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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Med.</journal-id>
<journal-title>Frontiers in Medicine</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Med.</abbrev-journal-title>
<issn pub-type="epub">2296-858X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fmed.2017.00048</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Medicine</subject>
<subj-group>
<subject>Case Report</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Liver Abscess Caused by <italic>Pannonibacter phragmitetus</italic>: Case Report and Literature Review</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name><surname>Wang</surname> <given-names>Mingxi</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<xref ref-type="author-notes" rid="fn001"><sup>&#x02020;</sup></xref>
</contrib>
<contrib contrib-type="author">
<name><surname>Zhang</surname> <given-names>Xia</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<xref ref-type="author-notes" rid="fn001"><sup>&#x02020;</sup></xref>
</contrib>
<contrib contrib-type="author">
<name><surname>Jiang</surname> <given-names>Tao</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
</contrib>
<contrib contrib-type="author">
<name><surname>Hu</surname> <given-names>Shaohua</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<uri xlink:href="http://frontiersin.org/people/u/393603"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Yi</surname> <given-names>Zhengjun</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name><surname>Zhou</surname> <given-names>Yajun</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<xref ref-type="corresp" rid="cor1">&#x0002A;</xref>
<uri xlink:href="http://frontiersin.org/people/u/355872"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name><surname>Ming</surname> <given-names>Desong</given-names></name>
<xref ref-type="aff" rid="aff3"><sup>3</sup></xref>
<xref ref-type="corresp" rid="cor1">&#x0002A;</xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name><surname>Chen</surname> <given-names>Shicheng</given-names></name>
<xref ref-type="aff" rid="aff4"><sup>4</sup></xref>
<xref ref-type="corresp" rid="cor1">&#x0002A;</xref>
<uri xlink:href="http://frontiersin.org/people/u/45445"/>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup><institution>Yun Leung Laboratory for Molecular Diagnostics, School of Biomedical Sciences, Huaqiao University</institution>, <addr-line>Xiamen, Fujian</addr-line>, <country>China</country></aff>
<aff id="aff2"><sup>2</sup><institution>Department of Medical Laboratory, Institute of Nanomedicine Technology, Weifang Medical University</institution>, <addr-line>Weifang, Shandong</addr-line>, <country>China</country></aff>
<aff id="aff3"><sup>3</sup><institution>Department of Clinical Laboratory, Quanzhou First Hospital Affiliated to Fujian Medical University</institution>, <addr-line>Fujian</addr-line>, <country>China</country></aff>
<aff id="aff4"><sup>4</sup><institution>Department of Microbiology and Molecular Genetics, Michigan State University</institution>, <addr-line>East Lansing, MI</addr-line>, <country>USA</country></aff>
<author-notes>
<fn fn-type="edited-by"><p>Edited by: Dongsheng Zhou, Beijing Institute of Microbiology and Epidemiology, China</p></fn>
<fn fn-type="edited-by"><p>Reviewed by: T. G. Nagaraja, Kansas State University, USA; Jose M. Ramia, SESCAM Regional Public Health System of Castilla La Mancha, Spain</p></fn>
<corresp content-type="corresp" id="cor1">&#x0002A;Correspondence: Yajun Zhou, <email>1400216018&#x00040;hqu.edu.cn</email>; Desong Ming, <email>mds6430&#x00040;126.com</email>; Shicheng Chen, <email>shicheng&#x00040;msu.edu</email></corresp>
<fn fn-type="other" id="fn001"><p><sup>&#x02020;</sup>These authors have contributed equally to this work.</p></fn>
<fn fn-type="other" id="fn002"><p>Specialty section: This article was submitted to Infectious Diseases &#x02013; Surveillance, Prevention and Treatment, a section of the journal Frontiers in Medicine</p></fn>
</author-notes>
<pub-date pub-type="epub">
<day>25</day>
<month>04</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection">
<year>2017</year>
</pub-date>
<volume>4</volume>
<elocation-id>48</elocation-id>
<history>
<date date-type="received">
<day>30</day>
<month>10</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>10</day>
<month>04</month>
<year>2017</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#x000A9; 2017 Wang, Zhang, Jiang, Hu, Yi, Zhou, Ming and Chen.</copyright-statement>
<copyright-year>2017</copyright-year>
<copyright-holder>Wang, Zhang, Jiang, Hu, Yi, Zhou, Ming and Chen</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p></license>
</permissions>
<abstract abstract-type="executive-summary">
<sec id="ST1">
<title>Background</title>
<p>Bacterial hepatic abscess is a common occurrence in developing countries, which is mostly caused by <italic>Klebsiella pneumoniae</italic> and <italic>Escherichia coli</italic>. <italic>Pannonibacter phragmitetus</italic> is a Gram-negative alkali-tolerant bacillus that exists in the natural environment. Human infection by this bacterium is rare, with only four cases reported.</p>
</sec>
<sec id="ST2">
<title>Method</title>
<p>We presented one of these cases with a bacterial liver abscess by a polymicrobial infection involving <italic>P. phragmitetus</italic> and <italic>Streptococcus oralis</italic>, with <italic>P. phragmitetus</italic> being the predominate isolate.</p>
</sec>
<sec id="ST3">
<title>Result and discussion</title>
<p>Our strain of <italic>P. phragmitetus</italic> was resistant to more antibiotics than the other reported two strains. This case further verified the infectivity of <italic>P. phragmitetus</italic>.</p>
</sec>
</abstract>
<kwd-group>
<kwd>bacterial hepatic abscess</kwd>
<kwd><italic>Klebsiella pneumoniae</italic></kwd>
<kwd><italic>Pannonibacter phragmitetus</italic></kwd>
<kwd>polymicrobial infection</kwd>
<kwd><italic>Streptococcus oralis</italic></kwd>
</kwd-group>
<counts>
<fig-count count="1"/>
<table-count count="0"/>
<equation-count count="0"/>
<ref-count count="21"/>
<page-count count="4"/>
<word-count count="2297"/>
</counts>
</article-meta>
</front>
<body>
<sec id="S1">
<title>Background</title>
<p><italic>Pannonibacter phragmitetus</italic> (<italic>P. phragmitetus</italic>) is a Gram-negative, motile rod that is frequently found to be star-shaped aggregates under microscopy (<xref ref-type="bibr" rid="B1">1</xref>). It is a facultative anaerobe and chemo-organotrophic (<xref ref-type="bibr" rid="B1">1</xref>). Before 2006, it was misidentified as <italic>Achromobacter</italic> groups B and E. Actually, <italic>P. phragmitetus</italic> and <italic>Achromobacter</italic> groups B and E are a single taxon (<xref ref-type="bibr" rid="B2">2</xref>). <italic>P. phragmitetus</italic> can survive in a high alkaline environment, such as Hungarian soda lake (<xref ref-type="bibr" rid="B1">1</xref>), and geothermal habitat (<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B4">4</xref>). It has the capacities of reducing hexavalent chromium (<xref ref-type="bibr" rid="B5">5</xref>&#x02013;<xref ref-type="bibr" rid="B12">12</xref>). Isolation of this bacterium from a human sample was first reported in 1975 (<xref ref-type="bibr" rid="B13">13</xref>). So far, only four cases of infection by <italic>P. phragmitetus</italic> were reported: one case of replacement valve endocarditis (<xref ref-type="bibr" rid="B14">14</xref>), two cases of septicemia (<xref ref-type="bibr" rid="B15">15</xref>), and one case of recurrent septicemia (<xref ref-type="bibr" rid="B16">16</xref>). Here, we presented one case of liver abscess infected by <italic>P. phragmitetus</italic>, suspiciously combined with <italic>Streptococcus oralis</italic> (<italic>S. oralis</italic>).</p>
</sec>
<sec id="S2">
<title>Case Report</title>
<p>A 44-year-old male consumed more than 150&#x02009;g of alcohol and smoked 20 cigarettes per day for 20&#x02009;years. He was admitted to our hospital due to pain in the right upper abdomen for 14&#x02009;days with normal body temperature. On a physical examination, he displayed right lateral upper abdominal tenderness. The liver edge was palpated 5 and 10&#x02009;cm under the right costal margin and the xiphoid process, respectively, with surface protuberance and tenderness. Laboratory tests showed an elevated inflammatory reaction [white blood cell count (WBC) 1.7&#x02009;&#x000D7;&#x02009;10<sup>10</sup>/L, neutrophil 81.6%, C-reactive protein (CRP) level 325&#x02009;mg/L] and anemia (RBC 3.28&#x02009;&#x000D7;&#x02009;10<sup>12</sup>/L, HGB 112&#x02009;g/L). Abnormal liver function parameters were also noted [aspartate aminotransferase 47&#x02009;IU/L, gamma-glutamyl transpeptidase 139&#x02009;IU/L, and alkaline phosphatase 133&#x02009;IU/L]. Ultrasonography detected a large abscess (82&#x02009;mm&#x02009;&#x000D7;&#x02009;78&#x02009;mm) within the right liver lobe (Figure <xref ref-type="fig" rid="F1">1</xref>).</p>
<fig id="F1" position="float">
<label>Figure 1</label>
<caption><p><bold>Abdominal ultrasonography scan of liver abscess in right lobe of the liver</bold>. Large (82&#x02009;mm&#x02009;&#x000D7;&#x02009;78&#x02009;mm) multiple low-signal areas (shown by arrows) were detected before percutaneous abscess drainage. Its size (&#x0002B;, &#x000D7;) was greatly reduced after percutaneous liver abscess drainage.</p></caption>
<graphic xlink:href="fmed-04-00048-g001.tif"/>
</fig>
<p>Intravenous injections of cefodizime sodium (1.5&#x02009;g, b.i.d) and metronidazole (0.5&#x02009;g, b.i.d) were administered daily from the first day after his admission to the end of the hospitalization (20&#x02009;days). The patient underwent percutaneous abscess drainage using an 8.5-Fr catheter guided by ultrasonography on the fifth day of his hospitalization, which was left in place for 7&#x02009;days. The patient fully recovered with the combination of antibiotic therapy and percutaneous abscess drainage. This was demonstrated by normal blood WBC count, CRP, negative blood, and abscess culture.</p>
<p>Using BD BACTEC 9240 auto blood culture system, <italic>P. phragmitetus</italic> strain 31801 was isolated from a blood sample collected within 24&#x02009;h after his admission. The identity of <italic>P. phragmitetus</italic> strain 31801 was verified by 16S rRNA gene sequencing (GenBank number FJ882624.1) and whole genome sequencing strategy (accession number CP013068). The antimicrobial susceptibility test (AST) was conducted with the Kirby&#x02013;Bauer disk diffusion test (OXOID, England) and BD Phoenix&#x02122; 100 Automated Microbiology System using NMIC/ID-109 identification/antibiotic susceptibility cards (Becton, Dickinson and Company). <italic>P. phragmitetus</italic> 31801 was sensitive to amikacin, imipenem, ceftazidime, cefepime, amoxicillin, piperacillin/tazobactam, gatifloxacin, and levofloxacin, while it was immediately sensitive to cefotaxime and ceftriaxone. It was resistant against gentamicin, tobramycin, piperacillin, trimethoprim/sulfamethoxazole, furazolidone, and tetracycline. Further studies showed that this strain was positive for extra-extended-spectrum &#x003B2;-lactamase as shown by the Kirby&#x02013;Bauer test. It was shown to carry the ampicillin-inducible &#x003B2;-lactamase with some clones in the zone of CAZ&#x02009;&#x0002B;&#x02009;CA disk and ant (3&#x02033;)-I that were verified by polymerase chain reaction. Using a blood agar plate, <italic>S. oralis</italic> was cultured from the liver abscess and collected on the fifth day after the patient&#x02019;s admission when the abscess drainage was performed. It was unable to be recovered from the pus and blood sample collected later.</p>
</sec>
<sec id="S3" sec-type="discussion">
<title>Discussion</title>
<p>In China, the most common bacterial hepatic abscesses have been consistently caused by <italic>Escherichia coli</italic> and <italic>Klebsiella</italic> sp. (accounts for 83%) (<xref ref-type="bibr" rid="B17">17</xref>). However, other bacteria were also reported to be isolated from the liver abscess. A recent survey showed that Gram-negative bacteria <italic>Enterobacter</italic> spp. (9%), <italic>Proteus</italic> spp. (6%), and <italic>Pseudomonas</italic> spp. (5%) were factors that caused this disease, next to <italic>E. coli</italic> and <italic>Klebsiella</italic> sp. (<xref ref-type="bibr" rid="B17">17</xref>). Frequently, many cases were caused by Gram-positive bacteria, mainly including <italic>Staphylococcus</italic> spp. (13%), <italic>Streptococcus</italic> spp. (8%), and <italic>Enterococcus</italic> spp. (7%) (<xref ref-type="bibr" rid="B17">17</xref>). It is uncommon for polymicrobial infections in hepatic abscesses due to most of the cases being monomicrobial (<xref ref-type="bibr" rid="B18">18</xref>). In our patient, <italic>S. oralis</italic>, a Gram-positive bacterium, was isolated from the pus. It should be noted that liver abscess due to its infection is quite rare. It was only isolated from the pus samples from two liver abscess patients (<xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B20">20</xref>). However, no report was found on the application of cefodizime for treating <italic>S. oralis</italic> infections, and it was known that <italic>S. oralis</italic> was not sensitive to metronidazole (<xref ref-type="bibr" rid="B19">19</xref>). Our patient was cured by metronidazole, cefodizime, and catheter drainage. Although we could not rule out the possibility that <italic>S. oralis</italic> was acquired from environmental contamination, we speculated that its contribution to this liver abscess was not significant.</p>
<p>Instead, <italic>P. phragmitetus</italic> 31801 may be the real pathogen of our patient seeing as it was isolated from the blood sample collected within 24&#x02009;h after his admission to the hospital, and the liver abscess in our patient could be diagnosed by abdominal ultrasonography along with an elevated inflammatory reaction on the first day that he was admitted. The chance of contamination during collection of the blood is low. It was initially identified as <italic>Achromobacter</italic> species, with the use of BD Phoenix&#x02122; 100 Automated Microbiology System and verified by 16S rRNA gene sequencing. Although it was not isolated from abscess fluid, we believed that <italic>P. phragmitetus</italic> strain 31801 was the actual pathogen. We had misidentified <italic>P. phragmitetus</italic> strain 31801 as <italic>Sphingomonas paucimobilis</italic> during our interpretation of the result of BD Phoenix&#x02122; 100 Automated Microbiology System before it was verified by 16S rRNA gene sequencing. The infectivity of <italic>P. phragmitetus</italic> had been demonstrated even though only four cases of infection have been reported (<xref ref-type="bibr" rid="B13">13</xref>, <xref ref-type="bibr" rid="B15">15</xref>, <xref ref-type="bibr" rid="B16">16</xref>). The pathogenic mechanisms of <italic>P. phragmitetus</italic> were unknown; in fact, we found many virulence factors in <italic>P. phragmitetus</italic> when we analyzed the sequenced genome (unpublished). In an antimicrobial susceptibility test, this bacterium was resistant against several classifications of antibiotics mentioned above. Furthermore, it has extra-extended-spectrum &#x003B2;-lactamase, which was inducible and ant (3&#x02033;)-I (<xref ref-type="bibr" rid="B21">21</xref>).</p>
<p><italic>Pannonibacter phragmitetus</italic> 31801 was resistant to more antibiotics than the strain isolated by Jenks and Shaw, which was sensitive to gentamicin, trimethoprim/sulfamethoxazole, and tetracycline (<xref ref-type="bibr" rid="B16">16</xref>), and the strain isolated by McKinley et al., which was sensitive to trimethoprim/sulfamethoxazole and tetracycline (<xref ref-type="bibr" rid="B14">14</xref>), while <italic>P. phragmitetus</italic> 31801 was resistant against these three antibiotics: tobramycin, piperacillin, and furazolidone.</p>
<p>In conclusion, this case report raises awareness to the possibility of infectivity and multiple-drug resistance of <italic>P. phragmitetus</italic>.</p>
</sec>
<sec id="S4">
<title>Ethics Statement</title>
<p>The written informed consent for the publication of this case report was obtained from the patient. This work was already approved by the Ethics Committee of Quanzhou First Hospital.</p>
</sec>
<sec id="S5" sec-type="author-contributor">
<title>Author Contributions</title>
<p>Conception and design of the work: MW, XZ, and YZ. Data collection: MW, XZ, TJ, SH, ZY, YZ, and DM. Data analysis and interpretation, manuscript writing, and critical revision of the article: MW, XZ, YZ, and SC. Approval of the final version of the article: MW, XZ, TJ, SH, ZY, YZ, DM, and SC.</p>
</sec>
<sec id="S6">
<title>Conflict of Interest Statement</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
</body>
<back>
<sec id="S7">
<title>Funding</title>
<p>This work was supported by Huaqiao University Graduate Student Scientific Research Innovation Ability Cultivation Plan Projects, the Fong Shu Fook Tong and Fong Yun Wah Foundations (14X30127), the Xiamen Southern Oceanographic Center (14GYY008NF08), the Technology Planning Projects of Quanzhou Social Development Fields (2014Z24), and the Major Support Research Project of National Key Colleges Construction of Quanzhou Medical College (2013A13).</p>
</sec>
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