Liver and brain abscess caused by Aggregatibacter paraphrophilus in association with a large patent foramen ovale: a case report

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Liver and brain abscess caused by Aggregatibacter paraphrophilus in association with a large patent foramen ovale: a case report
  CASE REPORT Open Access Liver and brain abscess caused by  Aggregatibacter paraphrophilus  in association witha large patent foramen ovale: a case report Shaumya Ariyaratnam 1 , Parag R Gajendragadkar 1 , Richard J Dickinson 1 , Phil Roberts 1 , Kathryn Harris 2 ,Andrew Carmichael 3 , Johannis A Karas 1,4* Abstract Introduction:  Aggregatibacter paraphrophilus  (former name  Haemophilus paraphrophilus ) is a normal commensal of the oral flora. It is a rare cause of hepatobiliary or intracerebral abscesses. Case presentation:  We report a case of a 53-year-old Caucasian man with a liver abscess and subsequent brainabscesses caused by  Aggregatibacter paraphrophilus . The probable source of the infection was the oral flora of ourpatient following ingestion of a dental filling. The presence of a large patent foramen ovale was a predisposingfactor for multifocal abscesses. Conclusion:  In this case report, we describe an unusual case of a patient with both liver and brain abscessescaused by an oral commensal  Aggregatibacter paraphrophilus  that can occasionally show significant pathogenicpotential. Introduction  Aggregatibacter paraphrophilus  (former name  Haemo- philus paraphrophilus ) is a species of Gram-negativecoccobacilli formerly in the genus Haemophilus, now Aggregatibacter [1]. It is a normal commensal of thehuman oral cavity and pharynx. It is documented asbeing a rare cause of subacute bacterial endocarditis,brain abscess, sinusitis, arthritis and osteomyelitis and isoften associated with recent dental treatment [2]. Diag-nosis unfortunately is hindered by its fastidious andslow-growing nature [3].Here we describe a rare case of a patient with bothliver and brain abscesses caused by   Aggregatibacter  paraphrophilus , incidentally found to have a patent fora-men ovale. Case presentation A 53-year-old Caucasian man presented with a five-day history of malaise, productive cough, fever and rigors.He had been treated by his primary care doctor for twodays with oral clarithromycin without improvement. Hehad undergone dental root canal surgery two monthspreviously; the dental filling fell out the day beforeadmission and our patient may have accidentally swal-lowed it. He never injected drugs intravenously orreceived blood transfusion. He never smoked, rarely drank alcohol and took no other medication. On exami-nation, he had a fever of 39°C, blood pressure of 132/68mmHg, sinus tachycardia of 110 beats per minute. Aus-cultation of the chest revealed some crackles at the rightlung base. His heart sounds were normal, and abdom-inal examination was normal.The haemoglobin level was 13.0 g/dL (mean corpuscu-lar volume of 85fl); the platelet count was 84 × 10 9 /L;the white cell count 10.0 × 10 9 /L, with a neutrophilia of 9.0 × 10 9 /L. The serum albumin was reduced at 29 g/L,bilirubin 2 micromoles/L, alkaline phosphatase 466 U/L(normal range 25 to 140) and alanine aminotransferase239 U/L (normal range 10 to 40). The C-reactive pro-tein (CRP) was raised at 178 mg/L. Serum urea, creati-nine, electrolytes, glucose and coagulation were withinnormal reference ranges. Urine analysis showed nitrites,1+ protein, 1+ bilirubin, and trace blood. The ECGshowed sinus tachycardia. Chest radiography showed a * Correspondence:  1 Department of Medicine, Hinchingbrooke Health Care NHS Trust,Hinchingbrooke Hospital, Hinchingbrooke Park, Huntingdon, PE29 6NT, UK  Ariyaratnam  et al  .  Journal of Medical Case Reports  2010,  4 :69 JOURNAL OF MEDICAL CASE REPORTS © 2010 Ariyaratnam et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the CreativeCommons Attribution License (, which permits unrestricted use, distribution, andreproduction in any medium, provided the srcinal work is properly cited.  prominent right hilum. Blood cultures taken on ourpatient after admission showed no growth.Community-acquired pneumonia was suspected forwhich our patient was treated with intravenous amoxi-cillin-clavulanic acid 1.2 g every 8 hours and oral clari-thromycin 500 mg every 12 hours. A liver ultrasoundperformed because of the abnormal liver function testsrevealed two well-defined areas of mixed echogenicity inthe right lobe of the liver measuring 49 mm and 40 mmin diameter. Metastatic tumor was suspected.The fever of our patient continued, and on the thirdday, he developed a severe headache with persistent vomiting. Fundoscopy was normal. Computer tomogra-phy (CT) scanning of the head with contrast was nor-mal. Lumbar puncture was performed which showed nowhite cells or red cells and no organisms identified onGram stain or upon culture of the cerebrospinal fluid(CSF). A CT scan of the chest revealed minor basalatelectasis. A CT scan of the abdomen and pelvisrevealed a single enhancing low attenuation 4.5 cmmass in the right lobe of the liver which showed somecontrast enhancement [figure 1]. The other solid organsand appendix were normal, and a metal artefact wasseen in the colon [figure 2].Because he was not improving, he underwent percuta-neous aspiration of the liver lesion under ultrasound gui-dance after six days. This drained 30 ml of pus from ourpatient. Gram stain showed no organisms and culturewas negative. He continued to have upper abdominalpain and high fever. A repeat abdominal CT scan showedpersistence of the liver abscess, and a mildly dilatedappendix (approx. 12 mm diameter). Plain abdominalradiography confirmed a dense radio-opaque object con-sistent with amalgam dental filling in the right lowerquadrant. A percutaneous pigtail drain was inserted anda further 20 ml of pus was aspirated. He was treated withintravenous ertapenem 1 g once daily and intravenousmetronidazole 500 mg three times a day.Both samples of pus that were aspirated from the liverabscess were culture negative. The causative organismwas identified as  Aggregatibacter paraphrophilus  by polymerase chain reaction (PCR) amplification of thebacterial 16S ribosomal DNA followed by nucleotidesequencing, using published primers [4]. Serologicaltests for influenza A and B, parainfluenza, adenovirus,respiratory syncytial virus, Chlamydia, and Mycoplasmawere negative. All urine, stool, cerebrospinal fluid andmethicillin resistant  Staphylococcus aureus  multisite cul-tures were negative. A trans-thoracic echocardiogram(TTE) prior to discharge did not show evidence of endocarditis. Repeat CT scan of the abdomen after 14days showed improvement in the liver abscess and somebilateral basal consolidation. The fever of our patientwas resolved. After completing 19 days of intravenousertapenem, it was shifted to oral amoxicillin 500 mgevery eight hours for two weeks. During discharge after29 days, his liver function tests had returned to normal,but he was anaemic with a haemoglobin of 10.7 g/dL,an erythrocyte sedimentation rate (ESR) of 94 mm/hrand CRP of 17 mg/L.Three weeks after discharge and two weeks after hav-ing completed the course of oral amoxicillin, our patient Figure 1  Computed tomography of the abdomen showing amildly enhancing peripheral hypodense lesion in liver . Scantaken during the initial admission. Figure 2  Computed tomography of the abdomen showing ametallic artefact (likely dental amalgam) in appendix region .Scan taken during the initial admission. Ariyaratnam  et al  .  Journal of Medical Case Reports  2010,  4 :69 2 of 4  re-presented to our hospital. Since discharge, he hadbeen bumping into objects on his left side and for oneday he had headache, rigors and a sore throat - he wasre-admitted on that day 51. On examination, he wasfebrile with no signs of infective endocarditis. Ophthal-mological examination revealed a left homonymoushemianopia with normal fundi. Repeat blood testsshowed a haemoglobin of 11.4 g/dl (MCV 86.0fl) and aCRP of 62 mg/L; his renal and liver function tests werenormal. A CT scan of the head with contrast performedon day 52 revealed multiple brain abscesses: a ring-enhancing lesion in the left occipital lobe and a non-enhancing low attenuation lesion in the right occipitallobe, with no mass effect. A CT scan of the abdomenshowed a small resolving area of low attenuation in theliver; the appendix was normal. He was treated withintavenous meropenem 2 g every eight hours and trans-ferred to a tertiary hospital. Magnetic resonance imaging(MRI) of the head confirmed multiple brain abscesses;there were multiple foci of contrast enhancement nearthe grey-white junction of both cerebral hemispheres, amore confluent area of signal change and enhancementwas seen in the right occipital lobe, and a small enhan-cing lesion was seen in the right cerebellar hemisphere[figure 3].On day 53, a mini-craniotomy and biopsy was per-formed on a left occipital ring-enhancing lesion. Onmicroscopy, pus cells were seen but no organisms wereobserved on gram staining, and enriched aerobic,anaerobic and fungal cultures were negative. Results of the 16S rDNA PCR of the brain abscess biopsy againdetected the sequence of   Aggregatibacter paraphrophi-lus . Histopathology showed appearances typical of abrain abscess. A trans-oesophageal echo performed onday 55 showed no evidence of endocarditis but therewas evidence of a patent foramen ovale (PFO) and anatrial septal aneurysm. A bubble echo was performedon day 60; during provocation by Valsalva maneuver,there was a large right-to-left shunt through the patentforamen ovale. Ultrasound scanning of the liver showedno remaining collection. Maxillo-facial assessmentincluding dental panoramic tomography revealed noongoing dental infection. His immunoglobulins werenormal, anti-nuclear antibody and anti-neutrophil cyto-plasmic antibody negative, and serological tests forhuman immunodeficiency virus, syphilis and toxoplasmawere negative. He continued treatment with intravenousmeropenem 2 g every eight hours and oral metronida-zole 400 mg every eight hours added on day 54, andremained afebrile. He was discharged on day 65 sincefirst presentation (white cell count 7.3 × 10 9 /L and CRP5 mg/L) with intravenous ceftriaxone 2 g every 12 hours to complete four weeks of out-patient antibio-tics via a peripherally inserted central line.Follow-up CT scan of the head on day 71 showed sur-gical changes deep to the left occipital craniotomy;resolving right frontal and left occipital lobe abscesses;and a large hypodense area in the right occipital lobe inkeeping with an established occipital infarct. Follow-upcranial MRI on day 81 revealed improvement in the sizeof the multiple small enhancing subcortical white matterlesions (likely microabscesses); with persistence of theright occipital infarct.On outpatient follow-up, intravenous antibiotics wereextended to complete a six week course in total; ourpatient was then switched to oral amoxicillin-clavulanicacid 625 mg every eight hours for a duration of twoweeks. Unfortunately, his left homonymous hemianopiapersisted.Cardiology follow-up concluded that it was prudent toclose the PFO as there was a possibility of further para-doxical emboli and this is planned. Our patient was puton anti-coagulant and anticonvulsant therapy and a cra-nial MRI on day 137 has shown further improvement of the cerebral abscesses. Conclusion In this case, we highlight the potential for  Aggregatibac-ter paraphrophilus  to cause widespread systemic infec-tions especially following dental treatment. Given thefastidious nature of the organism [3], it also emphasizesthe value of bacterial 16S rDNA PCR amplification andsequencing in identifying bacteria in abscesses which are Figure 3  T1 weighted magnetic resonance imaging of thehead showing multiple foci of contrast enhancement(abscesses) . Scan taken during the second admission showinglesions suspicious of abscesses near the grey-white junction of bothcerebral hemispheres, and a small enhancing lesion in the rightcerebellar hemisphere. Ariyaratnam  et al  .  Journal of Medical Case Reports  2010,  4 :69 3 of 4  culture-negative as a result of prior antibiotic adminis-tration [4].Following the root canal surgery, our patient may havedeveloped bacterial endocarditis related to his atrial sep-tal aneurysm and patent foramen ovale, but it was notpossible to confirm this because he received treatmentwith antibiotics before blood cultures were taken.Minor, unrecalled trauma to the liver has beendescribed in the literature as a predisposing factor forlocalisation of infection [5] and the presence of the den-tal filling in the colon may have given rise to the portalbacteraemia. We suspect that the shunt through thepatent foramen ovale was a contributory factor in thedevelopment of the multiple brain abscesses by permit-ting infected material to bypass the lungs and enter thesystemic circulation. The foramen ovale serves as ashunt during intrauterine life and occludes after birthwith closure becoming anatomic over time. It remainspatent in a small proportion of the population and isassociated with embolic stroke. The association withcerebral abscess is less strong and reported only in alow number of case reports in the literature [6,7]. Another contributing factor in our patient developingbrain abscesses may have been the fact that he was trea-ted with ertapenem for his initial liver abscess. Ertape-nem, unlike meropenem, is not licensed for treatment of meningitis as it exhibits wide variability in CSF/plasmaratios that preclude its use in CSF infections [8,9]. Consent Written informed consent was obtained from ourpatient for publication of this case report and any accompanying images. A copy of the written consent isavailable for review. Acknowledgements Department of Microbiology, Great Ormond Street Hospital for Children,London, UK for identification of isolates Author details 1 Department of Medicine, Hinchingbrooke Health Care NHS Trust,Hinchingbrooke Hospital, Hinchingbrooke Park, Huntingdon, PE29 6NT, UK. 2 Department of Microbiology, Level 4 Camelia Botnar Laboratories, GreatOrmond Street Hospital for Children NHS Trust, Great Ormond Street,London, WC1N 3JH, UK.  3 Department of Infectious Diseases, Addenbrooke ’ sHospital, Cambridge University Hospitals NHS Foundation Trust, Hills Road,Cambridge, CB2 0QQ, UK.  4 Health Protection Agency, East of England,Microbiology Laboratory, Papworth Hospital, Ermine Road, Papworth Everard,CB23 3RE, UK. Authors ’  contributions SA, PG, RD, PR, AC, JK for clinical, and KH for laboratory work, all contributedto writing the article. All have read and approved the final manuscript Competing interests  The authors declare that they have no competing interests. Received: 29 September 2009 Accepted: 24 February 2010Published: 24 February 2010 References 1. Nørskov-Lauritsen N, Kilian M:  Reclassification of   Actinobacillusactinomycetemcomitans ,  Haemophilus aphrophilus ,  Haemophilus paraphrophilus  and  Haemophilus segnis  as  Aggregatibacter actinomycetemcomitans  gen. nov., comb. nov.,  Aggregatibacter aphrophilus  comb. nov. and  Aggregatibacter segnis  comb.nov., andemended description of   Aggregatibacter aphrophilus  to include V factor-dependent and V factor-independent isolates.  Int J Syst Evol Microbiol  2006,  56(Pt 9) :2135-46.2. Huang ST, Lee HC, Lee NY, Liu KH, Ko WC:  Clinical characteristics of invasive  Haemophilus aphrophilus  infections.  J Microbiol Immunol Infect  2005,  38(4) :271-276.3. Chadwick PR, Malnick H, Ebizie AO:  Haemophilus paraphrophilus infection:a pitfall in laboratory diagnosis.  J Infect   1995,  30(1) :67-69.4. Harris KA, Hartley JC:  Development of broad range 16S rDNA PCR for usein the routine clinical microbiology service.  J Med Microbiol   2003, 52 :685-691.5. Haight DO, Toney JF, Greene JN, Sandin RL, Vincent AL:  Liver abscessfollowing blunt trauma: a case report and review of the literature.  SouthMed J   1994,  87(8) :811-813.6. Kawamata T, Takeshita M, Ishizuka N, Hori T:  Patent foramen ovale as apossible risk factor for cryptogenic brain abscess: report of two cases. Neurosurgery   2001,  49 :204-207.7. Stathopoulos GT, Mandila CG, Koukoulitsios GV, Katsarelis NG,Pedonomos M, Karabinis A:  Adult brain abscess associated with patentforamen ovale: a case report.  J Med Case Reports  2007,  1 :68.8.  Data sheet for ertapenem sodium.  Medsafe - New Zealand Medicines and Devices Safety Authority   [ Invanzinj.htm].9. Nau R, Lassek C, Kinzig-Schippers M, Thiel A, Prange HW, Sörgel F: Disposition and elimination of meropenem in cerebrospinal fluid of hydrocephalic patients with external ventriculostomy.  Antimicrob AgentsChemother   1998,  42(8) :2012-2016. doi:10.1186/1752-1947-4-69 Cite this article as:  Ariyaratnam  et al  .:  Liver and brain abscess caused by  Aggregatibacter paraphrophilus  in association with a large patentforamen ovale: a case report.  Journal of Medical Case Reports  2010  4 :69. 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