Sphingobacterium multivorum cellulitis: case report and mini-review.

Background

Sphingobacterium multivorum, first described in 1981 [ 1 ], is a gram-negative, obligate aerobe, non-fermentative, oxidase-positive, catalase-positive bacillus. It belongs to the genus Sphingobacterium , which houses bacteria containing large amounts of sphingophospholipids in their membranes [ 2 ]. Previously classified as Flavobacterium multivorum because of its capacity to produce yellow pigments (from Latin flavus , yellow), S. multivorum is ubiquitous [ 3 ] and previously considered a contaminant of the public transport system [ 4 ]. Initially designated as non-pathogenic [ 5 ], several human infections have been reported since the 1980s ( Table 1 ) [ 6 ]. Two additional cases were reported by Blahova et al. [ 7 ].

Case presentation

An 84-year-old woman was admitted for profound fatigue and orthostatic hypotension that occurred a few days after gardening bare-handed at home; she sustained no injuries during the gardening. She had a history of type 2 diabetes, chronic kidney disease, and refractory psoriatic arthritis (with hand lesions), treated with tocilizumab. Two days after admission, her condition worsened with fever and the appearance of a swollen erythematous lesion of the right upper arm ( Fig. 1 A). Laboratory findings showed leukocytosis (14.5 G/l), thrombocytopenia (109 G/l), and a slight CRP increase (29.90 mg/l). According to the quick Sequential Organ Failure Assessment score [ 8 ], the patient did not meet the sepsis criteria. Ultrasonography showed synovitis of the extensor carpi ulnaris tendon with infiltration of the subcutaneous tissues. Two sets of blood cultures were obtained before antibiotics administration. Empirical antibiotics (IV amoxicillin/clavulanate, 1.2 gr/12h) were then started.

Bacterial growth was detected in the two aerobic bottles after 7 h of incubation in the BD BACTEC™ FX system. MALDI-TOF MS (Bruker Daltonics) identified S. multivorum with a score value > 2. Minimum inhibitory concentrations (MIC) were determined using the E-test method according to the manufacturer's instructions (bioMérieux). S. multivorum isolate was susceptible to trimethoprim/sulfamethoxazole (TMP/SMX), meropenem, and levofloxacin (MIC = 0.064, 1.5 and 0.750 mg/L, respectively). Detailed antibiotic susceptibility testing results ( Table 2 ) revealed a complex pattern.

Despite therapy, cellulitis extended to the arm over 48 h. An MRI concluded a diffuse dermo-hypodermitis of the right arm, forearm, and postero-lateral abdominal wall, as well as fasciitis of the biceps and triceps brachialis and of the extensors and flexors of the carpus without osteomyelitis ( Fig. 1 B).

Amoxicillin/clavulanate treatment was stopped and meropenem treatment initiated (1.5 gr/12h) with rapid regression of cellulitis. On day 3, the treatment was simplified to oral trimethoprim/sulfamethoxazole (TMP/SMX) (800/160 mg/24h) due to the patient's challenging venous access and the high sensitivity of S. multivorum to TMP/SMX. The renal function deteriorated rapidly. The decline in kidney function was believed to be due to a prerenal cause, supported by a favorable Fractional Excretion of Sodium (FeNa) and Fractional Excretion of Urea (FeUrea), and the absence of signs indicating intrinsic or post-renal causes. Moreover, kidney function demonstrated slight improvement with volume repletion. However, since acute kidney injury can be linked to the use of TMP/SMX, we chose to take a cautious approach and switched back to meropenem for the rest of the treatment 14 days of total antibiotic treatment). To note, blood cultures were obtained one week after initiating effective antibiotic treatment, and they came back negative.

Due to the patient's worsening condition, which included severe chronic pain and several comorbidities, she made the decision to stop receiving treatment intended to extend her life. She was moved to the palliative care unit, where she passed away shortly afterwards of causes unrelated to S. multivorum infection.

Discussion

S. multivorum has been identified in urinary tract infections [ 9 ], respiratory tract infections [ [10] , [11] , [12] , [13] ], spontaneous peritonitis [ 6 ], superinfected wound 9 ∗ 10 ∗ , cellulitis 11,12 ∗, septic arthritis [ 13 ], necrotizing fasciitis [ 11 ], meningitis [ 14 ], bacteraemia [ [15] , [16] , [17] ] and septic shock without any apparent source of infection [ 18 , 19 ]. Ours is the third skin and soft tissue infection sustained by S. multivorum . Grimaldi et al. have reported a case of necrotizing fasciitis with septic shock [ 15 ].

All age groups can develop S. multivorum (range two months-84 years old; Table 1 ). 6, 9, 11-24, S. multivorum most often affects individuals with risk factors like immunosuppression [ [11] , [12] , [13] , 16 , 22 ] and comorbidities [ 6 , 11 , 15 , [19] , [20] , [21] , [22] , [23] , [24] ]. S. multivorum is an environmental bacterium. Cases are reported from North America [ 6 , 12 , 19 ], South America [ 9 , 13 ], Southeast Asia [ 16 , 17 , 22 ], Europe [ 10 , 11 , 15 , 18 , 20 , 21 , 23 , 24 ] and the eastern Mediterranean area [ 14 ]. S. multivorum infections are acquired following cutaneous lesions [ [9] , [10] , [11] , 18 ], dog-related skin lesions [ 12 ], accidents [ 14 ], precarious hygiene conditions [ 18 ]. The quality of water [ 16 , 19 ] and soil maintenance [ 19 ] have been questioned in hospitals and rehabilitation facilities. S. multivorum can potentially cause healthcare–associated infections [ 9 , 10 , 17 , 20 ]. Nielsen et coll [ 20 ]. were alerted by inoculation of S. multivorum in the prostate by prostate biopsies; the use of non-sterile material was incriminated, and revision of the urological procedure solved the problem. In a hemodialysis center, water or dialysis water baths or contamination from the dialysate through an undetectable leak in the dialyzer membrane were suspected [ 15 ]. The source often remains unidentified [ 22 , 24 ] or not mentioned [ 6 , 13 , 21 , 23 ]. Sphingobacterium spp. can survive in moist environments and contaminate laboratory culture media [ 19 ].

The patient in our case report presented multiple predisposing factors (psoriasis, diabetes, chronic kidney disease, immunosuppression). She was likely infected while gardening through a breach in the skin barrier.

Sphingobacterium spp. are intrinsically resistant to many antibiotics; moreover, S. multivorum can produce an extended-spectrum–β-lactamase and a metallo-β-lactamase conferring resistance to third-generation cephalosporins and carbapenems respectively [ 3 , 7 , 22 ]. The antibiogram susceptibility profile varies among isolates without a typical susceptibility pattern ( Table 2 ). TMP/SMX, quinolones, and tetracyclines are the most common susceptible therapies. Given the rarity of these infections, potential severity, and diverse antimicrobial susceptibility profiles, it is essential to rapidly identify S. multivorum and introduce appropriate treatment. Antibiotic susceptibility testing ( Table 2 ) revealed that the isolate was resistant to piperacillin-tazobactam, ceftazidime, and imipenem but susceptible to cefepime and meropenem. Among aminoglycosides, resistance was observed for amikacin and tobramycin, but gentamicin remained susceptible. Discrepant results were obtained for quinolones (ciprofloxacin resistance levofloxacin susceptibility). Therefore, empiric therapy should contain a combination of drugs (e.g., a carbapenem and fluoroquinolone) to minimize treatment failure risks before obtaining the isolated organism's antimicrobial susceptibility profile.

Conclusions

S. multivorum is a ubiquitous bacterium which can cause serious infections. Until now, the adequate management of these infections has been delayed by the time required to obtain bacteriological identification and antibiotic resistance profile. Available microbiological tools can shorten these steps and permit adequate targeted therapy. Wearing protective equipment adapted to the activities (gloves, shoes, and clothing), regular maintenance of the environment of the accommodation premises, and respect for hygiene recommendations during medical procedures should make it possible to avoid such infections.

Availability of data and materials

Data sharing does not apply to this article as no datasets were generated or analyzed during the current study.

CRediT authorship contribution statement

Matteo Coen: Writing – review & editing, Writing – original draft, Investigation, Formal analysis, Data curation, Conceptualization. Aurélie Foulex: Writing – review & editing, Data curation, Conceptualization. Ilias Bagetakos: Writing – review & editing, Data curation, Conceptualization. Abdessalam Cherkaoui: Writing – review & editing, Data curation, Conceptualization. Jacques Serratrice: Writing – review & editing, Writing – original draft, Data curation, Conceptualization. Jacques Schrenzel: Writing – review & editing, Writing – original draft, Data curation, Conceptualization. Anne Iten: Writing – review & editing, Writing – original draft, Formal analysis, Data curation, Conceptualization.

Search strategy

To achieve a comprehensive understanding of the diverse clinical manifestations of S. multivorum , an extensive research effort was undertaken. A review was conducted with no restrictions on publication dates, covering literature from the inception of the PubMed database through September 2024. This approach aimed to gather relevant articles detailing various clinical presentations and infections associated with this microorganism. The search strategy was meticulously developed to ensure a thorough review of the literature. We employed a structured approach using a range of keywords and Medical Subject Headings (MeSH) terms, such as “ Sphingobacterium multivorum ”, “infection”, “cutaneous infection”, and “sepsis”. This strategy was designed to encompass a wide spectrum of clinical manifestations and pathological presentations related to S. multivorum . The review sought to provide an in-depth analysis of S. multivorum infections, including both common and rare presentations. By integrating MeSH terms and specific keywords, we aimed to deliver a detailed and nuanced understanding of the pathogen's role in infectious diseases. We included seminal studies from the 1980s, as well as recent case reports, to reflect the evolution of knowledge and the latest developments in the field. In addition to examining clinical manifestations, the research focused on identifying trends in treatment approaches, including patterns of antibiotic resistance and effective therapeutic options. By synthesizing information from a broad range of sources, the review aimed to enhance our understanding of S. multivorum 's impact on various patient populations and provide valuable insights for clinicians managing infections caused by this pathogen.

Ethics approval and consent to participate

An ethical waiver was obtained from the Ethics Committee of Geneva.

Consent for publication was obtained from the patient (before her death). Moreover, the patient's next of kin has given written permission to publish her relative's clinical details and images.

Funding source(s)

Not applicable.

Declaration of competing interest

The Authors declare no competing interests.

Acknowledgments

Not applicable.

Handling Editor: Patricia Schlagenhauf

Abbreviations

Magnetic Resonance Imaging

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

trimethoprim/sulfamethoxazole

minimum inhibitory concentration

References

1. Holmes B., Owen R.J., Weaver R.E. Flavobacterium multivorum, a new species isolated from human clinical specimens and previously known as group IIk, biotype 2. Int J Syst Bacteriol. 1981;31:21–34.

2. Yabuuchi E., Kaneko T., Yano I., et al. Sphingobacterium gen. nov. Sphingobacterium spritovorum comb. nov. Sphingobacterieum multivorum comb. nov. Sphingobactierium mizutae sp. nov. and Flavobacterium indologenes sp. nov. : glucose-nonfermenting gram-negative rods in CDC groups IIK-2 and IIb. Int J Syst Bacteriol. 1983;33:580–598.

3. Schreckenberger P.C., Graevenitz A.V. In: Manuel of clinical microbiology. seventh ed. Murray P.R., Baron E.J., Pfaller M.A., Tenover F.C., Yolken R.H., editors. ASM Press; Washington D.C.: 1999. Acinetobacter, achromobacter, alcaligenes, Moraxella, methylobacterium and other nonfermentative gram-negative rods; p. 539.

4. Mendonça R.G., Olival G.S., Mimica L.M., et al. Potential infeccioso do transporte publico de passageiros da cidade de Sao Paulo. Arq Med Hosp Fac Cienc Med Santa Casa Sao Paulo. 2008;53:53–57.

5. Manfredi R., Nanetti A., Ferri M., et al. Flavobacterium spp. Organisms as opportunistic bacterial pathogens during advanced HI disease. J Infect. 1999;39:146–152. doi: 10.1016/s0163-4453(99)90007-5.

6. Dhawan V., Rajashekaraiah K., Metzger W., et al. Spontaneous bacterial peritonitis due to a group IIk-2 strain. J Clin Microbiol. 1980;11:492–495. doi: 10.1128/jcm.11.5.492-495.1980.

7. Blahova J., Krfilikovfiva K., Kremery V., et al. Hydrolysis of imipenem, meropenem, ceftazidime, and cefepime by multiresistant nosocomial strains of Sphingobacterium multivorum. Eur J Clin Microbiol Infect Dis. 1997;16:178–181. doi: 10.1007/BF01709484.

8. Singer M., Deutschman C.S., Seymour C.W., et al. The third international consensus definitions for sepsis and septic shock (Sepsis-3) JAMA. 2016 23;315:801–810. doi: 10.1001/jama.2016.0287.

9. Highton E., Guarracino J.F., Navarro M., Pinheiro J.L., Isasmendi A., Rosanova M.T. Sphingobacterium multivorum infection in a child with an extensive burn. Rev Chilena Infectol. 2021;38:452–454. doi: 10.4067/S0716-10182021000300452.

10. Pernas-Pardavila H., Vallejo-Alonso A.M., Novo-Veleiro I., Navarro del la Cruz D., González-Quintela A. Sphingobacterium multivorum: an atypical bacterium in an atypical place. Eur J Case Rep Intern Med. 2019 Sep 11;6 doi: 10.12890/2019_001214.

11. Grimaldi D., Doloy A., Fichet J., et al. Necrotizing fasciitis and septic shock related to the uncommon Gram negativ pathogen Sphingobacterium multivorum. J Clin Microbiol. 2012;50:202–203. doi: 10.1128/JCM.05151-11.

12. Konala V.M., Naramala S., Bose S., Gayam V., Madhira B.R., Adapa S. Bacteremia secondary to uncommon gram-negative bacilli transmitted from the canine in a patient with multiple myelom. J. Investig. Med. High Impact Case Rep. 2020;8:1–3. doi: 10.1177/2324709620969500.

13. Mendes M., Cavallo R., Carvalhães C., et al. Septic arthritis by Sphingobacterium multivorum in immunocompromised pediatric patient. Rev Paul Pediatr. 2016;34:379–383. doi: 10.1016/j.rppede.2016.03.014.

14. Abro A., Rahimi Shahmirzadi M., Jasim L., et al. Sphingobacterium multivorum bacteremia and acute meningitis in an immunocompetent adult patient: a case report Iran red crescent. Med J. 2016;18 doi: 10.5812/ircmj.38750.

15. Potvliege C., Dejaegher-Baudin C., Hansen W., et al. Flavobacterium multivorum septicemia in a hemodialyzed patient. J Clin Microbiol. 1984;19:568–569. doi: 10.1128/jcm.19.4.568-569.1984.

16. Freney J., Hansen W., Ploton C., et al. Septicemia caused by Sphingobacterium multivorum. J Clin Microbiol. 1987;25:1126–1128. doi: 10.1128/jcm.25.6.1126-1128.1987.

17. Muzaffar S.N., Gurjar M., Prajapati S., Gupta S.S., Roy S. A case of Sphingobacterium multivorum bloodstream infection in a critically-Ill patient. J Global Infect Dis. 2023;15:87–88. doi: 10.4103/jgid.jgid_236_22.

18. Aydogan M., Yumuk Z., Dündar V., et al. Sphingobacterium multivorum septicemia in an infant: report of a case and review of the literature. Türk Mikrobiyol Cem Derg. 2006;36:44–48.

19. Barahona F., Slim J. Sphingobacterium multivorum: case report and literature review. New Microbes New Infect. 2015;7:33–36. doi: 10.1016/j.nmni.2015.04.006.

20. Nielsen T.K., Pinholt M., Norgaard N., et al. Inoculation of Sphingobacterium multivorum in the prostate by prostate biopsy. Scand J Urol. 2014;48:116–118. doi: 10.3109/21681805.2013.807871.

21. Reina J., Borrell N., Figuerola J. Sphingobacterium multivorum isolated from a patient with Cystic fibrosis. Eur J Clin Microbiol Infect Dis. 1992;11:81–82. doi: 10.1007/BF01971283.

22. Areekul S., Vongsthongsri U., Mookto T., et al. Sphingobacterium multivorum septicemia: a case report. Med Assoc Thai. 1996;79:395–398.

23. Vella J., Rodríguez A. [Respiratory infection caused by Sphingobacterium multivorum] An Med Interna. 2001;18:655–656.

24. Lambiase A., Rossano F., Del Pezzo M., et al. Sphingobacterium respiratory tract infection in patients with cystic fibrosis. BMC Res Notes. 2009;2:262. doi: 10.1186/1756-0500-2-262.

Associated Data

Data Availability Statement

Data sharing does not apply to this article as no datasets were generated or analyzed during the current study.