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Thoracic empyema caused by Campylobacter rectus
J Infect Chemother xxx (2016) 1e4
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Journal of Infection and Chemotherapy journal homepage: http://www.elsevier.com/locate/jic
Case Report
Thoracic empyema caused by Campylobacter rectus Tomoyuki Ogata a, Teruo Urata b, Daisuke Nemoto c, Shigemi Hitomi d, * a
Department of Respiratory Medicine, JA Toride Medical Center, Japan Department of Clinical Laboratories, JA Toride Medical Center, Japan c Department of Clinical Laboratories, University of Tsukuba Hospital, Japan d Department of Infectious Diseases, University of Tsukuba Hospital, Japan b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 8 June 2016 Received in revised form 19 August 2016 Accepted 21 August 2016 Available online xxx
We report a case of thoracic empyema caused by Campylobacter rectus, an organism considered as a periodontal pathogen but rarely recovered from extraoral specimens. The patient fully recovered through drainage of purulent pleural fluid and administration of antibiotics. The present case illustrates that C. rectus can be a cause of not only periodontal disease but also pulmonary infection. © 2016 Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Keywords: Campylobacter rectus Thoracic empyema Sulbactam-ampicillin Garenoxacin
1. Introduction The genus Campylobacter is a group of spiral, curved, or straight rod-shaped Gram-negative bacteria. They require microaerobic and/or anaerobic conditions for their growth and typically demonstrate a characteristic corkscrew-like motion using a flagellum attached at one or both ends of cells [1]. To date, more than 15 Campylobacter species have been established or suspected as human pathogens. Gastroenteritis and extraintestinal infections, commonly due to Campylobacter jejuni and Campylobacter fetus, respectively, are major manifestations of human campylobacteriosis. These pathogens are generally reserved in domestic animals and transmitted to patients through consumption of contaminated food and water. In contrast, certain Campylobacter species reside in the human oral cavities, some of which are putatively associated with periodontal diseases [2]. Campylobacter rectus, formerly named as Wolinella recta [3], is one of the campylobacteria considered as periodontal pathogens [4]. The organism has commonly been found in various intraoral materials of both periodontically healthy and morbid individuals [5,6]. However, C. rectus has rarely been recovered from extraoral
* Corresponding author. Department of Infectious Diseases, University of Tsukuba Hospital, 2-1-1 Amakubo, Tsukuba, Ibaraki 305-8576, Japan. Fax: þ81 29 853 3479. E-mail address: [email protected] (S. Hitomi).
specimens [7]. Here, we describe a case of thoracic empyema, in which C. rectus was solely recovered from purulent pleural effusion. 2. Case report A 75-year-old Japanese man was referred because of fever and respiratory discomfort lasting for a week. He had regularly received medications for hypertension, hyperlipidemia, and diabetes mellitus with slightly impaired renal function. At the referral, the patient was alert and complained of left-sided chest pain. He had axillary temperature of 38.1 C, a heart rate of 100/min, blood pressure of 139/52, and arterial oxygen saturation at room air of 92%. Blood tests showed leukocytosis (14,320/mm3), slight hepatic injury (aspartate aminotransferase: 33 IU/L, alanine aminotransferase: 58 IU/L), renal impairment (urea nitrogen: 30 mg/dL, creatinine: 1.64 mg/dL), an elevation of the C-reactive protein level (19.44 mg/ dL), and hyperglycemia (glucose: 254 mg/dL, hemoglobin A1C: 6.7%). Chest X-ray and computed tomography revealed the presence of pleural effusion in the left thoracic cavity but no apparent infiltration in the lung field (Fig. 1). Blood culture was not performed. After hospitalization, a chest tube was inserted into the left thoracic cavity, through which purulent effusion was drained. Gram staining of the effusion exhibited many polymorphonucleocytes but no apparent microorganism. Intravenous administration of sulbactam-ampicillin (6 g/day, a dose reduced according to an
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Please cite this article in press as: Ogata T, et al., Thoracic empyema caused by Campylobacter rectus, J Infect Chemother (2016), http://dx.doi.org/ 10.1016/j.jiac.2016.08.013
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T. Ogata et al. / J Infect Chemother xxx (2016) 1e4
using the primers 27F and 1492R [8] and sequenced directly. A homology search using the Basic Local Alignment Search Tool showed that the sequence of 1517 base pairs was most closely related to that of C. rectus JCM 6301T (GenBank accession number: AB595133.1) and contained an extra 189-base-pair portion identical to the intervening sequence of C. rectus strains described by Lam et al. (GenBank accession numbers: HQ890330 and HQ890331) [7]. With exclusion of the intervening portion, the sequence was 99.5% identical to that of C. rectus JCM 6301T. Minimum inhibitory concentrations against the recovered organism, rieux) on Brucella HK measured with the Epsilometer test (bioMe (RS) agar broth incubated anaerobically at 37 C for 72 h, were as follows; penicillin: 0.047 mg/ml, amoxicillin: 0.094 mg/ml, levofloxacin: 0.032 mg/ml, and metronidazole: 0.75 mg/ml. No organism was cultured from the discharged material obtained from the spontaneously ruptured subcutaneous abscess on day 45. Fig. 1. Computed tomography of the chest taken on the day before hospitalization at the referring facility. An open arrow indicates pleural effusion in the left thoracic cavity.
estimated creatinine clearance of 30 ml/min) and intrathoracic irrigation with normal saline through the chest tube were initiated. The patient became afebrile on the next day. The chest tube was removed on day 17 and the intravenous antibiotic was switched to oral garenoxacin (400 mg/day) on day 2. The patient was discharged on day 25 with taking the antibiotic. On day 45, the patient visited an outpatient clinic because subcutaneous abscess, having emerged at the site where the chest tube had been inserted, ruptured spontaneously. The oral antibiotic was changed to levofloxacin (500 mg/day) according to the decision of a physician in the clinic and given until day 55. Dental consultation five months after the reference revealed that the patient had periodontitis with massive dental plaque, for which only dental cleansing was given. On a follow-up after one year, the patient was well and abnormal shadows on chest X-ray disappeared almost completely. The purulent pleural effusion obtained on admission was centrifuged and the sediment was inoculated into HK Semisolid Medium (Kyokuto Pharmaceutical Industrial Co. Ltd., Tokyo, Japan). After incubation at 37 C for 48 h, the lower layer of the broth became turbid, indicating growth of motile anaerobes. The turbid portion was inoculated onto Brucella HK (RS) agar broth (Kyokuto) and incubated anaerobically. Translucent, rough, flat, nonhemolytic colonies emerged after a few days (Fig. 2a). The organism was Gram-negative, straight rod-shaped (Fig. 2b), both catalase and oxidase tests-negative, and unculturable on sheep blood agar rieux, Marcybroth under 5% CO2. Assays with API 20A (bioMe rieux) failed to l’Etoile, France) and VITEK® 2 ANC ID Card (bioMe identify the organism. Hence, a part of the 16S ribosomal RNA gene of the organism was amplified with polymerase chain reaction
3. Discussion In the present case, the drained pleural effusion appeared purulent and contained many polymorphonucleocytes, confirming the diagnosis of thoracic empyema. Although Gram staining did not reveal any apparent microorganisms, recovery of C. rectus solely from the material, which was obtained without previous administration of antibiotics, indicates the recovered organism to be the causative agent. The present case illustrates that C. rectus, an organism generally considered as a periodontal pathogen, can be a cause of lower respiratory tract infection. C. rectus is a small, unbranched, straight Gram-negative organism. Other typical characteristics include growth in an anaerobic condition, motility, formation of translucent colonies on blood agar plates, and negative reaction to both catalase and oxidase tests [9], all of which the organism recovered in the present case exhibited. Our attempt to identify the recovered organism using commercial identification kits for anaerobes failed because C. rectus was not included in their lists of identifiable organisms. Instead, we utilized a phylogenic analysis of the 16S ribosomal RNA gene, through which C. rectus strains recovered in recent cases of extraoral infection were also identified [7,10e13]. To our knowledge, ten cases of extraoral C. rectus infection have been reported in the literature (Table 1) [7,10e16]. Normally sterile organs were involved without preceding injury in approximately two thirds of the cases [7,11e13,15,16], indicating hematogenous dissemination of causative organisms. In the present case, we speculate that the causative organism was also transmitted to the pleural space via the bloodstream, albeit a less common mode of transmission in cases of empyema [17], because the patient had neither apparent risk nor history of both aspiration and thoracic trauma and radiological abnormality in the left lung field was minimal at the referral. The indication of periodontitis with
Fig. 2. Colonies (a) and Gram staining (b) of organisms after anaerobic incubation on Brucella HK (RS) agar broth for 3 days. A bar indicates 10 mm.
Please cite this article in press as: Ogata T, et al., Thoracic empyema caused by Campylobacter rectus, J Infect Chemother (2016), http://dx.doi.org/ 10.1016/j.jiac.2016.08.013
T. Ogata et al. / J Infect Chemother xxx (2016) 1e4
3
Table 1 Summary of reported extraoral infection due to C. rectus. Case Age/sex
Diagnosis
Intraoral status
Other underlying condition
Concomitant isolateb
Treatmentc
Reference
1
62/male
Chest wall abscess
Alcoholism
P: Actinomyces viscosus
Incision, antibiotic (penicillin)
[14]
2
62/female Brain abscess
Not described
P: Streptococcus intermedius
37/male
Not described
B: Actinomyces odontolyticus
4
32/female Breast abscess
P: Non-A beta-hemolytic Streptococcus
5
54/male
Subdural empyema
Not described
24/male
Vertebral abscess
7a
41/female Subdural empyema
No evident odontogenic lesion Not described
Repeated evacuation, antibiotics (VCM, CAZ, METRO, CTRX, PCG) Hemilaminectomy, antibiotics (CTRX, CLDM) Craniectomy, evacuation, antibiotics (VCM, CTRX, METRO)
[11]
6
Nipple piercing, neutropenia due to chemotherapy for lymphoma, Diabetes mellitus, sinusitis Meningoradiculitis
Repeated aspiration, antibiotics (PCG, CP, CLDM) Antibiotics (IMP/CS, penicillin, CLDM) Drainage, antibiotics (VCM, CLDM, AZT)
[15]
3
Multiple caries, severe periodontitis Well-conditioned teeth Severe periodontitis Not described
8
64/male
Necrotizing soft tissue infection
Gingivitis, multiple caries
9
56/male
Thoracic empyema
10
55/male
11
75/male
Cavernous sinus thrombosis Thoracic empyema
Gingivitis, multiple caries Previous molar tooth extraction Periodontitis
Sarcoiliitis
Ruptured intracranial aneurysm Not described
P: None P: Actinomyces sp., Eubacterium brachy B: Porphyromonas gingivalis; P: Propionibacterium acnes
[16] [10]
[12] [7]
Amputation, antibiotics (AMPC/ CVA, CPFX)
[7]
Not described
P: Porphyromonas gingivalis, diphtheroid, coagulase- negative Staphylococcus P: Fusobacterium nucleatum
Drainage, Antibiotic (AMPC/CVA)
[7]
Not described
B: None
[13]
Diabetes mellitus
P: None
Antibiotics (VCM, CLDM, PIPC/TAZ, ertapenem) Drainage, antibiotics (ABPC/SBT, GRNX, LVFX)
Present case
a
A fatal case. B: cultured from the blood, P: cultured from the purulent material. c ABPC/SBT: ampicillin-sulbactam, AMPC/CVA: amoxicillin-clavulanate, AZT: aztreonam, CAZ: ceftazidime, CLDM: clindamycin, CP: chloramphenicol, CPFX: ciprofloxacin, CTRX: ceftriaxone, GRNX: garenoxacin, IMP/CS: imipenem-cilastatin, LVFX: levofloxacin, METRO: metronidazole, PCG: penicillin G, PIPC/TAZ: piperacillin-tazobactam, VCM: vancomycin. b
massive dental plaques at the dental consultation after discharge suggests that the patient already had the chronic condition before the hospitalization, which may have affected the onset of thoracic empyema because the presence of periodontal disease is associated with elevated levels of C. rectus in intraoral materials [4,18,19]. All of the reported extraoral C. rectus infections were treated favorably except for two cases, one with fatal complication of transtentorial herniation following rupture of intracranial aneurysm and the other with amputation of a gangrenous leg [7]. Antibiotics used in the successfully managed cases include penicillin with or without combination of beta-lactamase inhibitors, ceftriaxone, imipenem, clindamycin, and metronidazole. These antibiotics have also shown high activity against collected C. rectus strains in vitro [20e22], indicating them to be drugs of choice for treatment of serious C. rectus infection. In contrast, those in the classes of quinolone and fluoroquinolone were never used solely. In the present case, we administered oral garenoxacin, an antibiotic widely effective for intraoral organisms including streptococci and anaerobes [23], following intravenous sulbactam-ampicillin because prolonged administration of antibiotics is recommended for treatment of thoracic empyema [24] but identification and drug susceptibility of the recovered organism were still undetermined even at the patient's discharge. Complete cure of the patient suggests that the recovered organism was susceptible to not only levofloxacin, whose efficacy was confirmed in vitro, but also garenoxacin. Of course, the drainage of purulent effusion, recommended in the management of thoracic empyema as well as administration of antibiotics [24,25], may have been critical for the prompt improvement of the patient's conditions. Intraoral organisms, such as streptococci and anaerobes, are major causes of pleural infection, especially in community-acquired cases [26,27]. However, recovery of C. rectus in materials associated
with lower respiratory tract infection has rarely been reported [7]. A clone library analysis of pleural effusion obtained from 26 cases of bacterial pleurisy showed that major phylotypes did not include those of intraoral campylobacteria [28], suggesting that the rarity is not due to the difficulty in culture or identification of the organism. Further studies are required to clarify the reasons why C. rectus causes pleural infection only infrequently despite common detection in intraoral materials and why the patient in the present case was predisposed to develop thoracic empyema due to the organism. Conflicts of interest None. Acknowledgment We thank Prof. John A. Tokarz for his kind assistance in preparing this manuscript. References [1] Vandamme P, Debruyne L, de Brandt E, Falsen E. Reclassification of Bacteroides ureolyticus as Campylobacter ureolyticus comb. nov, and emended description of the genus Campylobacter. Int J Syst Evol Microbiol 2010;60:2016e22. [2] Kaakoush NO, Castano-Rodriguez N, Mitchell HM, Man SM. Global epidemiology of Campylobacter infection. Clin Microbiol Rev 2015;28:687e720. [3] Vandamme P, Falsen E, Rossau R, Hoste B, Segers P, Tytgat R, et al. Revision of Campylobacter, Helicobacter, and Wolinella taxonomy: emendation of generic descriptions and proposal of Arcobacter gen. nov. Int J Syst Bacteriol 1991;41: 88e103. [4] Macuch PJ, Tanner ACR. Campylobacter species in health, gingivitis, and periodontitis. J Dent Res 2000;79:785e92.
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€ no € nen E, Paju S, Pussinen PJ, Hyvo € nen M, di Tella P, Suominen-Taipale L, [5] Ko et al. Population-based study of salivary carriage of periodontal pathogens in adults. J Clin Microbiol 2007;45:2446e51. [6] Cortelli JR, Aquino DR, Cortelli SC, Fernandes CB, de Carvalho-Filho J, Franco GCN, et al. Etiological analysis of initial colonization of periodontal pathogens in oral cavity. J Clin Microbiol 2008;46:1322e9. [7] Lam JYW, Wu AKL, Ngai DC, Teng JLL, Wong ESY, Lau SKP, et al. Three cases of severe invasive infections caused by Campylobacter rectus and first report of fatal C. rectus infection. J Clin Microbiol 2011;49:1687e91. [8] Lane DJ. 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. New York: John Wiley & Sons; 1991. p. 115e75. [9] Tanner ACR, Badger S, Lai C-H, Listgarten MA, Vosconti RA, Socransky SS. Wolinella gen. nov., Wolinella succinogenes (Vibrio succinogenes Wolin et al.) comb. nov., and description of Bacteroides gracilis sp. nov., Wolinella recta sp. nov., Campylobacter consisus sp. nov., and Eikenella corrodens from humans with periodontal disease. Int J Syst Bacteriol 1981;31:432e45. [10] Han XY, Tarrand JJ, Rice DC. Oral Campylobacter species involved in extraoral abscess: a report of three cases. J Clin Microbiol 2005;43:2513e5. [11] Walters HL, Perloff S, Jungkind D, Measley R. A Campylobacter rectus subdural empyema. Infect Dis Clin Pract 2008;16:332e4. [12] de Vries JJC, Arents NLA, Manson WL. Campylobacter species isolated from extra-oro-intestinal abscess: a report of four cases and literature review. Eur J Clin Microbiol Infect Dis 2008;27:1119e23. [13] Leo QJN, Bolger DT. Septic cavernous sinus thrombosis due to Campylobacter rectus infection. BMJ Case Rep 2014. http://dx.doi.org/10.1136/bcr-2013-203351. [14] Spiegel CA, Telford G. Isolation of Wolinella recta and Actinomyces viscosus from an actinomycotic chest wall mass. J Clin Microbiol 1984;20:1187e9. [15] Marrie TJ, Kerr E. Brain abscess due to Wolinella recta and Streptococcus intermedius. Can J Infect Dis 1990;1:31e4. [16] Harvey P, Bayardelle P, Belanger R, Fortin L. Sarcoiliitis and septicemia caused by Campylobacter rectus and Actinomyces odontolyticus. Can J Infect Dis 1994;5:133e6.
[17] Smith JA, Mullerworth MH, Westlake GW, Tatoulis J. Empyema thoracis: 14year experience in a teaching center. Ann Thorac Surg 1991;51:39e42. [18] Tanner A, Maiden MFJ, Macuch PJ, Murray LL, Kent Jr RL. Microbiota of health, gingivitis, and initial periodontitis. J Clin Periodontol 1998;25:85e98. [19] Lee H-J, Kim J-K, Cho J-Y, Lee J-M, Hong S-H. Quantification of subgingival bacterial pathogens at different stages of periodontal diseases. Curr Microbiol 2012;65:22e7. [20] Rams TE, Feik D, Slots J. Campylobacter rectus in human periodontitis. Oral Microbiol Immunol 1993;8:230e5. [21] King A, Downes J, Nord C-E, Phillips I. Antimicrobial susceptibility of nonBacteroides fragilis group anaerobic Gram-negative bacilli in Europe. Clin Microbiol Infect 1999;5:404e16. [22] Blandino G, Milazzo I, Fazio D, Puglisi S, Pisano M, Speciale A, et al. Antimicrobial susceptibility and b-lactamase production of anaerobic and aerobic bacteria isolated from pus specimens from orofacial infections. J Chemother 2007;19:495e9. [23] Takahata M, Mitsuyama J, Yamashiro Y, Yonezawa M, Araki H, Todo Y, et al. In vitro and in vivo antimicrobial activities of T-3811ME, a novel des-F(6)quinolone. Antimicrob Agents Chemother 1999;43:1077e84. [24] Davies HE, Davies RJO, Davies CWH. Management of pleural infection in adults: British Thoracic Society pleural disease guideline 2010. Thorax 2010;65:ii41e53. [25] Sahn SA. Diagnosis and management of parapneumonic effusions and empyema. Clin Infect Dis 2007;45:1480e6. [26] Brook I, Frazier EH. Aerobic and anaerobic microbiology of empyema: a retrospective review in two military hospitals. Chest 1993;103:1502e7. [27] Maskell NA, Batt S, Hedley EL, Davies CWH, Gillespie SH, Davies RJO. The bacteriology of pleural infection by genetic and standard methods and its mortality significance. Am J Respir Crit Care Med 2006;174:817e23. [28] Kawanami T, Fukuda K, Yatera K, Kido M, Mukae H, Taniguchi H. A higher significance of anaerobes: the clone library analysis of bacterial pleuristy. Chest 2011;139:600e8.
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Contents lists available at ScienceDirect
Journal of Infection and Chemotherapy journal homepage: http://www.elsevier.com/locate/jic
Case Report
Thoracic empyema caused by Campylobacter rectus Tomoyuki Ogata a, Teruo Urata b, Daisuke Nemoto c, Shigemi Hitomi d, * a
Department of Respiratory Medicine, JA Toride Medical Center, Japan Department of Clinical Laboratories, JA Toride Medical Center, Japan c Department of Clinical Laboratories, University of Tsukuba Hospital, Japan d Department of Infectious Diseases, University of Tsukuba Hospital, Japan b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 8 June 2016 Received in revised form 19 August 2016 Accepted 21 August 2016 Available online xxx
We report a case of thoracic empyema caused by Campylobacter rectus, an organism considered as a periodontal pathogen but rarely recovered from extraoral specimens. The patient fully recovered through drainage of purulent pleural fluid and administration of antibiotics. The present case illustrates that C. rectus can be a cause of not only periodontal disease but also pulmonary infection. © 2016 Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Keywords: Campylobacter rectus Thoracic empyema Sulbactam-ampicillin Garenoxacin
1. Introduction The genus Campylobacter is a group of spiral, curved, or straight rod-shaped Gram-negative bacteria. They require microaerobic and/or anaerobic conditions for their growth and typically demonstrate a characteristic corkscrew-like motion using a flagellum attached at one or both ends of cells [1]. To date, more than 15 Campylobacter species have been established or suspected as human pathogens. Gastroenteritis and extraintestinal infections, commonly due to Campylobacter jejuni and Campylobacter fetus, respectively, are major manifestations of human campylobacteriosis. These pathogens are generally reserved in domestic animals and transmitted to patients through consumption of contaminated food and water. In contrast, certain Campylobacter species reside in the human oral cavities, some of which are putatively associated with periodontal diseases [2]. Campylobacter rectus, formerly named as Wolinella recta [3], is one of the campylobacteria considered as periodontal pathogens [4]. The organism has commonly been found in various intraoral materials of both periodontically healthy and morbid individuals [5,6]. However, C. rectus has rarely been recovered from extraoral
* Corresponding author. Department of Infectious Diseases, University of Tsukuba Hospital, 2-1-1 Amakubo, Tsukuba, Ibaraki 305-8576, Japan. Fax: þ81 29 853 3479. E-mail address: [email protected] (S. Hitomi).
specimens [7]. Here, we describe a case of thoracic empyema, in which C. rectus was solely recovered from purulent pleural effusion. 2. Case report A 75-year-old Japanese man was referred because of fever and respiratory discomfort lasting for a week. He had regularly received medications for hypertension, hyperlipidemia, and diabetes mellitus with slightly impaired renal function. At the referral, the patient was alert and complained of left-sided chest pain. He had axillary temperature of 38.1 C, a heart rate of 100/min, blood pressure of 139/52, and arterial oxygen saturation at room air of 92%. Blood tests showed leukocytosis (14,320/mm3), slight hepatic injury (aspartate aminotransferase: 33 IU/L, alanine aminotransferase: 58 IU/L), renal impairment (urea nitrogen: 30 mg/dL, creatinine: 1.64 mg/dL), an elevation of the C-reactive protein level (19.44 mg/ dL), and hyperglycemia (glucose: 254 mg/dL, hemoglobin A1C: 6.7%). Chest X-ray and computed tomography revealed the presence of pleural effusion in the left thoracic cavity but no apparent infiltration in the lung field (Fig. 1). Blood culture was not performed. After hospitalization, a chest tube was inserted into the left thoracic cavity, through which purulent effusion was drained. Gram staining of the effusion exhibited many polymorphonucleocytes but no apparent microorganism. Intravenous administration of sulbactam-ampicillin (6 g/day, a dose reduced according to an
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Please cite this article in press as: Ogata T, et al., Thoracic empyema caused by Campylobacter rectus, J Infect Chemother (2016), http://dx.doi.org/ 10.1016/j.jiac.2016.08.013
2
T. Ogata et al. / J Infect Chemother xxx (2016) 1e4
using the primers 27F and 1492R [8] and sequenced directly. A homology search using the Basic Local Alignment Search Tool showed that the sequence of 1517 base pairs was most closely related to that of C. rectus JCM 6301T (GenBank accession number: AB595133.1) and contained an extra 189-base-pair portion identical to the intervening sequence of C. rectus strains described by Lam et al. (GenBank accession numbers: HQ890330 and HQ890331) [7]. With exclusion of the intervening portion, the sequence was 99.5% identical to that of C. rectus JCM 6301T. Minimum inhibitory concentrations against the recovered organism, rieux) on Brucella HK measured with the Epsilometer test (bioMe (RS) agar broth incubated anaerobically at 37 C for 72 h, were as follows; penicillin: 0.047 mg/ml, amoxicillin: 0.094 mg/ml, levofloxacin: 0.032 mg/ml, and metronidazole: 0.75 mg/ml. No organism was cultured from the discharged material obtained from the spontaneously ruptured subcutaneous abscess on day 45. Fig. 1. Computed tomography of the chest taken on the day before hospitalization at the referring facility. An open arrow indicates pleural effusion in the left thoracic cavity.
estimated creatinine clearance of 30 ml/min) and intrathoracic irrigation with normal saline through the chest tube were initiated. The patient became afebrile on the next day. The chest tube was removed on day 17 and the intravenous antibiotic was switched to oral garenoxacin (400 mg/day) on day 2. The patient was discharged on day 25 with taking the antibiotic. On day 45, the patient visited an outpatient clinic because subcutaneous abscess, having emerged at the site where the chest tube had been inserted, ruptured spontaneously. The oral antibiotic was changed to levofloxacin (500 mg/day) according to the decision of a physician in the clinic and given until day 55. Dental consultation five months after the reference revealed that the patient had periodontitis with massive dental plaque, for which only dental cleansing was given. On a follow-up after one year, the patient was well and abnormal shadows on chest X-ray disappeared almost completely. The purulent pleural effusion obtained on admission was centrifuged and the sediment was inoculated into HK Semisolid Medium (Kyokuto Pharmaceutical Industrial Co. Ltd., Tokyo, Japan). After incubation at 37 C for 48 h, the lower layer of the broth became turbid, indicating growth of motile anaerobes. The turbid portion was inoculated onto Brucella HK (RS) agar broth (Kyokuto) and incubated anaerobically. Translucent, rough, flat, nonhemolytic colonies emerged after a few days (Fig. 2a). The organism was Gram-negative, straight rod-shaped (Fig. 2b), both catalase and oxidase tests-negative, and unculturable on sheep blood agar rieux, Marcybroth under 5% CO2. Assays with API 20A (bioMe rieux) failed to l’Etoile, France) and VITEK® 2 ANC ID Card (bioMe identify the organism. Hence, a part of the 16S ribosomal RNA gene of the organism was amplified with polymerase chain reaction
3. Discussion In the present case, the drained pleural effusion appeared purulent and contained many polymorphonucleocytes, confirming the diagnosis of thoracic empyema. Although Gram staining did not reveal any apparent microorganisms, recovery of C. rectus solely from the material, which was obtained without previous administration of antibiotics, indicates the recovered organism to be the causative agent. The present case illustrates that C. rectus, an organism generally considered as a periodontal pathogen, can be a cause of lower respiratory tract infection. C. rectus is a small, unbranched, straight Gram-negative organism. Other typical characteristics include growth in an anaerobic condition, motility, formation of translucent colonies on blood agar plates, and negative reaction to both catalase and oxidase tests [9], all of which the organism recovered in the present case exhibited. Our attempt to identify the recovered organism using commercial identification kits for anaerobes failed because C. rectus was not included in their lists of identifiable organisms. Instead, we utilized a phylogenic analysis of the 16S ribosomal RNA gene, through which C. rectus strains recovered in recent cases of extraoral infection were also identified [7,10e13]. To our knowledge, ten cases of extraoral C. rectus infection have been reported in the literature (Table 1) [7,10e16]. Normally sterile organs were involved without preceding injury in approximately two thirds of the cases [7,11e13,15,16], indicating hematogenous dissemination of causative organisms. In the present case, we speculate that the causative organism was also transmitted to the pleural space via the bloodstream, albeit a less common mode of transmission in cases of empyema [17], because the patient had neither apparent risk nor history of both aspiration and thoracic trauma and radiological abnormality in the left lung field was minimal at the referral. The indication of periodontitis with
Fig. 2. Colonies (a) and Gram staining (b) of organisms after anaerobic incubation on Brucella HK (RS) agar broth for 3 days. A bar indicates 10 mm.
Please cite this article in press as: Ogata T, et al., Thoracic empyema caused by Campylobacter rectus, J Infect Chemother (2016), http://dx.doi.org/ 10.1016/j.jiac.2016.08.013
T. Ogata et al. / J Infect Chemother xxx (2016) 1e4
3
Table 1 Summary of reported extraoral infection due to C. rectus. Case Age/sex
Diagnosis
Intraoral status
Other underlying condition
Concomitant isolateb
Treatmentc
Reference
1
62/male
Chest wall abscess
Alcoholism
P: Actinomyces viscosus
Incision, antibiotic (penicillin)
[14]
2
62/female Brain abscess
Not described
P: Streptococcus intermedius
37/male
Not described
B: Actinomyces odontolyticus
4
32/female Breast abscess
P: Non-A beta-hemolytic Streptococcus
5
54/male
Subdural empyema
Not described
24/male
Vertebral abscess
7a
41/female Subdural empyema
No evident odontogenic lesion Not described
Repeated evacuation, antibiotics (VCM, CAZ, METRO, CTRX, PCG) Hemilaminectomy, antibiotics (CTRX, CLDM) Craniectomy, evacuation, antibiotics (VCM, CTRX, METRO)
[11]
6
Nipple piercing, neutropenia due to chemotherapy for lymphoma, Diabetes mellitus, sinusitis Meningoradiculitis
Repeated aspiration, antibiotics (PCG, CP, CLDM) Antibiotics (IMP/CS, penicillin, CLDM) Drainage, antibiotics (VCM, CLDM, AZT)
[15]
3
Multiple caries, severe periodontitis Well-conditioned teeth Severe periodontitis Not described
8
64/male
Necrotizing soft tissue infection
Gingivitis, multiple caries
9
56/male
Thoracic empyema
10
55/male
11
75/male
Cavernous sinus thrombosis Thoracic empyema
Gingivitis, multiple caries Previous molar tooth extraction Periodontitis
Sarcoiliitis
Ruptured intracranial aneurysm Not described
P: None P: Actinomyces sp., Eubacterium brachy B: Porphyromonas gingivalis; P: Propionibacterium acnes
[16] [10]
[12] [7]
Amputation, antibiotics (AMPC/ CVA, CPFX)
[7]
Not described
P: Porphyromonas gingivalis, diphtheroid, coagulase- negative Staphylococcus P: Fusobacterium nucleatum
Drainage, Antibiotic (AMPC/CVA)
[7]
Not described
B: None
[13]
Diabetes mellitus
P: None
Antibiotics (VCM, CLDM, PIPC/TAZ, ertapenem) Drainage, antibiotics (ABPC/SBT, GRNX, LVFX)
Present case
a
A fatal case. B: cultured from the blood, P: cultured from the purulent material. c ABPC/SBT: ampicillin-sulbactam, AMPC/CVA: amoxicillin-clavulanate, AZT: aztreonam, CAZ: ceftazidime, CLDM: clindamycin, CP: chloramphenicol, CPFX: ciprofloxacin, CTRX: ceftriaxone, GRNX: garenoxacin, IMP/CS: imipenem-cilastatin, LVFX: levofloxacin, METRO: metronidazole, PCG: penicillin G, PIPC/TAZ: piperacillin-tazobactam, VCM: vancomycin. b
massive dental plaques at the dental consultation after discharge suggests that the patient already had the chronic condition before the hospitalization, which may have affected the onset of thoracic empyema because the presence of periodontal disease is associated with elevated levels of C. rectus in intraoral materials [4,18,19]. All of the reported extraoral C. rectus infections were treated favorably except for two cases, one with fatal complication of transtentorial herniation following rupture of intracranial aneurysm and the other with amputation of a gangrenous leg [7]. Antibiotics used in the successfully managed cases include penicillin with or without combination of beta-lactamase inhibitors, ceftriaxone, imipenem, clindamycin, and metronidazole. These antibiotics have also shown high activity against collected C. rectus strains in vitro [20e22], indicating them to be drugs of choice for treatment of serious C. rectus infection. In contrast, those in the classes of quinolone and fluoroquinolone were never used solely. In the present case, we administered oral garenoxacin, an antibiotic widely effective for intraoral organisms including streptococci and anaerobes [23], following intravenous sulbactam-ampicillin because prolonged administration of antibiotics is recommended for treatment of thoracic empyema [24] but identification and drug susceptibility of the recovered organism were still undetermined even at the patient's discharge. Complete cure of the patient suggests that the recovered organism was susceptible to not only levofloxacin, whose efficacy was confirmed in vitro, but also garenoxacin. Of course, the drainage of purulent effusion, recommended in the management of thoracic empyema as well as administration of antibiotics [24,25], may have been critical for the prompt improvement of the patient's conditions. Intraoral organisms, such as streptococci and anaerobes, are major causes of pleural infection, especially in community-acquired cases [26,27]. However, recovery of C. rectus in materials associated
with lower respiratory tract infection has rarely been reported [7]. A clone library analysis of pleural effusion obtained from 26 cases of bacterial pleurisy showed that major phylotypes did not include those of intraoral campylobacteria [28], suggesting that the rarity is not due to the difficulty in culture or identification of the organism. Further studies are required to clarify the reasons why C. rectus causes pleural infection only infrequently despite common detection in intraoral materials and why the patient in the present case was predisposed to develop thoracic empyema due to the organism. Conflicts of interest None. Acknowledgment We thank Prof. John A. Tokarz for his kind assistance in preparing this manuscript. References [1] Vandamme P, Debruyne L, de Brandt E, Falsen E. Reclassification of Bacteroides ureolyticus as Campylobacter ureolyticus comb. nov, and emended description of the genus Campylobacter. Int J Syst Evol Microbiol 2010;60:2016e22. [2] Kaakoush NO, Castano-Rodriguez N, Mitchell HM, Man SM. Global epidemiology of Campylobacter infection. Clin Microbiol Rev 2015;28:687e720. [3] Vandamme P, Falsen E, Rossau R, Hoste B, Segers P, Tytgat R, et al. Revision of Campylobacter, Helicobacter, and Wolinella taxonomy: emendation of generic descriptions and proposal of Arcobacter gen. nov. Int J Syst Bacteriol 1991;41: 88e103. [4] Macuch PJ, Tanner ACR. Campylobacter species in health, gingivitis, and periodontitis. J Dent Res 2000;79:785e92.
Please cite this article in press as: Ogata T, et al., Thoracic empyema caused by Campylobacter rectus, J Infect Chemother (2016), http://dx.doi.org/ 10.1016/j.jiac.2016.08.013
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Please cite this article in press as: Ogata T, et al., Thoracic empyema caused by Campylobacter rectus, J Infect Chemother (2016), http://dx.doi.org/ 10.1016/j.jiac.2016.08.013