- Email: [email protected]
Eggerthella lenta bacteremia in solid tumor cancer patients: Pathogen or witness of frailty?
Anaerobe 47 (2017) 70e72
Contents lists available at ScienceDirect
Anaerobe journal homepage: www.elsevier.com/locate/anaerobe
Clinical microbiology
Eggerthella lenta bacteremia in solid tumor cancer patients: Pathogen or witness of frailty? Paul-Louis Woerther a, *, Sami Antoun b, Elisabeth Chachaty a, Mansouria Merad b a b
Department of Microbiology, Gustave Roussy Cancer Campus, Villejuif, France Oncology Emergency Department, Gustave Roussy Cancer Campus, Villejuif, France
a r t i c l e i n f o
a b s t r a c t
Article history: Received 31 January 2017 Received in revised form 27 March 2017 Accepted 20 April 2017 Available online 22 April 2017
Eggerthella lenta is increasingly found in patients with severe comorbidities. Because oncologic patients are exposed to emerging pathogens, we aimed to describe the factors associated with E. lenta bacteremia in this immunosuppressed population. Oncology patients with blood cultures positive for E. lenta were retrospectively recorded from 2009 to 2015. Socio-demographic and medical/biological data as well as potential risk factors and mortality were recorded and analyzed. Twenty-three patients were included. Gastro intestinal (GI) and gynecological cancers were reported in 12/23 (52%) and 7/23 cases (30%), respectively. Eleven/23 patients (48%) had metastatics lesions and 6/ 23 (26%) had peritoneal carcinomatosis. No associated tissue infection was found in 14/23 cases (61%). Blood cultures yielded at least one other species in addition to E. lenta in 10/23 cases (43%). Mortality associated with E. lenta bacteremia was 22% (5/23). E. lenta bacteremia often occurred in patients with advanced cancer disease without documented infection. In most of the cases, intestinal obstruction and/or isolated fever were the only recorded symptoms. In these cases, the damages of intestinal barrier induced by the cancer and/or its specific treatments may be the cause of bacterial translocation. © 2017 Elsevier Ltd. All rights reserved.
Handling Editor: Elisabeth Nagy Keywords: Eggerthella lenta bacteremia Oncology patients Gastro-intestinal tract frailty
Eggerthella lenta is an anaerobic non-sporuling Gram positive bacillus belonging to the Coriobacteriaceae family [1]. Because E. Lenta is part of the normal human intestinal microbiota, bacteremia due to this species generally originate from the gastrointestinal tract (GIT). Although rarely identified in blood cultures, E. lenta is increasingly found in patients with severe comorbidities. A combination of factors might induce oncological patients to be exposed to emerging pathogens. These factors include immunosuppression, mucosal barrier damage related to drugs toxicities, surgery or advancement of the cancer disease. In order to describe the clinical features, the associated factors and the outcome of E. lenta bacteremia in oncological settings, we conducted a retrospective study at the Gustave Roussy Institute, a 400-bed tertiary cancer center. From 2009 to 2015, blood cultures positive for E. lenta were recorded. Blood specimens were collected in FA and FN bottles and placed into the BacT/Alert 3D blood culture
* Corresponding author. Centre hospitalier Universitaire Henri Mondor, 51, chal de Lattre de Tassigny, 94010 Cre teil cedex, France. Avenue du Mare E-mail address: [email protected] (P.-L. Woerther). http://dx.doi.org/10.1016/j.anaerobe.2017.04.010 1075-9964/© 2017 Elsevier Ltd. All rights reserved.
rieux, Marcy-l’Etoile, France) for a total of 5 instrument (bio-Me days. Identification of the strains was performed with the VITEK2 rieux, Marcy l’Etoile, France) until March 2014 and system (bio-Me with the LT-2 Maldi-Tof system (Andromas, Paris, France) thereafter. Antibiotic susceptibility testing was determined using the disk-diffusion method, as described (http://www.sfm. microbiologie.org). Collected data included socio demographic, medical and biological data, immunosuppression (long-term corticotherapy, hemopathy and diabetes) potential risk factors (surgery, recent endoscopy or interventional radiology), outcomes and 30-day overall mortality. Data were independently collected by a microbiologist (PLW) and a clinician (MM). When the conclusions differed, the opinion of another clinician (SA) was asked. The protocol of the study was reviewed and approved by the Institutional Review Board of the Gustave Roussy Institute. A total of 23 patients took part in our study (Table 1). Median age was 57 years and 11 (48%) of the patients were men. GIT cancers and gynecological cancers were reported in 12 (52%) and 7 cases (30%), respectively. Eleven patients (48%) had metastatic lesions and 6 (26%) had peritoneal carcinomatosis. Infection was diagnosed in 9 cases (39%),
Table 1 Characteristic of the 23 included patients. Patients
Biology clinical symptoms
underlying cancer
stage of diseasea
m
63
colon
PC
f m f f
57 52 51 59
ovarian colon ovarian sarcomas
m
63
rectum
m
71
rectum
intestinal occlusion locoregional fever locoregional none PC þ metastasis peritonitis PC þ metastasis intestinal occlusion locoregional stomial dysfunction metastasis peritonitis
f
49
uterine
locoregional
m
52
sacromas
f
76
f
51
cholangiocarcinoma gastric
a
Treatment
(ly)/mm3 CRP level mg/L
polybacterial blood immuno culture suppression
previous surgery
Current antibioticsb
Surgical procedures
Mortality (D30)
8800
600
43
no
corticotherapy
no
no
gastrostomy
no
5400 6800 13300 26200
100 900 700 600
132 275 233 89
no no no yes
hemopathy no no no
yes yes yes no
IPM na IPM CRO
intestinal resection no pelvic collection drainage no
no no no yes
9300
1000
36
yes
no
yes
na
ostomy ile
no
700
400
235
no
no
no
TZP
peritoneal yes drainage þ intestinal resection intestinal resection no
4500
500
143
yes
diabetes
no
na
local
intestinal occlusion septic shock
24200
200
299
no
no
yes
na
metastasis
angiocholitis
8500
1300
97
yes
no
no
na
na
476
yes
7400 2100 7100 4100 22300 14700
1000 200 1100 200 1100 600
272 55 76 137 171 353
no yes no no yes yes
corticotherapy/ diabetes diabetes no no no no no
17000 11200
1100 na
168 28
no yes
38700
2000
281
2100 28800 8800
900 0 700
109 334 135
12364 [700 e38700]
724 [0 e2000]
182 [28 e476]
intestinal occlusion m 68 colon local peritonitis m 60 rectum metastasis none m 53 rectum PC þ metastasis anal abcess f 64 ovarian PC septic shock m 48 gastric local anal abcess f 56 gastric locoregional abdominal evisceration m 75 renal metastasis rectorragy f 49 appendicular PC abdominal wall abcess f 52 uterine locoregional intestinal occlusion f 62 colon metastasis fever m 48 sarcoma metastasis fever f 57 sarcoma metastasis intestinal occlusion Averages and ranges of laboratory results
b
Risk factors
(PMNL)/mm3
metastasis
CRO
retroperinoneal collection drainage biliary tract drainage
no no
no
TZP
no
yes
yes yes no no yes yes
TZP þ AN AMC na TZP CRO þ MTZ TZP þ MTZ
sigmoid ectomy no anal abcess drainage no no no
yes no no no no no
corticotherapy no
no yes
na no
no no
no no
no
corticotherapy
no
TZP þ MTZ
no
yes
no no yes
diabetes corticotherapy no
no no no
TZP TZP TZP
colostomy no no
no no no
P.-L. Woerther et al. / Anaerobe 47 (2017) 70e72
gender age (yrs)
PC: peritoneal carcinomatosis. na: information not available; IPM: imipenem; CRO: ceftriaxone (third generation cephalosporin); TZP: piperacillin þ tazobactam; AN: amikacin; AMP: penicillin; MTZ: metronidazole.
71
72
P.-L. Woerther et al. / Anaerobe 47 (2017) 70e72
including peritonitis (n ¼ 3), abdominal abscess (n ¼ 3), septic shock (n ¼ 2) and angiocholitis (n ¼ 1). In the 14 other cases (61%), intestinal obstruction (n ¼ 6), fever (n ¼ 3) or other non-specific symptoms (n ¼ 5) were the only symptoms. Association with immunosuppression was found in 39% of the cases (n ¼ 9). Blood cultures yielded at least one other species in addition to E. lenta in 43% of the cases (n ¼ 10). The bacteria isolated belonged to Enterobacteriaceae (Escherichia coli: three cases; Klebsiella pneumoniae: three cases), Gram positive cocci (Enterococcus faecalis: one case; Streptococcus constellatus: one case) and/or strict anaerobic bacteria (Bacteroides vulgatus: 1 case; Bacteroides ovatus: two cases; Bacteroides sp.: one case; Clostridium ramosum: one case; Bacteroides fragilis: one case). More than one species was found in addition to E. lenta in two cases. Data about antimicrobial treatment were available in 17 cases. In 9/17 (53%) of them, patients had been treated with piperacillin/tazobactam. In 2 of the cases, the administered antibiotics were not efficient against E. lenta (ceftriaxone: two cases). In our hospital, efficient antibiotic treatment is usually given for a total duration of 8e10 days, in absence of complication. Surgical procedure was required in 11/23 cases (48%). The 30-days crude mortality reached 5/23 patients (22%). In the other cases, bacteremia was stopped and the outcome was mainly linked to the underlying cancer disease. All the E. lenta strains were susceptible to piperacillin/tazobactam, imipenem/cilastatin and metronidazole. E. lenta bacteremia has been associated with a wide spectrum of infections linked to serious GIT pathologies. The severity of the prognosis associated with E. lenta bacteremia has already been underlined in a cohort of 25 patients [2]. More recently, a retrospective study of 33 patients has pointed the gastrointestinal infections as a major risk factor to develop E. lenta bacteremia (27/33; 82%) [3]. Regarding the patient's risk factors, the authors found that more than one half of the cohort presented a chronic gastrointestinal pathology (19/33; 57.6%). Immunosuppression, diabetes and renal failure were present in 5/33 (15%), 9/33 (27%) and 12/33 (36%) of the cases, respectively, suggesting the involvement of immunosuppression in the pathogenesis of E. lenta bacteremia. Association with malignancy was found in 14/33 of the cases (43%). Among the few published cases of E. lenta bacteremia, a possible association with cancer has already been noticed [4]. In a series of 7 cases with E. lenta bacteremia, association with cancer was found in 4/7 of the cases (57%) before steroid treatment, diabetes and kidney terminal insufficiency (2, 1 and 2 cases, respectively) [5]. In our study
focused on oncological patients, E. lenta bacteremia was found in almost half of the cases in absence of any identified infected site. Intestinal obstruction and/or fever were the most common clinical presentation. These patients didn't present other known factors of translocation: they were not neutropenic and didn't present any symptoms of diarrhea or mucositis. E. lenta is a rare cause of bacteremia and studies covering this subject are limited. Our results, obtained from the study of a retrospective cohort of 23 oncology patients over a 7-years period, showed that E. lenta occurred infrequently in patients with immunosuppression and advanced cancer disease. In nearly two third of these cases, bacteremia occurred in absence of documented infection. Although septic shock was noted in two cases, intestinal obstruction and/or isolated fever were most of the time the only recorded symptoms. These results are in accordance with the current trends showing the increase of involvement of anaerobic bacteria in oncology patient's bacteremia, even in absence of any clinical infectious focus [6,7]. In these cases, the damages of intestinal barrier induced by the cancer and/or its specific treatments could be the most likely cause of bacterial translocation from the GIT. References [1] W.G. Wade, J. Downes, D. Dymock, S.J. Hiom, A.J. Weightman, F.E. Dewhirst, et al., The family Coriobacteriaceae: reclassification of Eubacterium exiguum (Poco et al. 1996) and Peptostreptococcus heliotrinreducens (Lanigan 1976) as Slackia exigua gen. nov., comb. nov. and Slackia heliotrinireducens gen. nov., comb. nov., and Eubacterium lentum (Prevot 1938) as Eggerthella lenta gen. nov., comb. nov, Int. J. Syst. Bacteriol. 49 (Pt 2) (1999) 595e600. [2] A.A. Venugopal, S. Szpunar, L.B. Johnson, Risk and prognostic factors among patients with bacteremia due to Eggerthella lenta, Anaerobe 18 (2012) 475e478. [3] B.J. Gardiner, A.Y. Tai, D. Kotsanas, M.J. Francis, S.A. Roberts, S.A. Ballard, et al., Clinical and microbiological characteristics of Eggerthella lenta bacteremia, J. Clin. Microbiol. 53 (2015) 626e635. [4] D. Wong, F. Aoki, E. Rubinstein, Bacteremia caused by Eggerthella lenta in an elderly man with a gastrointestinal malignancy: a case report, Can. J. Infect. Dis. Med. Microbiol. 25 (2014) e85e6. [5] M.R. Lee, Y.T. Huang, C.H. Liao, T.Y. Chuang, W.J. Wang, S.W. Lee, et al., Clinical and microbiological characteristics of bacteremia caused by Eggerthella, Paraeggerthella, and Eubacterium species at a university hospital in Taiwan from 2001 to 2010, J. Clin. Microbiol. 50 (2012) 2053e2055. [6] I. Brook, The role of anaerobic bacteria in bacteremia, Anaerobe 16 (2010) 183e189. [7] S. Spanik, J. Trupl, A. Kunova, P. Pichna, L. Helpianska, I. Ilavska, et al., Bloodstream infections due to anaerobic bacteria in cancer patients: epidemiology, etiology, risk factors, clinical presentation and outcome of anaerobic bacteremia, Neoplasma 43 (1996) 235e238.
Contents lists available at ScienceDirect
Anaerobe journal homepage: www.elsevier.com/locate/anaerobe
Clinical microbiology
Eggerthella lenta bacteremia in solid tumor cancer patients: Pathogen or witness of frailty? Paul-Louis Woerther a, *, Sami Antoun b, Elisabeth Chachaty a, Mansouria Merad b a b
Department of Microbiology, Gustave Roussy Cancer Campus, Villejuif, France Oncology Emergency Department, Gustave Roussy Cancer Campus, Villejuif, France
a r t i c l e i n f o
a b s t r a c t
Article history: Received 31 January 2017 Received in revised form 27 March 2017 Accepted 20 April 2017 Available online 22 April 2017
Eggerthella lenta is increasingly found in patients with severe comorbidities. Because oncologic patients are exposed to emerging pathogens, we aimed to describe the factors associated with E. lenta bacteremia in this immunosuppressed population. Oncology patients with blood cultures positive for E. lenta were retrospectively recorded from 2009 to 2015. Socio-demographic and medical/biological data as well as potential risk factors and mortality were recorded and analyzed. Twenty-three patients were included. Gastro intestinal (GI) and gynecological cancers were reported in 12/23 (52%) and 7/23 cases (30%), respectively. Eleven/23 patients (48%) had metastatics lesions and 6/ 23 (26%) had peritoneal carcinomatosis. No associated tissue infection was found in 14/23 cases (61%). Blood cultures yielded at least one other species in addition to E. lenta in 10/23 cases (43%). Mortality associated with E. lenta bacteremia was 22% (5/23). E. lenta bacteremia often occurred in patients with advanced cancer disease without documented infection. In most of the cases, intestinal obstruction and/or isolated fever were the only recorded symptoms. In these cases, the damages of intestinal barrier induced by the cancer and/or its specific treatments may be the cause of bacterial translocation. © 2017 Elsevier Ltd. All rights reserved.
Handling Editor: Elisabeth Nagy Keywords: Eggerthella lenta bacteremia Oncology patients Gastro-intestinal tract frailty
Eggerthella lenta is an anaerobic non-sporuling Gram positive bacillus belonging to the Coriobacteriaceae family [1]. Because E. Lenta is part of the normal human intestinal microbiota, bacteremia due to this species generally originate from the gastrointestinal tract (GIT). Although rarely identified in blood cultures, E. lenta is increasingly found in patients with severe comorbidities. A combination of factors might induce oncological patients to be exposed to emerging pathogens. These factors include immunosuppression, mucosal barrier damage related to drugs toxicities, surgery or advancement of the cancer disease. In order to describe the clinical features, the associated factors and the outcome of E. lenta bacteremia in oncological settings, we conducted a retrospective study at the Gustave Roussy Institute, a 400-bed tertiary cancer center. From 2009 to 2015, blood cultures positive for E. lenta were recorded. Blood specimens were collected in FA and FN bottles and placed into the BacT/Alert 3D blood culture
* Corresponding author. Centre hospitalier Universitaire Henri Mondor, 51, chal de Lattre de Tassigny, 94010 Cre teil cedex, France. Avenue du Mare E-mail address: [email protected] (P.-L. Woerther). http://dx.doi.org/10.1016/j.anaerobe.2017.04.010 1075-9964/© 2017 Elsevier Ltd. All rights reserved.
rieux, Marcy-l’Etoile, France) for a total of 5 instrument (bio-Me days. Identification of the strains was performed with the VITEK2 rieux, Marcy l’Etoile, France) until March 2014 and system (bio-Me with the LT-2 Maldi-Tof system (Andromas, Paris, France) thereafter. Antibiotic susceptibility testing was determined using the disk-diffusion method, as described (http://www.sfm. microbiologie.org). Collected data included socio demographic, medical and biological data, immunosuppression (long-term corticotherapy, hemopathy and diabetes) potential risk factors (surgery, recent endoscopy or interventional radiology), outcomes and 30-day overall mortality. Data were independently collected by a microbiologist (PLW) and a clinician (MM). When the conclusions differed, the opinion of another clinician (SA) was asked. The protocol of the study was reviewed and approved by the Institutional Review Board of the Gustave Roussy Institute. A total of 23 patients took part in our study (Table 1). Median age was 57 years and 11 (48%) of the patients were men. GIT cancers and gynecological cancers were reported in 12 (52%) and 7 cases (30%), respectively. Eleven patients (48%) had metastatic lesions and 6 (26%) had peritoneal carcinomatosis. Infection was diagnosed in 9 cases (39%),
Table 1 Characteristic of the 23 included patients. Patients
Biology clinical symptoms
underlying cancer
stage of diseasea
m
63
colon
PC
f m f f
57 52 51 59
ovarian colon ovarian sarcomas
m
63
rectum
m
71
rectum
intestinal occlusion locoregional fever locoregional none PC þ metastasis peritonitis PC þ metastasis intestinal occlusion locoregional stomial dysfunction metastasis peritonitis
f
49
uterine
locoregional
m
52
sacromas
f
76
f
51
cholangiocarcinoma gastric
a
Treatment
(ly)/mm3 CRP level mg/L
polybacterial blood immuno culture suppression
previous surgery
Current antibioticsb
Surgical procedures
Mortality (D30)
8800
600
43
no
corticotherapy
no
no
gastrostomy
no
5400 6800 13300 26200
100 900 700 600
132 275 233 89
no no no yes
hemopathy no no no
yes yes yes no
IPM na IPM CRO
intestinal resection no pelvic collection drainage no
no no no yes
9300
1000
36
yes
no
yes
na
ostomy ile
no
700
400
235
no
no
no
TZP
peritoneal yes drainage þ intestinal resection intestinal resection no
4500
500
143
yes
diabetes
no
na
local
intestinal occlusion septic shock
24200
200
299
no
no
yes
na
metastasis
angiocholitis
8500
1300
97
yes
no
no
na
na
476
yes
7400 2100 7100 4100 22300 14700
1000 200 1100 200 1100 600
272 55 76 137 171 353
no yes no no yes yes
corticotherapy/ diabetes diabetes no no no no no
17000 11200
1100 na
168 28
no yes
38700
2000
281
2100 28800 8800
900 0 700
109 334 135
12364 [700 e38700]
724 [0 e2000]
182 [28 e476]
intestinal occlusion m 68 colon local peritonitis m 60 rectum metastasis none m 53 rectum PC þ metastasis anal abcess f 64 ovarian PC septic shock m 48 gastric local anal abcess f 56 gastric locoregional abdominal evisceration m 75 renal metastasis rectorragy f 49 appendicular PC abdominal wall abcess f 52 uterine locoregional intestinal occlusion f 62 colon metastasis fever m 48 sarcoma metastasis fever f 57 sarcoma metastasis intestinal occlusion Averages and ranges of laboratory results
b
Risk factors
(PMNL)/mm3
metastasis
CRO
retroperinoneal collection drainage biliary tract drainage
no no
no
TZP
no
yes
yes yes no no yes yes
TZP þ AN AMC na TZP CRO þ MTZ TZP þ MTZ
sigmoid ectomy no anal abcess drainage no no no
yes no no no no no
corticotherapy no
no yes
na no
no no
no no
no
corticotherapy
no
TZP þ MTZ
no
yes
no no yes
diabetes corticotherapy no
no no no
TZP TZP TZP
colostomy no no
no no no
P.-L. Woerther et al. / Anaerobe 47 (2017) 70e72
gender age (yrs)
PC: peritoneal carcinomatosis. na: information not available; IPM: imipenem; CRO: ceftriaxone (third generation cephalosporin); TZP: piperacillin þ tazobactam; AN: amikacin; AMP: penicillin; MTZ: metronidazole.
71
72
P.-L. Woerther et al. / Anaerobe 47 (2017) 70e72
including peritonitis (n ¼ 3), abdominal abscess (n ¼ 3), septic shock (n ¼ 2) and angiocholitis (n ¼ 1). In the 14 other cases (61%), intestinal obstruction (n ¼ 6), fever (n ¼ 3) or other non-specific symptoms (n ¼ 5) were the only symptoms. Association with immunosuppression was found in 39% of the cases (n ¼ 9). Blood cultures yielded at least one other species in addition to E. lenta in 43% of the cases (n ¼ 10). The bacteria isolated belonged to Enterobacteriaceae (Escherichia coli: three cases; Klebsiella pneumoniae: three cases), Gram positive cocci (Enterococcus faecalis: one case; Streptococcus constellatus: one case) and/or strict anaerobic bacteria (Bacteroides vulgatus: 1 case; Bacteroides ovatus: two cases; Bacteroides sp.: one case; Clostridium ramosum: one case; Bacteroides fragilis: one case). More than one species was found in addition to E. lenta in two cases. Data about antimicrobial treatment were available in 17 cases. In 9/17 (53%) of them, patients had been treated with piperacillin/tazobactam. In 2 of the cases, the administered antibiotics were not efficient against E. lenta (ceftriaxone: two cases). In our hospital, efficient antibiotic treatment is usually given for a total duration of 8e10 days, in absence of complication. Surgical procedure was required in 11/23 cases (48%). The 30-days crude mortality reached 5/23 patients (22%). In the other cases, bacteremia was stopped and the outcome was mainly linked to the underlying cancer disease. All the E. lenta strains were susceptible to piperacillin/tazobactam, imipenem/cilastatin and metronidazole. E. lenta bacteremia has been associated with a wide spectrum of infections linked to serious GIT pathologies. The severity of the prognosis associated with E. lenta bacteremia has already been underlined in a cohort of 25 patients [2]. More recently, a retrospective study of 33 patients has pointed the gastrointestinal infections as a major risk factor to develop E. lenta bacteremia (27/33; 82%) [3]. Regarding the patient's risk factors, the authors found that more than one half of the cohort presented a chronic gastrointestinal pathology (19/33; 57.6%). Immunosuppression, diabetes and renal failure were present in 5/33 (15%), 9/33 (27%) and 12/33 (36%) of the cases, respectively, suggesting the involvement of immunosuppression in the pathogenesis of E. lenta bacteremia. Association with malignancy was found in 14/33 of the cases (43%). Among the few published cases of E. lenta bacteremia, a possible association with cancer has already been noticed [4]. In a series of 7 cases with E. lenta bacteremia, association with cancer was found in 4/7 of the cases (57%) before steroid treatment, diabetes and kidney terminal insufficiency (2, 1 and 2 cases, respectively) [5]. In our study
focused on oncological patients, E. lenta bacteremia was found in almost half of the cases in absence of any identified infected site. Intestinal obstruction and/or fever were the most common clinical presentation. These patients didn't present other known factors of translocation: they were not neutropenic and didn't present any symptoms of diarrhea or mucositis. E. lenta is a rare cause of bacteremia and studies covering this subject are limited. Our results, obtained from the study of a retrospective cohort of 23 oncology patients over a 7-years period, showed that E. lenta occurred infrequently in patients with immunosuppression and advanced cancer disease. In nearly two third of these cases, bacteremia occurred in absence of documented infection. Although septic shock was noted in two cases, intestinal obstruction and/or isolated fever were most of the time the only recorded symptoms. These results are in accordance with the current trends showing the increase of involvement of anaerobic bacteria in oncology patient's bacteremia, even in absence of any clinical infectious focus [6,7]. In these cases, the damages of intestinal barrier induced by the cancer and/or its specific treatments could be the most likely cause of bacterial translocation from the GIT. References [1] W.G. Wade, J. Downes, D. Dymock, S.J. Hiom, A.J. Weightman, F.E. Dewhirst, et al., The family Coriobacteriaceae: reclassification of Eubacterium exiguum (Poco et al. 1996) and Peptostreptococcus heliotrinreducens (Lanigan 1976) as Slackia exigua gen. nov., comb. nov. and Slackia heliotrinireducens gen. nov., comb. nov., and Eubacterium lentum (Prevot 1938) as Eggerthella lenta gen. nov., comb. nov, Int. J. Syst. Bacteriol. 49 (Pt 2) (1999) 595e600. [2] A.A. Venugopal, S. Szpunar, L.B. Johnson, Risk and prognostic factors among patients with bacteremia due to Eggerthella lenta, Anaerobe 18 (2012) 475e478. [3] B.J. Gardiner, A.Y. Tai, D. Kotsanas, M.J. Francis, S.A. Roberts, S.A. Ballard, et al., Clinical and microbiological characteristics of Eggerthella lenta bacteremia, J. Clin. Microbiol. 53 (2015) 626e635. [4] D. Wong, F. Aoki, E. Rubinstein, Bacteremia caused by Eggerthella lenta in an elderly man with a gastrointestinal malignancy: a case report, Can. J. Infect. Dis. Med. Microbiol. 25 (2014) e85e6. [5] M.R. Lee, Y.T. Huang, C.H. Liao, T.Y. Chuang, W.J. Wang, S.W. Lee, et al., Clinical and microbiological characteristics of bacteremia caused by Eggerthella, Paraeggerthella, and Eubacterium species at a university hospital in Taiwan from 2001 to 2010, J. Clin. Microbiol. 50 (2012) 2053e2055. [6] I. Brook, The role of anaerobic bacteria in bacteremia, Anaerobe 16 (2010) 183e189. [7] S. Spanik, J. Trupl, A. Kunova, P. Pichna, L. Helpianska, I. Ilavska, et al., Bloodstream infections due to anaerobic bacteria in cancer patients: epidemiology, etiology, risk factors, clinical presentation and outcome of anaerobic bacteremia, Neoplasma 43 (1996) 235e238.