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Bacteremia caused by Bergeyella zoohelcum in an infective endocarditis patient: case report and review of literature

  • Yili Chen1,
  • Kang Liao1,
  • Lu Ai1,
  • Penghao Guo1,
  • Han Huang1,
  • Zhongwen Wu1 and
  • Min Liu1Email author
Contributed equally
BMC Infectious DiseasesBMC series – open, inclusive and trusted201717:271

https://doi.org/10.1186/s12879-017-2391-z

Received: 31 December 2016

Accepted: 7 April 2017

Published: 12 April 2017

Abstract

Background

Bergeyella zoohelcum is an aerobic, Gram-negative bacterium that is frequently isolated from the upper respiratory tract of dogs, cats and other mammals. Clinically, B. zoohelcum has been reported causing cellulitis, tenosynovitis, leg abscess and septicemia, which is closely connected with animal bites. Here we describe a case of bacteremia in an infective endocarditis (IE) patient caused by B. zoohelcum, in China.

Case presentation

A 27-year-old infective endocarditis woman who had no history of dog bite nor other mammal exposure suffered bacteremia caused by B. zoohelcum. This patient, without evidence of polymicrobial infection, was treated with cefuroxime and had a good outcome.

Conclusions

B. zoolhelcum bacteremia is rarely reported in IE patients. Our report expands the range of known bacterial causes of infective endocarditis.

Keywords

Bergeyella zoohelcum Bacteremia Infective endocarditis

Background

Bergeyella (formerly Weeksella) zoohelcum is an aerobic, rod-shaped, Gram-negative, non-motile, non-saccharolytic bacterium which is usually isolated from the upper respiratory tract of dogs, cats and other mammals [13]. Most reported cases of human infection by these bacteria are due to animal bites or are associated with prolonged exposure to pets [47]. Additionally, it is reported that a patient suffered B. zoohelcum bacteremia after eating the food prepared with coagulated goat blood [8]. A tsunami victim with cellulitis due to B. zoohelcum has been reported as well [9]. Here, we report a case of bacteremia caused by B. zoohelcum in an infective endocarditis patient and review of literature.

Case presentation

A 27-year-old Chinese woman was admitted to hospital (The First Affiliated Hospital of Sun Yat-sen University, Guangzhou, China) due to repeated fever for 3 months, chest distress, tachypnea, and palpitation for a month. The patient has been in her usual state of health before admission. Because of tonsillitis, she got fever and sore throat. She slightly improved after symptomatic treatment but suffered a relapse several days later, with maximum body temperature at 40.3 °C. A detailed history disclosed that the patient did not keep any pets, smoke, drink alcohol, or use illicit drugs. She denied sustaining any dog or cat bites, either. She did not have any recent travel history, either within or outside of China. Moreover, she did not visit farms or any markets with live animals, denying any other potential environmental exposures.

On examination, she had a tympanic temperature of 38.2 °C, blood pressure of 105/43 mmHg, pulse rate of 103/min and respiratory rate of 20/min. Physical examination revealed that 2/6 level systolic murmur was audible at the mitral area, and diastolic murmur was at aortic area. Ultrasonic cardiogram revealed infective endocarditis that the formation of vegetations on the mitral valve with severe mitral insufficiency, aortic valve vegetations with severe aortic insufficiency, and prolapse of anterior tricuspid valve leaflet with moderate tricuspid insufficiency. Laboratory evaluation revealed leukocyte count of 6740/mm3 with 65.5% neutrophils and 23.5% band forms, erythrocyte sedimentation rate of 120 mm/h (normal range, 0-20 mm/h), C-reactive protein of 89 mg/L (normal range, <1 mg/L), brain natriuretic peptide of 702.1 pg/ml (normal range, 0–84.0 pg/ml), and microscopic hematuria.

Blood cultures were obtained on admission day and empiric antibiotic treatment with intravenous drip of cefuroxime 1.5 g every 8 h was started. Both sets of blood cultures were positive after 2 days and isolated a Gram negative rod-shaped bacteria. The organism tested positive for oxidase, catalase, urea and indole; while PYR and DNAase test were negative. Initially, the isolate was misidentified as Brevundimonas diminuta by Vitek 2 system with only 87.6% identity (bioMérieux SA, Marcy, France). To confirm the identity of the isolate, a fragment of the 16S rRNA gene was amplified using primer sets 16S–forward (5′- AGA GTT TGA TCC TGG CTC AG-3′) and 16S–reverse (5′- ACG GCT ACC TTG TTA CGA CTT-3′) by the polymerase chain reaction [10] and the resultant polymerase chain reaction product sequenced. The sequencing data were queried against the GenBank 16S rRNA gene database. The best match returned was the Bergeyella zoohelcum, ATCC 43767 type strain, with 98.2% identity, whereas the next best match was the Riemerella anatipestifer, ATCC 11845 strain, with only 91.2% identity. Although, according to the identity algorithm of the CLSI guideline MM18-A about glucose non-fermenting Gram negative bacilli [11], the 98.2% identity of this Bergeyella zoohelcum strain was a bit lower than the requirement of ≥99.0% identity (With >0.8% separation from most closely related species); taken together, the biological characteristics and 16S rRNA gene sequencing data strongly supported the identification of B. zoohelcum.

The antibiotic susceptibility of the Bergeyella zoohelcum strain was determined by the Kirby-Bauer disk diffusion method on Mueller-Hinton agar plates with 5% horse blood with use of Oxoid disks (Oxoid Ltd., Basingstoke, Hants, RG24 8PW, UK). Although there are no categorical interpretative criteria for antimicrobial susceptibility testing (AST) data for B. zoohelcum, the isolate exhibited large inhibition zone (millimeter) for all antimicrobials tested: ampicillin 40 mm, cefixoxime 42 mm, ceftriaxone 38 mm, meropenem 40 mm, erythromycin 26 mm, clindamycin 28 mm, trimethoprim/sulfamethoxazole 40 mm, gentamicin 26 mm, levofloxacin 28 mm, which suggested the B. zoohelcum isolate was susceptible to β-lactams and fluoroquinolones. Moreover, the isolate presented negative for the production ofβ-lactamase according to the cefinase disk assay (bioMérieux SA, Marcy, France).

On day 3, the patient showed improvement of the clinical symptoms of fever, chest distress, and tachypnea. On day 10, the patient underwent combination of mitral and aortic valve bioprosthesis replacement, and tricuspid valvoplasty. However, tissue cultures taken from the surgical specimens did not produce notable bacterial growth. The patient completed a 6-week course of treatment with cefuroxime. She was discharged from the hospital in a stable condition and resumed her normal daily activities.

Discussion

B. zoohelcum, formerly belonging to Weeksella zoohelcum, is a nonfermentative Gram-negative rod which is a member of the family Flavobacteriaceae [12, 13]. It grows well on blood agar; while most strains do not grow on MacConkey’s agar. Colonies are entire, circular, semitransparent, smooth, glossy, butyrous and very sticky, making them hard to remove from solid media. In broth, growth is weak. The colonies show no hemolysis on blood agar plates, while greening occasionally exists around colonies [14].The organisms show positive for oxidase, catalase and indole test, negative for PYR, resistant to colistin, and are non-pigmented [15].

Some strains of B. zoohelcum showed fastidious which only grew on chocolate agar and biochemically inactive, thus, preventing them from recovery and identification [8]. Therefore, in this case, the B. zoohelcum isolate was misidentified as Brevundimonas diminuta by the Vitek 2 system, with only 87.6% identity initially. Similarly, in both of the infective endocarditis cases reported by Kyung Mok Sohn et al. [16], Vitek 2 automated system misidentified the pathogen as Brevundimonas spp. Brevundimonas spp., of which 16S rRNA gene sequences indicated a similarity of 94.9% with Bergeyella zoohelcum, suggesting that they belonged to a new species of Bergeyella. Notably, it was reported by Jumi Yi et al. [10], that B. zoohelcum isolate could be identified by MALDI-TOF MS on the Bruker Biotyper platform (Bruker Daltonics, Billerica, MA) [log(score) value >2.0], due to its competency of detecting the species-specific biomarkers instead of an organism’s metabolic activity for identification.

B. zoohelcum isolates are proved to be susceptible to penicillin, and resistant to colistin. However, these features are often used for identification rather than antimicrobial susceptibility testing [17]. Though there is no standard antimicrobial agent recommended for the treatment of B. zoohelcum infections, it shows highly susceptible to β-lactams and fluoroquinolones. Successful treatment with ampicillin/sulbactam [8], amoxicillin/clavulanic acid, cefazolin with gentamicin, cefuroxime, cefotaxime and ciprofloxacin has been reported [5, 6, 810]. In this case, the patient showed improvement of the clinical symptoms of fever, chest tightness, and tachypnea after 3 days of intravenous drip of cefuroxime 1.5 g every 8 h.

B. zoohelcum has become an increasingly recognized cause of leg abscess, cellulitis, pneumonia, tenosynovitis, septicemia and meningitis, which is closely related to animal bites [7, 10, 15]. Moreover, worldwide, infective endocarditis caused by B. zoohelcum has been reported only in 2 cases ever [16] (Table 1). Although in the present case, the culture from the specimen of the mitral valve vegetation was negative, given that both sets of blood culture isolated B. zoohelcum, we assume, this is another rare report on IE caused by B. zoohelcum. Notably, most of the cases of Bergeyella zoohelcum bacteremia showed the presence of animal bites or mammals exposure (Table 1). B. zoolhelcum bacteremia has been previously reported in an 80-year-old diabetic woman who suffered from bed sores and had cat contact [18]. It has also been reported in a 33-year-old man after a dog bite over his left forearm [5]. Kivinen et al. reported that a 77-year-old patient presented with severe skin infection and B. zoolhelcum bacteremia after cat contact, who was in poor health taking steroidal and diabetic medication [19]. Beltran et al. reported that a 44-year-old woman got diarrhea and bacteremia, who consumed the food prepared with goat’s blood [8].Wei-Ru lin et al. reported another case of a man who developed B. zoolhelcum bacteremia with dog contact history [15]. But recently, Kyung Mok Sohn et al. reported a 26-year-old male and a 47-year-old male who developed B. zoolhelcum bacteremia and infective endocarditis without any pets’ exposure [16]. In the present case, the IE patient asserted that she had no history of dog bite nor other mammals exposure. Therefore, in this case, we assumed that dog bites, contact with a cat, or the ingestion of contaminated food may not be the only portal of entry for B. zoohelcum, but another unknown route of infection is subject to detection.
Table 1

Summary of reported cases of Bergeyella zoohelcum infection

Reference

Age (yr)/Sex

Infection

Exposure

Underlying disease

Treatment

Outcome

Noel et al., 1989 [18]

80/F

Bed sore infection

Cat contact

Diabetes mellitus

Cefotaxime

Recovered

Montejo et al., 2001 [5]

33/M

Wound infection

Dog bite

None

Day 1–14: amoxicillin-clavulanic

Recovered

Kivinen et al., 2003 [19]

77/F

Skin infection

Cat contact

Diabetes mellitus, steriod use

Cefotaxime

Recovered

Shukla SK et al., 2004 [7]

60/F

Cellulitis and lymphangitis

Cat bite

Not reported

Day 1: Amoxicillin/clavulanate

Day 2–7: Ampicillin/sulbactam

Recovered

Beltran et al., 2006 [8]

44/F

Diarrhea

Goats blood ingestion

None

Day 2–9: ciprofloxacin

Recovered

Wei-Ru lin et al., 2007 [15]

73/M

Cellulitis

Dog contact

Liver cirrhosis, transitional cell carcinoma of urinary bladder

Day 1–14: Cefazolin and gentamicin

Recovered

Kyung Mok Sohn et al., 2015 [16]

26/M

Infective endocarditis

None

None

Day 4–5:ampicillin/sulbactam

Day 6–48:ceftriaxone

Recovered

47/M

Infective endocarditis

None

Paroxysmal supraventricular tachycardia

Day 1–3: ceftriaxone, ampicillin, and gentamicin

Day 4–32: piperacillin/tazobactam and amikacin

Day33–36:ampicillin/sulbactam

Recovered

This present case

27/F

Infective endocarditis

None

None

Day1–42:Cefuroxime

Recovered

Conclusions

In conclusion, B. zoolhelcum bacteremia is rarely reported in IE patients. Our report expands the range of known bacterial causes of infective endocarditis. Since, traditional biochemical identification equipment may misidentify such organisms, MALDI-TOF MS and molecular assays will provide more accurate result on identification.

Notes

Abbreviations

B. zoohelcum: 

Bergeyella zoohelcum

IE: 

Infective endocarditis

MALDI-TOF MS: 

Matrix-Assisted Laser Desorption/Ionization Time of Flight Mass Spectrometry

Declarations

Acknowledgements

None.

Funding

None.

Availability of data and materials

Data and materials of this report are publicly available.

Authors’ contributions

YLC traced the case, was responsible for identifying the bacteria, and was a major contributor in writing the manuscript. KL interpreted the patient data regarding the infection disease. LA participated in the design and analyzing the sequence. PHG, HH and ZWW participated in strain collection and literature searching. All authors read and approved the final manuscript.

Competing interest

The authors declare that they have no competing interests.

Consent for publication

Written informed consent for publication of the clinical details including the medical history, bacteria cultures, pictures, videos and text was obtained from the patient.

Ethics approval and consent to participate

This report was approved by the Clinical Research and Ethics Committee of the First Affiliated Hospital of Sun Yat-sen University.

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Authors’ Affiliations

(1)
Department of Laboratory Medicine, The First Affiliated Hospital of Sun Yat-sen University

References

  1. Bailie WE, Stowe EC, Schmitt AM. Aerobic bacterial flora of oral and nasal fluids of canines with reference to bacteria associated with bites. J Clin Microbiol. 1978;7(2):223–31.PubMedPubMed CentralGoogle Scholar
  2. Talan DA, Citron DM, Abrahamian FM, Moran GJ, Goldstein EJ. Bacteriologic analysis of infected dog and cat bites. Emergency medicine animal bite infection study group. N Engl J Med. 1999;340(2):85–92.View ArticlePubMedGoogle Scholar
  3. Botha WC, Jooste PJ, Britz TJ. The taxonomic relationship of certain environmental flavobacteria to the genus Weeksella. J Appl Bacteriol. 1989;67(5):551–9.View ArticlePubMedGoogle Scholar
  4. Isotalo PA, Edgar D, Toye B. Polymicrobial tenosynovitis with Pasteurella multocida and other gram negative bacilli after a Siberian tiger bite. J Clin Pathol. 2000;53(11):871–2.View ArticlePubMedPubMed CentralGoogle Scholar
  5. Montejo M, Aguirrebengoa K, Ugalde J, Lopez L, Saez NJ, Hernandez JL. Bergeyella zoohelcum bacteremia after a dog bite. Clin Infect Dis. 2001;33(9):1608–9.View ArticlePubMedGoogle Scholar
  6. Reina J, Borrell N. Leg abscess caused by Weeksella zoohelcum following a dog bite. Clin Infect Dis. 1992;14(5):1162–3.View ArticlePubMedGoogle Scholar
  7. Shukla SK, Paustian DL, Stockwell PJ, Morey RE, Jordan JG, Levett PN, Frank DN, Reed KD. Isolation of a fastidious Bergeyella species associated with cellulitis after a cat bite and a phylogenetic comparison with Bergeyella zoohelcum strains. J Clin Microbiol. 2004;42(1):290–3.View ArticlePubMedPubMed CentralGoogle Scholar
  8. Beltran A, Bdiiwi S, Jani J, Recco RA, Go EE, Zaman MM. A case of Bergeyella zoohelcum bacteremia after ingestion of a dish prepared with goat blood. Clin Infect Dis. 2006;42(6):891–2.View ArticlePubMedGoogle Scholar
  9. Kallman O, Lundberg C, Wretlind B, Ortqvist A. Gram-negative bacteria from patients seeking medical advice in Stockholm after the tsunami catastrophe. Scand J Infect Dis. 2006;38(6–7):448–50.View ArticlePubMedGoogle Scholar
  10. Yi J, Humphries R, Doerr L, Jerris RC, Westblade LF. Bergeyella zoohelcum associated with Abscess and Cellulitis after a dog bite. Pediatr Infect Dis J. 2016;35(2):214–6.View ArticlePubMedGoogle Scholar
  11. Clinical and Laboratory Standards Institute. Interpretive criteria for identification of bacteria and fungi by DNA target sequencing: approved guideline. MM18-a. Wayne: Clinical and Laboratory Standards Institute; 2008.Google Scholar
  12. Vandamme P, Segers P, Vancanneyt M, van Hove K, Mutters R, Hommez J, Dewhirst F, Paster B, Kersters K, Falsen E, et al. Ornithobacterium rhinotracheale gen. Nov., sp. nov., isolated from the avian respiratory tract. Int J Syst Bacteriol. 1994;44(1):24–37.View ArticlePubMedGoogle Scholar
  13. Holmes B, Steigerwalt AG, Weaver RE, Brenner DJ. Weeksella zoohelcum sp. nov. (formerly group IIj) from human clinical specimens. Syst Appl Microbiol. 1986;8(3):191–6.Google Scholar
  14. Saphir DA, Carter GR. Gingival flora of the dog with special reference to bacteria associated with bites. J Clin Microbiol. 1976;3(3):344–9.PubMedPubMed CentralGoogle Scholar
  15. Lin WR, Chen YS, Liu YC. Cellulitis and bacteremia caused by Bergeyella zoohelcum. J Formos Med Assoc. 2007;106(7):573–6.View ArticlePubMedGoogle Scholar
  16. Sohn KM, Huh K, Baek JY, Kim YS, Kang CI, Peck KR, Lee NY, Song JH, Ko KS, Chung DR. A new causative bacteria of infective endocarditis, Bergeyella cardium sp. nov. Diagn Microbiol Infect Dis. 2015;81(3):213–6.View ArticlePubMedGoogle Scholar
  17. Vaneechoutte M, Dijkshoorn L, Nemec A, et al. Acinetobacter, Chryseobacterium, Moraxella, and other nonfermentative gram-negative rods. In: Versalovic J, Carroll KC, Jorgensen JH, et al., editors. Manual of clinical microbiology, vol. 1. 10th ed. Washington, DC: ASM Press; 2011. p. 714–38.View ArticleGoogle Scholar
  18. Noell F, Gorce MF, Garde C, Bizet C. Isolation of Weeksella zoohelcum in septicaemia. Lancet. 1989;2(8658):332.View ArticlePubMedGoogle Scholar
  19. Kivinen PK, Lahtinen MR, Ruotsalainen E, Harvima IT, Katila ML. Bergeyella zoohelcum septicaemia of a patient suffering from severe skin infection. Acta Derm Venereol. 2003;83(1):74–5.PubMedGoogle Scholar

Copyright

© The Author(s). 2017

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