Systematic review

doi:10.1111/j.1463-1318.2009.01814.x

Streptococcus bovis endocarditis, a silent sign for colonic tumour

A. Gupta, R. Madani and H. Mukhtar
Department of Surgery, Whittington NHS Trust Hospital, University College London Received 17 February 2008; accepted 9 January 2009

Abstract
Aim An association between colonic carcinoma and Streptococcus bovis endocarditis bacteraemia was rst suggested in 1951. This knowledge has great clinical implications, yet we found scant awareness amongst general surgical trainees. The aim of this article was to review the evidence available in the literature and explore the pathophysiology behind this association. Method The literature was reviewed, between 1950 and 2008, using Pubmed, Embase and Ovid database searches. We utilized different combinations of the keywords: Streptococcus bovis, endocarditis, septicaemia and colon cancer carcinoma. Quality assessment was determined using the Oxford Centre for Evidence-based Medicine Levels of Evidence (May 2001). Studies were selected based on their relevance to the aims to be addressed. Results We included nine case reports and found 24 studies demonstrating an association between S. bovis bacteraemia endocarditis and colon cancer; the reported incidence in studies was variable (667%). The majority of studies (20) were retrospective analysis of data; only four studies were prospective. A total of 12 of 24 studies also reported an association with extra-colonic malignancy (1 22%) and 12 with liver disease (357%). Eight studies relevant to the pathophysiology of this association were identied. Conclusion Streptococcus bovis endocarditis and or bacteraemia is an early clue to the likely presence of colorectal cancer. Whilst further studies are required to determine the precise pathophysiology, clinicians should be aware of this association. It is advisable to investigate rigorously for colon cancer in all patients presenting with S. bovis endocarditis bacteraemia; such patients may also present with liver disease or, occasionally, extra-colonic malignancy. Keywords Streptococcus bovis, endocarditis, septicaemia, colon cancer carcinoma

Background
Streptococcus bovis

as: Streptococcus gallolyticus, Streptococcus infantarius and Streptococcus pasteurianus, respectively [3]. Therefore, these names can be used inter-changeably in literature.

Streptococcus bovis is a group of gram-positive cocci that belong to group D of the Lanceeld classication. Group D streptococci include enterococci and nonenterococcal species, and S. bovis belongs to the later group. Streptococcus bovis is a commensal organism, normally habitant in the human and animal gastrointestinal tracts. It is the second greatest cause of endocarditis from streptococci [1] and is responsible for 1015% of all patients with bacterial endocarditis [2]. The nomenclature is variable; S. bovis I, S. bovis II 1 and S. bovis II 2 have, more recently, been named

Aims
The association between S. bovis endocarditis septicaemia and colon cancer, rst documented over 50 years ago [4], has great clinical importance in the diagnosis, management and treatment of patients. However, we found scant awareness amongst general surgical trainees. Therefore, the aim of this article was to re-visit this relationship and review the evidence available in the literature; we also aimed to explore studies addressing the pathophysiology underlying this association. In addition, we aimed to present any evidence supporting other associations of S. bovis endocarditis septicaemia with extra-colonic malignancy or liver disease.

Correspondence to: A. Gupta, University College London Medical School, London, UK. E-mail: abhinav.gupta@ucl.ac.uk

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Streptococcus bovis endocarditis, a silent sign for colonic tumour

Method of review
Search strategy

Results
We found 24 studies examining the association of S. bovis endocarditis bacteraemia with colon cancer; a description of included studies and quality assessment is shown in Table 1. Twelve of these 24 studies also reported an association between S. bovis endocarditis bacteraemia and extra-colonic malignancy, and 12 reported an association with liver disease. Nine case reports, describing an association of S. bovis endocarditis septicaemia with colon cancer, were additionally included, as were eight studies relevant to the pathophysiology of this association.

The literature was reviewed using PubMed, Ovid and Embase searches (up to December 2008). For Ovid and Embase, keywords were used as shown in Fig. 1.
Results of literature search

The literature search obtained 101 results for EMBASE 1980 to 2008; eight results for EMBASE classic 1947 to 1979 and 146 results for Ovid MEDLINE (R) 1950 to 2008. Pubmed was searched using the condition, colon cancer, S. bovis endocarditis and this obtained 73 hits (six reviews).
Selection of studies and quality assessment

Discussion
Streptococcus bovis and colon cancer

The authors read through search results; abstracts and or full text of all articles written in English were reviewed (abstracts only were reviewed for articles in a foreign language). Any study not electronically found was hand-searched. Studies were selected for inclusion based on their relevance to the question to be addressed: the association of S. bovis endocarditis bacteraemia with colon cancer. Relevant studies examining the pathophysiology of this association were also included, as were any addressing associations with extra-colonic malignancy or liver disease. Where applicable, the references of reviewed articles were also used to identify pertinent literature. All studies were assessed for quality using the Oxford Centre for Evidence-based Medicine Levels of Evidence (May 2001) [5] and some reader discretion.

An association between colonic carcinoma and S. bovis endocarditis septicaemia was rst suggested in a case report by McCoy and Mason in 1951 [4]. Over two decades later, Klein demonstrated this association in two further patients [6], and this has been followed by numerous other such case reports by various authors [1,713]. In the current review, we also found 24 studies addressing this association; the level of evidence and main ndings of each study are outlined in Tables 1 and 2, respectively. There was a wide variance in the reported incidence of association, ranging from 6% in a retrospective analysis by Pigrau et al. [20] to 67% in a retrospective review by Beeching et al. [31]. This may be due to the fact that most studies were retrospective and not all patients with S. bovis endocarditis bacteraemia undergo bowel investigations. The largest study found, in which all patients with S. bovis bacteraemia did undergo colon

Figure 1 Search strategy utilized for Ovid and Embase database searches.

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Reference

Author(s)

Design

Quality assessment (Level of evidence)

Table 1 Design and quality assessment of included studies.

Studies addressing the association of S. bovis endocarditis bacteraemia and colon cancer 4 McCoy and Mason Case report 4 7 Robbins and Klein Case report 4 8 Waisberg and Matheus Case report 4 9 Kok et al. Case report 4 10 Muhlemann et al. Case report 4 11 Mansur et al. Case report 4 12 Levy et al. Case report 4 1 Dunham et al. Case report 4 13 Steinberg and Naggar Case report 4 14 Murray and Roberts Retrospective review 3b 15 Reynolds et al. Retrospective review 3b 16 Kupferwasser et al. Retrospective review 3b 17 Leport et al. Retrospective review 3b 18 Zarkin et al. Retrospective review 3b 19 Ruoff et al. Retrospective review 3b 20 Pigrau et al. Retrospective review 3b 21 Klein et al. (1979) Prospective controlled study 2c 22 Hoen et al. Retrospective case-control 3b 23 Hoppes and Lerner Retrospective study 3b 24 Gonzalez-Quintela et al. Retrospective review 3b 25 Tripodi et al. Prospective case-control 2c 26 Alazmi et al. Retrospective review 3b 27 Gold et al. Retrospective review 3b 28 Herrero et al. Retrospective review 3b 29 Wilson et al. Prospective study 2c 30 Friedrich et al. Retrospective review 3b 31 Beeching et al. Retrospective review 3b 32 Honberg and Gutschik Retrospective review 3b 33 Ballet et al. Retrospective review 3b 34 Duval et al. Retrospective review 3b 35 Pergola et al. Retrospective review 3b 36 Lee et al. Retrospective review 3b 53 Corredoira et al. Prospective study 2c Studies addressing the pathophysiology of this association 6 Klein et al. (1977) Retrospective case-control 38 Darjee and Gibb Retrospective case-control 39 Tjalsma et al. Retrospective case-control 48 Ellmerich et al. Lab experiments 51 Noreet et al. Prospective study 49 Dubrow et al. Prospective case-control 50 Potter et al. Prospective controlled study 52 Biarc et al. Lab experiments

3b 3b 3b 5 2c 2c 2c 5

evaluation, was a retrospective review by Ballet et al. [33], and this study reported colonic neoplasm in 27 out of 53 patients (51%). Most of the studies found did not distinguish between the different biotypes of S. bovis (see Background section). However, in one retrospective review of 38 patients by Ruoff et al. [19], bacteraemia with S. bovis I was

highly correlated with an underlying colonic neoplasm (71%), compared with bacteraemia due to S. bovis II or S. salivarius (17%). In other studies also, colon cancer was mainly associated with S. bovis type I endocarditis (94%), compared to S. bovis Type II endocarditis (18%) [37]. In view of this association, all patients who may benet from identication of an occult neoplasm are

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Streptococcus bovis endocarditis, a silent sign for colonic tumour

Table 2 Studies addressing the association of Streptococcus bovis bacteraemia endocarditis and colon cancer. No. of patientsa with S. bovis bacteraemia 36 19 22 34 92 38 16 29 32 14 20 30 38 41 12 21 20 12 90 53 20 40 37 133 S. bovis endocarditis 26 (72) 14 (78) 22 (100)e 34 (100) 26 (28) 19 (50) 5 (31) 13 (45) 32 (100) 14 (100) 10 (50) 30 (100)p 7 (18) 12 (29) 12 (100) 21 (100) NA 10 (83) NAv 53 (100) 20 (100) 40 (100) 4 (11) NA Colon evaluation NA 10 (56) 21 (96) 23 (68) 43 (47) NAk NA 15 (52) 32 (100) NA 13 (65) 28 (93) 10 (26) 17 (41) 9 (75) NA 20 (100)t 9 (75) NA 43 (81) 16 (80) 40 (100) NA NA Colonic neoplasmb 9 (25)c 6 (33) 6 (27) 15 (44)f 16 (17)g 15 (39) 1 (6) 12 (41)m 18 (56) 4 (29)n 6 (30) 14 (47) 6 (16)r 16 (39) 3 (25) 5 (24) 5 (25) 8 (67) 14 (16) 27 (51) 11 (55) 18 (45)x 4 (11)y 54 (41) Colonic carcinoma 2 (6) 2 (11) 2 (9) 6 (18) 7 (8)h NA 1 (6) 8 (28) 3 (9) 0 (0) 3 (15) 1 (3) 3 (8) 3 (20) 2 (17) 1 (5) 2 (10) 3 (25) NA 7 (13) 3 (15)f 4 (10) 4 (11) NA Extra-colonic malignancy 1 (3)d 1 (6) 1 (5) NA 2 (2)i NA NA 4 (14) NA 0 (0) 1 (5)o 1 (3)q 3 (8) 10 (22)s NA NA NA NA 1 (1) 0 (0) NA NA 4 (11) 22 (17) Liver disease NA NA 1 (5) NA 48 (52)j NAl 4 (25) NA 1 (3) 3 (21)n 10 (50) 17 (57)j 9 (24) 5 (12) NA NA NA 1 (8)u NA 0 (0)w 4 (20) NA 7 (19) NA

Reference 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 53

The absolute number of patients with each characteristic is presented; this is expressed as a percentage of all patients with S. bovis bacteraemia in parentheses. NA, not applicable. a Only data on adult patients are presented; ve studies included children or infants but none developed colonic neoplasm or liver disease. b Any premalignant or malignant lesion. c One patient had caecal lymphoma. d Peritoneal carcinomatosis. e All studies where 100% of patients with S. bovis bacteraemia had endocarditis implies that this was a criterion for entry into study. f One colon cancer occurred before bacteraemia. g Of the 26 patients with S. bovis endocarditis, ve had colonic polyps and six had colon adenocarcinoma. h One patient had carcinoma 4 years after bacteraemia. i Patients had liver failure secondary to metastatic inltration (one breast cancer and one leukaemia). j Determined by serum chemistry; CT or ultrasound scans; and or liver biopsy. k Colonic evaluation carried out in 12 patients with S. bovis I bacteraemia but no gure for other S. bovis biotypes. l Nine patients had clinically evident cholecystitis, cholangitis, or pathologically documented cirrhosis. m Three patients with incomplete gastrointestinal evaluation had colonic masses thought to be neoplasms, but biopsies were not performed. n All colonic neoplasms and liver disease were antecedent to the current episode of S. bovis endocarditis. o Pancreatic adenocarcinoma with metastasis to liver. p A total of 199 consecutive patients with infective endocarditis were included in the trial; 30 had S. bovis endocarditis. q One patient with liver failure had undergone previous partial hepatectomy for hepatocellular carcinoma. r None of the seven patients with endocarditis had evidence of colon cancer; one patient had evidence of colon polyps. s This study included 41 adults and four children; 10 patients out of all 45, including children, had an extra-colonic malignancy. t Fourteen patients had complete evaluation; six had partial evaluation. u Acute hepatic failure detected on presentation with bacteraemia; patient had history of alcoholic cirrhosis. v Only information given is that the initial diagnosis was S. bovis endocarditis in four out of 15 patients with gastrointestinal cancer. w Method of liver evaluation not specied. x Out of 20 patients, 18 had colon polyposis and four patients had colon cancer; no further details given. y Authors do not mention how many of the four patients with endocarditis, if any, had colon cancer.

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advised to be investigated for bowel pathology, specically cancer, after diagnosis of an episode of S. bovis bacteraemia endocarditis. If this is not possible in the acute setting, due to poor health or co-morbidity, it should be carried out at a later date. Tumours have been reported years after an episode of endocarditis [7,10,18]; therefore, patients with normal colonoscopy should still be considered a group at risk for developing colonic cancer, and repeat colonoscopies are advised. It is worth noting that some authors have attempted to identify a marker for the detection of colonic cancer based on the detection of S. bovis. There is no doubt that such a marker would be a useful diagnostic tool for early detection of colon cancer. Darjee and Gibb [38] tested 16 cancer patients and 16 age-matched controls by ELISA for antibodies against S. bovis; the cancer group had an increased mean antibody titre to S. bovis, but the test was of limited predictive value. Tjalsma et al. [39], however, found that S. bovis antigen proles could distinguish 11 out of 12 colon cancer patients from eight control subjects; antigen proles from E.coli were not diagnostic for colon cancer. Interestingly, colon cancer has also been reported in the presence of S. bovis infection from other sources, including: septic arthritis [40], infection postknee replacement [41], neck abscess [42], thoracic empyema [43] and even a surgical wound posttransvesical prostate resection for an adenoma [44]. In addition, although at a much lower prevalence, there have also been reports linking colon cancer with other streptococcus species, including: endocarditis from Streptococcus suis [45], Streptococcus faecalis [11], Streptococcus pneumonia [46] and Streptococcus equines [17], or bacteraemia with Streptococcus sanguis [47] and Streptococcus salivaris [19].
Pathophysiology of this association

prospective case-control study by Dubrow et al. [49], only two of 18 current adenoma patients (11%) were found to have S. bovis in their stool compared with 12 of 84 controls (14%). Another prospective controlled study, by Potter et al. [50], found no signicant difference in preoperative faecal carriage rates between the study (19 patients with colorectal cancer) and control (23 patients without malignancy) populations (11% vs 13%). Finally, Noreet et al. [51], in a prospective study, cultured S. bovis in only one stool sample out of 35 precolonoscopy samples from patients with suspected colorectal cancer. In addition, S. bovis was cultured from one of 33 adenomas biopsied, none of six adenocarcinomas and one of 40 biopsies from normal muscosa; these data did not support selective colonisation of colorectal neoplasms by S. bovis. In patients with liver disease, however, there may be an increased faecal carriage of S. bovis, culminating in entry to the portal venous system or passage from the portal to systemic circulation and bacteraemia [18]. Streptococcus bovis is also a low-grade pathogen capable of causing a chronic inammation in the colon, and chronic infection inammation may, in turn, also contribute to cancer development or carcinogenesis, when bacterial components interfere with cell function [52]. More recently, it has been suggested that it is the colonic lesions themselves that provide a specic niche for S. bovis, resulting in tumour-associated silent infections that only become apparent when patients become immuno-compromised, as in bacteraemia, or have coincidental cardiac valve lesions and develop endocarditis [39].
Streptococcus bovis, extra-colonic malignancy and liver disease

Despite the knowledge of this association for over ve decades, to date, there has been no satisfactory explanation. As early as 1979, Klein speculated the production of carcinogens by S. bovis that induced cancer [21]. More recently, it has been shown in animal models that the cell wall antigens of S. bovis stimulate the production of inammatory cytokines and promote premalignant lesions through the increased formation of hyper-neoplastic aberrant colonic crypts [48]. These cytokines promote vasodilatation and increased vascular permeability, which may potentially act as port of entry for the microbe. Interestingly, it has also been reported previously that the prevalence of S. bovis in faecal cultures is signicantly increased in patients with carcinoma of the colon (56%) compared with that of the controls (11%) [6]. However, this has not been conrmed by subsequent studies. In a

Although less common, some studies have also reported an association between S. bovis bacteraemia and extracolonic malignancy (see Table 2), at a variable incidence (122%). The most recent, a large prospective study over 20 years by Correidoira et al. [53], found 22 cases of noncolonic cancer in 133 patients (17%). The malignancies observed include: oesophageal carcinoma [20,21], gastric carcinoma [15,16,21,22], gastric lymphoma [21] and pancreatic carcinoma [24,27]. Two retrospective analyses also reported, between them, an association with duodenal, gallbladder, lung, ovarian and endometrial cancer [27], as well as vaginal carcinoma and acute myelogenous leukaemia [26]. Associations with other extra-colonic malignancies are also in the literature, as case reports, including: squamous cell carcinoma of the mouth [54], lymphosarcoma [12] and Kaposi sarcoma [55]. There is also an association between S. bovis bacteraemia endocarditis and liver disease; we found 12 studies

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reporting an incidence of between 3 and 57%. A recent prospective case-control study, by Tripodi et al. [25], also found that the prevalence of chronic liver disease among patients with S. bovis I endocarditis was signicantly higher than in those with endocarditis of another aetiology (60% vs 15.3%; P < 0.001). There are possible explanations for this association. Liver disease may result in altered hepatic secretion of bile salts and or secretory immunoglobulins [56], which may promote the translocation of bacteria from the intestinal lumen into the portal venous system [18]. Furthermore, portal hypertension may result in bypass of the hepatic reticulo-endothelial system and access to systemic circulation. It is also known that, in contrast to most ahaemolytic streptococci, S. bovis is able to grow in bile [57]; a property that renders it is able to survive in bile and cause acute infection, especially in the presence of preexisting biliary tract disease [36]. Given this association with liver disease, authors have proposed that, in the presence of S. bovis bacteraemia endocarditis, the liver as well as bowel should be fully investigated [18,25]. Indeed, some studies in this review report the simultaneous occurrence of liver disease and colon cancer in patients with S. bovis endocarditis bacteraemia [24]; Zarkin et al. [18] noting such an association in 27% of patients. Finally, it is worth mentioning that other benign gastro-intestinal diseases, like ulcerative colitis [58] or diverticular disease [15] have also been linked to S. bovis bacteraemia. In addition, a recent retrospective study, analysing the microbiology database, even reported an association with AIDS [26].

References
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Conclusions
Streptococcus bovis endocarditis and or septicaemia is an early clue to the likely presence of colorectal cancer and warrants rigorous investigation. Although the incidence is variable (667%), there is strong evidence for an association and it is important for clinicians to be aware of this, given the important implications for patient diagnosis and management. Clinicians should also be aware that S. bovis may be associated with extra-colonic malignancy or liver disease; in such cases, routine investigation or a low-index of suspicion is advisable. Several theories may explain the link between S. bovis endocarditis bacteraemia and colon cancer, including: the carcinogenic or premalignant properties of S. bovis cell wall antigens, chronic S. bovis infection and inammation, or tumour-associated silent S. bovis infection in colonic lesions. Further studies are required, however, to determine the precise pathophysiology of this relationship and ascertain whether S. bovis bacteraemia is an independent predictor of malignancy.

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