Campylobacter bacteremia: clinical characteristics, incidence, and outcome over 23 years.
Campylobacter is a very rare cause of bloodstream infection, although it has been found relatively frequently in patients infected with human immunodeficiency virus (HIV). The impact of highly active antiretroviral therapy (HAART) and new forms of immunosuppression on the incidence of Campylobacter bacteremia has not been sufficiently assessed. In this study we analyzed the incidence and microbiologic and clinical characteristics of Campylobacter bacteremia over 23 years.We reviewed the clinical records of all patients who had Campylobacter bacteremia from 1985 to 2007. Available strains were reidentified using universal polymerase chain reaction (PCR).During the study period, there were 71 episodes of Campylobacter bacteremia in 63 patients (0.24% of all bloodstream infections), and the incidence remained stable (mean, 0.06/1000 admissions per year and 0.47/100,000 inhabitants per year). Median age was 52 years (interquartile range, 31.25-72.5 yr), and 82% of patients were male. The underlying conditions included liver disease (21/64, 32.8%), HIV infection (15/64, 23.4%), malignancy (7/64, 10.9%), solid organ transplantation (2/64, 3%), hypogammaglobulinemia (10/64, 15.6%), and other (18/64, 31.2%). Twelve patients shared more than 1 underlying condition. Campylobacter bacteremia was community acquired in 81% of the episodes. The origin of the bloodstream infection was abdominal (43.5%), primary (26%), or extraintestinal (31%: respiratory 15%, cellulitis 4.8%, urinary 8%, other 3%). C jejuni was recovered in 66% of cases, C fetus in 19%, and C coli in 12%.Universal PCR was performed on 14 available strains. Molecular and conventional identification matched in 8 isolates. In contrast, molecular methods classified as C fetus (n = 2) and C jejuni (n = 1) 3 strains formerly identified only to genus level as Campylobacter species. In another 3 isolates, molecular identification was not consistent with the phenotypic identification (C fetus identified as C jejuni).Complications appeared in 23.9% of patients. Quinolone resistance was observed in 50% of the isolates. Only 37.8% of patients received appropriate empirical therapy. Mortality was 16.4%, although it was higher in HIV-infected patients than uninfected patients (33% vs. 10%; p = 0.04), in cases of hospital-acquired Campylobacter bacteremia compared with community-acquired cases (38.5% vs. 9.4%; p = 0.02), and in the presence of complications compared with patients without complications (100% vs. 0%; p < 0.001). The incidence of recurrence was 5% (3 patients with humoral immunodeficiency). There was a higher proportion of HIV-infected patients among patients with Campylobacter bacteremia in the pre-HAART era (1985-1996) than in the HAART era (1997-2007)-27.5% (11/40) vs. 14.3% (4/28)-although the difference was not statistically significant. Debilitating diseases such as chronic obstructive pulmonary disease emerged as predisposing conditions in the HAART era (0% before HAART era vs. 14.3% in HAART era; p = 0.032).Campylobacter bacteremia is no longer a significant disease of HIV-positive patients on HAART, but often affects other immunocompromised patients as well. Campylobacter bacteremia has an extraintestinal origin in as many as 31% of cases, and humoral immunodeficiency must be sought in patients with recurrent episodes. Quinolones should not be considered for empirical therapy.
Fernández-Cruz
Ana
A
From Department of Microbiology and Infectious Diseases (AFC, PM, RM*, MV, MM, LA, MRC, EC, EB), Hospital General Universitario Gregorio Marañón, Universidad Complutense de Madrid, Madrid; *presently at Hospital Severo Ochoa (RM), Leganés, Madrid, Spain; Centro de Investigación Biomédica en Red de Enfermedades Respiratorias (CIBERES) (PM, MM, LA, MRC, EC, EB).
Muñoz
Patricia
P
Mohedano
Rosa
R
Valerio
Maricela
M
Marín
Mercedes
M
Alcalá
Luis
L
Rodriguez-Créixems
Marta
M
Cercenado
Emilia
E
Bouza
Emilio
E
D000293:Adolescent; D000328:Adult; D000368:Aged; D000369:Aged, 80 and over; D023241:Antiretroviral Therapy, Highly Active / Q000379:methods; D002169:Campylobacter Infections / Q000453:epidemiology* / Q000235:genetics / Q000382:microbiology*; D002648:Child; D005260:Female; D020022:Genetic Predisposition to Disease; D015658:HIV Infections / Q000188:drug therapy / Q000453:epidemiology; D006304:Health Status; D006801:Humans; D015994:Incidence; D008297:Male; D008875:Middle Aged; D016133:Polymerase Chain Reaction; D011446:Prospective Studies; D012335:RNA, Ribosomal / Q000235:genetics; D013997:Time Factors; D016896:Treatment Outcome; D055815:Young Adult
D012335:RNA, Ribosomal
Barros-Velazquez J, Jimenez A, Villa TG. Isolation and typing methods for the epidemiologic investigation of thermotolerant campylobacters. Int Microbiol. 1999;2:217-226.
Behl D, Manchanda R, Thomas C. Camplyobacter empyema due to food aspiration. J Hosp Med. 2008;3:81-83.
Blaser MJ. Campylobacter fetus-emerging infection and model system for bacterial pathogenesis at mucosal surfaces. Clin Infect Dis. 1998;27:256-258.
Blaser MJ. Extraintestinal Campylobacter infections. West J Med. 1986;144:353-354.
Bourke B, Chan VL, Sherman P. Campylobacter upsaliensis: waiting in the wings. Clin Microbiol Rev. 1998;11:440-449.
Brunel V, Allegre T, Cailleres S, Blanc AP. [Hematologic manifestations in Campylobacter coli septicemia. Apropos of a case]. Rev Med Interne. 1993;14:39-40.
Butzler JP. Campylobacter, from obscurity to celebrity. Clin Microbiol Infect. 2004;10:868-876.
Callahan C, Greene JN, Sandin RL, Ruge D, Johnson J. Campylobacter jejuni bacteremia in an HIV-positive patient with non-Hodgkin's lymphoma. Cancer Control. 1998;5:357-360.
Carnahan AM, Beadling J, Watsky D, Ford N. Detection of Campylobacter upsaliensis from a blood culture by using the BacT/Alert system. J Clin Microbiol. 1994;32:2598-2599.
Chua K, Gurtler V, Montgomery J, Fraenkel M, Mayall BC, Grayson ML. Campylobacter insulaenigrae causing septicaemia and enteritis. J Med Microbiol. 2007;56:1565-1567.
Chuman Y, Takata T, Sameshima H, Takeuchi S, Takatsuka Y, Makino T, Blaser MJ, Utsunomiya A. Campylobacter fetus bacteremia in a patient with adult T cell leukemia. Clin Infect Dis. 2003;36:1497-1498.
Conde Martel A, Suarez Ortega S, Campos-Herrero Navas MI, Elcuaz Romano R. [Campylobacter fetus sepsis, pulmonary thromboembolism and an occult neoplasm]. An Med Interna. 1999;16:103.
Dingle KE, Clarke L, Bowler IC. Ciprofloxacin resistance among human Campylobacter isolates 1991-2004: an update. J Antimicrob Chemother. 2005;56:435-437.
Drancourt M, Berger P, Raoult D. Systematic 16S rRNA gene sequencing of atypical clinical isolates identified 27 new bacterial species associated with humans. J Clin Microbiol. 2004;42:2197-2202.
Epifane G, Barbon S, Sadino G, Bouchet D, Suarez ME, Mangiaterra S. [Bacteremia due to Campylobacter fetus isolated by conventional methods from an immunocompromised patient]. Rev Argent Microbiol. 2007;39:34-37.
Fearnley C, Manning G, Bagnall M, Javed MA, Wassenaar TM, Newell DG. Identification of hyperinvasive Campylobacter jejuni strains isolated from poultry and human clinical sources. J Med Microbiol. 2008;57:570-580.
Font C, Cruceta A, Moreno A, Miro O, Coll-Vinent B, Almela M, Mensa J. [A study of 30 patients with bacteremia due to Campylobacter spp.]. Med Clin (Barc). 1997;108:336-340.
Francioli P, Herzstein J, Grob JP, Vallotton JJ, Mombelli G, Glauser MP. Campylobacter fetus subspecies fetus bacteremia. Arch Intern Med. 1985;145:289-292.
Freeman AF, Holland SM. Persistent bacterial infections and primary immune disorders. Curr Opin Microbiol. 2007;10:70-75.
Galanis E. Campylobacter and bacterial gastroenteritis. CMAJ. 2007;177:570-571.
Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. CDC definitions for nosocomial infections, 1988. Am J Infect Control. 1988;16:128-140.
Gazaigne L, Legrand P, Renaud B, Bourra B, Taillandier E, Brun-Buisson C, Lesprit P. Campylobacter fetus bloodstream infection: risk factors and clinical features. Eur J Clin Microbiol Infect Dis. 2008;27:185-189.
Guerrant RL, Lahita RG, Winn WC Jr, Roberts RB. Campylobacteriosis in man: pathogenic mechanisms and review of 91 bloodstream infections. Am J Med. 1978;65:584-592.
Hagensee ME, Benyunes M, Miller JA, Spach DH. Campylobacter jejuni bacteremia and Guillain-Barre syndrome in a patient with GVHD after allogeneic BMT. Bone Marrow Transplant. 1994;13:349-351.
Heng AE, De Champs C, Souweine B, Guy L, Sirot J, Deteix P. Campylobacter fetus bacteraemia in a renal graft recipient. Nephrol Dial Transplant. 2002;17:689-690.
Jackson CJ, Fox AJ, Wareing DR, Sutcliffe EM, Jones DM. Genotype analysis of human blood isolates of Campylobacter jejuni in England and Wales. Epidemiol Infect. 1997;118:81-89.
Knobel H, Lopez-Colomes J, Saballs P, Drobnic L. [Unusual forms of bacteremia due to Campylobacter jejuni in patients with HIV infection]. Med Clin (Barc). 1994;103:239.
Kulkarni SP, Lever S, Logan JM, Lawson AJ, Stanley J, Shafi MS. Detection of campylobacter species: a comparison of culture and polymerase chain reaction based methods. J Clin Pathol. 2002;55:749-753.
Lau SK, Woo PC, Leung KW, Yuen KY. Emergence of cotrimoxazole- and quinolone-resistant Campylobacter infections in bone marrow transplant recipients. Eur J Clin Microbiol Infect Dis. 2002;21:127-129.
Lu PL, Hsueh PR, Hung CC, Chang SC, Luh KT, Lee CY. Bacteremia due to Campylobacter species: high rate of resistance to macrolide and quinolone antibiotics. J Formos Med Assoc. 2000;99:612-617.
Maccario M, Tarantino A, Nobile-Orazio E, Ponticelli C. Campylobacter jejuni bacteremia and Guillain-Barre syndrome in a renal transplant recipient. Transpl Int. 1998;11:439-442.
Maher M, Finnegan C, Collins E, Ward B, Carroll C, Cormican M. Evaluation of culture methods and a DNA probe-based PCR assay for detection of Campylobacter species in clinical specimens of feces. J Clin Microbiol. 2003;41:2980-2986.
Manfredi R. [Effects of the introduction of highly active antiretroviral therapy (HAART) on the temporal trend of diagnosis of AIDS and AIDS-defining disorders]. Infez Med. 2000;8:134-138.
Manfredi R, Calza L, Chiodo F. Enteric and disseminated Campylobacter species infection during HIV disease: a persisting but significantly modified association in the HAART era. Am J Gastroenterol. 2002;97:510-511.
Manfredi R, Nanetti A, Ferri M, Chiodo F. Fatal Campylobacter jejuni bacteraemia in patients with AIDS. J Med Microbiol. 1999;48:601-603.
Melero JM, Freitag SK, Perazzi BE, Vay CA, Famiglietti A. [Campylobacter jejuni bacteremia in a patient with non Hodgkin lymphoma and pneumonia]. Medicina (B Aires). 2000;60:407-408.
Miller WG, On SL, Wang G, Fontanoz S, Lastovica AJ, Mandrell RE. Extended multilocus sequence typing system for Campylobacter coli, C. lari, C. upsaliensis, and C. helveticus. J Clin Microbiol. 2005;43:2315-2329.
Monno R, Rendina M, Ceci G, Rizzo C, Luzzi I, Francavilla A, Rizzo G, Ierardi E. Campylobacter fetus bacteremia in an immunocompromised patient: case report and review of the literature. New Microbiol. 2004;27:281-285.
Morrison VA, Lloyd BK, Chia JK, Tuazon CU. Cardiovascular and bacteremic manifestations of Campylobacter fetus infection: case report and review. Rev Infect Dis. 1990;12:387-392.
Murakami H, Goto M, Ono E, Sawabe E, Iwata M, Okuzumi K, Yamaguchi K, Takahashi T. Isolation of Helicobacter cinaedi from blood of an immunocompromised patient in Japan. J Infect Chemother. 2003;9:344-347.
Nathwani D, Morris AJ, Smith CC. Simultaneous Streptococcus pneumoniae, Giardia lamblia and Campylobacter pylori infection: an adult presentation of X-linked hypogammaglobulinaemia. Scott Med J. 1989;34:502.
National Prevalence Survey of Hospital Acquired Infections: definitions. A preliminary report of the steering group of the Second National Prevalence Survey. J Hosp Infect. 1993;24:69-76.
Neuzil KM, Wang E, Haas DW, Blaser MJ. Persistence of Campylobacter fetus bacteremia associated with absence of opsonizing antibodies. J Clin Microbiol. 1994;32:1718-1720.
Nielsen H, Hansen KK, Gradel KO, Kristensen B, Ejlertsen T, Ostergaard C, Schonheyder HC. Bacteraemia as a result of Campylobacter species: a population-based study of epidemiology and clinical risk factors. Clin Microbiol Infect. 2010;16:57-61.
Ozaki M, Murase T, Park JW, Aoki M, Kawato M. [Campylobacter fetus bacteremia and thrombophlebitis in a patient with Waldenstrom's macroglobulinemia]. Kansenshogaku Zasshi. 1999;73:86-89.
Pacanowski J, Lalande V, Lacombe K, Boudraa C, Lesprit P, Legrand P, Trystram D, Kassis N, Arlet G, Mainardi JL, Doucet-Populaire F, Girard PM, Meynard JL. Campylobacter bacteremia: clinical features and factors associated with fatal outcome. Clin Infect Dis. 2008;47:790-796.
Perlman DM, Ampel NM, Schifman RB, Cohn DL, Patton CM, Aguirre ML, Wang WL, Blaser MJ. Persistent Campylobacter jejuni infections in patients infected with the human immunodeficiency virus (HIV). Ann Intern Med. 1988;108:540-546.
Pigrau C, Almirante B, Bartolome R, Pahissa A. [Bacteremia due to Campylobacter sp. in patients with HIV infection]. Med Clin (Barc). 1994;103:239.
Pigrau C, Almirante B, Pahissa A, Bartolome R. Campylobacter spp. bacteremia in AIDS patients. J Acquir Immune Defic Syndr Hum Retrovirol. 1996;12:93-95.
Pigrau C, Bartolome R, Almirante B, Planes AM, Gavalda J, Pahissa A. Bacteremia due to Campylobacter species: clinical findings and antimicrobial susceptibility patterns. Clin Infect Dis. 1997;25:1414-1420.
Reed RP, Friedland IR, Wegerhoff FO, Khoosal M. Campylobacter bacteremia in children. Pediatr Infect Dis J. 1996;15:345-348.
Sakran W, Raz R, Levi Y, Colodner R, Koren A. Campylobacter bacteremia and pneumonia in two splenectomized patients. Eur J Clin Microbiol Infect Dis. 1999;18:496-498.
Sanchez R, Fernandez-Baca V, Diaz MD, Munoz P, Rodriguez-Creixems M, Bouza E. Evolution of susceptibilities of Campylobacter spp. to quinolones and macrolides. Antimicrob Agents Chemother. 1994;38:1879-1882.
Sanz-Garcia M, Fernandez-Cruz A, Rodriguez-Creixems M, Cercenado E, Marin M, Munoz P, Bouza E. Recurrent Escherichia coli bloodstream infections: epidemiology and risk factors. Medicine (Baltimore). 2009;88:77-82.
Schonheyder HC, Sogaard P, Frederiksen W. A survey of Campylobacter bacteremia in three Danish counties, 1989 to 1994. Scand J Infect Dis. 1995;27:145-148.
Schuster M, Blaser MJ, Nachamkin I. Serendipitous detection of persistent Campylobacter jejuni subspecies jejuni bacteremia in a patient undergoing bone marrow transplantation. Clin Infect Dis. 1997;24:1270.
Skirrow MB, Jones DM, Sutcliffe E, Benjamin J. Campylobacter bacteraemia in England and Wales, 1981-91. Epidemiol Infect. 1993;110:567-573.
Sorvillo FJ, Lieb LE, Waterman SH. Incidence of campylobacteriosis among patients with AIDS in Los Angeles County. J Acquir Immune Defic Syndr. 1991;4:598-602.
Targan SR, Chow AW, Guze LB. Campylobacter fetus associated with pulmonary abscess and empyema. Chest. 1977;71:105-108.
Tauxe RV, Pegues DA, Hargrett-Bean N. Campylobacter infections: the emerging national pattern. Am J Public Health. 1987;77:1219-1221.
Tee W, Mijch A. Campylobacter jejuni bacteremia in human immunodeficiency virus (HIV)-infected and non-HIV-infected patients: comparison of clinical features and review. Clin Infect Dis. 1998;26:91-96.
Tilse MH, McAlister TV. Isolation of Campylobacter fetus from blood cultures. Med J Aust. 1981;2:337-338.
Vandamme P, Falsen E, Rossau R, Hoste B, Segers P, Tytgat R, De Ley J. Revision of Campylobacter, Helicobacter, and Wolinella taxonomy: emendation of generic descriptions and proposal of Arcobacter gen. nov. Int J Syst Bacteriol. 1991;41:88-103.
Van der Hilst JC, Smits BW, van der Meer JW. Hypogammaglobulinaemia: cumulative experience in 49 patients in a tertiary care institution. Neth J Med. 2002;60:140-147.
van der Meer JW, Mouton RP, Daha MR, Schuurman RK. Campylobacter jejuni bacteraemia as a cause of recurrent fever in a patient with hypogammaglobulinaemia. J Infect. 1986;12:235-239.
van der Meer JW, Zegers BJ. Agammaglobulinaemia. Neth J Med. 1994;45:250-256.
Zylberman M, Demonty G, Menchaca A, Ferro L, Tokumoto MB. [Campylobacter fetus fetus and colon adenocarcinoma]. Medicina (B Aires). 2000;60:665-666.