Peritonitis caused by Bifidobacterium longum: Case report and literature review

Peritonitis caused by Bifidobacterium longum: Case report and literature review

Anaerobe 27 (2014) 27e30 Contents lists available at ScienceDirect Anaerobe journal homepage: www.elsevier.com/locate/anaerobe Clinical microbiolog...

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Anaerobe 27 (2014) 27e30

Contents lists available at ScienceDirect

Anaerobe journal homepage: www.elsevier.com/locate/anaerobe

Clinical microbiology

Peritonitis caused by Bifidobacterium longum: Case report and literature review Daniel Tena a, *, Cristina Losa a, María José Medina b, Juan Antonio Sáez-Nieto b a

Sección de Microbiología, Hospital Universitario de Guadalajara, C/. Donante de sangre s/n, 19002 Guadalajara, Spain Servicio de Bacteriología, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Carretera de Majadahonda-Pozuelo Km 2, 28220 Majadahonda, Madrid, Spain b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 22 January 2014 Received in revised form 3 March 2014 Accepted 3 March 2014 Available online 19 March 2014

Bifidobacterium spp. rarely causes human infections. We report a case of a 42-year-old man with a history of pancolonic diverticulosis, who suffered a purulent peritonitis caused by Bifidobacterium longum secondary to intestinal perforation. Clinical outcome was good after urgent surgery and antibiotic treatment with imipenem and amoxicillin/clavulanic acid. Our case shows that Bifidobacterium spp. should be considered as a cause of peritonitis, especially in patients with risk of intestinal perforation. The review of the literature shows that these organisms can cause a wide spectrum of severe infections, especially in patients with underlying diseases. Infections caused by Bifidobacterium spp. may be overlooked or underreported since it may be considered normal microbiota. Ó 2014 Elsevier Ltd. All rights reserved.

Keywords: Peritonitis Bifidobacteria Bifidobacterium longum Probiotic

1. Introduction

2. Case report

Bifidobacterium spp. are nonsporulating anaerobic Grampositive rods that are part of the commensal flora of the mouth, gastrointestinal tract and female genital tract [1]. Most of the species of the genus Bifidobacterium have been considered nonpathogenic for humans. However, the clinical significance of most species is unclear. Three species, Bifidobacterium dentium, Bifidobacterium inopinatum, and Bifidobacterium denticolens, have been found in dental caries, and B. dentium may actually contribute to pathogenicity in these cases [2]. Some of the species, such as Bifidobacterium breve, Bifidobacterium longum, Bifidobacterium infantis and Bifidobacterium lactis, are used as probiotics for health benefits in the human gastrointestinal tract, especially in maintaining the intestinal microbial balance by inhibiting the growth of potential pathogens [3]. Little is known about the pathogenic potential of the bifidobacteria because these organisms have been rarely implicated in human infections. In the present report, we describe a case of acute peritonitis caused by B. longum secondary to intestinal perforation. In addition, we review the human infections caused by these organisms with available information.

A 42-year-old man presented with a history of acute abdominal pain of sudden onset and intensive sweating. His medical history was unremarkable. On admission the patient appeared conscious with bad general aspect. On initial physical examination, he had the following vital signs: blood pressure of 136/95 mmHg, pulse of 118 beats/min, respiratory rate of 20 breaths/min, oxygen saturation of 97% on ambient air and temperature of 36  C. Abdominal examination showed rebound tenderness, distension and intensive pain in mesogastrium and hypogastrium. Blood parameters revealed the following values: hemoglobin 15.1 g/dl, hematocrit 45.4%, white blood cells 16.960/mm3 (neutrophils 91%, lymphocytes 3.6%, monocytes 5.2%) and platelets 272.000/mm3. Abdominopelvic ultrasound showed abundant free fluid located on the abdominal cavity. Examination with contrast-enhanced computed tomography revealed pancolonic diverticulosis with inflammatory signs on the sigmoid colon, perforation on the top edge of the transverse colon, pneumoperitoneum and peritoneal fluid. A diagnosis of perforated sigmoid diverticulitis was made. Urgent surgery was performed and confirmed the presence of fecal peritonitis. He underwent colectomy and colostomy performed by the Hartmann’s procedure with washing and drainage of the abdominal cavity. Surgical prophylaxis was carried out with a single dose of intravenous amoxicillin/clavulanic acid (2 g). A sample of the peritoneal fluid was obtained for culture. Blood samples were not taken for

* Corresponding author. Tel.: þ34 949 209236; fax: þ34 949 209213. E-mail addresses: [email protected], [email protected] (D. Tena). http://dx.doi.org/10.1016/j.anaerobe.2014.03.005 1075-9964/Ó 2014 Elsevier Ltd. All rights reserved.

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Table 1 Clinical and microbiological data of patients with infections caused by Bifidobacterium species. Author (year)

Age/sex

Underlying conditions

Source of infection

Clinical presentation

Source of isolate

Microorganism isolated

Method used for identification

Mixed infectiona

Antibiotic therapy

Outcome

Georg et al., 1964 Thomas et al., 1974

37/M

Diabetes mellitus

ND

Lung abscess

No

Hematogenous spread

Pneumonia

GLC

No

Penicillin, tetracyclineb Penicillin, ampicillin

Cured

Smoking history

Bifidobacterium eriksonii Bifidobacterium eriksonii

GLC

33/M

Gorbach et al., 1974

ND

ND

ND

Pelvic abscess

Aspirate from abscess Sputum, throat, pleural fluid, lung tissue Aspirate from abscess

Bifidobacterium spp.

GLC

Bourne et al., 1978 Bourne et al., 1978

24/F

Pregnancy

ND

Bacteremia

Blood

GLC

58/M

Bowel obstruction, rectal cancer

ND

Bacteremia

Blood

Bifidobacterium spp. Bifidobacterium eriksonii

Yes (Peptococcus spp., Bacteroides fragilis, Eubacterium lentum, Veillonella spp.) No

GLC

No

Bourne et al., Bourne et al., Bourne et al., Bourne et al., Bourne et al., Bourne et al.,

39/F

Cholecystectomy

ND

Bacteremia

Blood

GLC

35/F

Pregnancy

ND

Bacteremia

Blood

29/F

Pregnancy

ND

Bacteremiac

Blood

21/F

Pregnancy

ND

Bacteremia

Blood

Bifidobacterium eriksonii Bifidobacterium eriksonii Bifidobacterium eriksonii Bifidobacterium eriksonii Bifidobacterium spp. Bifidobacterium spp.

1978 1978

1978 d

Blood

Clindamycin

Cured

None

Cured Died

No

Ampicillin, kanamycin, cephalothin None

Cured

GLC

No

Ampicillin

Cured

GLC

GLC

No

Ampicillin, kanamycin Ampicillin, kanamycin Ampicillin, gentamicin Oxacillin

Cured

GLC

Yes (Bacteroides fragilis) Yes (Peptostreptococcus spp.) No

GLC

Cured Cured

31/F

Pregnancy

ND

Bacteremia

24/F

Multiple abscess, systemic lupus erythematous Peritonitis, diverticulosis, systemic lupus erythematous Alcoholism, periodontal disease

ND

Bacteremia

Blood

ND

Bacteremia

Blood

Bifidobacterium adolescentis

GLC

No

Ampicillin, gentamicin, cephalothin

Died

Aspiration of oral secretions

Lung abscess, empyema, necrotizing pneumonia

Pus from thoracocentesis, pulmonar aspirate from necropsy Pus from abscess

Bifidobacterium eriksonii

ND

No

Penicillin þ kanamycine

Died

Bifidobacterium spp.

ND

Yes (Streptococcus milleri)

Penicillinf

Yes (Bacteroides ureolyticus, Streptococcus milleri, b-hemolytic streptococcus, Gram-positive rods) No

Clindamycin þ ceftriaxone

Cured with sequel (quadriparesis) Died

1978 1978

Bourne et al., 1978

60/F

Green, 1978

52/M

Cryan et al., 1991

57/F

Non-specific neck pain

Diagnostic discography

Epidural abscess

Epstein et al., 1992

63/M

Amelanotic melanoma, iatrogenic mediastinitis

Transbronchial needle aspiration

Pericarditis

Pericardial catheter drainage

Bifidobacterium spp.

ND

Ha et al., 1999

19/M

Acupuncture therapy

Sepsis

Blood

Bifidobacterium longum

GLC

Ohishi et al., 2010

0g/F

Herniated intervertebral disk, laminectomy Surgery for omphalocele

Sepsis

Blood

Bifidobacterium breve

Randomly amplified polymorphic DNA analysis

Jenke et al., 2012

0g/ND

Administration of probiotic (Bifidobacterium breve BBG-01) Administration of probiotic

Sepsis

Blood

Bifidobacterium infantis, Bifidobacterium longum

Mass spectrometry, strain-specific PCR

Prematurity, low-birthweight

Cured

Ticarcillin þ metronidazole

Cured

No

Meropenem þ amikacin

Cured

No

Cefotaxime þ vancomycin

Cured

D. Tena et al. / Anaerobe 27 (2014) 27e30

1978

Cured

Cured Imipenem, Amoxicillin/ clavulanic acid No 42/M PR

M: male; F: female; ND: no data; PR: present report; GLC: Gaseliquid chromatography; PCR: Polymerase chain reaction. a In parenthesis: other microorganisms isolated. b Antibiotic treatment associated with drainage. c Septic shock 5 days postpartum. d Fever 2 days postpartum. e Antibiotic treatment associated with drainage. f Antibiotic treatment associated with cervical laminectomy. g Neonate.

Sequence analysis of the 16S rRNA gene Bifidobacterium longum Peritoneal fluid Perforated sigmoid diverticulitis

Peritonitis

Bifidobacterium scardovii 80/F Barberis et al., 2012

Breast cancer, autoinmune hemolytic anemia, treatment with methylprednisolone Pancolonic diverticulosis

ND

Recurrent urinary infection

Urine

Sequence analysis of the 16S rRNA gene

No

Ampicilline sulbactam

Recurrence

D. Tena et al. / Anaerobe 27 (2014) 27e30

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culture. Empirical intravenous antimicrobial therapy with 1 g of imipenem every 8 h was started. The Gram stain of the peritoneal fluid revealed leukocytes and non-spore-forming Gram-positive rods. The sample was cultured on blood agar, chocolate agar and McConkey agar plates at 37  C in an atmosphere containing 5% CO2. In addition, the sample was also cultured on a Schaedler agar plate and incubated at 37  C in anaerobic conditions. Small colonies (0.1e 0.2 mm) were observed after 48 h of incubation on Schaedler agar. The colonies appeared whitish, mucoid and nonhemolytic. The catalase reaction was negative. The Gram stain of the colonies revealed non-spore-forming Gram-positive rods. Aerobically grown colonies were hardly visible even after 4 days. To differentiate from some vancomycin-resistant Lactobacillus species, a 30-mg vancomycin disk was used. Initial identification with the API ID32A method (bioMèrieux, Marcy l’Etoile, France; profile 4525033505) yielded Bifidobacterium spp. The isolate was sent to the National Center of Microbiology (Majadahonda, Madrid, Spain) for species identification. The isolate was identified as B. longum by means of 16S rRNA sequence analysis. A fragment of 1408 bp. was obtained by the PCR method previously described [4]. The sequence showed a homology of 99.1% with B. longum from the GeneBank (accession numbers: NR074744 and JQ805692). Antimicrobial susceptibility testing was performed using the E-Test method (AB Biodisk, Solna, Sweden) on Brucella agar plates incubated in anaerobic atmosphere for 48 h. The breakpoints used were those defined by the Clinical and Laboratory Standards Institute (CLSI) for anaerobic organisms [5]. The isolate was susceptible to penicillin (MIC: 0.016 mg/L), amoxicillin/clavulanic acid (MIC: 0.023 mg/L), cefotaxime (MIC: 0.012 mg/L), imipenem (MIC: 0.003 mg/L), moxifloxacin (MIC: 0.023 mg/L), vancomycin (MIC: 0.032 mg/L) and resistant to clindamycin (MIC: > 256 mg/L). There was no information about the consumption of probiotics. Treatment with imipenem continued for 5 days. The patient was discharged from the hospital 5 days after admission. He continued with oral antibiotic treatment with amoxicillin/clavulanic acid (500/125 mg) for 7 more days. 3. Discussion Bifidobacterium spp. is a very uncommon cause of human infection. The role of this group of organisms as primary pathogens is poorly understood. They are generally considered to be opportunists and when isolated are almost always part of polymicrobial infections [6]. Only sporadic infections have been previously described in the literature [7e17]. Relevant data of these cases are presented in Table 1. Our review shows that Bifidobacterium spp. can be the cause of a wide spectrum of severe infections, including bacteremia, sepsis, abscesses of different locations, pneumonia, pericarditis and urinary tract infection. Peritonitis caused by Bifidobacterium spp. is very rare and only sporadic cases have been reported [6,18]. Brook & Frazier reported 2 cases of peritonitis, associated with trauma in one instance and with spontaneous rupture of a viscus in the other [6]. In addition, 7 cases have been previously reported in children [18]. We have not included these cases in our review due to insufficient information. All patients previously reported with Bifidobacterium infections had underlying conditions. The source of infection can be associated with hematogenous spread, aspiration of oral secretions, diagnostic procedures, acupuncture therapy, administration of probiotics and alteration in the integrity of intestinal mucosa. It is remarkable that Bifidobacterium spp. was the only pathogen isolated from 75% of patients. This finding shows the potential of Bifidobacterium spp. to cause human infections. In our case, we think that B. longum had an important role in the pathogenesis of the peritonitis because it was the only organism isolated from the

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D. Tena et al. / Anaerobe 27 (2014) 27e30

peritoneal fluid and the Gram stain of the sample was concordant. In addition, the isolate was susceptible to imipenem and clinical response to this antibiotic was good in association with surgical treatment. The fecal peritonitis of our patient was monomicrobial and this is very uncommon. The fact that surgical prophylaxis was carried out with a single dose of intravenous amoxicillin/clavulanic acid could be one possible explanation to this finding. Although the clinical significance of Bifidobacterium spp. in some cases is not clear, especially in polymicrobial infections, our review shows that these organisms should be considered as a cause of human infections, especially in patients with underlying diseases. Bifidobacterium spp. may be underreported if clinical laboratories consider them normal flora. In addition, Bifidobacterium spp. may be not recovered because they are difficult to identify due to their fastidious growth requirements and the difficulty in distinguishing the organisms from other Gram-positive, non-sporeforming, anaerobic bacilli such as Eubacterium spp. or Lactobacillus spp. by conventional tests [10,17]. Definitive identification requires 16S rRNA gene sequencing or analysis of metabolic products by gaseliquid chromatography [1,19]. The MALDI TOF mass spectrometry can be a powerful complement to confirm species identification [20]. B. longum is one of the most frequently used probiotics. The impact of the ingestion of probiotics is still unclear. It is also not clear whether species which are used as probiotics, are different from normal flora species that have been associated with disease [1]. In a recent study, Hidemura et al. suggests that oral B. longum culture condensate administration enhanced polymorphonuclear neutrophil (PMN) recruitment into the local inflammatory site and local cytokine production in a severely murine peritonitis model [21]. This finding suggests that oral administration of probiotics containing B. longum could improve the outcome of infections via augmented PMN recruitment into the local inflammatory site. However, our study shows that B. longum can also be the cause of severe infections such as peritonitis or sepsis. For this reason, probiotics containing B. longum should be used carefully, especially in patients with underlying diseases or immunosuppression. Two sepsis in neonatos, who had received probiotic therapy, were caused by Bifidobacterium spp [15,16]. In one of them, the responsible strains were B. longum and B. infantis [16]. In our case, unfortunately, there was no information about the consumption of probiotics. Bifidobacterium spp. are generally susceptible in vitro to many antibiotics such as beta-lactams, erythromycin, clindamycin, tetracycline, linezolid and vancomycin which are commonly employed in treating Gram-positive organisms infections [22]. Penicillin has been shown to be effective against Bifidobacterium spp. and is the drug of choice for treating infections caused by these organisms [11]. Patients with bacteremia have been successfully treated with ampicillin (associated or not with kanamycin or gentamicin) or oxacillin [10]. Broad spectrum antibiotics have been administered in patients with sepsis and the clinical response was good [14e16]. Our patient was successfully treated with imipenem and amoxicillin/clavulanic acid but surgical treatment is the most important procedure for treating acute peritonitis. Although the clinical evolution of infections due to Bifidobacterium spp. is usually

good, cases with fatal outcome have been described, especially in patients with bacteremia, necrotizing pneumonia or pericarditis [10,11,13]. In conclusion, Bifidobacterium spp. should be considered as a cause of peritonitis, especially in patients with risk of intestinal perforation. The review of the literature shows that these organisms can cause a wide spectrum of severe infections, especially in patients with underlying diseases. Infections caused by Bifidobacterium spp. may be overlooked or underreported since it may be considered normal microbiota. References [1] Mahlen SD, Clarridge JE. Site and clinical significance of Alloscardovia omnicolens and Bifidobacterium species isolated in the clinical laboratory. J Clin Microbiol 2009;47:3289e93. [2] Modesto M, Biavati B, Mattarelli P. Occurrence of the family Bifidobacteriaceae in human dental caries and plaque. Caries Res 2006;40:271e6. [3] Guandalini S. Probiotics for children with diarrhea. J Clin Gastroenterol 2008;42:S53e7. [4] Drancourt M, Bollet C, Carliotz A, Martelin R, Gayralt JP, Raoult D. 16s ribosomal DNA sequence analysis of a large collection of environmental and clinical identified bacterial isolates. J Clin Microbiol 2000;38:2623e30. [5] Clinical and Laboratory Standards Institute. M100eS123. Performance standards for antimicrobial susceptibility testing, 23th informational supplement, vol. 33(1). Wayne, PA: Clinical and Laboratory Standards Institute; 2013. [6] Brook I, Frazier EH. Significant recovery of nonsporulating anaerobic rods from clinical specimens. Clin Infect Dis 1993;16:476e80. [7] Georg LK, Robertstad GW, Brink-Man SA, Hicklin MD. A new pathogenic anaerobic Actinomyces species. J Infect Dis 1965;115:88e99. [8] Thomas AV, Sodeman TH, Bentz RR. Bifidobacterium (Actinomyces) eriksonii infection. Am Rev Respir Dis 1974;110:663e8. [9] Gorbach SL, Thadepalli H. Clindamycin in pure and mixed anaerobic infections. Arch Intern Med 1974;134:87e92. [10] Bourne KA, Beebe JL, Lue YA, Ellner PD. Bacteremia due to Bifidobacterium, Eubacterium or Lactobacillus; twenty-one cases and review of the literature. Yale J Biol Med 1978;51:505e12. [11] Green SL. Case report fatal anaerobic pulmonary infection due to Bifidobacterium eriksonii. Postgrad Med 1978;63:187e9. [12] Cryan B, Azadian BS, Dunwoody GW, Richards PG. Epidural abscess due to Streptococcus milleri and Bifidobacterium species. J Infect 1991;23:214e5. [13] Epstein SK, Winslow CJ, Brecher SM, Falling LJ. Polymicrobial bacterial pericarditis after transbronchial needle aspiration. Case report with an investigation on the risk of bacterial contamination during fiberoptic bronchoscopy. Am Rev Respir Dis 1992;146:523e5. [14] Ha GY, Yang CH, Kim H, Chong Y. Case of sepsis caused by Bifidobacterium longum. J Clin Microbiol 1999;37:1227e8. [15] Ohishi A, Takahashi S, Ito Y, Ohishi Y, Tsukamoto K, Nanba Y, et al. Bifidobacterium septicemia associated with postoperative probiotic therapy in a neonate with omphalocele. J Pediatr 2010;156:679e81. [16] Jenke A, Ruf EA, Hoppe T, Heldmann M, Wirth S. Bifidobacterium septicaemia in an extremely low-birthweight infant under probiotic therapy. Arch Dis Child Fetal Neonatal Ed 2012;97:217e8. [17] Barberis CM, Cittadini RM, Almuzara MN, Feinsilberg A, Famiglietti AM, Ramírez MS, et al. Recurrent urinary infection with Bifidobacterium scardovii. J Clin Microbiol 2012;50:1086e8. [18] Brook I. Isolation of non-sporing anaerobic rods from infections in children. J Med Microbiol 1996;45:21e6. [19] Wüst J. Presumptive diagnosis of anaerobic bacteremia by gas-liquid chromatography of blood cultures. J Clin Microbiol 1977;6:586e90. [20] Angelakis E, Million M, Henry M, Raoult D. Rapid and accurate bacterial identification in probiotics and yoghurts by MALDI-TOF mass spectrometry. J Food Sci 2011;76:568e72. [21] Hidemura A, Saito H, Fukatsu K, Matsuda T, Kitayama J, Ikeda S, et al. Oral administration of Bifidobacterium longum culture condensate in a dietrestricted murine peritonitis model enhances polymorphonuclear neutrophil recruitment into the local inflammatory site. Nutrition 2003;19:270e4. [22] Moubareck C, Gavini F, Vaugien L, Butel MJ, Doucet-Populaire F. Antimicrobial susceptibility of bifidobacteria. J Antimicrob Chemother 2005;55:38e44.