Brain Abscess Due to Aggregatibacter Aphrophilus and Bacteroides Uniformis

Case report Acta Medica Academica 2015;44(2):181-185 DOI: 10.5644/ama2006-124.144

Brain abscess due to Aggregatibacter aphrophilus and Bacteroides uniformis

Maja Bogdan1*, Vlasta Zujić Atalić1, Ivan Hećimović2,3, Dubravka Vuković1

1Institute of Public Health for the Objective. The aim of this report was to describe the occurrence of a Osijek-Baranja County, Department of bacterial brain abscess in a healthy individual, without any predispos- Microbiology, Osijek, Croatia, 2University ing condition. Case report. A thirteen-year old boy was admitted to Hospital Center Osijek, Department of the Department of Neurosurgery after the onset of vomiting, headache Neurosurgery, Osijek, Croatia, 3University and dizziness. A neurological deficit was detected during the physi- “J. J. Strossmayer”, School of Medicine cal examination so urgent magnetic resonance imaging of the brain Department of Neurosurgery, Osijek was performed, revealing an intrahemispheric, right positioned soli- Croatia tary expansive mass with ring enhancement. Purulent material was obtained during osteoplastic craniotomy with total extirpation of the *Corresponding author: brain abscess. Aggregatibacter aphrophilus and Bacteroides uniformis [email protected] were isolated. The patient’s general condition improved and the neu- Tel.: + 385 31 225 772 rological deficit subsided as a result of the prompt recognition and Fax.: + 385 31 206 870 treatment of this life threatening condition. Conclusion. To achieve Received: 5 August 2015 a favourable clinical outcome, prompt recognition and surgical treat- Accepted: 23 September 2015 ment of a brain abscess are of primary importance,followed by administration of appropriate antimicrobial therapy. To our best knowledge, Key words: Child ■ Haemophilus this is the first report of this combination of microorganisms as the ■ Oropharynx ■ Odontogenic origin. cause of a brain abscess.

Introduction mophilus aphrophilus) is a member of the normal flora of the human oral cavity and A bacterial brain abscess is a relatively un- pharynx. It may cause brain abscess and in- common but extremely serious and life fective endocarditis, and has been isolated threatening infection. The incidence ranges from various other body sites, including the from 0.3-1.3/100,000 persons per year, with peritoneum, pleura, wounds and bone (4). around 2% associated with dental infections Bacteroides spp. is generally isolated from (1, 2). Intracranial abscesses can originate mixed infections with other aerobic and an- from infection of contiguous structures aerobic bacteria, forming a polymicrobial (e.g., otitis media, dental infection, mastoid- infection. Colonization of the oropharyn- itis, sinusitis), secondary to haematogenous geal cavity can lead to the isolation of these dissemination from a remote site (especially species from brain abscesses (5). in patients with cyanotic congenital heart The aim of this report was to describe for disease), after skull trauma or surgery, and, the first time the occurrence of a bacterial rarely, following meningitis. In at least 15% brain abscess due to this combination of mi- of cases, no source can be identified (3). croorganisms in a healthy child without any Aggregatibacter aphrophilus (formerly Hae- predisposing condition.

Case report Cardiovascular, respiratory and abdomi- nal examinations revealed no abnormalities. A healthy thirteen-old-boy was admitted Laboratory findings were: C-reactive protein to the Department of Neurosurgery at the 0.5 mg/l, erythrocyte sedimentation rate 18 University Hospital Centre, Osijek, due to mm/hour, and white blood cell count 6.6 frontally positioned headache, dizziness x109/l. Only dental problems (caries) were and vomiting. The patient was conscious, detected. Prior dental treatment was ex- and physical examination revealed mild left cluded. Paediatric HIV infection is very rare hemiparesis, driftage during walking and in Croatia. In the period of 1985-2014 only instability in the Romberg position without 14 HIV positive children from HIV positive signs of meningism. Terminal left diplopia mothers were reported (6). Therefore we did and inability of terminal abduction of left not regard HIV testing to be necessary. The bulbus were also detected during the exami- right parietal osteoplastic craniotomy was nation of his bulbomotoric abilities. Five days performed with complete evacuation of the before admission to the hospital, he had had purulent material and the abscess capsule. a case of diarrhoea with headache, dizziness Empirical therapy with ceftriaxone and met- and vomiting, and was subfebrile (37.5 ºC ronidazole was started. Samples obtained axillary measurement). He was examined by during the operation were immediately sent an infectious disease specialist who recom- to a microbiology laboratory for aerobic and mended a dietary regimen and rehydration anaerobic cultivation. Blood agar plate and at home. The headache did not subside and Brain-Heart infusion broth were inoculat- was even enhanced during movement, so ed and incubated aerobically at 37 ºC/24h. urgent magnetic resonance imaging (MRI) Chocolate agar plate after inoculation was of the brain was performed and revealed an incubated at 37 ºC in atmosphere with 5%-

intrahemispheric, right positioned, solitary 10% CO2. Columbia agar and thioglycolate expansive mass, diameter 41x31 mm, char- broth were also inoculated and incubated acteristically ring shaped with peripherally at 37 ºC/48h in anaerobic atmosphere. Di- contrast enhancing, peripheral oedema and rect sample smear revealed Gram-negative mass effect to the left (Figure 1). bacilli with heavy polymorfonuclear infil-

Figure 1 Characteristically ring shaped right positioned, intrahemispheric solitary expansive mass, with peripherally contrast enhancing and peripheral oedema.

182 Maja Bogdan et al.: Brain Abscess in a Child

tration. On the chocolate agar opaque, yel- merly Actinobacillus actinomycetemcomi- lowish, catalase, urease and oxidase nega- tans), Aggregatibacter aphrophilus (formerly tive colonies of Gram-negative bacilli grew, Haemophilus aphrophilus and Haemophilus identified by API NH system (bioMérieux, paraphrophilus), Cardiobacterium hominis, Marcy l’Etoile, France) as Haemophilus Eikenella corrodens and Kingella species in- aphrophilus. Antimicrobial susceptibility volved in the cases of bacterial endocarditis was detected by the Kirby- Bauer disc diffu- with or without predisposing heart disease sion method and the isolate was susceptible (8, 9). The species Haemophilus aphrophilus to ampicillin, amoxicillin-clavulonic acid, and Haemophilus paraphrophilus were re- sulfametoxasole-thrimetoprime, ceftriax- classified as single species Aggregatibacter one and meropenem, according to EUCAST aphrophilus. They are Gram-negative, short breakpoint standards (7). From the material regular bacilli, 0.5×1.5-1.7 μm with oc- cultivated in anaerobic condition whitish casional filamentous forms. They require colonies of non-spore forming Gram-neg- 5%-10% CO2 for primary isolation. Their ative bacilli were isolated. Using API 20 A growth may be enhanced by haemin, but X- system (bioMérieux, Marcy l’Etoile, France) factor is not an absolute requirement. Some colonies were identified as Bacteroides uni- isolates require V-factor (formerly Hae- formis, and for antimicrobial susceptibility mophilus paraphrophilus), whilst others are testing purposes ATB®ANA (bioMérieux, V-factor independent (formerly Haemophi- Marcy l’Etoile, France) was used. The strain lus aphrophilus). The colonies on chocolate was resistant to penicillin, clindamycin and agar are opaque, granular and yellowish, amoxicillin, and susceptible to metronida- catalase and urease negative, oxidase vari- zole, imipenem, amoxicillin-clavulonic acid, able (4). Congenital heart disease and dental piperacillin-tazobactam and cefotaxime. procedures have been described as poten- Metronidazole 4x250 mg and ceftriaxone tial predisposing factors for infection with 2x2 g were administered for sixteendays with this organism, which can be isolated from a switch to cefixime 1x400 mg for ten days, gingival scrapings, interdental material and on the recommendation of the infectious dental plaque (10). It is described as a cause disease specialist. Control head MRI re- of brain abscesses, and can develop even in vealed substantial brain oedema regression, otherwise healthy individuals with dental with minimal left ventricle compression. problems (11). There was no mass effect to the left ventricle Bacteroides spp. is a strict anaerobe, or signs of abscess residua. After the surgi- Gram-negative bacillus, and part of the cal drainage and antimicrobial therapy, the normal gastrointestinal flora. It can also patient’s general condition improved, with colonise the oral cavity of patients with poor complete regression of discrete neurological oral hygiene or those who have received an- deficit. Fifteen-month follow-up showed no timicrobial therapy, especially with β-lactam signs of recurrence of the abscess. agents (6). It is an important pathogen of various infections in children. The colonisa- Discussion tion of the oropharyngeal cavity can lead to the isolation of these species from paediatric Haemophilus aphrophilus is one of the nor- infections that originate in this area, such mal oral cavity flora. It is a fastidious Gram- as aspiration pneumonia, lung abscesses, negative bacillus part of the HACEK group, chronic otitis media, brain abscesses and which includes Haemophilus species, Ag- subcutaneous abscesses, or burns near the gregatibacter actinomycetemcomitans (for- oral cavity (6). Bacteroides spp. is generally

183 Acta Medica Academica 2015;44:181-185

isolated from mixed infections with other good general condition, without comorbidi- aerobic and anaerobic bacteria, forming ties, we believe that in this case the brain a polymicrobial infection (6). Organisms abscess originated from an odontogenic of the bacteroides group are often isolated infection. It signifies the importance of pre- from abscesses in the temporal lobe, al- serving good oral hygiene, otherwise a seri- though metastatic, haematogenous and ous infection may develop even in a healthy post-traumatic abscesses can be found in child. In conclusion, to achieve a favourable different sites (12). Brain abscesses are often clinical outcome, prompt recognition and polymicrobial, especially if they arise from a surgical treatment of the brain abscess are of dental source (13). Most odontogenic brain primary importance, followed by adminis- abscesses occur following dental treatment, tration of appropriate antimicrobial therapy. such as periodontal therapy and the extrac- tion of infected teeth, as the integrity of the Authors’ contributions: Conception and design: MB and VZA; Acquisition analysis and interpretation of vascular endothelium is breached. The fact data: MB, VZA and IH; Drafting the article: MB and that dental procedures frequently cause bac- VZA; Revising it critically for important intellectual teremia and extra oral infections is well doc- content: DV and IH. umented. However, extra oral abscesses are rare because the body’s immune system ex- Conflict of interest: The authors declare that they have no conflict of interest. punges most odontogenic bacteremia (14). Appropriate management of mixed aerobic and anaerobic infections requires the References administration of antimicrobials that are ef- 1. Ahamed SP, Lath S, DeGabriele GJ, Mathew fective against both aerobic and anaerobic VT. Cerebral abscess caused by Aggrega- components of the infection, in addition to tibacter aphrophilus. Neurosciences (Riyadh). surgical correction and drainage of the pus. 2010;15(1):40-2. The environment of an abscess is detrimen- 2. Tunkel AR. Brain abscess. In: Mandell GL, Ben- tal for many antimicrobials. The abscess nett JE, Dolin R, editors. Mandell, Douglas, and Bennett’s Principles and Practise of Infectuous capsule interferes with the penetration of diseases. 6th ed. Philadelphia (PA): Churhill Liv- antimicrobial agents, and the low pH and ingstone; 2006. p. 1150. the presence of binding proteins or inacti- 3. Mathisen GE, Johnson JP. Brain abscess. Clini- vating enzymes may impair the activity of cal infectious diseases: an official publication many antimicrobials (15). From samples ob- of the Infectious Diseases Society of America. tained during the intraoperative removal of 1997;25(4):763-79; quiz 80-1. 4. Norskov-Lauritsen N, Kilian M. Reclassification the brain abscess, Aggregatibacter aphrophi- of Actinobacillus actinomycetemcomitans, Hae- lus and Bacteroides uniformis were isolated. mophilus aphrophilus, Haemophilus paraphroph- This is the first time that this combination ilus and Haemophilus segnis as Aggregatibacter of microorganisms was isolated from a brain actinomycetemcomitans gen. nov., comb. nov., abscess in our microbiology department. Aggregatibacter aphrophilus comb. nov. and Ag- gregatibacter segnis comb. nov., and emended Reviewing the literature, we did not find any description of Aggregatibacter aphrophilus to in- reports of the same bacteria isolated from a clude V factor-dependent and V factor-indepen- brain abscess. dent isolates. Int J Syst Evol Microbiol. 2006;56(Pt 9):2135-46. 5. Brook I. Bacteroides infections in children. J Med Conclusion Microbiol. 1995;43(2):92-8. 6. Croatian Institute of Public Health. Croatian Since both bacteria can be found in the nor- Health Service Yearbook 2014 [in Croatian]. Za- mal human oral cavity, as well as the patient’s greb, 2015. [Updated 2015 May 12; Cited 2015

184 Maja Bogdan et al.: Brain Abscess in a Child

Sep 9]. Available from: http://www.hzjz.hr/wp- 10. Kao PT, Tseng HK, Su SC, Lee CM. Haemophilus content/uploads/2015/12/ljetopis_2014.pdf aphrophilus brain abscess: a case report. J Micro- 7. European Committee on Antimicrobial Suscepti- biol Immunol Infect. 2002;35(3):184-6. bility Testing. Breakpoint tables for interpretation 11. Tutuncu EE, Sencan I, Altay AF, Gurbuz Y. Brain of MICs and zone diameters. Version 1.1 April abscess due to Haemophilus aphrophilus. Neuro- 2010. [Updated 2010 Apr 27; cited 2015 Aug 5]. sciences (Riyadh). 2010;15(1):53-4. Available from: http://www.eucast.org/fileadmin/ 12. de Louvois J, Gortavai P, Hurley R. Bacteriol- src/media/PDFs/EUCAST_files/Disk_test_docu- ogy of abscesses of the central nervous sys- ments/Eucast_breakpoints_v1.1.xls. tem: a multicentre prospective study. Br Med J. 8. Winn WC Jr, Allen SD, Janda WM, Koneman EW, 1977;2(6093):981-4. Procop GW, Schreckenberger PC, et al. Miscel- 13. Simpson AJ, Das SS, Mitchelmore IJ. Polymi- laneous Fastidious Gram-Negative Bacilli. Color crobial brain abscess involving Haemophilus Atlas and Textbook of Diagnostic Microbiol- paraphrophilus and Actinomyces odontolyticus. ogy. 6th ed. Philadelphia: Lippincot Williams and Postgrad Med J. 1996;72(847):297-8. Wilkins; 2006. 14. Clifton TC, Kalamchi S. A case of odontogenic 9. Public Health England Identification of Hae- brain abscess arising from covert dental sepsis. mophilus Species and the HACEK Group of Or- Ann R Coll Surg Engl. 2012;94(1):e41-3. ganisms, UK Standards for Microbiology Inves- 15. Brook I. Microbiology of polymicrobial abscesses tigations. ID 12 Issue 3 2015. [Updated 2015 Feb and implications for therapy. J Antimicrob Che- 3; cited 2015 Aug 5]. Available from: https://www. mother. 2002;50(6):805-10. gov.uk/government/uploads/system/uploads/at- tachment_data/file/401404/ID_12i3.pdf.

185