CASE REPORT
Empyema Caused by Prevotella bivia Complicating an Unusual Case of Spontaneous Chylothorax Alessandro Di Marco Berardino,a Riccardo Inchingolo,a Andrea Smargiassi,a Antonina Re,a Riccardo Torelli,b Barbara Fiori,b Tiziana d’Inzeo,b Giuseppe Maria Corbo,a Salvatore Valente,a Maurizio Sanguinetti,b Teresa Spanub Pulmonary Medicine Department, Policlinico Universitario A. Gemelli, Università Cattolica del Sacro Cuore, Rome, Italya; Institute of Microbiology, Policlinico Universitario A. Gemelli, Università Cattolica del Sacro Cuore, Rome, Italyb
CASE REPORT
A
78-year-old man was admitted to the hospital with a 1-month history of weight loss (10 kg), asthenia, dyspnea, dry cough, right chest pain, and low-grade fever (37.1°C on admission). He was an exsmoker (60 packs/year) with moderately severe chronic obstructive pulmonary disease that was not associated with chronic respiratory failure. He also suffered from chronic periodontitis, was known to harbor the factor V Leiden mutation, and had been treated 3 months earlier for an episode of pulmonary microembolism. The physical examination revealed diminished chest expansion, tachypnea (24 breaths/min), reduced vesicular breathing on the right, and bilateral rales. The white blood cell (WBC) count was 14.8 ⫻ 109/liter with 94% neutrophils. Arterial blood gas analysis on room air revealed severe hypoxemia-compensated respiratory acidosis. A chest X-ray showed a right pleural effusion without clear evidence of consolidation (Fig. 1a). Ultrasound analysis disclosed two loculated pleural effusions in the right hemithorax. Computed tomography (CT) revealed two large right pleural effusions (anterior and lateral), a small posterior effusion, right middle lobe consolidation, and diffuse, bilateral “ground-glass” opacities (Fig. 1b). Empirical treatment with intravenous levofloxacin (750 mg every 24 h [q24h]) was started, and a chest tube was inserted on the right midaxillary line. A 50-ml sample of purulent fluid was characterized by a pH of 6.8, a lactate dehydrogenase (LDH) level of 1,320 IU/liter, a WBC count of 10,840 cells/l (96% neutrophils), high triglyceride levels (270 mg/dl versus serum level of 67 mg/dl), a low cholesterol level (10 mg/dl), and no identifiable cholesterol crystals. Microscopic examination of the fluid showed numerous neutrophils but no parasites or ova (1–4). Gram staining revealed short rod-shaped bacteria, and cytology was negative for malignancy. Ziehl-Nielsen staining detected no acid alcohol-resistant bacteria. A diagnosis of chylothorax with pleural infection was made. Two other chest tubes were inserted, and drainage samples from each were sent to the microbiology laboratory. In accordance with our routine protocol, the pleural fluid specimens were subjected to aerobic cultures on MacConkey (35°C) and Sabourad (30°C) agars; microaerobic cultures (35°C in air with 5% CO2); anaerobic cultures in an anaerobic growth chamber (Forma Scientific, Marietta, OH) containing 10% vol/vol hydrogen, 10% carbon dioxide, and 80% nitrogen on brucella blood, Columbia, and Schaedler agars (35°C); and aerobic and anaerobic cultures on enriched thioglycolate medium with vitamin K and hemin (plates and slants from
1284
jcm.asm.org
Journal of Clinical Microbiology
Becton, Dickinson Diagnostic Systems, Sparks, MD, and bioMérieux, Marcy l’Etoile, France). Specimens were also inoculated onto Lowenstein-Jensen solid medium and in MGIT liquid medium (Becton, Dickinson). Three sets of blood cultures (Becton, Dickinson) were drawn. Lymphatic scintigraphy with technetium-99m (99mTc)-human albumin revealed no possible sources of chyle leakage. Aerobic and microaerobic cultures yielded no growth, but after 36 h of incubation, anaerobic cultures of all three samples produced small, circular, convex, translucent, shiny white colonies of Gram-negative rods. Matrix-assisted laser desorption ionization–time of flight (MALDI-TOF) mass spectrometry (Bruker Biotyper system, version 3.1 software and database; Bruker Daltonik GmbH, Bremen, Germany) identified the isolates as Prevotella bivia with log (scores) of 1.78 to 1.81 (5). The isolates exhibited no growth in the presence of bile and no evidence of esculin hydrolysis. In light of these findings, the patient was switched to intravenous clindamycin treatment (600 mg/8 h), and the in vitro susceptibility of the isolates was assessed with the Etest (bioMérieux, Marcy l’Etoile, France), as previously described (6). Interpreted according to EUCAST breakpoints (7), the results revealed susceptibility to amoxicillin-clavulanate (MIC, 0.06 mg/liter), piperacillin-tazobactam (MIC, 0.12 mg/liter), meropenem (MIC, 0.002 mg/liter), clindamycin (MIC, 0.016 mg/liter), metronidazole (MIC, 0.06 mg/liter), and chloramphenicol (MIC, 2 mg/liter) and full resistance to penicillin (MIC, ⬎0.5 mg/liter). Beta-lactamase positivity was documented by the cefinase disk method. All of the blood cultures were negative. Chest tube drainage cultures for Mycobacterium tuberculosis and fungi yielded no growth. Isolates were retested on the Vitek 2 system with ANC cards (both from bioMérieux, Marcy l’Etoile, France), which identified all as P. bivia. The species-level identification was confirmed by 16S rRNA gene sequencing (100% match with P. bivia strain SEQ227
Received 22 November 2013 Returned for modification 5 December 2013 Accepted 17 January 2014 Published ahead of print 22 January 2014 Editor: A. J. McAdam Address correspondence to Riccardo Inchingolo, [email protected]. A.D.M.B. and R.I. contributed equally to this article. Copyright © 2014, American Society for Microbiology. All Rights Reserved. doi:10.1128/JCM.03282-13
p. 1284 –1286
April 2014 Volume 52 Number 4
Downloaded from http://jcm.asm.org/ on March 8, 2015 by WEST VIRGINIA UNIV
Spontaneous chylothorax is rare in adults. We present an unusual case that was complicated by Prevotella bivia empyema. Full recovery was achieved with chest tube drainage and prompt treatment with intravenous clindamycin.
Case Report
[GenBank accession no. JN867300]). On day 10, after 7 days of clindamycin treatment, the patient was transferred to a rehabilitation center with a prescription for oral clindamycin (300 mg every 6 h for 4 weeks). The 6-month follow-up assessment revealed full clinical and microbiological biological resolution of the empyema.
In 1990, 16 Bacteroides species were transferred to form the new genus Prevotella, which now includes 48 validated species of obligately anaerobic, pleomorphic, Gram-negative rods (8; http: //www.bacterio.net/). Human infections ascribed to P. bivia (or “Bacterioides bivius,” as it was known then) had first been reported in 1987 (9). They frequently involve the female urogenital tract or, less commonly, the oral cavity, and they have been linked to an increased risk of preterm delivery (10, 11), an effect attributed to increased prostaglandin formation (12). Recovery of P. bivia, alone or with other pathogens, has also been sporadically reported in patients with other types of infection (9, 13–27), including one with pleural effusions (9) and two with empyema (14). Unfortunately, none of the latter reports described the clinical findings of the cases or specified whether the infections were monomicrobial or polymicrobial. Chylothorax and chylous pleural effusions are uncommon in adults (28, 29). They are diagnosed when the pleural drainage contains high levels of triglycerides (⬎110 mg/dl) and no cholesterol crystals and the supernatant appears milky and opaque (28). Causes vary widely (malignancy, natural or surgical trauma, deepvein thrombosis, sarcoidosis, congestive heart failure, malformations of the lymphatic trunks, parasitic infections), and some cases are idiopathic (3, 28–30). Our patient had no history of surgery or trauma, and lymphoscintigraphy showed no evidence of a chyle leak. Chest CT scans performed to identify possible neoplastic disease revealed only nonspecific findings in the retrocrural area suggestive of inflammation, and there were still no signs of malignancy at the 1-year follow-up visit. Hepatic disease was excluded, and there were no signs or symptoms of lymphatic disorders. Pleural effusion can be provoked by any change in the pulmonary venous hydrostatic pressure, lymphatic pressure, or oncotic pressure, as well as by local tissue trauma or inflammation. Hydrostatic mechanisms seem to have been the most likely cause of our patient’s chylothorax. The cardiology work-up had revealed clear evidence of chronic cor pulmonale, with a left ventric-
April 2014 Volume 52 Number 4
ular ejection fraction of 40% and a pulmonary arterial pressure of 54 mm Hg. In addition, the patient’s recent episode of pulmonary microembolism might also have caused additional transient increases in the hydrostatic pressure of the pulmonary circulation. Collectively, these increases could have resulted in the leakage of chyle into the pleural space. Pleural infection is a significant and increasingly common cause of morbidity and mortality worldwide (31). Persistent infections can lead to empyema, which is manifested by pus in the pleural fluid, positive culture, or positive Gram’s stain (32). The infection is usually associated with pneumonia, but primary infections without evidence of parenchymal lung involvement have been reported (32). In the case described here, a simple chylous pleural effusion evolved into multiloculated fibrinopurulent collections associated with clinical and biochemical features of sepsis. The original effusion impeded reexpansion of the lung, impairing pulmonary function and creating a persistent pleural space at risk for infection, but it seems likely that alterations of the microbiota ecosystem also contributed to the onset of infection (31). Anaerobic organisms are being recovered more and more frequently from patients with empyema, particularly those who, like our patient, are elderly with comorbidities and/or poor oral hygiene (31). Indeed, our patient had been suffering for years from chronic periodontitis. Delayed diagnosis and treatment of empyema are common (31). The clinical presentation varies. As in this case, the course may be indolent with nonspecific constitutional symptoms such as weight loss and pleuritic chest pain. Prompt drainage and effective antimicrobial treatment are essential for successful management of empyema (31). Our patient was initially treated with levofloxacin, but as soon as the pleural isolates were identified with MALDI-TOF mass spectrometry (36 h after the culture was submitted), he was switched to clindamycin, which is characterized by good penetration of the pleural space (33). Twenty-four hours later, the appropriateness of this empirical decision was confirmed by in vitro susceptibility data. However, clindamycin resistance in Prevotella species is reportedly on the rise, so antibiogram guidance is imperative in severe infections caused by these organisms (6). ACKNOWLEDGMENTS We thank Marian Kent for editing the manuscript. This work was supported by Università Cattolica del Sacro Cuore (Fondi Ateneo, Linea D1-2012).
jcm.asm.org 1285
Downloaded from http://jcm.asm.org/ on March 8, 2015 by WEST VIRGINIA UNIV
FIG 1 Imaging findings. As performed at admission, a chest X-ray shows the right lateral pleural effusions with loculated features (a) and a CT scan shows the two loculated pleural effusions described in the text (b).
Case Report
REFERENCES
1286
jcm.asm.org
15. Busch N, Mertens PR, Schonfelder T, Nguyen H, Marschall HU, Kierdorf H, Haase G, Urhahn R, Sieberth HG, Matern S. 1996. Lemierre’s posttonsillitis sepsis with meningitis and intravascular consumption coagulopathy as complication of infectious mononucleosis with pansinusitis. Dtsch. Med. Wochenschr. 121:94 –98. (In German.) http://dx.doi.org /10.1055/s-2008-1042978. 16. Dumitriu S, Ba˘ncescu G, Murea A, Skaug N. 1998. Isolation and speciation of Prevotella strains from periodontal abscesses. Roum. Arch. Microbiol. Immunol. 57:5–10. 17. Schindl A, Schön H. 1999. Foot infection with Prevotella bivia, P. oralis and P. loescheii after wound licking. J. Med. Microbiol. 48:109. 18. Alegre-Sancho J, Juanola X, Narvaez FJ, Roig-Escofet D. 2000. Septic arthritis due to Prevotella bivia in a patient with rheumatoid arthritis. Joint Bone Spine 67:228 –229. 19. Hoshino T, Nakamura A. 2002. Clinical and bacteriological features of six cases with intracranial abscess in childhood. Kansenshogaku Zasshi 76: 83– 88. (In Japanese.) 20. Riesbeck K. 2003. Paronychia due to Prevotella bivia that resulted in amputation: fast and correct bacteriological diagnosis is crucial. J. Clin. Microbiol. 41:4901– 4903. http://dx.doi.org/10.1128/JCM.41.10.4901-4903.2003. 21. Huits R, Van Assen S, Wildeboer-Veloo AC, Verschuuren EA, Koeter GH. 2006. Prevotella bivia necrobacillosis following infectious mononucleosis. J. Infect. 53:e59 – e63. http://dx.doi.org/10.1016/j.jinf.2005.10.016. 22. Laiho K, Kotilainen P. 2001. Septic arthritis due to Prevotella bivia after intra-articular hip joint injection. Joint Bone Spine 68:443– 444. http://dx .doi.org/10.1016/S1297-319X(01)00303-7. 23. Nalmas S, Bishburg E, Chan T. 2007. Streptococcus constellatus and Prevotella bivia penile abscess. ScientificWorldJournal 7:1631–1633. http: //dx.doi.org/10.1100/tsw.2007.240. 24. Salman AS, Baharoon SA. 2009. Septic arthritis of the knee joint secondary to Prevotella bivia. Saudi Med. J. 30:426 – 428. 25. Hsu GJ, Chen CR, Lai MC, Luh SP. 2009. Chest wall abscess due to Prevotella bivia. J. Zhejiang Univ. Sci. B 10:233–236. http://dx.doi.org/10 .1631/jzus.B0820289. 26. Sagristà M, Martin-Ezquerra G, Gallardo F, Membrilla E, Salazar AJ, Salvadó M, Gómez J, Pujol RM. 2012. Inguinal syndrome secondary to Prevotella bivia after accidental bite in orogenital sex. Sex Transm. Infect. 88:250 –251. http://dx.doi.org/10.1136/sextrans-2011-050348. 27. Janssen S, van Donselaar-van der Pant KA, van der Weerd NC, Develter W, Bemelman FJ, Grobusch MP, Idu MM, Ten Berge IJ. 2013. Abdominal wall phlebitis due to Prevotella bivia following renal transplantation in a patient with an occluded inferior vena cava. Infection 41:271–274. http: //dx.doi.org/10.1007/s15010-012-0335-5. 28. Light RW. 2007. Chylothorax and pseudochylothorax, p 346 –361. In Light RW (ed), Pleural diseases, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA. 29. Skouras V, Kalomenidis I. 2010. Chylothorax: diagnostic approach. Curr. Opin. Pulm. Med. 16:387–393. http://dx.doi.org/10.1097/MCP.0b 013e328338dde2. 30. Agrawal V, Sahn S. 2008. Lipid pleural effusion. Am. J. Med. Sci. 335:16 – 20. http://dx.doi.org/10.1097/MAJ.0b013e31815d2634. 31. Davies HE, Davies RJO, Davies CWH, Pleural Disease Guideline Group. 2010. Management of pleural infection in adults: British Thoracic Society pleural disease guideline 2010. Thorax 65(Suppl 2):41–53. http: //dx.doi.org/10.1136/thx.2010.137000. 32. Ahmed RA, Marrie TJ, Huang JQ. 2006. Thoracic empyema in patients with community-acquired pneumonia. Am. J. Med. 119:877– 883. http: //dx.doi.org/10.1016/j.amjmed.2006.03.042. 33. Teixeira LR, Sasse SA, Villarino MA, Nguyen T, Mulligan ME, Light RW. 2000. Antibiotic levels in empyemic pleural fluid. Chest 117:1734 – 1739. http://dx.doi.org/10.1378/chest.117.6.1734.
Journal of Clinical Microbiology
Downloaded from http://jcm.asm.org/ on March 8, 2015 by WEST VIRGINIA UNIV
1. Mantini C, Souppart L, Noël C, Duong TH, Mornet M, Carroger G, Dupont P, Masseret EGoustille J, Capron M, Duboucher C, Dei-Cas E, Viscogliosi E. 2009. Molecular characterization of a new Tetratrichomonas species in a patient with empyema. J. Clin. Microbiol. 47:2336 –2339. http://dx.doi.org/10.1128/JCM.00353-09. 2. Lopez-Escamilla E, Sanchez-Aguillon F, Alatorre-Fernandez CP, Aguilar-Zapata D, Arroyo-Escalante S, Arellano T, Moncada-Barron D, Romero-Valdovinos M, Martinez-Hernandez F, Rodriguez-Zulueta P, Maravilla P. 2013. New tetratrichomonas species in two patients with pleural empyema. J. Clin. Microbiol. 51:3143–3146. http://dx.doi.org/10 .1128/JCM.01056-13. 3. Wright RS, Jean M, Rochelle K, Fisk D. 2011. Chylothorax caused by Paragonimus westermani in a native Californian. Chest 140:1064 –1066. http://dx.doi.org/10.1378/chest.10-2168. 4. Baron EJ, Miller JM, Weinstein MP, Richter SS, Gilligan PH, Thomson RB, Jr, Bourbeau P, Carroll KC, Kehl SC, Dunne WM, Robinson-Dunn B, Schwartzman JD, Chapin KC, Snyder JW, Forbes BA, Patel R, Rosenblatt JE, Pritt BS. 2013. A guide to utilization of the microbiology laboratory for diagnosis of infectious diseases: 2013 recommendations by the Infectious Diseases Society of America (IDSA) and the American Society for Microbiology (ASM) (a). Clin. Infect. Dis. 57:e22– e121. http://dx .doi.org/10.1093/cid/cit278. 5. Wybo I, Soetens O, De Bel A, Echahidi F, Vancutsem E, Vandoorslaer K, Piérard D. 2012. Species identification of clinical Prevotella isolates by matrix-assisted laser desorption ionization–time of flight mass spectrometry. J. Clin. Microbiol. 50:1415–1418. http://dx.doi.org/10.1128/JCM .06326-11. 6. Wybo I, Van den Bossche D, Soetens O, Vekens E, Vandoorslaer K, Claeys G, Glupczynski Y, Ieven M, Melin P, Nonhoff C, RodriguezVillalobos H, Verhaegen J, Piérard D. 5 September 2013. Fourth Belgian multicentre survey of antibiotic susceptibility of anaerobic bacteria. J. Antimicrob. Chemother. http://dx.doi.org/10.1093/jac/dkt344. 7. The European Committee on Antimicrobial Susceptibility Testing. 1 January 2014. Clinical breakpoints. Document version 4.0. http://www .eucast.org/clinical_breakpoints. 8. Shah HN, Collins DM. 1990. Prevotella, a new genus to include Bacteroides melaninogenicus and related species formerly classified in the genus Bacteroides. Int. J. Syst. Bacteriol. 40:205–208. http://dx.doi.org/10.1099 /00207713-40-2-205. 9. Holdeman LV, Johnson JL. 1977. Bacteroides disiens sp. nov. and Bacteroides bivius sp. nov. from human clinical infections. Int. J. Syst. Bacteriol. 27:337–345. http://dx.doi.org/10.1099/00207713-27-4-337. 10. Marconi C, de Andrade Ramos BR, Peraçoli JC, Donders GG, Da Silva MG. 2011. Amniotic fluid interleukin-1 beta and interleukin-6, but not interleukin-8 correlate with microbial invasion of the amniotic cavity in preterm labor. Am. J. Reprod. Immunol. 65:549 –556. http://dx.doi.org /10.1111/j.1600-0897.2010.00940.x. 11. Strömbeck L, Sandros J, Holst E, Madianos P, Nannmark U, Papapanou P, Mattsby-Baltzer I. 2007. Prevotella bivia can invade human cervix epithelial (HeLa) cells. APMIS 115:241–251. http://dx.doi.org/10 .1111/j.1600-0463.2007.apm_512.x. 12. Puapermpoonsiri S, Kato N, Watanabe K, Ueno K, Chongsomchai C, Lumbiganon P. 1996. Vaginal microflora associated with bacterial vaginosis in Japanese and Thai pregnant women. Clin. Infect. Dis. 23:748 – 752. http://dx.doi.org/10.1093/clinids/23.4.748. 13. Kentos A, Motte S, Nonhoff F, Jacobs F, De Smet JM, Serruys E, Thys JP. 1994. Prevotella bivia as an unusual cause of endocarditis. Eur. J. Clin. Microbiol. Infect. Dis. 13:142–145. http://dx.doi.org/10.1007/BF01982187. 14. Brook I, Frazier EH. 1993. Aerobic and anaerobic microbiology of empyema. A retrospective review in two military hospitals. Chest 103:1502– 1507.
Empyema Caused by Prevotella bivia Complicating an Unusual Case of Spontaneous Chylothorax Alessandro Di Marco Berardino,a Riccardo Inchingolo,a Andrea Smargiassi,a Antonina Re,a Riccardo Torelli,b Barbara Fiori,b Tiziana d’Inzeo,b Giuseppe Maria Corbo,a Salvatore Valente,a Maurizio Sanguinetti,b Teresa Spanub Pulmonary Medicine Department, Policlinico Universitario A. Gemelli, Università Cattolica del Sacro Cuore, Rome, Italya; Institute of Microbiology, Policlinico Universitario A. Gemelli, Università Cattolica del Sacro Cuore, Rome, Italyb
CASE REPORT
A
78-year-old man was admitted to the hospital with a 1-month history of weight loss (10 kg), asthenia, dyspnea, dry cough, right chest pain, and low-grade fever (37.1°C on admission). He was an exsmoker (60 packs/year) with moderately severe chronic obstructive pulmonary disease that was not associated with chronic respiratory failure. He also suffered from chronic periodontitis, was known to harbor the factor V Leiden mutation, and had been treated 3 months earlier for an episode of pulmonary microembolism. The physical examination revealed diminished chest expansion, tachypnea (24 breaths/min), reduced vesicular breathing on the right, and bilateral rales. The white blood cell (WBC) count was 14.8 ⫻ 109/liter with 94% neutrophils. Arterial blood gas analysis on room air revealed severe hypoxemia-compensated respiratory acidosis. A chest X-ray showed a right pleural effusion without clear evidence of consolidation (Fig. 1a). Ultrasound analysis disclosed two loculated pleural effusions in the right hemithorax. Computed tomography (CT) revealed two large right pleural effusions (anterior and lateral), a small posterior effusion, right middle lobe consolidation, and diffuse, bilateral “ground-glass” opacities (Fig. 1b). Empirical treatment with intravenous levofloxacin (750 mg every 24 h [q24h]) was started, and a chest tube was inserted on the right midaxillary line. A 50-ml sample of purulent fluid was characterized by a pH of 6.8, a lactate dehydrogenase (LDH) level of 1,320 IU/liter, a WBC count of 10,840 cells/l (96% neutrophils), high triglyceride levels (270 mg/dl versus serum level of 67 mg/dl), a low cholesterol level (10 mg/dl), and no identifiable cholesterol crystals. Microscopic examination of the fluid showed numerous neutrophils but no parasites or ova (1–4). Gram staining revealed short rod-shaped bacteria, and cytology was negative for malignancy. Ziehl-Nielsen staining detected no acid alcohol-resistant bacteria. A diagnosis of chylothorax with pleural infection was made. Two other chest tubes were inserted, and drainage samples from each were sent to the microbiology laboratory. In accordance with our routine protocol, the pleural fluid specimens were subjected to aerobic cultures on MacConkey (35°C) and Sabourad (30°C) agars; microaerobic cultures (35°C in air with 5% CO2); anaerobic cultures in an anaerobic growth chamber (Forma Scientific, Marietta, OH) containing 10% vol/vol hydrogen, 10% carbon dioxide, and 80% nitrogen on brucella blood, Columbia, and Schaedler agars (35°C); and aerobic and anaerobic cultures on enriched thioglycolate medium with vitamin K and hemin (plates and slants from
1284
jcm.asm.org
Journal of Clinical Microbiology
Becton, Dickinson Diagnostic Systems, Sparks, MD, and bioMérieux, Marcy l’Etoile, France). Specimens were also inoculated onto Lowenstein-Jensen solid medium and in MGIT liquid medium (Becton, Dickinson). Three sets of blood cultures (Becton, Dickinson) were drawn. Lymphatic scintigraphy with technetium-99m (99mTc)-human albumin revealed no possible sources of chyle leakage. Aerobic and microaerobic cultures yielded no growth, but after 36 h of incubation, anaerobic cultures of all three samples produced small, circular, convex, translucent, shiny white colonies of Gram-negative rods. Matrix-assisted laser desorption ionization–time of flight (MALDI-TOF) mass spectrometry (Bruker Biotyper system, version 3.1 software and database; Bruker Daltonik GmbH, Bremen, Germany) identified the isolates as Prevotella bivia with log (scores) of 1.78 to 1.81 (5). The isolates exhibited no growth in the presence of bile and no evidence of esculin hydrolysis. In light of these findings, the patient was switched to intravenous clindamycin treatment (600 mg/8 h), and the in vitro susceptibility of the isolates was assessed with the Etest (bioMérieux, Marcy l’Etoile, France), as previously described (6). Interpreted according to EUCAST breakpoints (7), the results revealed susceptibility to amoxicillin-clavulanate (MIC, 0.06 mg/liter), piperacillin-tazobactam (MIC, 0.12 mg/liter), meropenem (MIC, 0.002 mg/liter), clindamycin (MIC, 0.016 mg/liter), metronidazole (MIC, 0.06 mg/liter), and chloramphenicol (MIC, 2 mg/liter) and full resistance to penicillin (MIC, ⬎0.5 mg/liter). Beta-lactamase positivity was documented by the cefinase disk method. All of the blood cultures were negative. Chest tube drainage cultures for Mycobacterium tuberculosis and fungi yielded no growth. Isolates were retested on the Vitek 2 system with ANC cards (both from bioMérieux, Marcy l’Etoile, France), which identified all as P. bivia. The species-level identification was confirmed by 16S rRNA gene sequencing (100% match with P. bivia strain SEQ227
Received 22 November 2013 Returned for modification 5 December 2013 Accepted 17 January 2014 Published ahead of print 22 January 2014 Editor: A. J. McAdam Address correspondence to Riccardo Inchingolo, [email protected]. A.D.M.B. and R.I. contributed equally to this article. Copyright © 2014, American Society for Microbiology. All Rights Reserved. doi:10.1128/JCM.03282-13
p. 1284 –1286
April 2014 Volume 52 Number 4
Downloaded from http://jcm.asm.org/ on March 8, 2015 by WEST VIRGINIA UNIV
Spontaneous chylothorax is rare in adults. We present an unusual case that was complicated by Prevotella bivia empyema. Full recovery was achieved with chest tube drainage and prompt treatment with intravenous clindamycin.
Case Report
[GenBank accession no. JN867300]). On day 10, after 7 days of clindamycin treatment, the patient was transferred to a rehabilitation center with a prescription for oral clindamycin (300 mg every 6 h for 4 weeks). The 6-month follow-up assessment revealed full clinical and microbiological biological resolution of the empyema.
In 1990, 16 Bacteroides species were transferred to form the new genus Prevotella, which now includes 48 validated species of obligately anaerobic, pleomorphic, Gram-negative rods (8; http: //www.bacterio.net/). Human infections ascribed to P. bivia (or “Bacterioides bivius,” as it was known then) had first been reported in 1987 (9). They frequently involve the female urogenital tract or, less commonly, the oral cavity, and they have been linked to an increased risk of preterm delivery (10, 11), an effect attributed to increased prostaglandin formation (12). Recovery of P. bivia, alone or with other pathogens, has also been sporadically reported in patients with other types of infection (9, 13–27), including one with pleural effusions (9) and two with empyema (14). Unfortunately, none of the latter reports described the clinical findings of the cases or specified whether the infections were monomicrobial or polymicrobial. Chylothorax and chylous pleural effusions are uncommon in adults (28, 29). They are diagnosed when the pleural drainage contains high levels of triglycerides (⬎110 mg/dl) and no cholesterol crystals and the supernatant appears milky and opaque (28). Causes vary widely (malignancy, natural or surgical trauma, deepvein thrombosis, sarcoidosis, congestive heart failure, malformations of the lymphatic trunks, parasitic infections), and some cases are idiopathic (3, 28–30). Our patient had no history of surgery or trauma, and lymphoscintigraphy showed no evidence of a chyle leak. Chest CT scans performed to identify possible neoplastic disease revealed only nonspecific findings in the retrocrural area suggestive of inflammation, and there were still no signs of malignancy at the 1-year follow-up visit. Hepatic disease was excluded, and there were no signs or symptoms of lymphatic disorders. Pleural effusion can be provoked by any change in the pulmonary venous hydrostatic pressure, lymphatic pressure, or oncotic pressure, as well as by local tissue trauma or inflammation. Hydrostatic mechanisms seem to have been the most likely cause of our patient’s chylothorax. The cardiology work-up had revealed clear evidence of chronic cor pulmonale, with a left ventric-
April 2014 Volume 52 Number 4
ular ejection fraction of 40% and a pulmonary arterial pressure of 54 mm Hg. In addition, the patient’s recent episode of pulmonary microembolism might also have caused additional transient increases in the hydrostatic pressure of the pulmonary circulation. Collectively, these increases could have resulted in the leakage of chyle into the pleural space. Pleural infection is a significant and increasingly common cause of morbidity and mortality worldwide (31). Persistent infections can lead to empyema, which is manifested by pus in the pleural fluid, positive culture, or positive Gram’s stain (32). The infection is usually associated with pneumonia, but primary infections without evidence of parenchymal lung involvement have been reported (32). In the case described here, a simple chylous pleural effusion evolved into multiloculated fibrinopurulent collections associated with clinical and biochemical features of sepsis. The original effusion impeded reexpansion of the lung, impairing pulmonary function and creating a persistent pleural space at risk for infection, but it seems likely that alterations of the microbiota ecosystem also contributed to the onset of infection (31). Anaerobic organisms are being recovered more and more frequently from patients with empyema, particularly those who, like our patient, are elderly with comorbidities and/or poor oral hygiene (31). Indeed, our patient had been suffering for years from chronic periodontitis. Delayed diagnosis and treatment of empyema are common (31). The clinical presentation varies. As in this case, the course may be indolent with nonspecific constitutional symptoms such as weight loss and pleuritic chest pain. Prompt drainage and effective antimicrobial treatment are essential for successful management of empyema (31). Our patient was initially treated with levofloxacin, but as soon as the pleural isolates were identified with MALDI-TOF mass spectrometry (36 h after the culture was submitted), he was switched to clindamycin, which is characterized by good penetration of the pleural space (33). Twenty-four hours later, the appropriateness of this empirical decision was confirmed by in vitro susceptibility data. However, clindamycin resistance in Prevotella species is reportedly on the rise, so antibiogram guidance is imperative in severe infections caused by these organisms (6). ACKNOWLEDGMENTS We thank Marian Kent for editing the manuscript. This work was supported by Università Cattolica del Sacro Cuore (Fondi Ateneo, Linea D1-2012).
jcm.asm.org 1285
Downloaded from http://jcm.asm.org/ on March 8, 2015 by WEST VIRGINIA UNIV
FIG 1 Imaging findings. As performed at admission, a chest X-ray shows the right lateral pleural effusions with loculated features (a) and a CT scan shows the two loculated pleural effusions described in the text (b).
Case Report
REFERENCES
1286
jcm.asm.org
15. Busch N, Mertens PR, Schonfelder T, Nguyen H, Marschall HU, Kierdorf H, Haase G, Urhahn R, Sieberth HG, Matern S. 1996. Lemierre’s posttonsillitis sepsis with meningitis and intravascular consumption coagulopathy as complication of infectious mononucleosis with pansinusitis. Dtsch. Med. Wochenschr. 121:94 –98. (In German.) http://dx.doi.org /10.1055/s-2008-1042978. 16. Dumitriu S, Ba˘ncescu G, Murea A, Skaug N. 1998. Isolation and speciation of Prevotella strains from periodontal abscesses. Roum. Arch. Microbiol. Immunol. 57:5–10. 17. Schindl A, Schön H. 1999. Foot infection with Prevotella bivia, P. oralis and P. loescheii after wound licking. J. Med. Microbiol. 48:109. 18. Alegre-Sancho J, Juanola X, Narvaez FJ, Roig-Escofet D. 2000. Septic arthritis due to Prevotella bivia in a patient with rheumatoid arthritis. Joint Bone Spine 67:228 –229. 19. Hoshino T, Nakamura A. 2002. Clinical and bacteriological features of six cases with intracranial abscess in childhood. Kansenshogaku Zasshi 76: 83– 88. (In Japanese.) 20. Riesbeck K. 2003. Paronychia due to Prevotella bivia that resulted in amputation: fast and correct bacteriological diagnosis is crucial. J. Clin. Microbiol. 41:4901– 4903. http://dx.doi.org/10.1128/JCM.41.10.4901-4903.2003. 21. Huits R, Van Assen S, Wildeboer-Veloo AC, Verschuuren EA, Koeter GH. 2006. Prevotella bivia necrobacillosis following infectious mononucleosis. J. Infect. 53:e59 – e63. http://dx.doi.org/10.1016/j.jinf.2005.10.016. 22. Laiho K, Kotilainen P. 2001. Septic arthritis due to Prevotella bivia after intra-articular hip joint injection. Joint Bone Spine 68:443– 444. http://dx .doi.org/10.1016/S1297-319X(01)00303-7. 23. Nalmas S, Bishburg E, Chan T. 2007. Streptococcus constellatus and Prevotella bivia penile abscess. ScientificWorldJournal 7:1631–1633. http: //dx.doi.org/10.1100/tsw.2007.240. 24. Salman AS, Baharoon SA. 2009. Septic arthritis of the knee joint secondary to Prevotella bivia. Saudi Med. J. 30:426 – 428. 25. Hsu GJ, Chen CR, Lai MC, Luh SP. 2009. Chest wall abscess due to Prevotella bivia. J. Zhejiang Univ. Sci. B 10:233–236. http://dx.doi.org/10 .1631/jzus.B0820289. 26. Sagristà M, Martin-Ezquerra G, Gallardo F, Membrilla E, Salazar AJ, Salvadó M, Gómez J, Pujol RM. 2012. Inguinal syndrome secondary to Prevotella bivia after accidental bite in orogenital sex. Sex Transm. Infect. 88:250 –251. http://dx.doi.org/10.1136/sextrans-2011-050348. 27. Janssen S, van Donselaar-van der Pant KA, van der Weerd NC, Develter W, Bemelman FJ, Grobusch MP, Idu MM, Ten Berge IJ. 2013. Abdominal wall phlebitis due to Prevotella bivia following renal transplantation in a patient with an occluded inferior vena cava. Infection 41:271–274. http: //dx.doi.org/10.1007/s15010-012-0335-5. 28. Light RW. 2007. Chylothorax and pseudochylothorax, p 346 –361. In Light RW (ed), Pleural diseases, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA. 29. Skouras V, Kalomenidis I. 2010. Chylothorax: diagnostic approach. Curr. Opin. Pulm. Med. 16:387–393. http://dx.doi.org/10.1097/MCP.0b 013e328338dde2. 30. Agrawal V, Sahn S. 2008. Lipid pleural effusion. Am. J. Med. Sci. 335:16 – 20. http://dx.doi.org/10.1097/MAJ.0b013e31815d2634. 31. Davies HE, Davies RJO, Davies CWH, Pleural Disease Guideline Group. 2010. Management of pleural infection in adults: British Thoracic Society pleural disease guideline 2010. Thorax 65(Suppl 2):41–53. http: //dx.doi.org/10.1136/thx.2010.137000. 32. Ahmed RA, Marrie TJ, Huang JQ. 2006. Thoracic empyema in patients with community-acquired pneumonia. Am. J. Med. 119:877– 883. http: //dx.doi.org/10.1016/j.amjmed.2006.03.042. 33. Teixeira LR, Sasse SA, Villarino MA, Nguyen T, Mulligan ME, Light RW. 2000. Antibiotic levels in empyemic pleural fluid. Chest 117:1734 – 1739. http://dx.doi.org/10.1378/chest.117.6.1734.
Journal of Clinical Microbiology
Downloaded from http://jcm.asm.org/ on March 8, 2015 by WEST VIRGINIA UNIV
1. Mantini C, Souppart L, Noël C, Duong TH, Mornet M, Carroger G, Dupont P, Masseret EGoustille J, Capron M, Duboucher C, Dei-Cas E, Viscogliosi E. 2009. Molecular characterization of a new Tetratrichomonas species in a patient with empyema. J. Clin. Microbiol. 47:2336 –2339. http://dx.doi.org/10.1128/JCM.00353-09. 2. Lopez-Escamilla E, Sanchez-Aguillon F, Alatorre-Fernandez CP, Aguilar-Zapata D, Arroyo-Escalante S, Arellano T, Moncada-Barron D, Romero-Valdovinos M, Martinez-Hernandez F, Rodriguez-Zulueta P, Maravilla P. 2013. New tetratrichomonas species in two patients with pleural empyema. J. Clin. Microbiol. 51:3143–3146. http://dx.doi.org/10 .1128/JCM.01056-13. 3. Wright RS, Jean M, Rochelle K, Fisk D. 2011. Chylothorax caused by Paragonimus westermani in a native Californian. Chest 140:1064 –1066. http://dx.doi.org/10.1378/chest.10-2168. 4. Baron EJ, Miller JM, Weinstein MP, Richter SS, Gilligan PH, Thomson RB, Jr, Bourbeau P, Carroll KC, Kehl SC, Dunne WM, Robinson-Dunn B, Schwartzman JD, Chapin KC, Snyder JW, Forbes BA, Patel R, Rosenblatt JE, Pritt BS. 2013. A guide to utilization of the microbiology laboratory for diagnosis of infectious diseases: 2013 recommendations by the Infectious Diseases Society of America (IDSA) and the American Society for Microbiology (ASM) (a). Clin. Infect. Dis. 57:e22– e121. http://dx .doi.org/10.1093/cid/cit278. 5. Wybo I, Soetens O, De Bel A, Echahidi F, Vancutsem E, Vandoorslaer K, Piérard D. 2012. Species identification of clinical Prevotella isolates by matrix-assisted laser desorption ionization–time of flight mass spectrometry. J. Clin. Microbiol. 50:1415–1418. http://dx.doi.org/10.1128/JCM .06326-11. 6. Wybo I, Van den Bossche D, Soetens O, Vekens E, Vandoorslaer K, Claeys G, Glupczynski Y, Ieven M, Melin P, Nonhoff C, RodriguezVillalobos H, Verhaegen J, Piérard D. 5 September 2013. Fourth Belgian multicentre survey of antibiotic susceptibility of anaerobic bacteria. J. Antimicrob. Chemother. http://dx.doi.org/10.1093/jac/dkt344. 7. The European Committee on Antimicrobial Susceptibility Testing. 1 January 2014. Clinical breakpoints. Document version 4.0. http://www .eucast.org/clinical_breakpoints. 8. Shah HN, Collins DM. 1990. Prevotella, a new genus to include Bacteroides melaninogenicus and related species formerly classified in the genus Bacteroides. Int. J. Syst. Bacteriol. 40:205–208. http://dx.doi.org/10.1099 /00207713-40-2-205. 9. Holdeman LV, Johnson JL. 1977. Bacteroides disiens sp. nov. and Bacteroides bivius sp. nov. from human clinical infections. Int. J. Syst. Bacteriol. 27:337–345. http://dx.doi.org/10.1099/00207713-27-4-337. 10. Marconi C, de Andrade Ramos BR, Peraçoli JC, Donders GG, Da Silva MG. 2011. Amniotic fluid interleukin-1 beta and interleukin-6, but not interleukin-8 correlate with microbial invasion of the amniotic cavity in preterm labor. Am. J. Reprod. Immunol. 65:549 –556. http://dx.doi.org /10.1111/j.1600-0897.2010.00940.x. 11. Strömbeck L, Sandros J, Holst E, Madianos P, Nannmark U, Papapanou P, Mattsby-Baltzer I. 2007. Prevotella bivia can invade human cervix epithelial (HeLa) cells. APMIS 115:241–251. http://dx.doi.org/10 .1111/j.1600-0463.2007.apm_512.x. 12. Puapermpoonsiri S, Kato N, Watanabe K, Ueno K, Chongsomchai C, Lumbiganon P. 1996. Vaginal microflora associated with bacterial vaginosis in Japanese and Thai pregnant women. Clin. Infect. Dis. 23:748 – 752. http://dx.doi.org/10.1093/clinids/23.4.748. 13. Kentos A, Motte S, Nonhoff F, Jacobs F, De Smet JM, Serruys E, Thys JP. 1994. Prevotella bivia as an unusual cause of endocarditis. Eur. J. Clin. Microbiol. Infect. Dis. 13:142–145. http://dx.doi.org/10.1007/BF01982187. 14. Brook I, Frazier EH. 1993. Aerobic and anaerobic microbiology of empyema. A retrospective review in two military hospitals. Chest 103:1502– 1507.
