- Email: [email protected]
Early bioprosthetic aortic valve endocarditis from dual bacterial pathogens including a HACEK microorganism (Cardiobacterium hominis)
Journal of Indian College of Cardiology 8 (2018) 216–218
Contents lists available at ScienceDirect
Journal of Indian College of Cardiology journal homepage: www.elsevier.com/locate/jicc
Case Report
Early bioprosthetic aortic valve endocarditis from dual bacterial pathogens including a HACEK microorganism (Cardiobacterium hominis) Stuart Mossa,* , Jude Olingab , Vinayak Nagarajab , Joseph Matthewsc a b c
St George Hospital, 1 Grey St, Kogarah, 2217 New South Wales, Australia Prince of Wales Hospital, Barker St, Randwick, 2031 New South Wales, Australia The Sutherland Hospital, The Kingsway, Caringbah, 2229 New South Wales, Australia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 6 November 2018 Accepted 19 November 2018 Available online 22 November 2018
This article presents Bacillus thuringiensis, a new pathogen implicated in causing infective endocarditis, in combination with Cardiobacterium hominis, which has never been reported in a dual pathogen endocarditis scenario. This is the first reported case of dual pathogen HACEK endocarditis that was identified by the authors. Our patient presented with a subacute course of infective symptoms and investigations found prosthetic valve endocarditis with C. hominis and B. thuringiensis. This is the first instance where B. thuringiensis has been implicated in infective endocarditis, where it was thought to previously be non-pathogenic. This is the nineteenth case of C. hominis prosthetic valve endocarditis and eighth case of C. hominis prosthetic valve endocarditis requiring re-do surgery reported in the English language. The pathogens isolated in this instance provide insight into causative pathogens and appropriate treatment modalities for successful management of sub-acute bioprosthetic infective endocarditis. Crown Copyright © 2018 All rights reserved.
Keywords: Infective endocarditis Bioprosthetic valve endocarditis HACEK Cardiobacterum Bacilus thuringiensis
1. Case report A 71-year-old male presented to hospital with a 5 week history of pleuritic chest pain, persistent fevers, night sweats, malaise, and anaemia. He had undergone an aortic valve replacement (Carpentier Edwards Magna Ease Perimount Aortic Valve) and coronary artery grafting 8 months prior for severe bicuspid aortic valve stenosis and coronary artery disease. His background history includes metabolic syndrome with well controlled hypertension, hypercholesterolaemia, type 2 diabetes mellitus and obstructive sleep apnoea. He is an ex-smoker, having quit 31 years prior. On examination he appeared pale, cachectic, and septic. He was not in heart failure, andhad no peripheral stigmata of infective endocarditis. His heart sounds were dual with a loud aortic component of the second heart sound, consistent with the bioprosthetic aortic valve. There was no aortic regurgitation. His ECG showed a normal sinus rhythm with no evidence of conduction disease or heart block. Pathology revealed a normal white cell count and a raised C-Reactive protein level of 123 mg/L (<3 mg/L).
* Corresponding author. E-mail address: [email protected] (S. Moss). https://doi.org/10.1016/j.jicc.2018.11.010 1561-8811/Crown Copyright © 2018 All rights reserved.
A trans-oeseophageal echocardiogram showed a functioning bioprosthesis with a 15 mm mobile vegetation and a posterior aortic root abscess (Fig. 1). He underwent a redo aortic valve replacement, with implantation of a bioprosthetic valve, and aortic root abscess washout. Bacillus thuringiensis was isolated from the valve specimen sent for culture; sensitive to vancomycin and ciprofloxacin and a second isolate, Cardiobacterium hominis, was isolated in 11 out of 12 blood culture bottles; which was sensitive to ampicillin, cefepime, ceftriaxone, cefotaxime, ciprofloxacin, gentamicin and tazocin. His postoperative course was uneventful and a trans-thoracic echocardiogram showed a well seated, functioning bioprosthesis and a normally functioning left ventricle. He was commenced intravenous ceftriaxone infusion for a period of 6 weeks. Initially the plan was for life-long antibiotic prophylaxis, however instead opted for short term oral cover and active surveillance after multi-dicsiplinary team discussions. He remained under close surveillance from infectious disease specialists with monitoring of his CRP. After 6 weeks of intravenous ceftriaxone, he was stepped down to oral amoxicillin prophylaxis. After a period of 3 months on oral amoxicillin, he had antibiotic therapy ceased entirely, only to remain under active surveillance by both his cardiologist and infectious disease specialists.
S. Moss et al. / Journal of Indian College of Cardiology 8 (2018) 216–218
217
Fig. 1. Trans-oesophageal echocardiogram demonstrating 15 mm vegetation to the bioprosthetic aortic valve, together with an aortic root abscess.
2. Discussion This is the first documented case of both dual HACEK/B. thuringiensis prosthetic valve endocarditis and the first documented case of B. thuringiensis prosthetic valve endocarditis. The HACEK group refers to a group of Gram-negative bacilli which include Haemophilus species (Haemophilus parainfluenzae, Haemophilus aphrophilus, Haemophilus paraphrophilus), Aggregatibacteractino mycetemcomitans, Cardiobacterium hominis, Eikenella corrodens, and Kingella species. They are known to cause culture negative endocarditis and are most prevalent in Australia and New Zealand. 1–5 Our patient had C. hominis which is a known, but rare cause of prosthetic valve endocarditis, with only 19 cases reported in the English language. 2,6–9 There are seven cases already reported in the literature of C. hominis prosthetic valve endocarditis that required valvular re-do surgery. 1,8–10 Our second isolate B. thuringiensis is a commensal in soil 11 and has never been reported in available literature as a causative agent for infective endocarditis. It is currently classified as non-infectious to humans, 12 and is used in commonly available pesticides. It is marketed as natural and safe organic pesticide. The patient had a typical subacute course with five weeks of progressively worsening infective symptoms less than 12 months after aortic valve replacement. This is in-line with the known course of most HACEK valve endocarditis. Unlike other cases of HACEK reports, where the patients are usually younger (median age 47.4 years) and present with high proportion of vascular and immunological manifestations (32% vs. 18%), 5 our patient is older than the median age and was devoid of any peripheral immunological manifestations of infective endocarditis.
In this patient 11 out of 12 bottles were positive for C. hominis within 48 h; which is notable as it is usually slow growing and requires very specific conditions in order to be isolated including supplemental carbon dioxide and yeast extract in the growth media. 13–15 This suggests a very high burden of pathogens. Isolation of B. thuringiensis was completely novel and raises the possibility of initial subclinical infection from this organism followed by secondary C. hominis infection. To the best of our knowledge, the patient, hospital staff, and pathology staff were not directly or indirectly exposed to pesticides; however this cannot be guaranteed. There have been alerts that any other valves from the same manufacturer have been contaminated. It is possible this organism was a contaminant, or that it was an indolent organism and played no role in the event of endocarditis. C.hominis is rarely resistant to penicillin or ampicillin, 16,17 with only two cases of beta-lactamase producing C. hominis being noted in previous English literature. 16,17 Our case reaffirms this fact. As such the standard 6 weeks course of intravenous ceftriaxone was used in our case, but there are no guidelines on treatment of Bacillus thuringiensisprosthetic valve endocarditis,our team in conjunction with infectious diseases consultation, decided short term oral antibiotic prophylaxis, followed by active surveillance of clinical features and inflammatory markers. The excellent clinical outcome in our patient is typical of other cases reported of HACEK prosthetic valve endocarditis. The in hospital setting mortality from HACEK endocarditis is 3.8% as compared with 39% from non-HACEK endocarditis.18 Although HACEK endocarditis has higher complication rates from stroke, embolism and intracranial haemorrhage,5 our patient did not have any complications. This is likely due to the absence of immunological manifestations which are thought to underlie the pathogenesis of intracranial haemorrhages.
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S. Moss et al. / Journal of Indian College of Cardiology 8 (2018) 216–218
Chambers and colleagues 5 reported that in a multi-National cohort about 40% of patients with HACEK endocarditis will require surgery.5 Our patient underwent surgery primarily due to presence of the aortic root abscess. The postoperative coursewas not complicated and appeared to be similar to other reported cases of HACEK endocarditis without dual infection. It cannot be ascertained whether the presence of B. thuringiensis was significant, and whether it altered the clinical course and outcome for the patient. The uniqueness of this case is the dual infection with an organism currently thought to be non-infectious in humans, and was cultured from an excised bioprosthetic valve. This case sheds some insight in the successful treatment of infective endocarditis with the previously mentioned dual microorganisms. Responsibility for the work The concept, and writing of the submission has been performed and approved by the authors listed, with all parties involved in the care of the patient having been addressed prior to initial submission of the article. The article has been carefully constructed to include important intellectual content. Conflict of interest There has been no financial support, nor conflict of interests affiliated with any of the authors. Prior publication This article is not currently awaiting review with any other journal at the present time. Ethics approval This case did not require institutional approval or ethics committee approval. References 1. Currie P. Late aortic homograft valve endocarditis caused by Cardiobacterium hominis: A case report and review of the literature. Heart. 2000;83(5):579–581.
2. Malani A, Aronoff D, Bradley S, Kauffman C. Cardiobacterium hominis endocarditis: Two cases and a review of the literature. Eur J Clin Microbiol Infect Dis. 2006;25(9):587–595. 3. Mueller N, Kaplan V, Altwegg M. Diagnosis of Cardiobacterium hominisendocarditis by broad-range PCR from arterio-embolic tissue. Infection. 1999;27(4-5):278–279. 4. Taveras J, Campo R, Segal N, Urena P, Lacayo L. Apparent culture-negative endocarditis of the prosthetic valve caused by Cardiobacterium hominis. South Med J. 1993;86(12):1439–1440. 5. Chambers S, Murdoch D, Morris A, Holland D, Pappas P. HACEK infective endocarditis: Characteristics and outcomes from a large, multi-national cohort. PLoS One. 2013;8(5)e63181. 6. Paturel L, Casalta J, Habib G, Nezri M, Raoult D. Actinobacillusactinomycetemcomitans endocarditis. Clin Microbiol Infect. 2004;10(2):98–118. 7. Shivaprakasha S, Radhakrishnan K, Kamath P, Karim P. Late prostheticvalveendocarditis due to Cardiobacteriumhominis, an unusual complication. Indian J Med Microbiol. 2007;25(January (1)):64–66. 8. Pousios D, Gao F, Tsang G. Cardiobacterium hominis prosthetic valve endocarditis: An infrequent infection. Asian Cardiovasc Thorac Ann. 2012;20 (3):327–329. 9. Donovan J, Hatcher J, Riddell A, Tiberi S. Back pain, leg swelling and a cardiac arrest: An interesting case of endocarditis. Case Rep. 2014;2014(May23 1) bcr2013202215-bcr2013202215. 10. Maekawa Y, Sakamoto T, Umezu K, Ohashi N, Harada Y. Infective endocarditis in a child caused by Cardiobacterium hominis after right ventricular outflow tract reconstruction using an expanded tetrafluoroethylene conduit. Gen Thorac Cardiovasc Surg. 2011;59(6):429–432. 11. Chaufaux J, Marchal M, Gilois N, Jehanno I, Buisson C. Investigation of natural strains of Bacillus thuringiensis in different biotopes throughout the world. Can J Microbiol. 1997;43:337–343. 12. Bravo A, Likitvivatanavong S, Gill S, Soberón M. Bacillus thuringiensis: A story of a successful bioinsecticide. Insect Biochem Mol Biol. 2011;41(7):423–431. 13. Maury S, Leblanc T, Rousselot P, Legrand P, Arlet G, Cordonnier C. Bacteremiadue to Capnocytophagaspecies in patients with neutropenia: High frequency of β-lactamase producing strains. Clin Infect Dis. 1999;28 (5):1172–1174. 14. McGowan E, Steinberg J. Other Gram negative bacilli. In: Mandell GL, Bennett JE, Dolin R, eds. Mandell, Douglas and Bennett’s principles and practice of infectious diseases. 4th ed. New York, N.Y: Churchill Livingstone; 1995:2108– 2109. 15. Friedman ND, Kaye KS, Stout JE, McGarry SA, Trivette SL, et al. Healthcare associated blood stream infections in adults. Ann Intern Med. 2002;137:791– 797. 16. Le Quellec A, Bessis D, Perez C, Ciurana A. Endocarditis due to -lactamaseproducing Cardiobacterium hominis. Clin Infect Dis. 1994;19(5):994–995. 17. Lu P, Hsueh P, Hung C, Teng L, Jang T, Luh K. Infective endocarditis complicated with progressive heart failure due to β-lactamase-producing Cardiobacterium hominis. J ClinMicrobiol. 2000;38(May (5)):2015–2017. 18. Fowler VG, Jr, Miro JM, et al. Staphylococcus aureus endocarditis: A consequence of medical progress. JAMA. 2005;293:3012–3021.sue>. 18V.G.Fowler. Jr. J.M.Miro. Staphylococcus aureus endocarditis: A consequence of medical progressJAMA293:.
Contents lists available at ScienceDirect
Journal of Indian College of Cardiology journal homepage: www.elsevier.com/locate/jicc
Case Report
Early bioprosthetic aortic valve endocarditis from dual bacterial pathogens including a HACEK microorganism (Cardiobacterium hominis) Stuart Mossa,* , Jude Olingab , Vinayak Nagarajab , Joseph Matthewsc a b c
St George Hospital, 1 Grey St, Kogarah, 2217 New South Wales, Australia Prince of Wales Hospital, Barker St, Randwick, 2031 New South Wales, Australia The Sutherland Hospital, The Kingsway, Caringbah, 2229 New South Wales, Australia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 6 November 2018 Accepted 19 November 2018 Available online 22 November 2018
This article presents Bacillus thuringiensis, a new pathogen implicated in causing infective endocarditis, in combination with Cardiobacterium hominis, which has never been reported in a dual pathogen endocarditis scenario. This is the first reported case of dual pathogen HACEK endocarditis that was identified by the authors. Our patient presented with a subacute course of infective symptoms and investigations found prosthetic valve endocarditis with C. hominis and B. thuringiensis. This is the first instance where B. thuringiensis has been implicated in infective endocarditis, where it was thought to previously be non-pathogenic. This is the nineteenth case of C. hominis prosthetic valve endocarditis and eighth case of C. hominis prosthetic valve endocarditis requiring re-do surgery reported in the English language. The pathogens isolated in this instance provide insight into causative pathogens and appropriate treatment modalities for successful management of sub-acute bioprosthetic infective endocarditis. Crown Copyright © 2018 All rights reserved.
Keywords: Infective endocarditis Bioprosthetic valve endocarditis HACEK Cardiobacterum Bacilus thuringiensis
1. Case report A 71-year-old male presented to hospital with a 5 week history of pleuritic chest pain, persistent fevers, night sweats, malaise, and anaemia. He had undergone an aortic valve replacement (Carpentier Edwards Magna Ease Perimount Aortic Valve) and coronary artery grafting 8 months prior for severe bicuspid aortic valve stenosis and coronary artery disease. His background history includes metabolic syndrome with well controlled hypertension, hypercholesterolaemia, type 2 diabetes mellitus and obstructive sleep apnoea. He is an ex-smoker, having quit 31 years prior. On examination he appeared pale, cachectic, and septic. He was not in heart failure, andhad no peripheral stigmata of infective endocarditis. His heart sounds were dual with a loud aortic component of the second heart sound, consistent with the bioprosthetic aortic valve. There was no aortic regurgitation. His ECG showed a normal sinus rhythm with no evidence of conduction disease or heart block. Pathology revealed a normal white cell count and a raised C-Reactive protein level of 123 mg/L (<3 mg/L).
* Corresponding author. E-mail address: [email protected] (S. Moss). https://doi.org/10.1016/j.jicc.2018.11.010 1561-8811/Crown Copyright © 2018 All rights reserved.
A trans-oeseophageal echocardiogram showed a functioning bioprosthesis with a 15 mm mobile vegetation and a posterior aortic root abscess (Fig. 1). He underwent a redo aortic valve replacement, with implantation of a bioprosthetic valve, and aortic root abscess washout. Bacillus thuringiensis was isolated from the valve specimen sent for culture; sensitive to vancomycin and ciprofloxacin and a second isolate, Cardiobacterium hominis, was isolated in 11 out of 12 blood culture bottles; which was sensitive to ampicillin, cefepime, ceftriaxone, cefotaxime, ciprofloxacin, gentamicin and tazocin. His postoperative course was uneventful and a trans-thoracic echocardiogram showed a well seated, functioning bioprosthesis and a normally functioning left ventricle. He was commenced intravenous ceftriaxone infusion for a period of 6 weeks. Initially the plan was for life-long antibiotic prophylaxis, however instead opted for short term oral cover and active surveillance after multi-dicsiplinary team discussions. He remained under close surveillance from infectious disease specialists with monitoring of his CRP. After 6 weeks of intravenous ceftriaxone, he was stepped down to oral amoxicillin prophylaxis. After a period of 3 months on oral amoxicillin, he had antibiotic therapy ceased entirely, only to remain under active surveillance by both his cardiologist and infectious disease specialists.
S. Moss et al. / Journal of Indian College of Cardiology 8 (2018) 216–218
217
Fig. 1. Trans-oesophageal echocardiogram demonstrating 15 mm vegetation to the bioprosthetic aortic valve, together with an aortic root abscess.
2. Discussion This is the first documented case of both dual HACEK/B. thuringiensis prosthetic valve endocarditis and the first documented case of B. thuringiensis prosthetic valve endocarditis. The HACEK group refers to a group of Gram-negative bacilli which include Haemophilus species (Haemophilus parainfluenzae, Haemophilus aphrophilus, Haemophilus paraphrophilus), Aggregatibacteractino mycetemcomitans, Cardiobacterium hominis, Eikenella corrodens, and Kingella species. They are known to cause culture negative endocarditis and are most prevalent in Australia and New Zealand. 1–5 Our patient had C. hominis which is a known, but rare cause of prosthetic valve endocarditis, with only 19 cases reported in the English language. 2,6–9 There are seven cases already reported in the literature of C. hominis prosthetic valve endocarditis that required valvular re-do surgery. 1,8–10 Our second isolate B. thuringiensis is a commensal in soil 11 and has never been reported in available literature as a causative agent for infective endocarditis. It is currently classified as non-infectious to humans, 12 and is used in commonly available pesticides. It is marketed as natural and safe organic pesticide. The patient had a typical subacute course with five weeks of progressively worsening infective symptoms less than 12 months after aortic valve replacement. This is in-line with the known course of most HACEK valve endocarditis. Unlike other cases of HACEK reports, where the patients are usually younger (median age 47.4 years) and present with high proportion of vascular and immunological manifestations (32% vs. 18%), 5 our patient is older than the median age and was devoid of any peripheral immunological manifestations of infective endocarditis.
In this patient 11 out of 12 bottles were positive for C. hominis within 48 h; which is notable as it is usually slow growing and requires very specific conditions in order to be isolated including supplemental carbon dioxide and yeast extract in the growth media. 13–15 This suggests a very high burden of pathogens. Isolation of B. thuringiensis was completely novel and raises the possibility of initial subclinical infection from this organism followed by secondary C. hominis infection. To the best of our knowledge, the patient, hospital staff, and pathology staff were not directly or indirectly exposed to pesticides; however this cannot be guaranteed. There have been alerts that any other valves from the same manufacturer have been contaminated. It is possible this organism was a contaminant, or that it was an indolent organism and played no role in the event of endocarditis. C.hominis is rarely resistant to penicillin or ampicillin, 16,17 with only two cases of beta-lactamase producing C. hominis being noted in previous English literature. 16,17 Our case reaffirms this fact. As such the standard 6 weeks course of intravenous ceftriaxone was used in our case, but there are no guidelines on treatment of Bacillus thuringiensisprosthetic valve endocarditis,our team in conjunction with infectious diseases consultation, decided short term oral antibiotic prophylaxis, followed by active surveillance of clinical features and inflammatory markers. The excellent clinical outcome in our patient is typical of other cases reported of HACEK prosthetic valve endocarditis. The in hospital setting mortality from HACEK endocarditis is 3.8% as compared with 39% from non-HACEK endocarditis.18 Although HACEK endocarditis has higher complication rates from stroke, embolism and intracranial haemorrhage,5 our patient did not have any complications. This is likely due to the absence of immunological manifestations which are thought to underlie the pathogenesis of intracranial haemorrhages.
218
S. Moss et al. / Journal of Indian College of Cardiology 8 (2018) 216–218
Chambers and colleagues 5 reported that in a multi-National cohort about 40% of patients with HACEK endocarditis will require surgery.5 Our patient underwent surgery primarily due to presence of the aortic root abscess. The postoperative coursewas not complicated and appeared to be similar to other reported cases of HACEK endocarditis without dual infection. It cannot be ascertained whether the presence of B. thuringiensis was significant, and whether it altered the clinical course and outcome for the patient. The uniqueness of this case is the dual infection with an organism currently thought to be non-infectious in humans, and was cultured from an excised bioprosthetic valve. This case sheds some insight in the successful treatment of infective endocarditis with the previously mentioned dual microorganisms. Responsibility for the work The concept, and writing of the submission has been performed and approved by the authors listed, with all parties involved in the care of the patient having been addressed prior to initial submission of the article. The article has been carefully constructed to include important intellectual content. Conflict of interest There has been no financial support, nor conflict of interests affiliated with any of the authors. Prior publication This article is not currently awaiting review with any other journal at the present time. Ethics approval This case did not require institutional approval or ethics committee approval. References 1. Currie P. Late aortic homograft valve endocarditis caused by Cardiobacterium hominis: A case report and review of the literature. Heart. 2000;83(5):579–581.
2. Malani A, Aronoff D, Bradley S, Kauffman C. Cardiobacterium hominis endocarditis: Two cases and a review of the literature. Eur J Clin Microbiol Infect Dis. 2006;25(9):587–595. 3. Mueller N, Kaplan V, Altwegg M. Diagnosis of Cardiobacterium hominisendocarditis by broad-range PCR from arterio-embolic tissue. Infection. 1999;27(4-5):278–279. 4. Taveras J, Campo R, Segal N, Urena P, Lacayo L. Apparent culture-negative endocarditis of the prosthetic valve caused by Cardiobacterium hominis. South Med J. 1993;86(12):1439–1440. 5. Chambers S, Murdoch D, Morris A, Holland D, Pappas P. HACEK infective endocarditis: Characteristics and outcomes from a large, multi-national cohort. PLoS One. 2013;8(5)e63181. 6. Paturel L, Casalta J, Habib G, Nezri M, Raoult D. Actinobacillusactinomycetemcomitans endocarditis. Clin Microbiol Infect. 2004;10(2):98–118. 7. Shivaprakasha S, Radhakrishnan K, Kamath P, Karim P. Late prostheticvalveendocarditis due to Cardiobacteriumhominis, an unusual complication. Indian J Med Microbiol. 2007;25(January (1)):64–66. 8. Pousios D, Gao F, Tsang G. Cardiobacterium hominis prosthetic valve endocarditis: An infrequent infection. Asian Cardiovasc Thorac Ann. 2012;20 (3):327–329. 9. Donovan J, Hatcher J, Riddell A, Tiberi S. Back pain, leg swelling and a cardiac arrest: An interesting case of endocarditis. Case Rep. 2014;2014(May23 1) bcr2013202215-bcr2013202215. 10. Maekawa Y, Sakamoto T, Umezu K, Ohashi N, Harada Y. Infective endocarditis in a child caused by Cardiobacterium hominis after right ventricular outflow tract reconstruction using an expanded tetrafluoroethylene conduit. Gen Thorac Cardiovasc Surg. 2011;59(6):429–432. 11. Chaufaux J, Marchal M, Gilois N, Jehanno I, Buisson C. Investigation of natural strains of Bacillus thuringiensis in different biotopes throughout the world. Can J Microbiol. 1997;43:337–343. 12. Bravo A, Likitvivatanavong S, Gill S, Soberón M. Bacillus thuringiensis: A story of a successful bioinsecticide. Insect Biochem Mol Biol. 2011;41(7):423–431. 13. Maury S, Leblanc T, Rousselot P, Legrand P, Arlet G, Cordonnier C. Bacteremiadue to Capnocytophagaspecies in patients with neutropenia: High frequency of β-lactamase producing strains. Clin Infect Dis. 1999;28 (5):1172–1174. 14. McGowan E, Steinberg J. Other Gram negative bacilli. In: Mandell GL, Bennett JE, Dolin R, eds. Mandell, Douglas and Bennett’s principles and practice of infectious diseases. 4th ed. New York, N.Y: Churchill Livingstone; 1995:2108– 2109. 15. Friedman ND, Kaye KS, Stout JE, McGarry SA, Trivette SL, et al. Healthcare associated blood stream infections in adults. Ann Intern Med. 2002;137:791– 797. 16. Le Quellec A, Bessis D, Perez C, Ciurana A. Endocarditis due to -lactamaseproducing Cardiobacterium hominis. Clin Infect Dis. 1994;19(5):994–995. 17. Lu P, Hsueh P, Hung C, Teng L, Jang T, Luh K. Infective endocarditis complicated with progressive heart failure due to β-lactamase-producing Cardiobacterium hominis. J ClinMicrobiol. 2000;38(May (5)):2015–2017. 18. Fowler VG, Jr, Miro JM, et al. Staphylococcus aureus endocarditis: A consequence of medical progress. JAMA. 2005;293:3012–3021.sue>. 18V.G.Fowler. Jr. J.M.Miro. Staphylococcus aureus endocarditis: A consequence of medical progressJAMA293:.