
        • Gordon S.M.
        • et al.
        2016 American Association for Thoracic Surgery (AATS) consensus guidelines: surgical treatment of infective endocarditis. Executive summary.
        J Thorac Cardiovasc Surg. 2017; 153: 1241-1258
        • Sabik J.F.
        • Lytle B.W.
        • Blackstone E.H.
        • Marullo A.G.
        • Pettersson G.B.
        • Cosgrove D.M.
        Aortic root replacement with cryopreserved allograft for prosthetic valve endocarditis.
        Ann Thorac Surg. 2002; 74: 650-659
        • Elgharably H.
        • Hakim A.H.
        • Unai S.
        • Hussain S.T.
        • Shrestha N.K.
        • Gordon S.
        • et al.
        The incorporated aortomitral homograft for double-valve endocarditis: the “hemi-Commando” procedure. Early and mid-term outcomes.
        Eur J Cardiothorac Surg. 2018; 53: 1055-1061
        • Goldman A.I.
        Eventcharts: visualizing survival and other timed-event data.
        Am Stat. 1992; 46: 13-18
        • Ivert T.S.
        • Dismukes W.E.
        • Cobbs C.G.
        • Blackstone E.H.
        • Kirklin J.W.
        • Bergdahl L.A.
        Prosthetic valve endocarditis.
        Circulation. 1984; 69: 223-232
        • Blackstone E.H.
        • Naftel D.C.
        • Turner Jr., M.E.
        The decomposition of time-varying hazard into phases, each incorporating a separate stream of concomitant information.
        J Am Stat Assoc. 1986; 81: 615-624
        • Pepe M.S.
        • Mori M.
        Kaplan-Meier, marginal or conditional probability curves in summarizing competing risks failure time data?.
        Stat Med. 1993; 12: 737-751
        • Rajeswaran J.
        • Blackstone E.H.
        Competing risks: competing questions.
        J Thorac Cardiovasc Surg. 2017; 153: 1432-1433
        • Rajeswaran J.
        • Blackstone E.H.
        Identifying risk factors: challenges of separating signal from noise.
        J Thorac Cardiovasc Surg. 2017; 153: 1136-1138
        • Rubin D.B.
        Multiple Imputation for Non-Response in Surveys.
        Wiley, New York1987
        • Svensson L.G.
        • Pillai S.T.
        • Rajeswaran J.
        • Desai M.Y.
        • Griffin B.
        • Grimm R.
        • et al.
        Long-term survival, valve durability, and reoperation for 4 aortic root procedures combined with ascending aorta replacement.
        J Thorac Cardiovasc Surg. 2016; 151: 764-774
        • Johnston D.R.
        • Soltesz E.G.
        • Vakil N.
        • Rajeswaran J.
        • Roselli E.E.
        • Sabik III, J.F.
        • et al.
        Long-term durability of bioprosthetic aortic valves: implications from 12,569 implants.
        Ann Thorac Surg. 2015; 99: 1239-1247
        • Glaser N.
        • Jackson V.
        • Holzmann M.J.
        • Franco-Cereceda A.
        • Sartipy U.
        Prosthetic valve endocarditis after surgical aortic valve replacement.
        Circulation. 2017; 136: 329-331
        • Fukushima S.
        • Tesar P.J.
        • Pearse B.
        • Jalali H.
        • Sparks L.
        • Fraser J.F.
        • et al.
        Long-term clinical outcomes after aortic valve replacement using cryopreserved aortic allograft.
        J Thorac Cardiovasc Surg. 2014; 148: 65-72
        • Ostergaard L.
        • Valeur N.
        • Ihlemann N.
        • Smerup M.H.
        • Bundgaard H.
        • Gislason G.
        • et al.
        Incidence and factors associated with infective endocarditis in patients undergoing left-sided heart valve replacement.
        Eur Heart J. 2018; 39: 2668-2675
        • Butt J.H.
        • Ihlemann N.
        • De Backer O.
        • Sondergaard L.
        • Havers-Borgersen E.
        • Gislason G.H.
        • et al.
        Long-term risk of infective endocarditis after transcatheter aortic valve replacement.
        J Am Coll Cardiol. 2019; 73: 1646-1655
        • Brennan J.M.
        • Edwards F.H.
        • Zhao Y.
        • O'Brien S.
        • Booth M.E.
        • Dokholyan R.S.
        • et al.
        Long-term safety and effectiveness of mechanical versus biologic aortic valve prostheses in older patients: results from the Society of Thoracic Surgeons adult cardiac surgery national database.
        Circulation. 2013; 127: 1647-1655
        • Witten J.C.
        • Durbak E.
        • Houghtaling P.L.
        • Unai S.
        • Roselli E.E.
        • Bakaeen F.G.
        • et al.
        Performance and durability of cryopreserved allograft aortic valve replacements.
        Ann Thorac Surg. 2021; 111: 1893-1900
        • Moon M.R.
        • Miller D.C.
        • Moore K.A.
        • Oyer P.E.
        • Mitchell R.S.
        • Robbins R.C.
        • et al.
        Treatment of endocarditis with valve replacement: the question of tissue versus mechanical prosthesis.
        Ann Thorac Surg. 2001; 71: 1164-1171
        • d'Udekem Y.
        • David T.E.
        • Feindel C.M.
        • Armstrong S.
        • Sun Z.
        Long-term results of operation for paravalvular abscess.
        Ann Thorac Surg. 1996; 62: 48-53
        • Jassar A.S.
        • Bavaria J.E.
        • Szeto W.Y.
        • Moeller P.J.
        • Maniaci J.
        • Milewski R.K.
        • et al.
        Graft selection for aortic root replacement in complex active endocarditis: does it matter?.
        Ann Thorac Surg. 2012; 93: 480-487
        • Kim J.B.
        • Ejiofor J.I.
        • Yammine M.
        • Camuso J.M.
        • Walsh C.W.
        • Ando M.
        • et al.
        Are homografts superior to conventional prosthetic valves in the setting of infective endocarditis involving the aortic valve?.
        J Thorac Cardiovasc Surg. 2016; 151: 1239-1248
        • David T.E.
        • Regesta T.
        • Gavra G.
        • Armstrong S.
        • Maganti M.D.
        Surgical treatment of paravalvular abscess: long-term results.
        Eur J Cardiothorac Surg. 2007; 31: 43-48
        • Solari S.
        • Mastrobuoni S.
        • De Kerchove L.
        • Navarra E.
        • Astarci P.
        • Noirhomme P.
        • et al.
        Over 20 years experience with aortic homograft in aortic valve replacement during acute infective endocarditis.
        Eur J Cardiothorac Surg. 2016; 50: 1158-1164
        • Musci M.
        • Weng Y.
        • Hubler M.
        • Amiri A.
        • Pasic M.
        • Kosky S.
        • et al.
        Homograft aortic root replacement in native or prosthetic active infective endocarditis: twenty-year single-center experience.
        J Thorac Cardiovasc Surg. 2010; 139: 665-673
        • Yankah A.C.
        • Pasic M.
        • Klose H.
        • Siniawski H.
        • Weng Y.
        • Hetzer R.
        Homograft reconstruction of the aortic root for endocarditis with periannular abscess: a 17-year study.
        Eur J Cardiothorac Surg. 2005; 28: 69-75
        • Toyoda N.
        • Itagaki S.
        • Tannous H.
        • Egorova N.N.
        • Chikwe J.
        Bioprosthetic versus mechanical valve replacement for infective endocarditis: focus on recurrence rates.
        Ann Thorac Surg. 2018; 106: 99-106

      E-References

        • R Core Team
        R: A language and environment for statistical computing.
        Vienna, Austria, R: Foundation for Statistical Computing2018 (Available at:) (Accessed February 19, 2019)
        • Ishwaran H.
        • Kogalur U.B.
        RandomForestSRC: random forests for survival, regression and classification (RF-SRC). R package version 2.5.0.
        (Available at:) (Accessed February 19, 2019)
        • Ishwaran H.
        • Kogalur U.B.
        • Blackstone E.H.
        • Lauer M.S.
        Random survival forests.
        Ann Appl Stat. 2008; 2: 841-860
        • Ishwaran H.
        • Kogalar U.B.
        Random survival forests for R.
        Rnews. 2007; 7: 25-31
        • Breiman L.
        Random forests.
        Machine Learn. 2001; 45: 5-32
        • Tang F.
        • Ishwaran H.
        Random forest missing data algorithms.
        Stat Anal Data Mining. 2017; 10: 363-377
        • Glaser N.
        • Jackson V.
        • Holzmann M.J.
        • Franco-Cereceda A.
        • Sartipy U.
        Prosthetic valve endocarditis after surgical aortic valve replacement.
        Circulation. 2017; 136: 329-331
        • O'Brien M.F.
        • Harrocks S.
        • Stafford E.G.
        • Gardner M.A.
        • Pohlner P.G.
        • Tesar P.J.
        • et al.
        The homograft aortic valve: a 29-year, 99.3% follow up of 1,022 valve replacements.
        J Heart Valve Dis. 2001; 10: 334-345
        • Fukushima S.
        • Tesar P.J.
        • Pearse B.
        • Jalali H.
        • Sparks L.
        • Fraser J.F.
        • et al.
        Long-term clinical outcomes after aortic valve replacement using cryopreserved aortic allograft.
        J Thorac Cardiovasc Surg. 2014; 148: 65-72
        • Brennan J.M.
        • Edwards F.H.
        • Zhao Y.
        • O'Brien S.
        • Booth M.E.
        • Dokholyan R.S.
        • et al.
        Long-term safety and effectiveness of mechanical versus biologic aortic valve prostheses in older patients: clinical perspective.
        Circulation. 2013; 127: 1647-1655
        • Johnston D.R.
        • Soltesz E.G.
        • Vakil N.
        • Rajeswaran J.
        • Roselli E.E.
        • Sabik III, J.F.
        • et al.
        Long-term durability of bioprosthetic aortic valves: implications from 12,569 implants.
        Ann Thorac Surg. 2015; 99: 1239-1247
        • Ostergaard L.
        • Valeur N.
        • Ihlemann N.
        • Smerup M.H.
        • Bundgaard H.
        • Gislason G.
        • et al.
        Incidence of infective endocarditis among patients considered at high risk.
        Eur Heart J. 2018; 39: 623-629
        • Butt J.H.
        • Ihlemann N.
        • De Backer O.
        • Sondergaard L.
        • Havers-Borgersen E.
        • Gislason G.H.
        • et al.
        Long-term risk of infective endocarditis after transcatheter aortic valve replacement.
        J Am Coll Cardiol. 2019; 73: 1646-1655
        • McGiffin D.C.
        • Galbraith A.J.
        • McLachlan G.J.
        • Stower R.E.
        • Wong M.L.
        • Stafford E.G.
        • et al.
        Aortic valve infection. Risk factors for death and recurrent endocarditis after aortic valve replacement.
        J Thorac Cardiovasc Surg. 1992; 104: 511-520
        • Sabik J.F.
        • Lytle B.W.
        • Blackstone E.H.
        • Marullo A.G.M.
        • Pettersson G.B.
        • Cosgrove D.M.
        Aortic root replacement with cryopreserved allograft for prosthetic valve endocarditis.
        Ann Thorac Surg. 2002; 74: 650-659
        • Haydock D.
        • Barratt-Boyes B.
        • Macedo T.
        • Kirklin J.W.
        • Blackstone E.
        Aortic valve replacement for active infectious endocarditis in 108 patients. A comparison of freehand allograft valves with mechanical prostheses and bioprostheses.
        J Thorac Cardiovasc Surg. 1992; 103: 130-139
        • d'Udekem Y.
        • David T.E.
        • Feindel C.M.
        • Armstrong S.
        • Sun Z.
        Long-term results of operation for paravalvular abscess.
        Ann Thorac Surg. 1996; 62: 48-53
        • d'Udekem Y.
        • David T.E.
        • Feindel C.M.
        • Armstrong S.
        • Sun Z.
        Long-term results of surgery for active infective endocarditis.
        Eur J Cardio-Thorac Surg. 1997; 11: 46-52
        • Yankah A.C.
        • Pasic M.
        • Klose H.
        • Siniawski H.
        • Weng Y.
        • Hetzer R.
        Homograft reconstruction of the aortic root for endocarditis with periannular abscess: a 17-year study.
        Eur J Cardiothorac Surg. 2005; 28: 69-75
        • David T.E.
        • Regesta T.
        • Gavra G.
        • Armstrong S.
        • Maganti M.D.
        Surgical treatment of paravalvular abscess: long-term results.
        Eur J Cardiothorac Surg. 2007; 31: 43-48
        • Klieverik L.M.A.
        • Yacoub M.H.
        • Edwards S.
        • Bekkers J.A.
        • Roos-Hesselink J.W.
        • Kappetein A.P.
        • et al.
        Surgical treatment of active native aortic valve endocarditis with allografts and mechanical prostheses.
        Ann Thorac Surg. 2009; 88: 1814-1821
        • Musci M.
        • Weng Y.
        • Hubler M.
        • Amiri A.
        • Pasic M.
        • Kosky S.
        • et al.
        Homograft aortic root replacement in native or prosthetic active infective endocarditis: twenty-year single-center experience.
        J Thorac Cardiovasc Surg. 2010; 139: 665-673
        • Jassar A.S.
        • Bavaria J.E.
        • Szeto W.Y.
        • Moeller P.J.
        • Maniaci J.
        • Milewski R.K.
        • et al.
        Graft selection for aortic root replacement in complex active endocarditis: does it matter?.
        Ann Thorac Surg. 2012; 93: 480-487
        • Kim J.B.
        • Ejiofor J.I.
        • Yammine M.
        • Camuso J.M.
        • Walsh C.W.
        • Ando M.
        • et al.
        Are homografts superior to conventional prosthetic valves in the setting of infective endocarditis involving the aortic valve?.
        J Thorac Cardiovasc Surg. 2016; 151: 1239-1248
        • Solari S.
        • Mastrobuoni S.
        • De Kerchove L.
        • Navarra E.
        • Astarci P.
        • Noirhomme P.
        • et al.
        Over 20 years experience with aortic homograft in aortic valve replacement during acute infective endocarditis.
        Eur J Cardiothorac Surg. 2016; 50: 1158-1164
        • Toyoda N.
        • Itagaki S.
        • Tannous H.
        • Egorova N.N.
        • Chikwe J.
        Bioprosthetic versus mechanical valve replacement for infective endocarditis: focus on recurrence rates.
        Ann Thorac Surg. 2018; 106: 99-106

      Linked Article

      • Commentary: Aortic allograft for endocarditis: Prevention of recurrent infection or reconstructive solution?
        The Journal of Thoracic and Cardiovascular SurgeryVol. 165Issue 4
        • Preview
          Surgery for infective endocarditis (IE) of the aortic valve remains associated with high in-hospital mortality, which is estimated to be as high as 21%, according to the Society of Thoracic Surgeons (STS) national database.1 Initial data for IE described outcomes of using aortic allografts,2-6 and many have enthusiastically endorsed their exclusive use in the setting of IE. Arguably, allogeneic biomaterial may be more resistant to recurrent infection than mechanical and xenograft implants. Lately however, this concept has been challenged by recent data suggesting that conventional prostheses—whether stented or stentless xenografts, or mechanical valves—may demonstrate similar long-term survival and freedom from recurrent IE, as compared with allograft implants.
        • Full-Text
        • PDF
      • Commentary: We should not forget the aortic valve allograft
        The Journal of Thoracic and Cardiovascular SurgeryVol. 165Issue 4
        • Preview
          Short- and long-term outcomes of surgical treatment of patients with active aortic valve bacterial endocarditis are influenced by multiple factors, including microbiology, patient-related factors, optimal perioperative care, timing of intervention, meticulous surgical techniques, and eventually by the type of the replacement device.1
        • Full-Text
        • PDF