Superior vena cava and right atrium wall infectiveendocarditis in patients receiving hemodialysis

Saurabh Thakar, MDa,*, Kalyana C. Janga, MDa, Tatyana Tolchinsky, MDb,Sheldon Greenberg, MDb, Kavita Sharma, MDc, Adnan Sadiq, MDd,

Edgar Lichstein, MDa, Jacob Shani, MDd

aDepartment of Internal Medicine, Maimonides Medical Center, Brooklyn, New YorkbDivision of Nephrology, Maimonides Medical Center, Brooklyn, New York

cDivision of Infectious Diseases, Maimonides Medical Center, Brooklyn, New YorkdDivision of Cardiology, Maimonides Medical Center, Brooklyn, New York

a r t i c l e i n f o

Article history:Received 27 March 2011Revised 25 June 2011Accepted 30 June 2011Online 3 September 2011

Conflict of Interest: none* Corresponding author: Saurabh Thakar, M

Brooklyn, NY 11219.E-mail addresses: saurabhthakar@rediffm

0147-9563/$ - see front matter Published bydoi:10.1016/j.hrtlng.2011.06.010

a b s t r a c t

Infective endocarditis is significantly more common and causes greatermorbidity and mortality in patients receiving hemodialysis than in the generalpopulation. Episodes of bacteremia during hemodialysis are primarily the resultof frequent vascular access through an arteriovenous fistula, a vascular graft, oran indwelling vascular catheter. This leads to dialysis access infection andsecondary bacteremia. We describe 4 cases of patients receiving hemodialysis,with an indwelling intravascular dialysis catheter, who developed right-sidedendocarditis with vegetations located exclusively on the superior vena cavaand right atriumwall. All patients had persistent bacteremia with Staphylococcus,secondary to an indwelling intravascular hemodialysis catheter, which led toseeding of the right-sided cardiac wall, causing infective endocarditis. The ratesof acceptance for hemodialysis are increasing, along with improved survival inthis group of patients. This will probably lead to an increase in the incidence ofinfective endocarditis, with atypical presentations such as superior vena cavaand right-sided cardiac wall endocarditis.

Infective endocarditis (IE) is significantly more risk of IE in the population receiving hemodialysis

common and causes greater morbidity and mortalityin patients receiving hemodialysis than in the generalpopulation. Dialysis access infections, with secon-dary septicemia, contribute significantly to patientmortality. By using the US Renal Data System Data-base, Abbott and Agodoa1 and Strom et al2 found anincreased age-adjusted incidence ratio and relative

D, Department of Intern

ail.com, sthakar@maimo

Elsevier Inc.

compared with the general population. Patients withend-stage renal disease have an increased incidenceof degenerative heart valve disease, which is a majorrisk factor for IE.3 In patients receiving hemodialysis,the mitral valve (50%) is the most commonly affectedvalve, followed by the aortic valve (30%) and right-sided IE.4 Furthermore, degenerative heart valve

al Medicine, Maimonides Medical Center, 964 49th St, Apt C-4,

nidesmed.org (S. Thakar).

h e a r t & l ung 4 1 ( 2 0 1 2 ) 3 0 1e3 0 7302

disease appears to begin 10 to 20 years earlier than inthe general population.5 The accelerated developmentof valvular calcification in patients with end-stagerenal disease is thought to be related to the abnor-malities of calcium-phosphorus homeostasis in thesetting of secondary hyperparathyroidism and thechronic microinflammatory milieu of uremia.5

We describe 4 cases of patients receiving hemo-dialysis with indwelling intravascular catheters whodeveloped right-sided IE with vegetations locatedexclusively on the superior vena cava (SVC) and rightatrium (RA) walls, all confirmed by transesophagealechocardiography (TEE). These cases were encoun-tered over a 4-year period from July 2006 to June 2010.

Case Reports

Case 1

A 44-year-old woman was admitted with abdominalpain, nausea, and diarrhea, which started after shereceived hemodialysis. She had a history of asthma,diabetes mellitus, hypertension, and end-stage renaldisease due to diabetic nephropathy with nephroticrange proteinuria. Physical examination showeddecreased intensity of breath sounds and dullness topercussion over the left lower lung base along withtenderness on abdominal examination in the epigas-trium and left upper quadrant. Chest radiographyshowed left pleural effusion. Computed tomography(CT) of the abdomen revealed a large splenic infarctcaused by the patient’s hypercoagulable state resultingfrom nephrotic syndrome. She subsequently hadaltered mental status and went into septic shock withacute respiratory failure. CT of the brain showed noevidence of stroke or thromboembolism. Pulmonaryembolism was ruled out with CT angiography of thechest. She was intubated and transferred to theintensive care unit. The patient had a right internaljugular vein dual lumen dialysis catheter, which wasremoved, and a new right femoral vein dual lumencatheter was inserted. The right internal jugular dial-ysis catheter exit site was clean with no erythema orexudate. TEE showed highly mobile large vegetationsin the SVC extending into the RA, which was moder-ately enlarged, accompanied by vegetation adherent tothe posterior tricuspid annulus (Figure 1A, B). A singleset of blood cultures was positive for multidrug-resistant Escherichia coli, and 2 sets of blood cultures(each from the peripheral blood and blood through theinitial dialysis catheter) were positive for coagulase-negative Staphylococcus. Treatment was started withintravenous (IV) cefepime and vancomycin. Thehemodialysis catheter in the right femoral vein wassubsequently removed, and a fresh triple lumen dial-ysis catheter was placed in the left internal jugularvein. The patient became hemodynamically stable and

afebrile. She was discharged with a total of 6 weeks ofIV antibiotics (cefepime and daptomycin) via the leftinternal jugular vein Hickman catheter, which wasplaced on discharge after removal of the triple lumendialysis catheter in the same position. Repeat trans-thoracic echocardiography (TTE) 4 months afterdischarge showed old, healed vegetation on thetricuspid valve. Repeat TTE 6 months later showed novegetation in the heart.

Case 2

A 49-year-old man was admitted with a high-gradefever (103.4�F), vomiting, and diarrhea. He had dia-betes mellitus, hypertension, and end-stage renaldisease, and was receiving hemodialysis througha right subclavian dual lumen catheter. Physicalexamination showed an immature right arm arterio-venous fistula for hemodialysis and erythema withpurulent discharge at the site of the dialysis catheter.Laboratory results revealed neutrophilic leukocytosis.The right subclavian vein catheter was removed, anda new left femoral dual lumen dialysis catheter wasinserted. Three sets of peripheral blood cultures and 2sets of blood cultures from the initial right subclaviandialysis catheter were positive for methicillin-sensitiveStaphylococcus aureus (MSSA). The dialysis catheter tipcultures also showed MSSA. TEE was performed afterremoval of the right subclavian vein catheter, whichshowed a highly mobile pedunculated 2 � .3-cmvegetation measuring attached to the lateral wall ofRA 1.5 cm above the tricuspid valve (Figure 2A, B). Thepatient was initially treated with IV nafcillin and laterwith IV vancomycin and piperacillin-tazobactam forseptic shock. The patient’s condition graduallyimproved, and he became afebrile and hemodynami-cally stable. The patient was discharged with a leftfemoral dual lumen dialysis catheter and 6 weeks of IVdaptomycin. A repeat TEE 1 month after dischargeshowed no evidence of endocarditis with a disappear-ance of the RA wall vegetation.

Case 3

The patient was a 54-year-old man who had cardiacarrest on admission secondary to hyperkalemia afterhe missed 2 sessions of hemodialysis. His history wassignificant for coronary artery disease, a bleedingduodenal ulcer, hypertension, stroke, left subclavianvein thrombosis with an SVC filter, and end-stage renaldisease on hemodialysis via a right subclavian duallumen catheter. Advanced Cardiac Life Supportprotocol was initiated with spontaneous return ofcirculation. On admission, laboratory investigationsrevealed neutrophilic leukocytosis and elevatedcardiac enzymes suggestive of type 2 noneST-eleva-tion myocardial infarction (consequent to decreasedoxygen supply due to hypotension) as a result ofcardiac arrest. CT of the head showed acute left pari-etal and frontal infarct. Chest x-ray showed right lower

Figure 1 e A, Transesophageal echocardiogram. High-esophageal short-axis view showing SVC withvegetation (arrow) attached to the anterior wall of the SVC. B, Transesophageal echocardiogram. High-esophageal long-axis view of SVC with vegetation (arrow) attached to the anterior wall of the SVC.

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lobe pneumonia. Two sets of peripheral blood culturesand another 2 sets of blood cultures from the rightsubclavian dialysis catheter were positive formethicillin-resistant Staphylococcus aureus (MRSA). Theright subclavian dialysis catheter exit site was cleanwith no erythema or exudate. TEE showed a 2.7-cmvegetation attached to the posterior wall of the SVCadjacent to the SVC-RA junction and patent foramenovale (Figure 3A, B). The right subclavian dialysiscatheter was removed, and a new dual lumen dialysiscatheter was placed in the left femoral vein. IV van-comycin and piperacillin-tazobactam were started.The patient’s condition stabilized, and he was dis-charged with a total of 6 weeks of IV vancomycin. Afterhis discharge, the patient did not follow up for a repeatechocardiogram or blood cultures.

Case 4

A 56-year-old man presented to the emergencydepartment with weakness caused by anemia. He hadbeen recently discharged from the hospital 1 weekpreviously after being treated for sepsis caused by aninfected right subclavian dual lumen hemodialysiscatheter, which was removed. During the last hospitalstay, hemodialysis was started through the left armarteriovenous fistula, which had matured. The patienthad 2 sets of negative blood cultures on discharge. Thepatient’s TTE during this last hospital admissionshowed no evidence of endocarditis or vegetation inthe heart. His medical history included coronary arterydisease, diabetes mellitus, end-stage renal disease onhemodialysis through the left arm arteriovenousfistula, hypertension, and hyperlipidemia. He was stillreceiving treatment with IV vancomycin at the time of

the current hospital admission for catheter sepsis. Thepatient went into septic shock with congestive heartfailure, leading to respiratory failure and requiringintubation. TTE at this time showed a 1.2 � 1.1-cmvegetation at the SVC-RA junction and vegetation onthe posterior mitral leaflet along with leaflet perfora-tion causing moderate to severe mitral regurgitation.TEE confirmed TTE findings and showed a smallsecundum-atrial septal defect. At least 4 sets ofperipheral blood cultures were positive for MSSA. IVnafcillin was started as an antibiotic. The patientinitially refused surgery but ultimately agreed andunderwent mitral valve replacement with a mechan-ical valve along with closure of atrial septal defect after4 weeks of IV antibiotics. The patient was alsoadministered IV cefepime in addition to nafcillin forgram-negative coverage because of fulminant sepsisand septic shock. The postoperative period wascomplicated by a complete heart block, respiratoryfailure, stroke, and gastrointestinal bleeding. He ulti-mately died secondary to multisystem organ failureafter a long hospital stay.

Discussion

All 4 patients had persistent bacteremia with Staphy-lococcus as evidenced by multiple positive bloodcultures, secondary to an indwelling intravascularhemodialysis catheter, leading to seeding of a right-sided cardiac wall causing SVC-RA wall IE. Thesecases differ from usual cases of IE that involve thecardiac valves, most commonly the mitral or aorticvalves, in patients receiving hemodialysis.

Figure 2 e A, Transesophageal echocardiogram. Mid-esophageal short-axis view at the aortic valve levelshowing vegetation (arrow) on the lateral wall of the RA. B, Transesophageal echocardiogram. Mid-esophageal 4-chamber view showing vegetation (arrow) on the lateral wall of the RA. LA, left atrium; LV, leftventricle; RV, right ventricle.

Figure 3 e A, Transesophageal echocardiogram. High-esophageal long-axis view of SVC with vegetation(arrow) attached to the posterior wall of the SVC. B, Transesophageal echocardiogram. High-esophageal short-axis view of SVC with vegetation (arrow) attached to the posterior wall of the SVC. LA, left atrium; RA, rightatrium.

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Table 1 summarizes the clinical characteristics, TEEfindings, and outcome of all 4 patients. It also includes2 similar cases reported in literature by Tzortzis et al6

and Gressianu et al7 with central venous catheter-related SVC-RA endocarditis due to septic thrombusformation.

A similar study was done by Chrissoheris et al8

about health care associated endocarditis compli-cating central venous catheter bloodstream infections.

Two-thirds of cases were right-sided, often associatedwith the presence of a catheter tip in the RA, andfrequently necessitating TEE for diagnosis. Trauma tothe endocardial surface by catheter tip promptingthrombus or vegetation formation was the proposedmechanism.

Episodes of bacteremia during hemodialysis arerelatively common, developing at an estimated rate of 1episode per 100 patient-care months.9,10 They are

Table

1e

Patientdata

Age/sex

Diabetes

mellitus

Initial

dialysisacc

ess

Organism

Dialysisca

theter

skin

exitsite

TEE

Succ

ess

ful

treatm

ent

Repeatfollow-u

pech

oca

rdiogram

Case

144y/female

Yes

Rightintern

aljugular

duallumenca

theter

Escherichia

coli,

coagulase

-negative

Staphylococcu

s

Clean

Vegetationin

SVCextending

into

RA,vegetationadherentto

posteriortricusp

idannulus

Yes

Novegetation

Case

249y/m

ale

Yes

Rightsu

bclaviandual

lumenca

theter

MSSA

Eryth

emaand

puru

lent

disch

arge

Peduncu

latedvegetation

attach

edto

lateralwallofRA

Yes

Novegetation

Case

354y/m

ale

No

Rightsu

bclaviandual

lumenca

theter

MRSA

Clean

Vegetationattach

edto

posterior

SVCwall,patentforamenovale

Yes

Notdone

Case

456y/m

ale

Yes

Rightsu

bclavian

duallumen

cath

eter,

left

arm

arteriovenousfistula

MSSA

Clean

VegetationatSVC-R

Ajunction,

vegetationonposteriormitral

leaflet,se

cundum-atrialse

ptal

defect

No

Notdone

Tzo

rtzis

etal6

case

72y/female

No

Subclaviance

ntral

venousca

theter

Candida

albicans

—Roundso

litary

vegetationattach

ed

toSVCpro

trudinginto

RA,atrial

septalabsc

ess

Yes

Noth

rombus

orvegetation

Gressianu

etal7

case

48y/female

Yes

Indwellingce

ntral

venousport

cath

eter

Torulopsis

(Candida)

glabrata

—Vegetation-likemass

adherentto

theca

thetertipextending

into

RA

Yes

Noth

rombus

orvegetation

h e a r t & l ung 4 1 ( 2 0 1 2 ) 3 0 1e3 0 7 305

primarily the result of frequent intravascular accessthrough an arteriovenous fistula, a vascular graft, or anindwelling vascular catheter.10 A hierarchy of bacter-emia risk exists among various types of hemodialysisvascular access; infection rates are highest amongtemporary catheters and lowest among permanentnative arteriovenous fistulae or synthetic grafts.11

Bacteremia may originate from an endogenous source(ie, a patient’s own cutaneous flora, the major cause ofStaphylococcal infection in thesepatients).12 Patientswithend-stage renal disease are inherently prone to bacter-emia and IE as a result of an impairment of the immunesystem. Metabolic abnormalities associated with end-stage renal disease, malnutrition, and associatedcomorbidities (eg, diabetes mellitus) impair poly-morphonuclear cell function and granulocyte mobility.This leads to reduction of cellular host defense andclearance of bacteria from the bloodstream.10

S. aureus is the main cause of vascular access-related bacteremia among patients receiving long-term hemodialysis (up to 75% of cases).13 More than50% of patients receiving dialysis are indeed carriers ofS. aureus, with the nose as the reservoir. Nasal carriageof S. aureus has been shown to be a major risk factor ofsubsequent infection, such as IE.14 S. aureus is thepredominant causative pathogen of IE in patientsreceiving hemodialysis and is more frequent than inthe general population.9,15-18 Strains of S. aureus thatinfect hemodialysis intravascular devices are particu-larly virulent and usually resistant to thrombin-induced platelet microbicidal protein. Therefore,these strains are more likely to disseminate in thebloodstream, causing bacteremia and IE.19 Univariateanalysis for factors affecting 60-day survival show thatthe presence of right-sided IE, a vegetation size greaterthan 2.0 cm3, a diagnosis of diabetes mellitus, and aninitial leukocyte count greater than 12.5 � 10/L arepoor prognostic factors.9 These patients require closemonitoring and prolonged antibiotic therapy (4-6weeks).

Many patients receiving hemodialysis havea vascular access device in situ, which is a potentialprimary focus of infection. Fever is less common inthese patients because of uremia-related impairedcellular host defense.15 Therefore, it is questionable toapply theDuke criteria in their strictest form topatientsreceiving hemodialysis, because the criteria couldunderdiagnose IE and significantly delay the time todiagnosis in these patients.20 Any patient receivinghemodialysis with suspected IE should be evaluated byTTE. TEE is more sensitive than TTE in detecting vege-tations, endocarditis-related complications, and right-sided endocarditis. Therefore, TEE can be consideredthe initial imaging modality or should always be per-formed after a negative TTE result in any patientreceiving chronic hemodialysis with a high clinicalsuspicion for features of IE. This is especially truewhentypical organisms for IE in patients receiving hemodi-alysis (S. aureus, coagulase-negative Staphylococcus) arecausative pathogen of bacteremia or if bacteremia is

h e a r t & l ung 4 1 ( 2 0 1 2 ) 3 0 1e3 0 7306

relapsing after antibiotic discontinuation. These highclinical suspicion features include the presence of new-onset congestive heart failure, development ofhemodialysis-related hypotension in a previouslyhypertensive patient, persistent bacteremia, andpersistently positive serial blood cultures with sepsis/septic shock.9,13,17,20,21

IE is significantly more common and lethal inpatients receiving hemodialysis than in the generalpopulation, the greatest mortality being observedwithin the first year of diagnosis.20 The first 30 to 60days after the diagnosis of IE are associated with thehighest mortality in patients receiving hemodialysis.This period requires the closest monitoring, duringwhich repeat echocardiography, adjustment of medi-cations/antibiotics, and removal of infected arteriove-nous grafts or catheters may be most beneficial inreducing mortality.9 Prevention of bacteremia isundoubtedly the best strategywith the early placementof arteriovenous fistulae. Dialysis catheter exit-sitebacterial infection leading to subsequent colonizationand biofilm formation can be prevented by the use oftopical mupirocin or bacitracin-polymyxin B andgentamicin or citrate.22

One of the known distinctions between right-sidedand left-sided cardiac vegetations in IE is the ach-ieved bacterial density. A number of studies show thatbacterial densities in aortic valve vegetations arehigher than in tricuspid vegetations. The mechanismmay be related to the increased oxygen tensions on theleft side of the heart.23-25 Substantial data in bothhuman and experimental IE confirm that the intra-vegetational bacterial acquisition of antibiotic resis-tance is more common in left-sided IE. Bacteremiatends to be high-grade (>100 colony-forming units/mLof blood) and long-lasting in left-sided IE, whereasbacteremia tends to be short-lived and intermittent inright-sided IE.26 There is a more prominent trend ofself-sterilization of vegetations in right-sided IEcompared with left-sided IE after removal of infectedcatheters. Polymorphonuclear cells play a significantrole in eradicating intravegetational bacteria andreducing bacterial density, keeping endocardial infec-tion in check. Impairment of polymorphonuclear cellfunction in patients with end-stage renal disease canin turn impair the process of sterilization of vegeta-tions of IE in these patients.23-26

Recent guidelines suggest that long-term catheters,including hemodialysis catheters, should be removedfrom patients with catheter-related bloodstreaminfection associated with severe sepsis, endocarditis,or infections due to S. aureus, Pseudomonas aeruginosa,fungi, or mycobacteria. In these patients, a temporarynontunneled catheter should be inserted into anotheranatomic site. Only if absolutely no alternative sitesare available for dialysis catheter insertion shouldthe infected catheter be exchanged over a guidewire.When a hemodialysis catheter is removed forcatheter-related bloodstream infection, a long-termhemodialysis catheter can be placed once blood

cultures with negative results are obtained. A 4- to 6-week antibiotic course should be administered ifthere is persistent bacteremia (ie, >72 hours in dura-tion) after hemodialysis catheter removal or forpatients with endocarditis.27 Temporarily transferringthe patient on peritoneal dialysis might be a moredesirable option because of the risk of persistentcatheter-related bacteremia.13,28 If catheter salvage isattempted in patients without alternative vascularaccess sites, a longer duration of antibiotic treatmentand repeated echocardiographic examinations arerecommended.28

Friction of the dialysis catheter on the right atrialendocardium can lead to thrombus formation at thislocation. Infection of these clots can lead to right-sidedor cardiac wall IE; therefore, positioning the distalsegment of the dialysis catheters in the RA should beavoided.29

Conclusions

Although the mitral and aortic valves are the mostcommonly affected valves in IE in the populationreceiving hemodialysis, right-sided IE on the valves orcardiac wall can occur, especially in patients withpersistent bacteremia caused by infected indwellingdialysis catheters. There should be a lower threshold toperform TEE in patients receiving hemodialysis withindwelling dialysis catheters if there is a suspicion ofendocarditis. Long-term catheters, including hemodi-alysis catheters, should be removed from patients withcatheter-related bloodstream infection associatedwith severe sepsis, endocarditis, or infections due toS. aureus, P. aeruginosa, fungi, or mycobacteria. A 4- to6-week antibiotic course should be administered ifthere is persistent bacteremia (ie, >72 hours in dura-tion) after hemodialysis catheter removal or forpatients with endocarditis. Given that rates of accep-tance into hemodialysis are increasing, along withimproved survival in these patients, the incidence of IEin this group of patients will probably increase withatypical presentations, such as right-sided and cardiacwall IE.

References

1. Abbott KC, Agodoa LY. Hospitalizations for bacterialendocarditis after initiation of chronic dialysis in theUnited States. Nephron 2002;91:203-9.

2. Strom BL, Abrutyn E, Berlin JA, Kinman JL,Feldman RS, Stolley PD, et al. Risk factors for infectiveendocarditis: oral hygiene and nondental exposures.Circulation 2000;102:2842-8.

3. Umana E, Ahmed W, Alpert MA. Valvular andperivalvular abnormalities in end-stage renal disease.Am J Med Sci 2003;325:237-42.

h e a r t & l ung 4 1 ( 2 0 1 2 ) 3 0 1e3 0 7 307

4. Robinson D, Fowler V, Sexton D, Corey R, Conlon P.Bacterial endocarditis in hemodialysis patients. Am JKid Dis 1997;30:521-4.

5. Madu EC, D’Cruz IA, Wall B, Mansour N, Shearin S.Transesophageal echocardiographic spectrum ofcalcific mitral abnormalities in patients with end-stage renal disease. Echocardiography 2000;17:29-35.

6. Tzortzis S, Apostolakis S, Xenakis K, Spiropoulos G,Lazaridis K. Catheter-related septic thrombophlebitisof the superior vena cava involving the atrial septum:a case report. Cases J 2008;1:272.

7. Gressianu MT, Dhruva VN, Arora RR, Patel S, Lopez S,Jihayel AK, et al. Massive septic thrombus formationon a superior vena cava indwelling catheter followingTorulopsis (Candida) glabrata fungemia. IntensiveCare Med 2002;28:379-80.

8. Chrissoheris MP, Libertin C, Ali RG, Ghantous A,Bekui A, Donohue T. Endocarditis complicatingcentral venous catheter bloodstream infections:a unique form of health care associated endocarditis.Clin Cardiol 2009;32:48-54.

9. McCarthy JT, Steckelberg JM. Infective endocarditis inpatients receiving long-term hemodialysis. Mayo ClinProc 2000;75:1008-14.

10. Powe NR, Jaar B, Furth SL, Hermann J, Briggs W.Septicemia in dialysis patients: incidence, riskfactors, and prognosis. Kidney Int 1999;55:1081-90.

11. Stevenson KB, Adcox MJ, Mallea MC, Narasimhan N,Wagnild JP. Standardized surveillance ofhemodialysis vascular access infections: 18-monthexperience at an outpatient, multifacilityhemodialysis center. Infect Control Hosp Epidemiol2000;21:200-3.

12. Sexton DJ. Vascular access infections in patientsundergoing dialysis with special emphasis on the roleand treatment of Staphylococcus aureus. Infect DisClin North Am 2001;15:731-42.

13. Maraj S, Jacobs LE, Maraj R, Kotler MN. Bacteremiaand infective endocarditis in patients onhemodialysis. Am J Med Sci 2004;327:242-9.

14. Wertheim HF, Melles DC, Vos MC, Van leeuwen W,Van belkum A, Verbrugh HA, et al. The role of nasalcarriage in Staphylococcus aureus infections. LancetInfect Dis 2005;5:751-62.

15. Maraj S, Jacobs LE, Kung SC, Raja R, Krishnasamy P,Maraj R, et al. Epidemiology and outcome of infectiveendocarditis in hemodialysis patients. Am J Med Sci2002;324:254-60.

16. Doulton T, Sabharwal N, Cairns HS, Schelenz S,Eykyn S, O’Donnell P, et al. Infective endocarditis indialysis patients: new challenges and old. Kidney Int2003;64:720-7.

17. Spies C, Madison JR, Schatz IJ. Infective endocarditisin patients with end-stage renal disease: clinicalpresentation and outcome. Arch Intern Med 2004;164:71-5.

18. Nori US, Manoharan A, Thornby JI, Yee J,Parasuraman R, Ramanathan V. Mortality risk factorsin chronic hemodialysis patients with infectiveendocarditis. Nephrol Dial Transplant 2006;21:2184-90.

19. Fowler VG Jr, McIntyre LM, Yeaman MR, Peterson GE,Barth RL, Corey GR, et al. In vitro resistance tothrombin-induced platelet microbicidal protein inisolates of Staphylococcus aureus from endocarditispatients correlates with an intravascular devicesource. J Infect Dis 2000;182:1251-4.

20. Nucifora G, Badano LP, Viale P, Gianfagna P, Allocca G,Montanaro D, et al. Infective endocarditis in chronichemodialysis patients: an increasing clinicalchallenge. Eur Heart J 2007;28:2307-12.

21. Wu EB, Witherspoon ML, Gillmore JD, Pattison JM,Chambers JB. The role of transesophagealechocardiography in patients with chronic renalfailure at low and high risk of endocarditis. J HeartValve Dis 1997;6:249-52.

22. Schubert C, Moosa MR. Infective endocarditis ina hemodialysis patient: a dreaded complication.Hemodial Int 2007;11:379-84.

23. Bayer A, Norman D. Valve site-specific pathogeneticdifferences between right-sided and left-sidedbacterial endocarditis. Chest 1990;98:200-5.

24. Perlman BB, Freedman LR. Experimental endocarditis:natural history of catheter- induced Staphylococcalendocarditis following catheter removal. Yale J BioMed 1971;44:214-24.

25. Durack DT, Beeson PB, Petersdorf RG. Experimentalbacterial endocarditis: production and progress of thedisease in rabbits. Br J Exp Pathol 1973;54:142-51.

26. Archer G, Fekety FR. Experimental endocarditis due toPseudomonas aeruginosa: description of a model.J Infect Dis 1976;134:1-7.

27. Mermel LA, Allon M, Bouza E, Craven DE, Flynn P,O’Grady NP, et al. Clinical practice guidelines for thediagnosis and management of intravascular catheter-related infection: 2009 update by the infectiousdiseases society of America. Clin Infect Dis 2009;49:1-45.

28. Hoen B. Infective endocarditis: a frequent disease indialysis patients. Nephrol Dial Transplant 2004;19:1360-2.

29. Ghani MK, Boccalandro F, Denktas AE, Barasch E.Right atrial thrombus formation associated withcentral venous catheters utilization in hemodialysispatients. Intensive Care Med 2003;29:1829-32.