https://orcid.org/0000-0003-4558-4532
Figures
Abstract
Background
Bartonella spp. are fastidious bacteria frequently identified as the cause of blood culture-negative (BCN) endocarditis. However, Bartonella infections are difficult to diagnose in routine laboratory testing and their incidence is probably underestimated. We investigated the epidemiological and clinical features of Bartonella endocarditis cases diagnosed between 2009 and 2021 on Reunion Island (Southwest Indian Ocean).
Method
We retrospectively included all patients diagnosed with Bartonella endocarditis at Reunion Island University Hospital during this period. Endocarditis was diagnosed on the basis of microbiological findings, including serological tests (IFA) and PCR on cardiac valves, and the modified Duke criteria. We used then the multispacer typing (MST) method to genotype the available Bartonella strains.
Findings
We report 12 cases of B. quintana endocarditis on Reunion Island (83.3% in men, median patient age: 32 years). All the patients originated from the Comoros archipelago. The traditional risk factors for B. quintana infection (homelessness, alcoholism, exposure to body lice) were absent in all but two of the patients, who reported head louse infestations in childhood. Previous heart disease leading to valve dysfunction was recorded in 50% of patients. All patients underwent cardiac valve surgery and antimicrobial therapy with a regimen including doxycycline. All patients presented high C-reactive protein concentrations, anemia and negative blood cultures. The titer of IgG antibodies against Bartonella sp. exceeded 1:800 in 42% of patients. Specific PCR on cardiac valves confirmed the diagnosis of B. quintana endocarditis in all patients. Genotyping by the MST method was performed on four strains detected in preserved excised valves and was contributive for three, which displayed the MST6 genotype.
Author summary
Bartonella quintana, best known as the cause of trench fever in soldiers during the First World War, can also cause endocarditis in humans. It is transmitted predominantly by the feces of body lice. After entering the bloodstream, it may become localized in damaged valves or tissues. Nevertheless, B. quintana remains an uncommon cause of infective endocarditis with few cases reported worldwide. However, the number of reported cases of this pathogen has recently increased mostly in refugee camps and among underhoused individuals in Europe and the USA.
We describe here 12 cases of B. quintana endocarditis in patients from Mayotte/the Comoros archipelago in the Southwest Indian Ocean. We highlight the presence of this pathogen in patients from this region characterized by high rates of poverty and population exchanges with Southern Africa.
Genotyping analysis on three strains from this cohort revealed the presence of a single genotype, different from those observed in Europe and Africa, suggesting the presence of a single B. quintana genotype in the Comoros archipelago, or a potential common source of contamination.
This study sheds light on the etiology of this neglected form of endocarditis and should raise local awareness of this disease.
Citation: Sarsiat L, Garrigos T, Houhamdi L, Dauwalder O, Kuli B, Braunberger E, et al. (2023) Case series of 12 Bartonella quintana endocarditis from the Southwest Indian Ocean. PLoS Negl Trop Dis 17(9): e0011606. https://doi.org/10.1371/journal.pntd.0011606
Editor: Volkhard A. J. Kempf, University Hospital of Frankfurt, GERMANY
Received: April 21, 2023; Accepted: August 20, 2023; Published: September 7, 2023
Copyright: © 2023 Sarsiat et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All data are available in the article and tables.
Funding: The author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Bartonella quintana is a small Gram-negative bacillus from class Alphaproteobacteria. These fastidious bacteria are generally transmitted by arthropod vectors, predominantly in the feces of body lice, and can cause various human infections. B. quintana was initially identified as the cause of trench fever in soldiers during World War I, but now mostly affects people living in poor sanitary conditions worldwide [1]. This re-emerging bacterium causes bacteremia and infective endocarditis (IE) in homeless and alcohol-dependent individuals in Europe and America. It is now often referred to as “urban trench fever” [2]. B. quintana can also cause bacillary angiomatosis and peliosis hepatitis in immunocompromised patients [3].
The first case of B. quintana endocarditis was reported in 1993 [4], and several hundred cases have since been described, mostly in Europe [5]. Other Bartonella species have also been implicated in endocarditis, notably B. henselae, and occasionally B. elizabethae, B. vinsonii subsp. berkhoffii, B. vinsonii subsp. arupensis, B. koehlerae, B. alsatica and “Candidatus Bartonella mayotimonensis” [6–13]. Published epidemiological data suggest that the prevalence of Bartonella endocarditis follows a European-African gradient, with prevalence increasing from north to south [5, 14]. Bartonella species are facultative intraerythrocytic bacteria with slow replication that are known to cause blood culture-negative endocarditis (BCNE), accounting for up to 28.4% of cases [5, 15]. They are, therefore, no readily detected in routine diagnostic procedures if their presence is not initially suspected, rendering diagnosis difficult [5].
Very few data are available concerning B. quintana endocarditis in South-East Africa and the Indian subcontinent, and no case has ever before been reported in the Southwest Indian Ocean area. Moreover, very few studies on B. quintana endocarditis have reported data for strain genotyping. Such analyses are useful for epidemiological investigations aiming to determine the source of the infection [16, 17].
The aim of this study was to review the epidemiological and clinical data, and outcomes of the documented cases of B. quintana endocarditis diagnosed on Reunion Island from 2009 to 2021, and to discuss possible links between cases or a common source of infection.
Methods
Ethics statement
Since this was a retrospective study based on archived patient records, it falls into the category of research not involving the human person (article L.1121-1 of the French Public Health Code, deliberation no. 2018–155 of the French Data Protection Authority (CNIL)). In addition, this research was performed in accordance with the Declaration of Helsinki. Consequently, committee approval was not required.
Patient recruitment
All definite cases of Bartonella endocarditis diagnosed at Reunion Island University Hospital from 2009 to 2021 were retrospectively included in this study. All patients diagnosed with infective endocarditis (IE) on Reunion Island are treated at this hospital. For each case, medical records were analyzed and various data were extracted, including age, sex, year of diagnosis, country of residence, medical history, clinical presentation, presence of fever, possible exposure, suspected infection pathway, affected valve, surgical intervention, determination of C-reactive protein and hemoglobin levels, antibacterial treatment and outcome.
Case definition
The diagnosis of definite Bartonella endocarditis is based on at least two major Duke score criteria: (i) echocardiogram positive for endocarditis, as defined in the modified Duke criteria [18, 19] and (ii) Bartonella-positive PCR on infected cardiac tissue, as defined in the recent update of the modified Duke criteria [18, 20, 21]. According to the guidelines followed in our medical laboratory [19], blood is collected for culture in cases of suspected endocarditis and incubated for 15 days. In cases of negative blood culture, serological testing is performed for Bartonella spp. and Coxiella burnetii. PCR analysis is also performed in patients undergoing valve surgery.
Serological analyses were based on immunofluorescence assays (IFA), as previously described [22], to determine the titers of antibodies directed against B. henselae, B. quintana (Bartonella IFA-Focus Diagnostics) and Coxiella burnetii (Q Fever IFA-Focus Diagnostics). PCR analyses were performed on bacterial DNA extracted from surgically excised valves. Two PCR were performed on an Ingenius instrument (ELITech Groupe France), targeting (i) Bartonella spp. (16S rRNA gene, Bartonella PROGENIE kit-Orgentec) and (ii) B. quintana (ribC gene, homemade PCR).
Genotyping
We used the multispacer typing (MST) genotyping method to identify and compare B. quintana strains. The culture of Bartonella spp. is challenging, and the MST approach makes it possible to circumvent the difficulties of culture, by making it possible to use directly extracted DNA, with sufficient resolution to discriminate between Bartonella clones. The MST method for Bartonella was set up by Foucault et al. through the amplification and sequencing of 34 spacers from a collection of 71 isolates, and can be used to characterize several genotypes based on the combined single-nucleotide polymorphism (SNP) profiles of two spacers (336 and 894) [23]. This method is suitable for use in epidemiological and evolutionary studies. In this study, DNA was extracted from preserved B. quintana PCR-positive cardiac samples, when available. The analysis was performed by the French National Reference Center (IHU Méditerranée Infection, Marseille, France).
Results
Characteristics of the patients and epidemiological data (Table 1)
In total, 12 cases were included in the study. Most of the infected patients were male (83.3%) and the median age was 32 years (IQR: 23.75–40.5 years). The recorded sites of residence of the patients were: Mayotte (n = 6, 50%), Comoros (n = 5, 41.7%) and Reunion Island (n = 1, 8.3%). Five of the six patients from Mayotte had recently traveled to or originated from Comoros. The only patient living on Reunion Island had also recently moved there from Mayotte (Table 1). None of the patients was immunocompromised or homeless, although information about living conditions was not available for all patients. However, three patients (25%) reported living in poor socioeconomic conditions: sheet metal house, clay ground and absence of running water. The population of Comoros is mostly Muslim, so alcohol consumption is uncommon. None of the patients had an alcohol use disorder. A history of contact with head lice was reported for only two patients (16.7%), and two patients, both farmers, reported contact with animals.
Clinical features (Table 2)
Eight patients (66.7%) had fever at initial presentation. Heart failure was the main presenting form of endocarditis caused by B. quintana in our cohort, reported in 11 patients (91.7%). Heart failure was mostly due to valvular insufficiency (10/11 patients). Acute renal failure complicating severe chronic renal failure was observed in one of the 12 patients (8.3%). Embolic phenomena were recorded in seven patients (58.3%, Table 2), most frequently taking the form of splenic (3 patients, 25%) or intracranial mycotic aneurysms (2 patients, 16.6%). All patients had native valves during the first episode of IE. The mitral valve was affected in 10 patients (83.3%), four of whom also had aortic valve involvement, with one patient also having tricuspid valve involvement. In two patients (16.7%) only the aortic valve was involved.
Treatment and outcome (Table 2)
In this study, all patients received doxycycline for at least four weeks. Seven patients (58.3%) received concomitant gentamicin for at least two weeks. Two patients received rifampicin, and one received amoxicillin in place of gentamicin, in combination with doxycycline.
Cardiac valve surgery was performed in all patients. Significant postoperative complications occurred in eight patients: six suffered from cardiac rhythm disorders, and two had mediastinitis. One of the two cases of postoperative mediastinitis involved Staphylococcus epidermidis, whereas the causal organism was not documented in the other case. None of the patients died from IE, and none suffered a relapse of B. quintana IE. However, one patient experienced three episodes of other types of bacterial endocarditis and sepsis in the following months and years. One patient had to undergo a second operation to replace the mitral valve seven years after his initial IE. Two patients developed heart failure sequelae: follow-up heart scintigraphy on patient 6 showed an altered post-stress left ventricular ejection fraction one month after medical care, whereas patient 8 presented grade 1 aortic regurgitation and grade 2 mitral regurgitation three years after surgery.
Diagnosis
All patients had B. quintana infection confirmed by molecular testing on a cardiac specimen. Blood cultures were performed and were negative for all patients. Serological testing was performed for 11 patients, and nine patients (75%) had antibody titers >1:100. The French National Reference Center considers IFA results to be positive if the IgG antibody titer is ≥1:100, and uses a titer of 1:800 as the cutoff for IE diagnosis [5]. Six patients (54.5%) had antibody titers >1:800. Serological results were negative for two patients (16.7%). Laboratory tests revealed high C-reactive protein levels (median: 61 mg/L, range: 14.3–189 mg/L) and anemia (median Hb: 9.35 g/dL, range: 7.6–11.1 g/dL) in all patients.
Echocardiography records were obtained for all patients. In Table 3, echocardiograms are described as TTE if transthoracic, TEE if transesophageal and ECHO if the type of echocardiogram was not specified. Vegetations were observed in 10 patients (83.3%).
All patients required valve replacement, due to cardiac valve destruction or insufficiency. The results of PCR for B. quintana on the DNA extracted from cardiac valve tissue or vegetations were positive for all 12 patients.
Sequence typing
Residual biological material (cardiac specimens or serum samples) was available for sequence typing for only four of the 12 cases. MST analysis was informative in three of these cases. It was performed on three cardiac samples, from patients 8, 10 and 12. Spacers 336 and 894 were amplified by PCR and their nucleotide sequence was determined. All three strains were found to have the same MST profile, with type 1 as the sequence profile for spacer 336, and type 5 for spacer 894. Based on this combination of sequence types, we classified the three isolates as genotype MST 6 (S1 Table).
Discussion
We report here a first series of 12 cases of B. quintana infective endocarditis occurring in the Southwest Indian Ocean area from 2009 to 2021.
Cases of Bartonella infective endocarditis have been reported worldwide, mostly in the Americas and Europe with bacteria of this genus accounting for 0 to 4.5% of infective endocarditis cases. The most frequently reported species in such cases is B. quintana [5, 15, 24–44]. However, only a few cases from other countries have been reported to date [15, 44–54], and the incidence of Bartonella infective endocarditis in the Southwest Indian Ocean remains unknown.
The Cardiothoracic Surgery Department of Reunion Island University Hospital is the reference center for the diagnosis and treatment of endocarditis in the Southwest Indian Ocean area, providing care for all patients from this region. Based on the data collected at Reunion Island University Hospital for 2020, the prevalence of Bartonella endocarditis was 3.1% among the documented cases of IE. However, the prevalence of Bartonella IE in this region is almost certainly underestimated, as only the most serious clinical cases benefit from medical evacuation from Mayotte to Reunion Island, as demonstrated by the high rates of heart failure and valve damage in our series of patients (all of whom required surgery).
Our findings confirm published data indicating a male preponderance and low median age [41, 55–57]. Clinical presentation was similar to that for other types of subacute bacterial endocarditis. However, severe acute symptoms (acute pulmonary edema, acute coronary syndrome, subarachnoid hemorrhage) were often present at initial presentation, as previously reported [15, 45]. This finding may be explained by the subacute pathophysiology of Bartonella IE, and by late diagnosis and care, as access to healthcare is often very difficult in poor areas, such as Mayotte and Comoros. It is important to remind that patients in this cohort are transferred from Mayotte/Comoros to Reunion Island at an advanced stage of the disease, thus presenting symptoms reported might be those of late evolution of endocarditis.
Half the patients in our study already had damaged valves at presentation. Interestingly, no prior valvular disease was documented for most of the published patients with B. quintana endocarditis [4, 42, 46]. However, some studies reported rheumatic heart disease as the risk factor most frequently associated with B. quintana IE [15, 50, 53]. This may reflect differences in the clinical course of the disease between the Southwest Indian Ocean region and Europe, where studies have suggested that B. quintana IE followed chronic bacteremia in patients without prior valve defects [42]. Moreover, the mitral valve was the valve most frequently affected (75%) in our patients, whereas the aortic valve was the valve most frequently affected in published cases [57]. One hypothesis could be an association between previous presence of rheumatic heart disease (41.7%) in the cohort, and mitral valve affect. A predominant mitral valve involvement has already been observed in cases reporting rheumatic heart disease in medical history [15, 50, 53].
The recommended treatment for B. quintana endocarditis according to European guidelines is oral doxycycline (100 mg/12 h) for four weeks plus gentamicin (3 mg/24 h) for two weeks [19]. All the patients in our cohort received at least one of these two antibiotics. However, three patients were not treated with the recommended double-therapy regimen: patients 6, 9 and 12 (patients 5 and 10 received gentamicin for 2 weeks before Bartonella infection diagnosis, as initial antibacterial treatment). They received doxycycline alone, or associated to amoxicillin or rifampicin. Although not in accordance with the guidelines, theses regimens showed clinical success. Gentamicin is known to cause renal toxicity, nevertheless, this complication has not been observed in the cohort following the use of this antibiotic. Bartonella IE is known to cause significant destruction of valve tissues, necessitating valve surgery more frequently than IE caused by other pathogens [58]. Our study confirmed these findings, with all 12 cases requiring surgical treatment. This greater need for surgical treatment may be due to delayed management or a pre-existing altered state potentially aggravated by undernutrition and poor socioeconomic conditions and underlying the higher rates of postoperative complications (66.7%) than for other types of bacterial IE [59].
BCNE is associated with a higher rate of in-hospital adverse events than blood culture-positive endocarditis, although recent publications have suggested similar long-term outcomes [60]. Two patients developed postoperative mediastinitis. Only one other case has ever been reported to develop post-sternotomy mediastinitis following B. quintana IE [44]. Despite the short-term complications observed, none of the patients died, contrasting with the previous estimate of 7–30% for Bartonella IE-related mortality [26]. Patient 2 developed recurrent IE caused by Streptococcus spp. months and years after initial B. quintana IE diagnosis. This case highlights the risk factor that chronic B. quintana IE represents for additional endocarditis, and the possibility of underestimating B. quintana if the infection was concomitant. This has already been described by Boodman et al. who mentioned “subacute B. quintana infection creates valvular damage and large vegetations, which provide a substrate for seeding when acute bacteremia occurs with a different pathogen” [30, 61]. Serological results were positive (IgG ≥1:100) in 81.8% of patients, slightly below the sensitivity of 91% estimated for IFA by Edouard et al. [5]. Nevertheless, serology guided diagnosis in 6 of 11 cases (54.5%), with IgG titers ≥1:800, the recommended cutoff for Bartonella IE diagnosis [5]. Serological assay showed low performance in this study, compared to other studies that show a sensitivity of 63–94% [5, 47]. Maurin et al. has already showed the low sensitivity of the IFA-Focus Diagnostics kit in detecting B. quintana IgG on B. quintana endocarditis patients [22]. In addition, we noted that patient 11 presented a negative serology, possibly due to his severe undernutrition that could cause relative immunosuppression. Moreover, it is noteworthy the serological titers measured against both B. quintana and B. henselae cross-react between these two species, as already published [22, 27, 29, 33, 37, 47]. Also, recent studies have demonstrated cross-seroreactivity at low level between Bartonella spp. and other species in cases of blood culture positive endocarditis. Consequently, anti-Bartonella serology may be insufficient without confirmation by another technique, such as PCR in this study [47, 62]. PCR therefore remains the best diagnostic tool, provided that sufficient tissue is available. However, RT-PCR has a low sensitivity when applied to blood and serum samples (33% and 36%, respectively) [5]. Overall, molecular assays on tissues and serological testing perform well for the diagnosis of B. quintana IE. An increase in C-reactive protein concentration and anemia were observed in all patients. The anemia could be attributed to endocarditis-related inflammation. Thus, given that confirmation analyses can take a long time, we believe that any patient from Mayotte or Comoros presenting with symptoms of endocarditis, a biological inflammatory syndrome, and vegetations detectable on an echocardiogram but with negative blood cultures should be considered a possible case of B. quintana (or Coxiella burnetti) IE, until proven otherwise. In such cases, the early administration of doxycycline, before confirmation of the diagnosis, may be beneficial.
The B. quintana genotype circulating in the Southwest Indian Ocean region appears to be different from those circulating in Europe and Africa. Interestingly, the MST 6 genotype identified in our cohort was previously identified only once, in aortic valve tissues from a patient with B. quintana endocarditis in Australia [51]. All three strains successfully analyzed by MST had identical sequence profiles, and two of these strains were isolated two years apart. Despite the very small population analyzed, these findings suggest that there may be only one B. quintana genotype (MST 6) circulating in the Comoros archipelago, or that there is a potential common source of contamination on Mayotte. This exposure factor has yet to be identified. One of these patients was a farmer who may have come into contact with animals and lived in a rural community. The known risk factors for B. quintana endocarditis are homelessness, alcohol dependence and exposure to body lice [1]. It is reasonable to assume that these markers are linked to poor socioeconomic status [4]. Exposure to head lice was identified only in two cases, but we believe that information about head louse infestation history were missing, probably because patients had been infected months or years before their admission to hospital for IE. Moreover, Sangaré et al. demonstrated the effective presence of B. quintana vectors in the Southwest Indian Ocean area (in 4.5% of body and 2.6% of head lice in Madagascar, with even higher rates in other African countries, including East African countries) [63]. Furthermore, all of the patients studied here originated from Mayotte or Comoros, where a high proportion of the population has an income below the threshold defining the national poverty line and there are many exchanges of population with Southern Africa [64]. However, one of the limitations of this retrospective study is that the bacterial diagnosis was established a long time after admission. It was therefore not possible to identify and record possible sources of infection for most of the cases.
Conclusion
We report here an original series of 12 cases of B. quintana IE from the Southwest Indian Ocean, where this disease has never before been described. Our data suggest that B. quintana is not an uncommon cause of native valve endocarditis in Comoros archipelago, particularly on Mayotte. Moreover, immigration from the Comoros archipelago to the French islands in this region is continuing, rendering this case series of particular interest. Local epidemiological and seroprevalence studies are required to determine the frequency of B. quintana infection in the Southwest Indian Ocean area. This study should raise local awareness of this neglected disease. B. quintana IE should be suspected in patients from Mayotte or Comoros with mitral valve dysfunction and blood culture-negative endocarditis, even in the absence of the traditional risk factors for Bartonella infection.
Supporting information
S1 Table. Multispacer typing (MST) genotyping results.
https://doi.org/10.1371/journal.pntd.0011606.s001
(DOCX)
References
- 1. Ruiz J. Bartonella quintana, past, present, and future of the scourge of World War I. APMIS Acta Pathol Microbiol Immunol Scand. 2018 Nov;126(11):831–7.
- 2. Ohl ME, Spach DH. Bartonella quintana and urban trench fever. Clin Infect Dis. 2000 Jul;31(1):131–5.
- 3. Foucault C, Brouqui P, Raoult D. Bartonella quintana characteristics and clinical management. Emerg Infect Dis. 2006 Feb;12(2):217–23.
- 4. Okaro U, Addisu A, Casanas B, Anderson B. Bartonella Species, an Emerging Cause of Blood-Culture-Negative Endocarditis. Clin Microbiol Rev. 2017 Jul;30(3):709–46.
- 5. Edouard S, Nabet C, Lepidi H, Fournier PE, Raoult D. Bartonella, a common cause of endocarditis: a report on 106 cases and review. J Clin Microbiol. 2015 Mar;53(3):824–9.
- 6. Daly JS, Worthington MG, Brenner DJ, Moss CW, Hollis DG, Weyant RS, et al. Rochalimaea elizabethae sp. nov. isolated from a patient with endocarditis. J Clin Microbiol. 1993 Apr;31(4):872–81.
- 7. Roux V, Eykyn SJ, Wyllie S, Raoult D. Bartonella vinsonii subsp. berkhoffii as an agent of afebrile blood culture-negative endocarditis in a human. J Clin Microbiol. 2000 Apr;38(4):1698–700.
- 8. Olarte L, Ampofo K, Thorell EA, Sanderson S, Doby E, Pavia AT, et al. Bartonella vinsonii endocarditis in an adolescent with congenital heart disease. Pediatr Infect Dis J. 2012 May;31(5):531–4.
- 9. Fenollar F, Sire S, Wilhelm N, Raoult D. Bartonella vinsonii subsp. arupensis as an agent of blood culture-negative endocarditis in a human. J Clin Microbiol. 2005 Feb;43(2):945–7.
- 10. Avidor B, Graidy M, Efrat G, Leibowitz C, Shapira G, Schattner A, et al. Bartonella koehlerae, a new cat-associated agent of culture-negative human endocarditis. J Clin Microbiol. 2004 Aug;42(8):3462–8.
- 11. Raoult D, Roblot F, Rolain JM, Besnier JM, Loulergue J, Bastides F, et al. First isolation of Bartonella alsatica from a valve of a patient with endocarditis. J Clin Microbiol. 2006 Jan;44(1):278–9.
- 12. Jeanclaude D, Godmer P, Leveiller D, Pouedras P, Fournier PE, Raoult D, et al. Bartonella alsatica endocarditis in a French patient in close contact with rabbits. Clin Microbiol Infect. 2009 Dec;15 Suppl 2:110–1.
- 13. Lin EY, Tsigrelis C, Baddour LM, Lepidi H, Rolain JM, Patel R, et al. Candidatus Bartonella mayotimonensis and endocarditis. Emerg Infect Dis. 2010 Mar;16(3):500–3. pmid:20202430
- 14. Lam JC, Fonseca K, Pabbaraju K, Meatherall BL. Case Report: Bartonella quintana Endocarditis Outside of the Europe-African Gradient: Comprehensive Review of Cases within North America. Am J Trop Med Hyg. 2019 May;100(5):1125–9.
- 15. Tasher D, Raucher-Sternfeld A, Tamir A, Giladi M, Somekh E. Bartonella quintana, an Unrecognized Cause of Infective Endocarditis in Children in Ethiopia. Emerg Infect Dis. 2017 Aug;23(8).
- 16. Kosoy M, McKee C, Albayrak L, Fofanov Y. Genotyping of Bartonella bacteria and their animal hosts: current status and perspectives. Parasitology. 2018 Apr;145(5):543–62.
- 17. Sato S, Shapira L, Tasher D, Maruyama S, Giladi M. Molecular epidemiology of Bartonella quintana endocarditis in patients from Israel and Eastern Africa. BMC Infect Dis. 2023 Mar 7;23(1):142.
- 18. Li JS, Sexton DJ, Mick N, Nettles R, Fowler VG, Ryan T, et al. Proposed modifications to the Duke criteria for the diagnosis of infective endocarditis. Clin Infect Dis. 2000 Apr;30(4):633–8. pmid:10770721
- 19. Habib G, Lancellotti P, Antunes MJ, Bongiorni MG, Casalta JP, Del Zotti F, et al. 2015 ESC Guidelines for the management of infective endocarditis: The Task Force for the Management of Infective Endocarditis of the European Society of Cardiology (ESC). Endorsed by: European Association for Cardio-Thoracic Surgery (EACTS), the European Association of Nuclear Medicine (EANM). Eur Heart J. 2015 Nov;36(44):3075–128. pmid:26320109
- 20. Durack DT, Lukes AS, Bright DK. New criteria for diagnosis of infective endocarditis: utilization of specific echocardiographic findings. Duke Endocarditis Service. Am J Med. 1994 Mar;96(3):200–9. pmid:8154507
- 21. Fowler VG, Durack DT, Selton-Suty C, Athan E, Bayer AS, Chamis AL, et al. The 2023 Duke-ISCVID Criteria for Infective Endocarditis: Updating the Modified Duke Criteria. Clin Infect Dis. 2023 May 4:ciad271.
- 22. Maurin M, Rolain JM, Raoult D. Comparison of in-house and commercial slides for detection by immunofluorescence of immunoglobulins G and M against Bartonella henselae and Bartonella quintana. Clin Diagn Lab Immunol. 2002 Sep;9(5):1004–9.
- 23. Foucault C, La Scola B, Lindroos H, Andersson SGE, Raoult D. Multispacer typing technique for sequence-based typing of Bartonella quintana. J Clin Microbiol. 2005 Jan;43(1):41–8.
- 24. Brouqui P, Raoult D. New insight into the diagnosis of fastidious bacterial endocarditis. FEMS Immunol Med Microbiol. 2006 Jun;47(1):1–13. pmid:16706783
- 25. Shepard Z, Barahona LV, Montalbano G, Rowan SE, Franco-Paredes C, Madinger N. Bartonella quintana Infection in People Experiencing Homelessness in the Denver Metropolitan Area. J Infect Dis. 2022 Jun;jiac238.
- 26. García-Álvarez L, García-García C, Muñoz P, Fariñas-Álvarez MDC, Cuadra MG, Fernández-Hidalgo N, et al. Bartonella Endocarditis in Spain: Case Reports of 21 Cases. Pathog Basel Switz. 2022 May;11(5):561.
- 27. Boodman C, MacDougall W, Hawkes M, Tyrrell G, Fanella S. Bartonella quintana endocarditis in a child from Northern Manitoba, Canada. PLoS Negl Trop Dis. 2022 May;16(5):e0010399.
- 28. Luciani L, El Baroudi Y, Prudent E, Raoult D, Fournier PE. Bartonella infections diagnosed in the French reference center, 2014–2019, and focus on infections in the immunocompromised. Eur J Clin Microbiol Infect Dis. 2021 Nov;40(11):2407–10.
- 29. Santhanam H, Nguyen MHN, Muthukumarasamy N, Mehta A, Francisco MT, Fountain RR, et al. Bartonella endocarditis in patients with right ventricle-to-pulmonary artery conduit: 2 case reports and literature review. IDCases. 2021 Oct;26:e01306.
- 30. Boodman C, Wuerz T, Lagacé-Wiens P, Lindsay R, Dibernardo A, Bullar J, et al. Serologic testing for Bartonella in Manitoba, Cana, 2010–2020: a retrospective case series. CMAJ Open. 2022 May;10(2):E476–E482.
- 31. Drummond MR, de Almeida AR, Valandro L, Pavan MHP, Stucchi RSB, Aoki FH, et al. Bartonella henselae endocarditis in an elderly patient. PLoS Negl Trop Dis. 2020 Jul;14(7):e0008376.
- 32. Promer K, Cowell AN, Reed SL, Castellanos LR, Aronoff-Spencer E. Bartonella quintana Endocarditis in a Homeless Man with Cat Exposure in San Diego, California. Vector Borne Zoonotic Dis Larchmt N. 2020 Jun;20(6):468–70.
- 33. Delama I, Mondaca R, Aguayo I, Roldán A, Ferrés M, Fica A. Infectious endocarditis by Bartonella species. Report of two cases. Rev Med Chil. 2019 Oct;147(10):1340–5.
- 34. Patel S, Richert ME, White R, Lambing T, Saleeb P. A Case of Bartonella quintana Culture-Negative Endocarditis. Am J Case Rep. 2019 Apr;20:602–6.
- 35. Pinheiro Santos J, Sousa R, Santos A, Laranjeira Santos Á, Fragata J. Infective Endocarditis Due to Bartonella quintana in a Patient with Biological Aortic Prosthesis. Rev Port Cir Cardio-Torac E Vasc Orgao. 2019 Mar;26(1):59–61.
- 36. Saison J, Harbaoui B, Bouchiat C, Pozzi M, Ferry T. Unexpected severe native aortic subacute endocarditis due to Bartonella quintana in a 40-year-old woman with good socioeconomic condition. BMJ Case Rep. 2016 Sep;2016:bcr2016216355.
- 37. Ghidey FY, Igbinosa O, Mills K, Lai L, Woods C, Ruiz ME, et al. Case series of Bartonella quintana blood culture-negative endocarditis in Washington, DC. JMM Case Rep. 2016 Aug;3(4):e005049.
- 38. Chaloner GL, Harrison TG, Birtles RJ. Bartonella species as a cause of infective endocarditis in the UK. Epidemiol Infect. 2013 Apr;141(4):841–6.
- 39. Dimopoulos S, Eleftherakis E, Charitos C, Sakellaridis T, Sinapidis D, Kostis E, et al. Bartonella quintana endocarditis as a cause of severe aortic insufficiency and heart failure. Hell J Cardiol HJC Hell Kardiologike Epitheorese. 2012 Dec;53(6):476–9.
- 40. Alozie A, Yerebakan C, Westphal B, Podbielski A. Bartonella quintana endocarditis of the tricuspid and mitral valves. Thorac Cardiovasc Surg. 2012 Jul;60(5):363–5.
- 41. Houpikian P, Raoult D. Blood Culture-Negative Endocarditis in a Reference Center: Etiologic Diagnosis of 348 Cases. Medicine (Baltimore). 2005 May;84(3):162–73. pmid:15879906
- 42. Fournier PE, Lelievre H, Eykyn SJ, Mainardi JL, Marrie TJ, Bruneel F, et al. Epidemiologic and clinical characteristics of Bartonella quintana and Bartonella henselae endocarditis: a study of 48 patients. Medicine (Baltimore). 2001 Jul;80(4):245–51.
- 43. Drancourt M, Mainardi JL, Brouqui P, Vandenesch F, Carta A, Lehnert F, et al. Bartonella (Rochalimaea) quintana Endocarditis in Three Homeless Men. N Engl J Med. 1995 Feb;332(7):419–23.
- 44. Plantinga NL, Vos RJ, Georgieva L, Roescher N. Bartonella quintana as a cause for prosthetic valve endocarditis and post-sternotomy mediastinitis. Access Microbiol. 2021 Mar;3(3):000217.
- 45. Mohammadian M, Butt S. Endocarditis caused by Bartonella quintana, a rare case in the United States. IDCases. 2019 Apr;17:e00533.
- 46. Pecoraro AA, Herbst PP, Pienaar CC, Taljaard JJ, Prozesky HH, Janson JJ, et al. Bartonella species as a cause of culture-negative endocarditis in South Africa. Eur J Clin Microbiol Infect Dis. 2021 Sep;40(9):1873–9.
- 47. Shapira L, Rasis M, Binsky Ehrenreich I, Maor Y, Katchman EA, Treves A, et al. Laboratory Diagnosis of 37 Cases of Bartonella Endocarditis Based on Enzyme Immunoassay and Real-Time PCR. J Clin Microbiol. 2021 May;59(6):e02217–20.
- 48. Lim MH, Chung DR, Kim WS, Park KS, Ki CS, Lee NY, et al. First case of Bartonella quintana endocarditis in Korea. J Korean Med Sci. 2012 Nov;27(11):1433–5.
- 49. Yamada Y, Ohkusu K, Yanagihara M, Tsuneoka H, Ezaki T, Tsuboi J, et al. Prosthetic valve endocarditis caused by Bartonella quintana in a patient during immunosuppressive therapies for collagen vascular diseases. Diagn Microbiol Infect Dis. 2011 Jul;70(3):395–8.
- 50. Balakrishnan N, Menon T, Fournier PE, Raoult D. Bartonella quintana and Coxiella burnetii as causes of endocarditis, India. Emerg Infect Dis. 2008 Jul;14(7):1168–9.
- 51. Woolley MW, Gordon DL, Wetherall BL. Analysis of the first Australian strains of Bartonella quintana reveals unique genotypes. J Clin Microbiol. 2007 Jun;45(6):2040–3.
- 52. Goldstein LH, Saliba WR, Elias M, Zlotnik A, Raz R, Giladi M. Bartonella quintana endocarditis in east Africa. Eur J Intern Med. 2005 Nov;16(7):518–9.
- 53. Posfay Barbe K, Jaeggi E, Ninet B, Liassine N, Donatiello C, Gervaix A, et al. Bartonella quintana endocarditis in a child. N Engl J Med. 2000 Jun;342(24):1841–2.
- 54. Simon-Vermont I, Altwegg M, Zimmerli W, Flückiger U. Duke criteria-negative endocarditis caused by Bartonella quintana. Infection. 1999;27(4–5):283–5.
- 55. Hoen B, Alla F, Selton-Suty C, Béguinot I, Bouvet A, Briançon S, et al. Changing profile of infective endocarditis: results of a 1-year survey in France. JAMA. 2002 Jul;288(1):75–81. pmid:12090865
- 56. Houpikian P, Raoult D. Western immunoblotting for Bartonella endocarditis. Clin Diagn Lab Immunol. 2003 Jan;10(1):95–102.
- 57. Raoult D, Fournier PE, Vandenesch F, Mainardi JL, Eykyn SJ, Nash J, et al. Outcome and Treatment of Bartonella Endocarditis. Arch Intern Med. 2003 Jan;163(2):226.
- 58. Brouqui P, Raoult D. Endocarditis Due to Rare and Fastidious Bacteria. Clin Microbiol Rev. 2001 Jan;14(1):177–207. pmid:11148009
- 59. Jakuska P, Ereminiene E, Muliuolyte E, Kosys V, Pavlavičius L, Zukovas G, et al. Predictors of early mortality after surgical treatment of infective endocarditis: a single-center experience. Perfusion. 2020 May;35(4):290–6. pmid:31480970
- 60. Meidrops K, Zuravlova A, Osipovs JD, Kalejs M, Groma V, Petrosina E, et al. Comparison of outcome between blood culture positive and negative infective endocarditis patients undergoing cardiac surgery. J Cardiothorac Surg. 2021 May;16(1):147. pmid:34044847
- 61. Barbier F, Fournier PE, Dauge MC, Gallien S, Raoult D, Andremont A, et al. Bartonella quintana coinfection in Staphylococcus aureus endocarditis: usefulness of screening in high-risk patients? Clin Infect Dis. 2009 May;48(9):1332–3.
- 62. Arregle F, Gouriet F, Amphoux B, Edouard S, Chaudet H, Casalta JP, et al. Western Immunoblotting for the Diagnosis of Enterococcus faecalis and Streptococcus gallolyticus Infective Endocarditis. Front Cell Infect Microbiol. 2019 Sep;9:314.
- 63. Sangaré AK, Boutellis A, Drali R, Socolovschi C, Barker SC, Diatta G, et al. Detection of Bartonella quintana in African body and head lice. Am J Trop Med Hyg. 2014 Aug;91(2):294–301.
- 64.
L’essentiel sur… Mayotte | Insee [Internet]. [cited 2022 Nov 20]. Available from: https://www.insee.fr/fr/statistiques/4632225.