Thebowel, the genitourinary tract, and infective endocarditis · In a few patients with infective endocarditis the portal ofentry ofthe causal organismis beyond dis-pute. In the vast

Br Heart J 1984; 51: 339-45

The bowel, the genitourinary tract, and infectiveendocarditisRICHARD BAYLISS, CYRIL CLARKE, C M OAKLEY, W SOMERVILLE,A G W WHITFIELD, S E J YOUNG

From the Royal College ofPhysicians Research Unit, the British Cardiac Society, and the Communicable DiseasesSurveillance Centre, London

SUMMARY Of 582 episodes of infective endocarditis 75 were attributable to organisms normally

resident in the bowel and 12 others were associated with alimentary tract operations, investigations,

or disease. The mean age of the 87 patients in this particular group was higher (59.7 years) than thatof all the patients with infective endocarditis (51.4 years). As far as could be ascertained 41% had no

pre-existing cardiac abnormality, and in a little under a half no predisposing event to initiate theillness was apparent. Where the portal of entry of the organism to the blood stream was evident itwas slightly more often in the genitourinary than the alimentary tract.

Bowel organisms are no less important than those associated with the teeth in causing infectiveendocarditis. It is suggested that in all those patients with known cardiac abnormalities and possiblyin those over the age of 60 with normal hearts antibiotic cover should be considered when theyundergo genitourinary or alimentary tract surgery or instrumentation.

The prognosis of infective endocarditis has improveddramatically since the advent of antibiotic treat-ment' -13 and more recently as a result of emergencyvalve replacement.58912 13 In the best centres themortality rate is now apparently less8 14 than thewidely quoted figure of 300/%.45 10 13-15 Nevertheless,the prevalence of the disease is probably increasingand it remains a serious threat to life in all who sufferfrom it. Doubtless there will be further reductions inmortality with advances in cardiology, microbiology,and surgery, but the major effort must be in preven-tion. Those with rheumatic, congenital, or degenera-tive heart disease, with prosthetic valves6 7 9 12 16-19 orwho have undergone other cardiac surgery,47 andthose with a history of infective endocarditis4 12 16 areat especial risk and should have antibiotic prophylaxisif they need dental treatment or investigatory ortherapeutic procedures related to the alimentary,genitourinary, or respiratory tracts. In.addition, theimmunosuppressed, those addicted to alcohol, andthose with diabetes3 or malignant disease4 are particu-larly vulnerable. Nevertheless, one tenth of patientswith infective endocarditis have a pre-existing cardiac

Requests for reprints to Royal College of Physicans Research Unit,11 St Andrews Place, London NW1 4LE.

Accepted for publication 1 November 1983

abnormality which is not known to either them ortheir doctor,20 and it is also becoming increasinglyclear that a large proportion of patients with infectiveendocarditis have clinically normal hearts before theonset of their illness,69 13 162021 which are importantfactors that influence the application of any plannedprophylactic regimen.

In a few patients with infective endocarditis theportal of entry of the causal organism is beyond dis-pute. In the vast majority, however, the mechanismor route by which the organism gains entry to theblood stream is unknown or unproved. Oral organ-isms are the most common, and dental surgery hasbeen suspected for many years; although this is doubt-less the cause in some patients, definite proof is lack-ing, and the proportion so attributable is probablysmall.22 Other infections are thought to arise from thealimentary, genitourinary, or respiratory tracts orfrom the skin but again the evidence, though strong,is largely circumstantial. In fact the only group inwhich causation appears certain is in the right sidedendocarditis of drug addicts.A recent investigation conducted jointly by the

Royal College of Physicians Research Unit and theBritish Cardiac Society and related especially to thedental prophylaxis of infective endocarditis has pro-vided the largest series of patients yet studied.2022

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This investigation concerned those patients in whomthe causal organism's normal, but not exdusive,habitat was the alimentary tract and those in whomthe illness followed some alimentary tract investiga-tion, operation, or disease. Could infective endocar-ditis have been prevented in this not inconsiderablegroup?

Methods

Members of the British Cardiac Society and fellowsand members of the Royal College of Physicians in theUnited Kingdom were asked to complete a proformain respect of all patients with infective endocarditisunder their care during 1981 and 1982. The informa-tion requested included inter alia the causal organism,whether there was any known or unknown pre-existing cardiac abnormality, whether there had beenany dental, other surgical, or investigative proceduresor injury during the three months before the onset ofillness, and if so whether antibiotic cover had beenprovided, and details of any other relevant factors.

Results

Proformas in respect of 582 episodes of infectiveendocarditis occurring in 577 patients were received,five patients having had a second episode within thetwo year period. The age range of the patients wasfrom 2 to 87 (mean age 51-4) years and there was amale preponderance (ratio 2:1).Among the 582 episodes the evidence suggested

that the alimentary or genitourinary tracts may havebeen responsible in 87 (15%). The causal organismwas an unspeciated enterococcus in 17, Streptococcusfaecalis in 14, Streptococcus bovis in 27 (Table 1),Escherichia coli and other Gram negative bacilli in 11,and Streptococcus durans or group D streptococci in six(Table 2). In addition there were 12 patients in whomthe illness was temporally related to some alimentarytract disease or operation but in whom the dominanthabitat of the causal organism was not the bowel(Table 3). Similarly details are given (but not other-wise considered here) of patients whose infectiveendocarditis was not caused by bowel organisms butwhose illness was associated with genitourinary dis-ease, investigation, or surgery (Table 3).The twofold male preponderance in the group as a

whole was the same in the 87 patients whose infectiveendocarditis may have arisen from the alimentarytract, but the mean age was higher in the latter (59-7compared with 51-4 years). Ten of the 87 patientsdied, a slightly smaller proportion than that in thetotal 577 patients.Of the 87 patients, 36 (41%) had, as far as could be

ascertained, no pre-existing cardiac abnormality, a

Bayliss, Clarke, Oakley, Somerville, Whitfield, Young

proportion exactly the same as in the total 577patients. The valves affected did not differ in thealimentary tract group from all those examined, theaortic valve being affected in 29 patients and themitral valve in 23.

Discussion

Table 1 shows that of the 17 cases due to unspeciatedenterococci one was associated with gall bladder dis-ease, one followed an appendicectomy and one a gas-trointestinal infection, one had undergone a total pan-createctomy and was a diabetic and dependent onalcohol, and one had had a dental filling without anti-biotic cover within the previous three months whenhis heart was thought to be normal. Three cases arosefrom the genitourinary tract: one after a transurethralprostatic resection, one after urethral dilatation, andone in association with a urinary tract infection. Inanother patient a lacerated hand was the portal ofentry, but in the remaining eight patients -there was noindication ofhow the organism gained entrance to theblood stream. These findings in respect of enterococ-cal infections are similar to those of other work-ers.2' 23 The fact that enterococci commonly colonisethe anterior urethra, the vagina, and the cervixexplains the cases arising from the genitourinary tract.

In the 14 S faecalis infections (Table 1) the causalfactor was evident in all but two patients, one ofwhom had had a previous attack of infective endocar-ditis. Three infections followed an alimentary tractoperation (hemicolectomy, haemorrhoidectomy, andsurgery for a gangrenous femoral hernia). One casefollowed dental sepsis -and one a Colles fracture andmay have arisen from it or from the anaesthetic for itsreduction. Five cases arose from the genitourinarytract (prostatectomy for carcinoma, cystoscopy, vagi-nal hysterectomy, insertion of a ring pessary, urinarytract infection), and one case developed during thethirty third week of pregnancy. Infective endocarditisduring pregnancy has been reported,'5 24 and Sfaecalis, like unspeciated enterococci, often colonisethe lower genitourinary tract and perineum. In 15 ofthe 27 cases due to S bozis (Table 1), however, therewas no indication of why the infection developedexcept that one of the 15 patients had had a previousepisode of infective endocarditis and one had aprosthetic mitral valve. Six cases were associated withalimentary tract disease or procedures (gastric polyp,tubocellular adenomata of colon, closure of colos-tomy, liver biopsy in a patient who probably had acarcinoma, and diverticular disease in two patients).In a further three patients dental sepsis was present,and one had had scaling within two months of theonset of illness with antibiotic cover. Of the remainingtwo patients, one was receiving prednisone for asthma



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The bowel, the genitourinary tract, and infective endocarditis

Table 1 Details ofpatents with infective endocarditis due to vaious bowel organimsmCase Sex Age Previous cardiac abnormalay Valve Portal of enty or oder OutcomeNo (yr) affected causal factor

Unspeciated enterococciNone AorticCongenital aortic stenosis and Aortic

previous AVRRheumatic heart disease Mitral

None NS

Rheumatic heart disease NSNone Aortic

Previous AVR for aortic stenosis AorticPrevious AVR for aortic stenosis AorticBicuspid aortic valve AorticKnown cardiac abnormality nature NS

uncertain

TURNone

DiedDied

Gastrointestinal infecton 3 weeksbefore onset

Diabetic. Alcoholic. Had had totalpancreatectomy

NoneDental filling within 3 months without

antibiotic coverNone DiedLacerated thumbNoneUrinary tract infection

None Aortic NoneRheumatic heart disease Mitral Urethral dilatationRheumatic heart disease Aortic AppendectomyNone NS NoneNone Aortic Galbl der diseaseNone NS NoneNone NS None

Streptococcus faecalisNone Aortic Right hemicolectomy for Died

an'iodysplasiaPrevious IE Mitral Previous IEVSD VSD 33 weeks' pregnantNone Mitral 8 weeks after Coiles fracture DiedRheumatic heart disease NS After operation for haemorrhoidsNone Mitral and None Died

aorticAortic stenosis Aortic After operation for gangrenous

femoral herniaKnown murmur Aortic NoneNone NS After vaginal hysterectomyKnown mitral incompetence Mitral Urinary tract infectionNone NS After insertion of a ring pessaryHad had MVR Mitral After cystoscopyMitral valve prolapse Mitral After prostatectomy for carcinoma of

prostateDegenerative heart disease Aortic Dental sepsis

Streptococcus bovisCongenital heart disease Congenital Dental sepsis

defectRheumatic heart disease NS NoneAortic incompetence Aortic and None

mitralNone NS Dental sepsisRheumatic heart disease NS NoneNone Mitral AlcoholismNone NS Dental sepsisRheumatic heart disease NS NoneMitral incompetence Mitral Gastric polyp, dental caries

Bicuspid aortic valve Aortic NoneRheumatic heart disease, Mitral None

previous MVRNone NS None

Mitral incompetence Mitral None Died

None Aortic Scaling 5-8 weeks previouslywithout antibiotic cover

None Aortic None

Myocardial infarction (1973) NS Closure of colostomyAortic sclerosis Aortic None

Mitral incompetence Mitral None

None Mitral None

None NS Diverticulitis

None NS Liver biopsy, probably carcinoma Died

None NS Prednisone for asthma

None NS Diverticular diseaseNone NS Two tubocellular adenomata of colon

None Aortic None

Rheumatic heart disease, IE (1981) NS None

Rheumatic heart disease Mitral None Died

TUR, transurethral resection; AVR, aortic valve replacement; VSD, ventricular septal defect; NS, not stated; IE, infective endocarditis;

MVR, mitral valve replacement.

6 M24 M

36 M

37 M

39 M59 M

85 M103 M106 M126 F

127 F243 M245 F331 M345 M413 F440 F

13 M

18 F87 F146 F157 F204 M

217 F

221 M309 F320 M435 F437 M481 M

506 M

16 F

21 F57 M

105 F112 M116 M150 M171 M175 M182 M233 F

240 M259 M273 M

327 M337 M389 F418 F447 M452 F461 M474 F480 M490 M493 .F538 M545 F

7561

61

38

6118

62604471

46762971635880

60

5827734768

73

71NS77796671

59

61

NS34

5442434462773846

556863

61717661726961616048637780

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342 Bayliss, Clarke, Oakley, Somerville, Whitfield, Young

Table 2 Details ofpatients with infective endocarditis due to E coli, gram negative bacilli, S durans, and group D streptococci

Case Sex Age Previous cardiac abnormality Organism Valve Portal of entry or otherNo (yr) affected causal factor

68 F 5979 F NS266 M 50322 F 65409 F 64462 M 68470 M 62495 M 27534 F NS552 M 32

553 M 33

32 M 2260 M 7296 M 72307 M 58

509 M 76569 F 59

E coli and Grawn negative bacilliNone Coliform NS Nephrectomy for pyelonephritisAVR (1972) B fragtlis Aortic NoneMyocardial infarction E coli Mitral TURRheumatic heart disease E coli NS NoneRheumatic heart disease E coli NS Urinary tract infectionIschaemic heart disease E coli NS NoneNone E coli NS Diabetes; carcinoma of bladderBicuspid aortic valve Gram negative bacillus Aortic NoneRheumatic heart disease E coli NS Urinary tract infectionCongenital heart disease; E coli Pacemaker Nonepacemaker

Marfan's syndrome; AVR E coli Aortic NoneS durans and group D streptococci

Known enlarged heart Group D streptococcus Aortic NoneNone Group D streptococcus NS NoneAVR for aortic stenosis Group D streptococcus Aortic NoneRheumatic heart disease S durans Aortic and None

mitralRheumatic heart disease S durans NS NoneNone Group D streptococcus NS Nerve conduction studies for

peroneal muscular atrophy

NS, not stated; AVR, aortic valve replacement; TUR, transurethral resection.

Table 3 Details ofpatients with infective endocarditis apparently related to the alimentary tract or the genitourinary tract

Case Sex Age Previous cardiac abnormality Organism* Valve Portal of entry or other CNo (yr) affected causal factor

114 . F 73

119 M 79192 M 66195 M 65

380 M 27

381 F 57434 F 63

457 M 71473 M 86

485 M 60512 M 78578 M 52

1 M 7541 M 74

131 M 57

144 F 37199 M 55209 F 71

210 F 38292 F 72

334 M 36

431 M 65

433 M 68

522 F 63

Alimentary tractNone a haemolytic streptococcus Aortic Cryptogenic cirrhosis; monilial

angular stomatitisIschaemic heart disease a haemolytic streptococcus NS Bilateral inguinal herniotomyRheumatic heart disease a haemolytic streptococcus Mitral Dilatation of oesophageal stricture:None Coagulase negative NS Right inguinal herniotomy

staphylococcusCongenital heart disease Group B streptococcus Congenital Down's syndrome;

lesion bleeding haemorrhoidsRheumatic heart disease a haemolytic streptococcus Aortic Gall bladder diseasePrevious MVR and TVR Negative Tricuspid Gastroscopy; dental sepsis

and mitralNone a haemolytic streptococcus Mitral GastroscopyNone S mutans Aortic Cholecystectomy for empyema of

gall bladderNone S sanguis Mitral Surgery for rectal carcinomaMitral incompetence S mutans Mitral Carcinoma of rectumNone Group B streptococcus NS Liver failure

Genitourinary tractRheumatic heart disease S viridans NS Urinary tract infectionNone Negative Aortic Within one month of retropubic

prostatectomyInfective endocarditis and valve Staphylococcus aureus NS Urethral dilatation; urinary tract

replacement (1973) infectionNone S viridans Mitral Followed parturitionAortic valve replacement (1973) Negative Aortic Urinary tract infectionNone Proteus sp Mitral Pyelonephritis; diabetes

mellitus; proteus sp in urineNone S viridans Aortic 22 weeks pregnantNone Staph aureus NS Within one month of repair of

vaginal prolapse; diabetes;myxoedema

None S sanguis Aortic and Renal calculus and colic;mitral ?Marfan's syndrome

Bicuspid aortic valve Pseudomonas aeruginosa Aortic Urinary tract infection(not known)

Calcific aortic stenosis Staphylococcus albus Aortic Followed transurethral prostaticresection; rheumatoid arthritis

Aortic and mitral valve S viridans Aortic and Carcinoma of cervix;replacements for rheumatic mitral dilatation and curettage andheart disease (1981) radiotherapy

TUR, transurethral resection; MVR, mitral valve replacement; TVR, tricuspid valve replacement; NS, not stated.*a haemolytic streptococcus was previously known as S vridans.



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and the other was dependent on alcohol.Table 2 shows the 11 E coli and other Gram nega-

tive infections. In five cases the organism appeared tocome from the urinary tract, while in the remainingsix there was no indication of how it gained entranceto the blood stream. E coli and other Gram negativebacilli are of course often responsible for urinary tractinfection. Of the six cases due to group D streptococcior S durans (Table 2), one followed nerve conductionstudies, but in the other five the portal of entry wasnot known, although one of the five had a prostheticvalve.By definition all patients shown in Table 3 had

some alimentary tract disorder or had undergone anoperation or investigation: liver disease (two), gallbladder disease (two), rectal carcinoma (two), her-niotomy (two), haemorrhoids (one), and dilatation ofan oesophageal stricture (one). In eight of the 12 casesthe organism was of the Streptococcus vridans group,in two a group B streptococcus (considered by some tobe a bowel organism), in one a coagulase negativestaphylococcus, and in one the culture was negative.Of the 75 cases of infective endocarditis due to organ-isms normally present in the bowel, there were there-fore 12 that appeared to arise from the alimentarytract and 15 from the genitourinary tract, while in 40the portal of entry was not known.

In addition to dental procedures many investiga-tions, diseases, and operations of the alimentary tractare known to be associated with transient symptom-less bacteraemia.

Bacteraemia has been reported after upper gastroin-testinal endoscopy25 and after endoscopic retrogradecholangiopancreatography,26 but in none of thesecases did infective endocarditis develop. In two of thepatients (cases 434 and 457), however, infectiveendocarditis followed gastroscopy. Case 434 hadprosthetic mitral and tricuspid valves and dental sep-sis; case 457 had no pre-existing cardiac abnormalitybut the causal organism was an a haemolytic strep-tococcus (previously termed S vindans). Gastroscopymay be associated with considerable mucosal trauma.Buchman and Bergland reported positive blood cul-tures after sigmoidoscopy in 13 of 100 patients butthought that most, if not all, were due to contamin-ants.27 Le Frock and his colleagues28 and Weins-tein,29 however, found transient symptomless bac-teraemia in 9.5% of 200 patients after sigmoidoscopy,but this was not confirmed by Engeling and his co-workers.30 Moreover, blood cultures after colonos-copy with or without biopsy have been negative31unless associated with colonic carcinoma,32 itself wellknown to be associated with infective endocarditis.33Two of our 90 patients had rectal carcinoma (cases485 and 512).

Transient symptomless bacteraemia has been

reported after a barium enema29 34 and even after anormal bowel action. Bacteraemia35 36 but not infec-tive endocarditis has been reported after percutaneousliver biopsy and after transrectal prostatic biopsy.37One of the patient's symptoms of infective endocar-ditis began after liver biopsy (case 461), but he prob-ably had carcinomatosis.There have been many reports linking S bovis

endocarditis with carcinoma of the colon38-40 andother colonic disorders,41-43 and in some theendocarditis has presented before any symptoms ofthe colonic lesion have been evident.39 Although 27 ofthe 75 patients with endocarditis caused by bowelorganisms had S bovis infections, only six had anyabnormality of the alimentary tract.

Disease of the biliary tract is often associated withbacteraemia, and there have been reports of infectiveendocarditis arising from it particularly when surgicalintervention is necessary.'5 1644 Gall bladder disease(case 345) and cholecystectomy (case 473) were theonly examples among the 87 patients.There have been excellent studies of enterococ-

cal,2' 23E coli,45 and group D streptococcus endocar-ditis,2346 each of which has reflected the frequencywith which the infection stems from the genitourinarytract. They also indicate the now well known fact thatwhile S bovis infections respond well to penicillinthose due to unspeciated enterococci and S faecalisrequire treatment with an aminoglycoside in combina-tion with penicillin. The nomenclature andclassification of the organisms confuse the issue asdoes the now well known difficulty of differentiatingbetween S bovis and S faecalis. 9

Transient symptomless bacteraemia obviously fol-lows alimentary and genitourinary surgical and inves-tigative procedures not infrequently and may alsooccur under physiological conditions. Only anextremely small proportion of such bacteraemiasprogress to infective endocarditis, and among the fac-tors influencing this development are the magnitudeof the bacteraemia, the virulence of the organism, andthe susceptibility of the host. The presence of aprosthetic valve, a previous episode of infectiveendocarditis, and a rheumatic, congenital, ordegenerative cardiac abnormality play an importantpart, but depression of defence mechanisms by age,malignancy, alcohol dependence, diabetes,immunosuppression, hepatic or renal failure, or otherserious illness are frequent contributory influences.Even so, in nearly half the 75 patients, in whom infec-tive endocarditis was due to organisms normally resi-dent in the gut, there was no explanation of why thebacteraemia occurred.With regard to the prophylaxis of infective

endocarditis due to bowel organisms, it is clear thatsuch infections occur in older patients and derive

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from the genitourinary tract slightly more often thanfrom the alimentary tract. Furthermore, only 16% ofcases of infective endocarditis are due to bowel organ-

isms, and nearly half of these are unexplained; in theface of the enormous number of operations and inves-tigatory procedures involving the alimentary andgenitourinary tracts the risk of infective endocarditisarising therefrom must be very small indeed.Nevertheless, despite the minimal danger of suchprocedures infective endocarditis remains an appreci-able cause of morbidity and mortality, and measures

for its prevention are important. Certainly, the pres-

ent findings indicate that all those with known cardiacabnormalities should be given antibiotic cover for all

surgical, alimentary, and genitourinary proceduresand for gastroscopy. Furthermore, in view of the highproportion of older patients with normal hearts con-

tracting infective endocarditis those in this age group

should be considered for similar prophylaxis. Themeasures suggested by the British Society for Anti-microbial Chemotherapy47 may be appropriate, but ineach patient there will be differing circumstances tobe taken into account. The case for antibiotic cover iscertainly as strong as that for dental procedures. Inthe 582 episodes of infective endocarditis, of the 329with "S viridans" infections or with negative bloodcultures, only 38 (12%) of those known to have a

cardiac abnormality had had a dental procedurewithin three months of the onset of illness, and eightof the 38 had had antibiotic prophylaxis which failed.In comparison, of the 87 patients in whom infectiveendocarditis was caused by bowel organisms or fol-lowed some alimentary tract investigation or opera-

tion, 15 (17%) had a known cardiac abnormality, andonly two received antibiotic prophylaxis at the relev-ant time, which failed. Nevertheless, it must be ack-nowledged that had prophylaxis such as we suggestbeen given to those of the 87 patients in whom itwould have been considered appropriate at most theinfective endocarditis would have been prevented inonly about a fifth. Many were particularly vulnerableon account of age and other serious illness.

We thank the members of the British Cardiac Societyand the fellows and members of the College who haveparticipated in this survey.

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Thebowel, the genitourinary tract, and infective endocarditis · In a few patients with infective endocarditis the portal ofentry ofthe causal organismis beyond dis-pute. In the vast