Original Article
Bartonella (Rochalimaea) quintana Bacteremia in Inner-City Patients with Chronic Alcoholism
N Engl J Med 1995; 332:424-428February 16, 1995
- Abstract
Background
Bartonella (Rochalimaea) quintana is a fastidious gram-negative bacterium known to cause trench fever, cutaneous bacillary angiomatosis, and endocarditis. Between January and June 1993 in Seattle, we isolated B. quintana from 34 blood cultures obtained from 10 patients not known to be infected with the human immunodeficiency virus (HIV).
Methods
After identifying the isolates as B. quintana by direct immunofluorescence and DNA-hybridization studies, we determined strain hybridization with studies of restriction-fragment–length polymorphisms (RFLPs) of the intergenic spacer (noncoding) region of ribosomal DNA amplified by the polymerase chain reaction (PCR). To characterize the epidemiologic and clinical features of bartonella infections in these patients, we performed a retrospective case–control study using as controls 20 patients from whom blood was obtained for culture at approximately the same time as from the index patients.
Results
B. quintana isolates from the 10 patients were indistinguishable by PCR–RFLP typing. All 10 patients had chronic alcoholism, and 8 were homeless (P = 0.001 for both comparisons with controls). The six patients who underwent HIV testing were seronegative. At the time of their initial presentation, seven patients had temperatures of at least 38.5°C. Six patients had three or more blood cultures that were positive for B. quintana, and in four of these patients B. quintana was isolated from blood cultures obtained 10 or more days apart. Subacute endocarditis developed in two patients and required surgical removal of the infected aortic valve in one of them. Nine patients recovered; one died of sepsis from Streptococcus pneumoniae infection.
Conclusions
B. quintana is a cause of fever, bacteremia, and endocarditis in HIV-seronegative, homeless, inner-city patients with chronic alcoholism.
Media in This Article
Figure 2
Number of Patients with B. quintana Bacteremia during a 14-Month Period at Harborview Medical Center in Seattle.Figure 1
PCR–RFLP Analysis of the Ribosomal DNA Intergenic Spacer Region in B. quintana Isolates.Article Activity
- Article
Bartonella quintana (formerly known as Rochalimaea quintana 1) is a fastidious gram-negative bacterium first identified as the cause of louse-borne epidemic trench fever in Europe during World War I.2 B. quintana was subsequently recognized as the cause of trench fever in Africa and Mexico.3 Descriptions of the clinical manifestations of this disease have varied, with an insidious onset of nonspecific symptoms reported in some patients and a more sudden illness characterized by fever, malaise, headache, bone pain, and a transient macular rash reported in others.4 In addition, several patterns of fever have been observed, including a single episode of fever, continuous fever for five to seven days, and recurrent febrile episodes occurring every four to five days.4 Studies involving inoculation of humans with B. quintana from infected louse feces suggest that the incubation period ranges from 5 to 20 days, depending on the size of the inoculum.4 Once humans become infected, B. quintana may circulate in the blood for weeks to months or even, in some cases, for longer than a year.4
Until recent years, bartonella species have not been isolated from humans in the United States. Several recent studies, all involving patients infected with the human immunodeficiency virus (HIV), have shown that B. quintana can cause cutaneous bacillary angiomatosis, bacteremia, endocarditis, and chronic lymphadenopathy.5-9 Thus far, however, B. quintana has not been reported in HIV-negative people in the United States. B. henselae, a closely related organism that has also recently been reported in HIV-infected patients, causes cutaneous bacillary angiomatosis, peliosis hepatis, and bacteremia.5,10-15 In addition, B. henselae has been shown to infect immunocompetent persons and cause cat scratch disease, cutaneous bacillary angiomatosis, bacillary splenitis, bacteremia, and endocarditis.16-20
Between January and June 1993, the microbiology laboratory at the Harborview Medical Center in Seattle isolated organisms presumptively identified as bartonella species in blood cultures from 10 patients.21 Subsequently, we conducted a retrospective case–control study to characterize the epidemiologic and clinical features of bartonella infections in these patients. In addition, we performed studies to identify the species and to determine the strain relatedness of these bartonella isolates.
Methods
Patients
All 10 patients were seen at Harborview Medical Center. Case patients were defined as those with bartonella species isolated from blood cultures at the hospital's microbiology laboratory from January through June 1993. For each case patient, we selected two control patients: one with blood specimens obtained for culture just before those obtained from the case patient and one with specimens obtained just after those from the case patient. Thus, there were 20 controls. Epidemiologic, clinical, and routine laboratory data were obtained from the medical records of the case and control patients.
Isolation of Bartonella in Blood Cultures
Routine blood samples from each patient were inoculated into one Bactec aerobic Plus 26 bottle (Becton Dickinson Diagnostic Instrument Systems, Sparks, Md.) and one Bactec anaerobic NR 7 bottle, as previously described.21 Before the blood cultures were discarded on day 8, a small aliquot of blood-culture broth was removed from the aerobic bottles for staining with acridine orange.21 This procedure had been routinely performed with all blood cultures since May 1988. When bacteria were stained with acridine orange, subcultures were performed as previously described.21 Isolates were identified at the genus level by biochemical testing and analysis of cellular fatty acids.21
Identification of Bartonella Species by Direct Immunofluorescence
The immunofluorescence assays were performed on one blood-culture isolate from each of the 10 patients, as described previously.22 In brief, murine polyclonal antibodies specific for B. henselae or B. quintana were used to distinguish the two species. The fluorescent antibody label was fluorescein-conjugated antimouse IgG (Organon Teknika, West Chester, Pa.).
DNA-Hybridization Studies
DNA relatedness was determined by comparing at least one blood-culture isolate from each of the 10 patients with type strains of all known bartonella species. The methods used to extract and purify DNA and the hydroxyapatite hybridization method for determining DNA relatedness were performed as described previously.23 All studies were performed twice. The change in the thermal-stability midpoint of the heterologous DNA reaction was compared with that of the homologous DNA reaction. Divergence (unpaired bases in a reassociated DNA sequence), which is approximately 1 percent for each degree of decreased thermal stability, was calculated to the nearest 0.5 percent.
Studies of Restriction-Fragment–Length Polymorphisms
Restriction-fragment–length polymorphisms (RFLPs) of B. quintana DNA amplified by the polymerase chain reaction (PCR) were studied in one blood-culture isolate from each of the 10 patients, as previously described,24 except that DdeI and RsaI were used to restrict the PCR-amplified ribosomal intergenic spacer region.
Results
Isolation and Characterization of B. quintana Isolates
B. quintana was isolated from a total of 34 Bactec nonradiometric aerobic resin bottles containing blood samples from the 10 patients.21 All 34 bottles were monitored with the Bactec NR-660 detection system for the first five days of incubation, and none produced sufficient levels of carbon dioxide to indicate growth. For 9 of the 10 patients, acridine-orange staining of the Bactec medium resulted in the first evidence of bacterial growth.21 After the isolates had been subcultured on chocolate agar, visible growth appeared in three to eight days. Representative isolates were negative for catalase, oxidase, and urease. The following major fatty acids, expressed as the percentage of total fatty acids, were detected in isolates from each of the 10 patients: C18:1 (60 to 65 percent), C18:0 (13 to 18 percent), and C16:0 (16 to 19 percent).
The isolates from all 10 patients were identified as B. quintana on the basis of immunofluorescence assays with species-specific polyclonal antibodies and DNA-hybridization studies (Table 1Table 1
DNA Relatedness of Isolates of Bartonella Species from the 10 Patients.). Repeat isolates from the four patients who had positive cultures of blood obtained 10 or more days apart were also identified as B. quintana (data not shown). The isolates from the 10 patients were indistinguishable from each other by PCR–RFLP typing (Figure 1Figure 1PCR–RFLP Analysis of the Ribosomal DNA Intergenic Spacer Region in B. quintana Isolates.).Demographic and Clinical Characteristics of the Case Patients and Controls
All cases of bartonella bacteremia occurred from January through June 1993 (Figure 2Figure 2
Number of Patients with B. quintana Bacteremia during a 14-Month Period at Harborview Medical Center in Seattle.). The group of 10 case patients and the group of 20 control patients did not differ significantly in terms of age, sex, or history of injection-drug use (Table 2Table 2
Demographic and Clinical Characteristics of the Case Patients with B. quintana Bacteremia and the Controls.). A univariate analysis showed that the patients with bartonella bacteremia were significantly more likely than the controls to be homeless (8 of 10 vs. 3 of 20, P = 0.001), to have a history of chronic alcohol abuse (10 of 10 vs. 7 of 20, P = 0.001), and to be nonwhite (9 of 10 vs. 7 of 20, P = 0.007). All 10 patients with bartonella bacteremia either resided or spent most of their time in downtown Seattle. Because 8 of these 10 patients were homeless, we could not determine precisely where in downtown Seattle they spent most of their time.Six of the 10 patients with bartonella bacteremia underwent HIV testing, and all 6 were seronegative. Information on the HIV status of the other four patients was not available, but none had risk factors for HIV infection. Of the seven control patients whose HIV status was known, two were seropositive.
Clinical Presentation of Patients with B. quintana Bacteremia
At the time of their initial presentation, the 10 patients with B. quintana bacteremia had a median temperature of 38.5°C; 7 of the 10 had a temperature of 38.5°C or higher, and 1 had hypothermia (35.5°C). Three patients reported a history of recent weight loss that exceeded 9.1 kg (20 lb). Other than fever, no consistent symptoms or abnormalities were noted on physical examination. Two patients had splenomegaly. Three patients reported a recent cat scratch, five were presumptively diagnosed as having scabies at the time of their initial presentation, and lice were detected on one patient. The mean white-cell count was 9600 per cubic millimeter.
Six patients had three or more positive blood cultures for B. quintana, and four of these patients had positive blood cultures 10 or more days apart. One patient, who did not comply with antimicrobial therapy, had positive blood cultures on five separate occasions over a period of eight weeks. One patient with B. quintana bacteremia also had a positive blood culture for Streptococcus pneumoniae.
Five patients underwent echocardiographic studies, and the results were normal in four of the five. However, one patient had echocardiographic evidence of an aortic-valve vegetation.25 After 21 days of antimicrobial therapy, surgical removal of the infected aortic valve was required; B. quintana was detected in the valve tissue by PCR techniques.25
Clinical Outcome
Nine of the 10 patients with B. quintana bacteremia survived; 1 patient died, presumably from overwhelming sepsis associated with S. pneumoniae infection. Follow-up of the surviving patients was limited, mainly because they were homeless (Table 3Table 3
Antimicrobial Therapy and Outcome in the 10 Patients with B. quintana Bacteremia.).Five patients were treated with ceftriaxone (given intravenously or intramuscularly) for seven days plus either oral erythromycin or oral azithromycin for at least three weeks. Three of these five patients returned for blood-culture testing after completing the antimicrobial therapy, and all the cultures were negative. The patient with endocarditis received more than four months of oral antimicrobial therapy after valve surgery and had negative blood cultures one year later. Another patient, who was lost to follow-up after an initial blood culture had been found to be positive for B. quintana, returned nine months later with fever, echocardiographic evidence of endocarditis, and multiple splenic lesions noted on computed tomography. Organisms were not reisolated from blood cultures, but blind subculturing was not performed. He did not require valve surgery.
Discussion
We studied 10 patients in Seattle with bacteremia caused by B. quintana, the agent of trench fever. None were known to be infected with HIV, and six had a documented seronegative status. It is highly unlikely that the B. quintana isolates in these patients represent contamination of blood cultures, since six of the patients had three or more positive blood cultures, some of which were performed 10 or more days apart. One patient had positive blood cultures on five separate occasions over an eight-week period.
Our patients with B. quintana typically had a symptomatic febrile illness resembling that reported by Slater et al. in five patients with B. henselae bacteremia.14 In addition, the B. quintana bacteremia in most of our patients was clinically similar to previous descriptions of trench fever — a disease also caused by B. quintana.2,4 Some of the clinical manifestations of trench fever that have occasionally been observed, such as rash, headache, and bone pain, were not observed in any of our patients.
Because the follow-up of our patients was limited, clear treatment recommendations cannot be given. Although the optimal type and duration of therapy for this and other bartonella infections are not clear, such infections appear to have a tendency to persist or recur,14,19,26,27 especially if antimicrobial therapy is given for less than 14 days. Indeed, the one patient in our study who did not comply with antimicrobial therapy had persistent (or relapsing) bacteremia until he finally completed a course of azithromycin. Careful follow-up to detect relapsing infection is essential.
Although the retrospective nature of our investigation did not permit us to obtain definitive information about how these 10 patients became infected with B. quintana, there are several possibilities. In classic cases of trench fever, B. quintana is transmitted by lice among persons in close contact with one another under poor sanitary conditions, most notably the crowded trenches in World Wars I and II.2,4 The B. quintana infections we describe occurred predominantly among homeless people with chronic alcoholism — conditions that may have resulted in close contact and poor hygiene. Although these conditions may have led to infestation with lice, only one patient was actually observed to have lice at the time of his presentation to the hospital.
Koehler and colleagues have recently shown that the domestic cat serves as a reservoir for B. henselae; in addition, they found B. henselae in fleas from an infected cat.28 Three of our patients reported a recent cat scratch, but none reported flea bites. Five of our patients had scabies infestation. The scabies mite, Sarcoptes scabiei, although it has never been shown to harbor either B. quintana or B. henselae, theoretically could have transmitted B. quintana to these patients. Further study is clearly warranted to determine whether one or more of the above-mentioned vectors transmit B. quintana.
There are several possible explanations for this sudden cluster of 10 cases of B. quintana bacteremia. Increased detection of infection could have occurred as a result of our laboratory's use of acridine-orange staining and rigorous subculturing of presumptively positive isolates. The microbiology laboratory, however, had routinely performed acridine-orange staining on all blood cultures for approximately five years before January 1993 without identifying other cases of bartonella bacteremia. In addition, during the 12-month period after these 10 cases of infection were diagnosed, we isolated B. quintana from only 1 patient, despite use of the same blood-culture techniques and vigilant surveillance. Thus, it seems unlikely that increased laboratory detection of B. quintana could be the sole explanation for the sudden occurrence of these 10 cases.
The finding that the isolates were indistinguishable from one another by PCR–RFLP analysis suggests that these cases are probably epidemiologically linked. Four PCR–RFLP patterns have previously been observed among 18 isolates of B. quintana from the San Francisco area (Koehler JE: personal communication). Our PCR–RFLP studies, however, do not clarify the mode of transmission of B. quintana in our patients. The outbreak could have occurred as a result of close contact among the patients, one of whom served as the initial source of infection. Because most of the patients were homeless, it is possible that they came into contact with each other on the street or at shelters. We do not, however, have epidemiologic evidence to validate this hypothesis. Whether B. quintana is endemic in our region or was imported is also not clear.
In summary, we have identified and characterized a cluster of 10 cases of symptomatic B. quintana bacteremia in Seattle. As compared with the controls, the infected patients were more likely to be homeless, alcoholic, and nonwhite. Because of the small sample size, a stratified or logistic-regression analysis of these characteristics was not possible. Further studies are needed to determine the prevalence, source, mode of transmission, and optimal management of B. quintana infections in populations with demographic and clinical characteristics similar to those of our 10 patients.
Presented at the 33rd Interscience Conference on Antimicrobial Agents and Chemotherapy, New Orleans, October 17–20, 1993.
We are indebted to the microbiology laboratory at Harborview Medical Center for its diligence in detecting and isolating these fastidious bacteria, to Arnold G. Steigerwalt at the Centers for Disease Control and Prevention for carrying out the DNA-relatedness studies, to the University of Oklahoma Medical Center microbiology staff for assistance with the serologic studies, and to Marcia Goldoft for helping to locate patients for follow-up.
Source Information
From the Division of Infectious Diseases and the Department of Medicine (D.H.S., R.K.R., W.E.S.) and the Department of Laboratory Medicine (M.J.D., A.M.L., M.B.C.), Harborview Medical Center and the University of Washington Medical Center, Seattle; the Department of Medicine, University of Washington Medical Center, Seattle (A.S.K.); the Emerging Bacterial and Mycotic Diseases Branch (D.J.B.) and the Foodborne and Diarrheal Diseases Branch (B.S., G.M.M.), Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, Atlanta; and the Department of Pediatrics and the Clinical Microbiology Laboratories, University of Oklahoma Health Sciences Center, Oklahoma City (D.F.W.).
Address reprint requests to Dr. Spach at Madison Clinic, ZA-09, 1001 Broadway, Suite 206, Seattle, WA 98122.
- References
References
1
Brenner DJ ,O'Connor SP ,Winkler HH ,Steigerwalt AG . Proposals to unify the genera Bartonella and Rochalimaea, with descriptions of Bartonella quintana comb. nov., Bartonella vinsonii comb. nov., Bartonella henselae comb. nov., and Bartonella elizabethae comb. nov., and to remove the family Bartonellaceae from the order Rickettsiales. Int J Syst Bacteriol 1993;43:777-786
CrossRef | Medline2
Slater LN, Welch DF. Rochalimaea species (recently renamed bartonella). In: Mandell GL, Bennett JE, Dolin R, eds. Principles and practice of infectious diseases. 4th ed. New York: Churchill Livingstone, 1995:1741-7.
3
Myers WF ,Grossman DM ,Wisseman CL Jr . Antibiotic susceptibility patterns in Rochalimaea quintana, the agent of trench fever. Antimicrob Agents Chemother 1984;25:690-693
Web of Science | Medline4
Vinson JW ,Varela G ,Molina-Pasquel C . Trench fever. III. Induction of clinical disease in volunteers inoculated with Rickettsia quintana propagated on blood agar. Am J Trop Med Hyg 1969;18:713-722
Web of Science | Medline5
Koehler JE ,Quinn FD ,Berger TG ,LeBoit PE ,Tappero JW . Isolation of rochalimaea species from cutaneous and osseous lesions of bacillary angiomatosis. N Engl J Med 1992;327:1625-1631
Full Text | Web of Science | Medline6
Maurin M ,Roux V ,Stein A ,Ferrier F ,Viraben R ,Raoult D . Isolation and characterization by immunofluorescence, sodium dodecyl sulfate-polyacrylamide gel electrophoresis, Western blot, restriction fragment length polymorphism-PCR, 16S rRNA gene sequencing, and pulsed-field gel electrophoresis of Rochalimaea quintana from a patient with bacillary angiomatosis. J Clin Microbiol 1994;32:1166-1171
Web of Science | Medline7
Welch DF ,Pickett DA ,Slater LN ,Steigerwalt AG ,Brenner DJ . Rochalimaea henselae sp. nov., a cause of septicemia, bacillary angiomatosis, and parenchymal bacillary peliosis. J Clin Microbiol 1992;30:275-280
Web of Science | Medline8
Spach DH ,Callis KP ,Paauw DS , et al. Endocarditis caused by Rochalimaea quintana in a patient infected with human immunodeficiency virus. J Clin Microbiol 1993;31:692-694
Web of Science | Medline9
Raoult D ,Drancourt M ,Carta A ,Gastaut JA . Bartonella (Rochalimaea) quintana isolation in patient with chronic adenopathy, lymphopenia, and a cat. Lancet 1994;343:977-977
CrossRef | Web of Science | Medline10
Relman DA ,Loutit JS ,Schmidt TM ,Falkow S ,Tompkins LS . The agent of bacillary angiomatosis -- an approach to the identification of uncultured pathogens. N Engl J Med 1990;323:1573-1580
Full Text | Web of Science | Medline11
Relman DA ,Falkow S ,LeBoit PE , et al. The organism causing bacillary angiomatosis, peliosis hepatis, and fever and bacteremia in immunocompromised patients. N Engl J Med 1991;324:1514-1514
Web of Science | Medline12
Perkocha LA ,Geaghan SM ,Yen TSB , et al. Clinical and pathological features of bacillary peliosis hepatis in association with human immunodeficiency virus infection. N Engl J Med 1990;323:1581-1586
Full Text | Web of Science | Medline13
Slater LN ,Welch DF ,Min K-W . Rochalimaea henselae causes bacillary angiomatosis and peliosis hepatis. Arch Intern Med 1992;152:602-606
CrossRef | Web of Science | Medline14
Slater LN ,Welch DF ,Hensel D ,Coody DW . A newly recognized fastidious gram-negative pathogen as a cause of fever and bacteremia. N Engl J Med 1990;323:1587-1593
Full Text | Web of Science | Medline15
Regnery RL ,Anderson BE ,Clarridge JE III ,Rodriguez-Barradas MC ,Jones DC ,Carr JH . Characterization of a novel Rochalimaea species, R. henselae sp. nov., isolated from blood of a febrile, human immunodeficiency virus-positive patient. J Clin Microbiol 1992;30:265-274
Web of Science | Medline16
Dolan MJ ,Wong MT ,Regnery RL , et al. Syndrome of Rochalimaea henselae adenitis suggesting cat scratch disease. Ann Intern Med 1993;118:331-336
Web of Science | Medline17
Zangwill KM ,Hamilton DH ,Perkins BA , et al. Cat scratch disease in Connecticut -- epidemiology, risk factors, and evaluation of a new diagnostic test. N Engl J Med 1993;329:8-13
Full Text | Web of Science | Medline18
Tappero JW ,Koehler JE ,Berger TG , et al. Bacillary angiomatosis and bacillary splenitis in immunocompetent adults. Ann Intern Med 1993;118:363-365
Web of Science | Medline19
Lucey D ,Dolan MJ ,Moss CW , et al. Relapsing illness due to Rochalimaea henselae in immunocompetent hosts: implication for therapy and new epidemiological associations. Clin Infect Dis 1992;14:683-688
CrossRef | Web of Science | Medline20
Hadfield TL ,Warren R ,Kass M ,Brun E ,Levy C . Endocarditis caused by Rochalimaea henselae. Hum Pathol 1993;24:1140-1141
CrossRef | Web of Science | Medline21
Larson AM ,Dougherty MJ ,Nowowiejski DJ , et al. Detection of Bartonella (Rochalimaea) quintana by routine acridine orange staining of broth blood cultures. J Clin Microbiol 1994;32:1492-1496
Web of Science | Medline22
Slater LN ,Coody DW ,Woolridge LK ,Welch DF . Murine antibody responses distinguish Rochalimaea henselae from Rochalimaea quintana. J Clin Microbiol 1992;30:1722-1727
Web of Science | Medline23
Brenner DJ ,McWhorter AC ,Knutson JK ,Steigerwalt AG . Escherichia vulneris: a new species of Enterobacteriaceae associated with human wounds. J Clin Microbiol 1982;15:1133-1140
Web of Science | Medline24
Matar GM ,Swaminathan B ,Hunter SB ,Slater LN ,Welch DF . Polymerase chain reaction-based restriction fragment length polymorphism analysis of a fragment of the ribosomal operon from Rochalimaea species for subtyping. J Clin Microbiol 1993;31:1730-1734
Web of Science | Medline25
Spach DH, Kanter AS, Daniels NA, et al. Bartonella (Rochalimaea) species as a cause of apparent culture-negative endocarditis. Clin Infect Dis (in press).
26
Schwartzman WA . Infections due to Rochalimaea: the expanding clinical spectrum. Clin Infect Dis 1992;15:893-900
CrossRef | Web of Science | Medline27
Koehler JE ,Tappero JW . Bacillary angiomatosis and bacillary peliosis in patients infected with human immunodeficiency virus. Clin Infect Dis 1993;17:612-624
CrossRef | Web of Science | Medline28
Koehler JE ,Glaser CA ,Tappero JW . Rochalimaea henselae infection: a new zoonosis with the domestic cat as a reservoir. JAMA 1994;271:531-535
CrossRef | Web of Science | Medline
- Citing Articles (65)
Citing Articles
1
Mosepele Mosepele, Dana Mazo, Jennifer Cohn. (2012) Bartonella Infection in Immunocompromised Hosts: Immunology of Vascular Infection and Vasoproliferation. Clinical and Developmental Immunology 2012, 1-5
CrossRef2
Kenji Satake, Isao Ohsawa, Noriyoshi Kobayashi, Ken Osaki, Hitoe Toyoda, Satoshi Horikoshi, Yasuhiko Tomino. (2011) Three cases of PR3-ANCA positive subacute endocarditis caused by attenuated bacteria (Propionibacterium, Gemella, and Bartonella) complicated with kidney injury. Modern Rheumatology 21:5, 536-541
CrossRef3
Yi-Lun Tsai, Chao-Chin Chang, Shih-Te Chuang, Bruno B. Chomel. (2011) Bartonella species and their ectoparasites: Selective host adaptation or strain selection between the vector and the mammalian host?. Comparative Immunology, Microbiology and Infectious Diseases 34:4, 299-314
CrossRef4
J.-C. Desenclos, A. Laporte, P. Brouqui. (2011) Les infections humaines transmises par les poux. Médecine et Maladies Infectieuses 41:6, 295-300
CrossRef5
Philippe Brouqui. (2011) Arthropod-Borne Diseases Associated with Political and Social Disorder. Annual Review of Entomology 56:1, 357-374
CrossRef6
Silpak Biswas, Jean-Marc Rolain. (2010) Bartonella infection: treatment and drug resistance. Future Microbiology 5:11, 1719-1731
CrossRef7
Anna Sander. 2010. Bartonella and Afipia. .
CrossRef8
Salvatore Incandela, Didier Raoult, Giustina Vitale, Anna Micalizzi, Pasquale Mansueto. (2008) Hepatosplenic cat-scratch fever with seropositivity for Bartonella quintana?. The Lancet Infectious Diseases 8:11, 663
CrossRef9
Masataka Yoda, Mitsumasa Hata, Akira Sezai, Satoshi Unosawa, Nobuyuki Furukawa, Kazutomo Minami. (2008) First Report of Bartonella Quintana Endocarditis in Japan. Circulation Journal 72:6, 1022-1024
CrossRef10
Nils-Gunnar Ilbäck, Göran Friman. (2007) Interactions Among Infections, Nutrients and Xenobiotics. Critical Reviews in Food Science and Nutrition 47:5, 499-519
CrossRef11
John L. Brusch. 2007. Microbiology of Infective Endocarditis and Clinical Correlates: Gram-Negative and Other Organisms. , 51-100.
CrossRef12
John C.M. Brust. 2007. Éthanol. , 385-516.
CrossRef13
Jonathan Iralu, Ying Bai, Larry Crook, Bruce Tempest, Gary Simpson, Taylor McKenzie, Frederick Koster. (2006) Rodent-associated Bartonella Febrile Illness, Southwestern United States. Emerging Infectious Diseases 12:7, 1081-1086
CrossRef14
Cédric Foucault, Philippe Brouqui, Didier Raoult. (2006) Bartonella quintana Characteristics and Clinical Management. Emerging Infectious Diseases 12:2, 217-223
CrossRef15
Laurie G. O'Rourke, Christian Pitulle, Barbara C. Hegarty, Sharon Kraycirik, Karen A. Killary, Paul Grosenstein, James W. Brown, Edward B. Breitschwerdt. (2005) Bartonella quintana in Cynomolgus Monkey ( Macaca fascicularis ). Emerging Infectious Diseases 11:12, 1931-1934
CrossRef16
Pierre Houpikian, Didier Raoult. (2005) Blood Culture-Negative Endocarditis in a Reference Center. Medicine 84:3, 162-173
CrossRef17
Dirk M. Elston. (2005) Life-threatening stings, bites, infestations, and parasitic diseases. Clinics in Dermatology 23:2, 164-170
CrossRef18
Philippe Brouqui, Andreas Stein, Herv?? Tissot Dupont, Pierre Gallian, Sekene Badiaga, Jean Marc Rolain, Jean Louis Mege, Bernard La Scola, Philippe Berbis, Didier Raoult. (2005) Ectoparasitism and Vector-Borne Diseases in 930 Homeless People From Marseilles. Medicine 84:1, 61-68
CrossRef19
Svena McGill, Lars Wesslén, Eva Hjelm, Martin Holmberg, Marja Kaisa Auvinen, Karl Berggren, Bodil Grandin-Jarl, Ulf Johnson, Staffan Wikström, Göran Friman. (2005) Bartonella spp. seroprevalence in healthy Swedish blood donors. Scandinavian Journal of Infectious Diseases 37:10, 723-730
CrossRef20
G. Aboudharam, P.-E. Fournier, M. Drancourt, D. Raoult, C. Foucault, P. Brouqui. (2004) Molecular detection of Bartonella quintana DNA in the dental pulp of a homeless patient. European Journal of Clinical Microbiology & Infectious Diseases
CrossRef21
J. E. Koehler, M. A. Sanchez, S. Tye, C. S. Garrido-Rowland, F. M. Chen, T. Maurer, J. L. Cooper, J. G. Olson, A. L. Reingold, W. K. Hadley, R. R. Regnery, J. W. Tappero. (2003) Prevalence of Bartonella Infection among Human Immunodeficiency Virus--Infected Patients with Fever. Clinical Infectious Diseases 37:4, 559-566
CrossRef22
SVENA McGILL, EVA HJELM, JOVAN RAJS, OLLE LINDQUIST, GÖRAN FRIMAN. (2003) Bartonella spp. Antibodies in Forensic Samples from Swedish Heroin Addicts. Annals of the New York Academy of Sciences 990:1, 409-413
CrossRef23
JEAN-MARC ROLAIN, D. ARNOUX, D. PARZY, J. SAMPOL, DIDIER RAOULT. (2003) Experimental Infection of Human Erythrocytes from Alcoholic Patients with Bartonella quintana. Annals of the New York Academy of Sciences 990:1, 605-611
CrossRef24
BRUNO B. CHOMEL, RICKIE W. KASTEN, JANE E. SYKES, HENRI-JEAN BOULOUIS, EDWARD B. BREITSCHWERDT. (2003) Clinical Impact of Persistent Bartonella Bacteremia in Humans and Animals. Annals of the New York Academy of Sciences 990:1, 267-278
CrossRef25
SVENA McGILL, JOVAN RAJS, EVA HJELM, OLLE LINDQUIST, GORAN FRIMAN. (2003) A study on forensic samples of Bartonella spp. antibodies in Swedish intravenous heroin addicts. APMIS 111:4, 507-513
CrossRef26
M Thiam, P.D Fall, S.B Gning, J.M Grinda, J.L Mainardi. (2002) Endocardite à Bartonella quintana. Chez un Sénégalais immunocompétent. La Revue de Médecine Interne 23:12, 1035-1037
CrossRef27
C. Foucault, K. Barrau, P. Brouqui, D. Raoult. (2002) Bartonella quintana Bacteremia among Homeless People. Clinical Infectious Diseases 35:6, 684-689
CrossRef28
B Pappalardo. (2001) Immunopathology of Bartonella vinsonii (berkhoffii) in experimentally infected dogs. Veterinary Immunology and Immunopathology 83:3-4, 125-147
CrossRef29
Didier Raoult, Cédric Foucault, Philippe Brouqui. (2001) Infections in the homeless. The Lancet Infectious Diseases 1:2, 77-84
CrossRef30
Shawn Starkenburg, Melissa E. Munroe, Carl Waltenbaugh. (2001) Early Alteration in Leukocyte Populations and Th1/Th2 Function in Ethanol-Consuming Mice. Alcoholism: Clinical and Experimental Research 25:8, 1221-1230
CrossRef31
PIERRE-EDOUARD FOURNIER, HERVÉ LELIEVRE, SUSANNAH J. EYKYN, JEAN-LUC MAINARDI, THOMAS J. MARRIE, FABRICE BRUNEEL, CHANTAL ROURE, JAMES NASH, DANIÈLE CLAVE, EDWARD JAMES, CATHERINE BENOIT-LEMERCIER, LIONEL DEFORGES, HERVÉ TISSOT-DUPONT, DIDIER RAOULT. (2001) Epidemiologic and Clinical Characteristics of Bartonella quintana and Bartonella henselae Endocarditis. Medicine 80:4, 245-251
CrossRef32
Diane H. Johnson, Burke A. Cunha. (2001) INFECTIONS IN CIRRHOSIS. Infectious Disease Clinics of North America 15:2, 363-371
CrossRef33
James A. Comer, Christopher D. Paddock, James E. Childs. (2001) Urban Zoonoses Caused by Bartonella , Coxiella , Ehrlichia , and Rickettsia Species. Vector-Borne and Zoonotic Diseases 1:2, 91-118
CrossRef34
Joseph A. Salerno, Carl Waltenbaugh, Nicholas P. Cianciotto. (2001) Ethanol Consumption and the Susceptibility of Mice to Listeria monocytogenes Infection. Alcoholism: Clinical and Experimental Research 25:3, 464-472
CrossRef35
Thomas Christian Roos, Murad Alam, Sabine Roos, Hans Friedrich Merk, David R. Bickers. (2001) Pharmacotherapy of Ectoparasitic Infections. Drugs 61:8, 1067-1088
CrossRef36
Hubert Lepidi, MD, PhD, Didier Raoult, MD, PhD, Pierre-Edouard Fournier, MD, PhD. (2000) Quantitative Analysis of Valvular Lesions During Bartonella Endocarditis. American Journal of Clinical Pathology 114:6, 880-889
CrossRef37
M.Y Kosoy, E.K Saito, D Green, E.L Marston, D.C Jones, J.E Childs. (2000) Experimental evidence of host specificity of Bartonella infection in rodents. Comparative Immunology, Microbiology and Infectious Diseases 23:4, 221-238
CrossRef38
M. E. Ohl, D. H. Spach. (2000) Bartonella quintana and Urban Trench Fever. Clinical Infectious Diseases 31:1, 131-135
CrossRef39
Barbe, Klara Pósfay, Jaeggi, Edgar, Ninet, BéatriceLiassine, Nadia, Donatiello, Cosima, Gervaix, Alain, Suter, Susanne, . (2000) Bartonella quintana Endocarditis in a Child. New England Journal of Medicine 342:24, 1841-1842
Full Text40
Ciro Maguiña, Eduardo Gotuzzo. (2000) BARTONELLOSIS. Infectious Disease Clinics of North America 14:1, 1-22
CrossRef41
Olivier Chosidow. (2000) Scabies and pediculosis. The Lancet 355:9206, 818
CrossRef42
Ludwig A. Lettau. (2000) The Language of Infectious Disease: A Light‐Hearted Review. Clinical Infectious Diseases 31:3, 734
CrossRef43
ERIK LARSSON, LARS WESSLÉN, OLLE LINDQUIST, ULRIK BAANDRUR, LARS ERIKSSON, ECKHARDT OLSEN, CHRISTER ROLF, GÖRAN FRIMAN. (1999) Sudden unexpected cardiac deaths among young Swedish orienteers - Morphological changes in hearts and other organs. APMIS 107:1-6, 325-336
CrossRef44
Cabot, Richard C.Scully, Robert E., Mark, Eugene J., McNeely, William F., Ebeling, Sally H., Skolnik, Paul R.Mark, Eugene J.. (1999) Case 5-1999. New England Journal of Medicine 340:7, 545-554
Full Text45
Brouqui, Philippe, Lascola, Bernard, Roux, Veronique, Raoult, Didier, . (1999) Chronic Bartonella quintana Bacteremia in Homeless Patients. New England Journal of Medicine 340:3, 184-189
Full Text46
Sophie Gasquet, Max Maurin, Philippe Brouqui, Hubert Lepidi, Didier Raoult. (1998) Bacillary angiomatosis in immunocompromised patients. AIDS 12:14, 1793-1803
CrossRef47
David H. Spach, Jane E. Koehler. (1998) BARTONELLA-ASSOCIATED INFECTIONS. Infectious Disease Clinics of North America 12:1, 137-155
CrossRef48
Koehler, Jane E., Sanchez, Melissa A., Garrido, Claudia S., Whitfeld, Margot J., Chen, Frederick M., Berger, Timothy G., Rodriguez-Barradas, Maria C., LeBoit, Philip E., Tappero, Jordan W., . (1997) Molecular Epidemiology of Bartonella Infections in Patients with Bacillary Angiomatosis–Peliosis. New England Journal of Medicine 337:26, 1876-1883
Full Text49
Tompkins, Lucy S., . (1997) Of Cats, Humans, and Bartonella. New England Journal of Medicine 337:26, 1916-1917
Full Text50
A. M. C. Bergmans, J. L. Coenen, R. Bakhuizen, B. W. Mooi, A. R. Ramdat Misier, B. Wilbrink, L. M. Schouls, M. J. H. M. Wolfhagen. (1997) Endocarditis in a Dutch patient caused by Bartonella quintana. Clinical Microbiology and Infection 3:6, 692-694
CrossRef51
Bruce A. Stewart. (1997) Human infection with Bartonella species. Clinical Microbiology and Infection 3:6, 677-689
CrossRef52
R WONG, J TAPPERO, C COCKERELL. (1997) Bacillary angiomatosis and other Bartonella species infections. Seminars in Cutaneous Medicine and Surgery 16:3, 188-199
CrossRef53
M. Maurin, R. Birtles, D. Raoult. (1997) Current knowledge ofBartonella species. European Journal of Clinical Microbiology & Infectious Diseases 16:7, 487-506
CrossRef54
Cabot, Richard C.Scully, Robert E., Mark, Eugene J., McNeely, William F., Ebeling, Sally H., Jacoby, George A.Hay, C. Mhorag. (1997) Case 2-1997. New England Journal of Medicine 336:3, 205-210
Full Text55
JAMES W. BASS, JUDY M. VINCENT, DONALD A. PERSON. (1997) The expanding spectrum of Bartonella infections: I. Bartonellosis and trench fever. The Pediatric Infectious Disease Journal 16:1, 2-10
CrossRef56
Robert C. Jerris, Russell L. Regnery. (1996) WILL THE REAL AGENT OF CAT-SCRATCH DISEASE PLEASE STAND UP? 1. Annual Review of Microbiology 50:1, 707-725
CrossRef57
H. -U. Schmidt, T. Kaliebe, J. Poppinger, C. Bühler, A. Sander. (1996) Isolation ofBartonella quintana from an HIV-positive patient with bacillary angiomatosis. European Journal of Clinical Microbiology & Infectious Diseases 15:9, 736-741
CrossRef58
Gad Baneth, Dorsey L. Kordick, Barbara C. Hegarty, Edward B. Breitschwerdt. (1996) Comparative seroreactivity to Bartonella henselae and Bartonella quintana among cats from Israel and North Carolina. Veterinary Microbiology 50:1-2, 95-103
CrossRef59
Stephen J. Gluckman. (1996) Q fever and trench fever. Clinics in Dermatology 14:3, 283-287
CrossRef60
W. Schwartzman, M.D. (1996) BARTONELLA ( ROCHALIMAEA ) INFECTIONS: Beyond Cat Scratch 1. Annual Review of Medicine 47:1, 355-364
CrossRef61
P Brouqui, D Raoult. (1996) Bartonella quintana invades and multiplies within endothelial cells in vitro and in vivo and forms intracellular blebs. Research in Microbiology 147:9, 719-731
CrossRef62
Michel Dupon, Anne-marie Savin De Larclause, Philippe Brouqui, Michel Drancourt, Didier Raoult, Antoine De Mascarel, Jean-Yves Lacut. (1996) Evaluation of Serological Response to Bartonella henselae, Bartonella quintana and Afipia felis Antigens in 64 Patients with Suspected Cat-scratch Disease. Scandinavian Journal of Infectious Diseases 28:4, 361-366
CrossRef63
Jane E. Koehler, Laurie Cederberg. (1995) Intra-abdominal mass associated with gastrointestinal hemorrhage: A new manifestation of bacillary angiomatosis. Gastroenterology 109:6, 2011-2014
CrossRef64
Thomas J. Marrie. (1995) Endocarditis of Uncertain Etiology. Zentralblatt für Bakteriologie 283:1, 1-4
CrossRef65
Relman, David A., . (1995) Has Trench Fever Returned?. New England Journal of Medicine 332:7, 463-464
Full Text
