Rothia aeria endocarditis in a patient with a bicuspid aortic valve: case report

Antonio Carlos Nicodemo Luiz Guilherme Gonçalves Fatuma Catherine Atieno Odongo Marines Dalla Valle Martino Jorge Luiz Mello Sampaio About the authors

Abstract

Rothia aeria is an uncommon pathogen mainly associated with endocarditis in case reports. In previous reports, endocarditis by R. aeria was complicated by central nervous system embolization. In the case we report herein, endocarditis by R. aeria was diagnosed after acute self-limited diarrhea. In addition to the common translocation of R. aeria from the oral cavity, we hypothesize the possibility of intestinal translocation. Matrix-assisted laser desorption ionization-time of flight mass spectrometry and genetic sequencing are important tools that can contribute to early and more accurate etiologic diagnosis of severe infections caused by Gram-positive rods.

Rothia aeria ; Endocarditis; Intestinal translocation; Molecular diagnosis


Introduction

Rothia is a genus of Gram-positive, non-acid-fast bacteria proposed by George and Brown in 1967. This genus grows well under aerobic conditions on BHI agar. Young colonies are smooth, tending to become rough, dry, convex and adherent to the culture medium when mature. The bacterial cells can appear coccoid, cocco-bacillary or filamentous. The species Rothia aeria was characterized in 2004 after isolation from the Russian space station Mir. Initially, it was known as Rothia dentocariosa genomovar II.11. Ying L, Yoshiaki K, Nagatoshi F, et al. Rothia aeria sp. nov., Rhodococcus baikonurensis sp. nov. and Arthrobacter russicus sp. nov., isolated from air in the Russian space laboratory Mir. Int J Syst Evol Microbiol. 2004;54:827–35. R. aeria is known to colonize human oral cavity, but has also been identified in duodenal biopsy as a colonizer of the upper gastrointestinal tract.22. Maram Z, Guoxian W, Floyd D, et al. Identification of Rothia bacteria as gluten-degrading natural colonizers of the upper gastro-intestinal tract. PLoS ONE. 2011;6:e24455. To our knowledge, this is the sixth case report of endocarditis by R. aeria.

Case report

A previously healthy 25-year-old man presented with acute self-limited diarrhea for three days after a trip to Salvador, Brazil. After diarrhea resolution, he started to experience daily fever spikes. He visited a physician who prescribed levofloxacin 500 mg daily for seven days with symptom improvement. However, fever recurred after stopping levofloxacin. He sought further medical assistance on the 4th week of illness. Examination was remarkable for a grade 2/6 aortic murmur and an enlarged spleen. Transesophageal echocardiography showed a bicuspid aortic valve with significant regurgitation and a vegetation of 4 mm. Two blood culture samples obtained from different venous sites both yielded Gram-positive rods. Empirical treatment with ampicillin 2 g q4h and vancomycin, initial loading dose of 25 mg/kg and maintenance dose of 15 mg/kg q12h, was started due to initial organism identification as Rothia spp. After complete identification of the bacteria as R. aeria, vancomycin was discontinued. Ampicillin was maintained because antimicrobial susceptibility test showed a 0.032 mcg/mL minimum inhibitory concentration (MIC) for penicillin. This isolate was susceptible to all of the tested antimicrobials (ciprofloxacin 1 mcg/mL, gentamicin 1.5 mcg/mL, linezolid 0.38 mcg/mL, and vancomycin 1.5 mcg/mL), except for daptomycin with a MIC of 6.0 μg/mL. Endocarditis treatment was uneventful. The patient progressively improved, fever completely resolved and inflammation markers normalized. Ampicillin was stopped after five weeks and follow-up echocardiography revealed complete resolution of the vegetation.

Discussion

Rothia is a genus of Gram-positive, non-acid-fast bacteria proposed by George and Brown in 1967. This genus grows well under aerobic conditions on BHI agar. Young colonies are smooth, tending to become rough, dry, convex and adherent to the culture medium when mature. The bacterial cells can appear coccoid, cocco-bacillary or filamentous. The species R. aeria was characterized in 2004 after isolation from the Russian space station Mir. Initially, it was known as R. dentocariosa genomovar II.11. Ying L, Yoshiaki K, Nagatoshi F, et al. Rothia aeria sp. nov., Rhodococcus baikonurensis sp. nov. and Arthrobacter russicus sp. nov., isolated from air in the Russian space laboratory Mir. Int J Syst Evol Microbiol. 2004;54:827–35. R. aeria is known to colonize human oral cavity, but has also been identified in duodenal biopsy as a colonizer of the upper gastrointestinal tract.22. Maram Z, Guoxian W, Floyd D, et al. Identification of Rothia bacteria as gluten-degrading natural colonizers of the upper gastro-intestinal tract. PLoS ONE. 2011;6:e24455. To our knowledge, this is the sixth case report of endocarditis by R. aeria.

After a literature search of R. aeria infections, our case is the eleventh case report of clinical infection and the sixth case report of endocarditis.33. Hiraiwa T, Izumi M. Successful management of Rothia aeria endocarditis with renal transplantation patient: a case report. Eur J Intern Med. 2013;24 Suppl. 1:e204.1212. Monju A, Shimizu N, Yamamoto M, Oda K, Kawamoto Y, Ohkusu K. First case report of sepsis due to Rothia aeria in a neonate. J Clin Microbiol. 2009;47:1605–6. The case reports include five cases of endocarditis,33. Hiraiwa T, Izumi M. Successful management of Rothia aeria endocarditis with renal transplantation patient: a case report. Eur J Intern Med. 2013;24 Suppl. 1:e204.77. Holleran K, Rasiah S. Atypical thunderclap headache. Case report presented to the 2nd international congress on neurology and epidemiology. Neuroepidemiology. 2012;39:177–283. one case of neck abscess,88. Falcone EL, Zelazny AM, Holland SM. Rothia aerianeck abscess in a patient with chronic granulomatous disease: case report and brief review of the literature. J Clin Immunol. 2012;32:1400–3. one case of shoulder joint infection99. Verrall AJ, Robinson PC, Tan CE, Mackie WG, Blackmore TK. Rothia aeria as a cause of sepsis in a native joint. J Clin Microbiol. 2010;48:2648–50.. two cases of lung infection1010. Michon J, Jeulin D, Lang JM, Cattoir V. Rothia aeria acute bronchitis: the first reported case. Infection. 2010;38:335–7.,1111. Hiyamuta H, Tsuruta N, Matsuyama T, Satake M, Ohkusu K, Higuchi K. First case report of respiratory infection with Rothia aeria. Nihon Kokyuki Gakkai Zasshi. 2010;48:219–23.; and one case of neonatal sepsis,1212. Monju A, Shimizu N, Yamamoto M, Oda K, Kawamoto Y, Ohkusu K. First case report of sepsis due to Rothia aeria in a neonate. J Clin Microbiol. 2009;47:1605–6. as shown in Table 1. Three cases had a previous history of dental caries and the neonatal sepsis occurred after maternal tooth extraction.33. Hiraiwa T, Izumi M. Successful management of Rothia aeria endocarditis with renal transplantation patient: a case report. Eur J Intern Med. 2013;24 Suppl. 1:e204.99. Verrall AJ, Robinson PC, Tan CE, Mackie WG, Blackmore TK. Rothia aeria as a cause of sepsis in a native joint. J Clin Microbiol. 2010;48:2648–50. These previous case reports show that R. aeria is capable of infecting various body sites and also show that infection by this agent is probably more in immunocompromised patients, as some patients were on immunosuppressive medications.33. Hiraiwa T, Izumi M. Successful management of Rothia aeria endocarditis with renal transplantation patient: a case report. Eur J Intern Med. 2013;24 Suppl. 1:e204.,88. Falcone EL, Zelazny AM, Holland SM. Rothia aerianeck abscess in a patient with chronic granulomatous disease: case report and brief review of the literature. J Clin Immunol. 2012;32:1400–3.1111. Hiyamuta H, Tsuruta N, Matsuyama T, Satake M, Ohkusu K, Higuchi K. First case report of respiratory infection with Rothia aeria. Nihon Kokyuki Gakkai Zasshi. 2010;48:219–23. All five case reports of endocarditis by R. aeria had central nervous system embolic complications; two cases had fatal central nervous system hemorrhage.33. Hiraiwa T, Izumi M. Successful management of Rothia aeria endocarditis with renal transplantation patient: a case report. Eur J Intern Med. 2013;24 Suppl. 1:e204.77. Holleran K, Rasiah S. Atypical thunderclap headache. Case report presented to the 2nd international congress on neurology and epidemiology. Neuroepidemiology. 2012;39:177–283. In one recent case report of mitral valve endocarditis with confirmed brain septic emboli, prompt antibiotic treatment and urgent metallic mitral valve replacement may have prevented further complications and allowed the patient to be successfully discharged on outpatient antibiotic treatment.44. Thiyagarajan A, Balendra A, Hillier D, et al. The first report of survival post Rothia aeria endocarditis. BMJ Case Rep. 2013; 2013, http://dx.doi.org/10.1136/bcr-2013-200534, pii: bcr2013200534.
http://dx.doi.org/10.1136/bcr-2013-20053...
So far, our case is the only R. aeria endocarditis infection where embolic complications have not occurred.

Table 1
Summarized case reports of Rothia aeria clinical infections

R. aeria and R. dentocariosa are both known to colonize unhealthy oral cavities. They may then translocate into blood and disseminate, causing endocarditis or other infection in individuals at risk.33. Hiraiwa T, Izumi M. Successful management of Rothia aeria endocarditis with renal transplantation patient: a case report. Eur J Intern Med. 2013;24 Suppl. 1:e204.,99. Verrall AJ, Robinson PC, Tan CE, Mackie WG, Blackmore TK. Rothia aeria as a cause of sepsis in a native joint. J Clin Microbiol. 2010;48:2648–50.,1212. Monju A, Shimizu N, Yamamoto M, Oda K, Kawamoto Y, Ohkusu K. First case report of sepsis due to Rothia aeria in a neonate. J Clin Microbiol. 2009;47:1605–6. Our patient had excellent dental hygiene and had not been submitted to any dental procedures in the last six months. Some studies have suggested colonization of the small intestine (duodenum) by this bacteria and its role in gluten metabolism.22. Maram Z, Guoxian W, Floyd D, et al. Identification of Rothia bacteria as gluten-degrading natural colonizers of the upper gastro-intestinal tract. PLoS ONE. 2011;6:e24455. Therefore, considering that this patient initially presented with acute self-limited diarrhea, we hypothesized that endocarditis may have resulted from intestinal translocation and infection of the thickened bicuspid aortic valve.

In our clinical case, initial identification after blood culture on agar revealed a Gram-positive rod, which was identified by Vitek 2 as R. aeria. Since R. aeria is a rarely reported human pathogen and due to commonly inconclusive results of the biochemical identification of Gram-positive rods, it was reasonable to confirm diagnosis by molecular methods. Gene sequence analysis by MicroSeq Library identified R. aeria with a 99.98% match. Additionally, the sequence was compared to those of other Rothia species available at the GenBank database – http://www.bacterio.net/qr/rothia.html.1313. List of prokaryotic names with standing in nomenclature. http://www.bacterio.net/qr/rothia.html [accessed 10.03.14].
http://www.bacterio.net/qr/rothia.html...
The highest similarity index (99.77%) was observed with a deposit pertaining to the type strain R. aeria (GenBank assession CP001368.1). The same result was obtained when performing a local BLAST using the Rothia species 16S rRNA nucleotide sequence. The second highest similarity (98.62%) was observed with the GenBank deposit CP002280.1, corresponding to the type strain of R. dentocariosa. Early identification of R. aeria can also be achieved using matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS).55. Crowe A, Ding N, Yong E, et al. Rothia aeriamitral valve endocarditis complicated by multiple mycotic aneurysms: laboratory identification expedited using MALDI-TOF MS. Infection. 2014;42(2):419–23.,88. Falcone EL, Zelazny AM, Holland SM. Rothia aerianeck abscess in a patient with chronic granulomatous disease: case report and brief review of the literature. J Clin Immunol. 2012;32:1400–3.

Treatment of R. aeria infection is variable and dependent on the assisting physicians and susceptibility tests, as we have seen from the case reports (Table 1). All case report isolates were shown to be sensitive to penicillins, which seemed to be the drugs of choice in some of the cases.33. Hiraiwa T, Izumi M. Successful management of Rothia aeria endocarditis with renal transplantation patient: a case report. Eur J Intern Med. 2013;24 Suppl. 1:e204.,88. Falcone EL, Zelazny AM, Holland SM. Rothia aerianeck abscess in a patient with chronic granulomatous disease: case report and brief review of the literature. J Clin Immunol. 2012;32:1400–3.1111. Hiyamuta H, Tsuruta N, Matsuyama T, Satake M, Ohkusu K, Higuchi K. First case report of respiratory infection with Rothia aeria. Nihon Kokyuki Gakkai Zasshi. 2010;48:219–23. One case was initially treated with a combination therapy of benzylpenicillin, rifampicin and gentamicin. Our patient promptly responded to treatment with ampicillin after antibiotic susceptibility results according to the Clinical and Laboratory Standards Institute (CLSI) guidelines.1414. Clinical and Laboratory Standards Institute (CLSI). Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria. second ed; 2010. M45–A2.

In conclusion, we summon attention to the seemingly high embolic complications of endocarditis by R. aeria. Therefore, R. aeriaendocarditis should be promptly managed with adequate antibiotic treatment and surgical valve replacement whenever necessary in order to improve patient prognosis. In addition to common translocation of R. aeria from the oral cavity, we hypothesize the possibility of intestinal translocation. MALDI-TOF MS and genetic sequencing are important tools that can contribute to early and more accurate etiologic diagnosis of severe infections caused by Gram-positive rods.

REFERENCES

  • 1
    Ying L, Yoshiaki K, Nagatoshi F, et al. Rothia aeria sp. nov., Rhodococcus baikonurensis sp. nov. and Arthrobacter russicus sp. nov., isolated from air in the Russian space laboratory Mir Int J Syst Evol Microbiol. 2004;54:827–35.
  • 2
    Maram Z, Guoxian W, Floyd D, et al. Identification of Rothia bacteria as gluten-degrading natural colonizers of the upper gastro-intestinal tract. PLoS ONE. 2011;6:e24455.
  • 3
    Hiraiwa T, Izumi M. Successful management of Rothia aeria endocarditis with renal transplantation patient: a case report. Eur J Intern Med. 2013;24 Suppl. 1:e204.
  • 4
    Thiyagarajan A, Balendra A, Hillier D, et al. The first report of survival post Rothia aeria endocarditis. BMJ Case Rep. 2013; 2013, http://dx.doi.org/10.1136/bcr-2013-200534, pii: bcr2013200534.
    » http://dx.doi.org/10.1136/bcr-2013-200534
  • 5
    Crowe A, Ding N, Yong E, et al. Rothia aeriamitral valve endocarditis complicated by multiple mycotic aneurysms: laboratory identification expedited using MALDI-TOF MS. Infection. 2014;42(2):419–23.
  • 6
    Tarumoto N, Sujino K, Yamaguchi T, et al. A first report of Rothia aeria endocarditis complicated by cerebral hemorrhage. Intern Med. 2012;51:3295–9.
  • 7
    Holleran K, Rasiah S. Atypical thunderclap headache. Case report presented to the 2nd international congress on neurology and epidemiology. Neuroepidemiology. 2012;39:177–283.
  • 8
    Falcone EL, Zelazny AM, Holland SM. Rothia aerianeck abscess in a patient with chronic granulomatous disease: case report and brief review of the literature. J Clin Immunol. 2012;32:1400–3.
  • 9
    Verrall AJ, Robinson PC, Tan CE, Mackie WG, Blackmore TK. Rothia aeria as a cause of sepsis in a native joint. J Clin Microbiol. 2010;48:2648–50.
  • 10
    Michon J, Jeulin D, Lang JM, Cattoir V. Rothia aeria acute bronchitis: the first reported case. Infection. 2010;38:335–7.
  • 11
    Hiyamuta H, Tsuruta N, Matsuyama T, Satake M, Ohkusu K, Higuchi K. First case report of respiratory infection with Rothia aeria Nihon Kokyuki Gakkai Zasshi. 2010;48:219–23.
  • 12
    Monju A, Shimizu N, Yamamoto M, Oda K, Kawamoto Y, Ohkusu K. First case report of sepsis due to Rothia aeria in a neonate. J Clin Microbiol. 2009;47:1605–6.
  • 13
    List of prokaryotic names with standing in nomenclature. http://www.bacterio.net/qr/rothia.html [accessed 10.03.14].
    » http://www.bacterio.net/qr/rothia.html
  • 14
    Clinical and Laboratory Standards Institute (CLSI). Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria. second ed; 2010. M45–A2.

Publication Dates

  • Publication in this collection
    Sept-Oct 2014

History

  • Received
    11 Apr 2014
  • Accepted
    06 May 2014
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