Bartonella quintana detection among arthropods and their hosts: a systematic review and meta-analysis.

BACKGROUND: Bartonella quintana is a body louse-borne bacterium causing bacteremia and infective endocarditis. We aimed to describe B. quintana detection among arthropods and their hosts. METHODS: We searched databases in PubMed Central/MEDLINE, Scopus, Embase, and Web of Science from January 1, 1915 (the year of B. quintana discovery) to January 1, 2024, to identify publications containing specific search terms relating to B. quintana detection among arthropods. Descriptive statistics and meta-analysis of pooled prevalence using random-effects models were performed for all arthropods and body and head lice. RESULTS: Of 1265 records, 62 articles were included, describing 8839 body lice, 4962 head lice, and 1692 other arthropods, such as different species of fleas, bedbugs, mites, and ticks. Arthropods were collected from 37 countries, of which 28 had arthropods with B. quintana DNA. Among articles that reported B. quintana detection among individual arthropods, 1445 of 14,088 (0.1026, 95% CI [0.0976; 0.1077]) arthropods tested positive for B. quintana DNA, generating a random-effects model global prevalence of 0.0666 (95% CI [0.0426; 0.1026]). Fifty-six studies tested 8839 body lice, of which 1679 had B. quintana DNA (0.1899, 95% CI [0.1818; 0.1983]), generating a random-effects model pooled prevalence of 0.2312 (95% CI [0.1784; 0.2843]). Forty-two studies tested 4962 head lice, of which 390 head lice from 20 studies originating from 11 different countries had B. quintana DNA (0.0786, 95% CI [0.0713; 0.0864]). Eight studies detected B. quintana DNA exclusively on head lice. Five studies reported greater B. quintana detection on head lice than body lice; all originated from low-resource environments. CONCLUSIONS: Bartonella quintana is a vector-borne bacterium with a global distribution, disproportionately affecting marginalized populations. Bartonella quintana DNA has been detected in many different arthropod species, though not all of these arthropods meet criteria to be considered vectors for B. quintana transmission. Body lice have long been known to transmit B. quintana. A limited number of studies suggest that head lice may also act as possible vectors for B. quintana in specific low-resource contexts.

Bartonella quintana Endocarditis in a Homeless Man with Cat Exposure in San Diego, California.

We report a case of Bartonella quintana endocarditis in a homeless man with congenital bicuspid aortic valve and significant cat exposure living in downtown San Diego, California.

Bartonella quintana and Typhus Group Rickettsiae Exposure among Homeless Persons, Bogotá, Colombia.

In 2015, we investigated Bartonella quintana and typhus group rickettsiae in body lice from homeless persons in Bogotá, Colombia. We found B. quintana-infected body lice and seroprevalence of this microorganism in 19% of homeless persons and typhus group rickettsiae in 56%. Public health professionals should start preemptive measures and active vector control.

Detection of bacterial pathogens including potential new species in human head lice from Mali.

In poor African countries, where no medical and biological facilities are available, the identification of potential emerging pathogens of concern at an early stage is challenging. Head lice, Pediculus humanus capitis, have a short life, feed only on human blood and do not transmit pathogens to their progeny. They are, therefore, a perfect tool for the xenodiagnosis of current or recent human infection. This study assessed the occurrence of bacterial pathogens from head lice collected in two rural villages from Mali, where a high frequency of head lice infestation had previously been reported, using molecular methods. Results show that all 600 head lice, collected from 117 individuals, belonged to clade E, specific to West Africa. Bartonella quintana, the causative agent of trench fever, was identified in three of the 600 (0.5%) head lice studied. Our study also shows, for the first time, the presence of the DNA of two pathogenic bacteria, namely Coxiella burnetii (5.1%) and Rickettsia aeschlimannii (0.6%), detected in human head lice, as well as the DNA of potential new species from the Anaplasma and Ehrlichia genera of unknown pathogenicity. The finding of several Malian head lice infected with B. quintana, C. burnetii, R. aeschlimannii, Anaplasma and Ehrlichia is alarming and highlights the need for active survey programs to define the public health consequences of the detection of these emerging bacterial pathogens in human head lice.

Comparison of the proliferation and excretion of Bartonella quintana between body and head lice following oral challenge.

Human body and head lice are highly related haematophagous ectoparasites but only the body louse has been shown to transmit Bartonella quintana, the causative agent of trench fever. The mechanisms by which body lice became a vector for B. quintana, however, are poorly understood. Following oral challenge, green fluorescent protein-expressing B. quintana proliferated over 9 days postchallenge with the number of bacteria being significantly higher in whole body vs. head lice. The numbers of B. quintana detected in faeces from infected lice, however, were approximately the same in both lice. Nevertheless, the viability of B. quintana was significantly higher in body louse faeces. Comparison of immune responses in alimentary tract tissues revealed that basal transcription levels of peptidoglycan recognition protein and defensins were lower in body lice and the transcription of defensin 1 was up-regulated by oral challenge with wild-type B. quintana in head but not in body lice. In addition, the level of cytotoxic reactive oxygen species generated by epithelial cells was significantly lower in body lice. Although speculative at this time, the reduced immune response is consistent with the higher vector competence seen in body vs. head lice in terms of B. quintana infection.

The centenary of the discovery of trench fever, an emerging infectious disease of World War 1.

In 1915, a British medical officer on the Western Front reported on a soldier with relapsing fever, headache, dizziness, lumbago, and shin pain. Within months, additional cases were described, mostly in frontline troops, and the new disease was called trench fever. More than 1 million troops were infected with trench fever during World War 1, with each affected soldier unfit for duty for more than 60 days. Diagnosis was challenging, because there were no pathognomonic signs and symptoms and the causative organism could not be cultured. For 3 years, the transmission and cause of trench fever were hotly debated. In 1918, two commissions identified that the disease was louse-borne. The bacterium Rickettsia quintana was consistently found in the gut and faeces of lice that had fed on patients with trench fever and its causative role was accepted in the 1920s. The organism was cultured in the 1960s and reclassified as Bartonella quintana; it was also found to cause endocarditis, peliosis hepatis, and bacillary angiomatosis. Subsequently, B quintana infection has been identified in new populations in the Andes, in homeless people in urban areas, and in individuals with HIV. The story of trench fever shows how war can lead to the recrudescence of an infectious disease and how medicine approached an emerging infection a century ago.

A Mixed Outbreak of Epidemic Typhus Fever and Trench Fever in a Youth Rehabilitation Center: Risk Factors for Illness from a Case-Control Study, Rwanda, 2012.

In August 2012, laboratory tests confirmed a mixed outbreak of epidemic typhus fever and trench fever in a male youth rehabilitation center in western Rwanda. Seventy-six suspected cases and 118 controls were enrolled into an unmatched case-control study to identify risk factors for symptomatic illness during the outbreak. A suspected case was fever or history of fever, from April 2012, in a resident of the rehabilitation center. In total, 199 suspected cases from a population of 1,910 male youth (attack rate = 10.4%) with seven deaths (case fatality rate = 3.5%) were reported. After multivariate analysis, history of seeing lice in clothing (adjusted odds ratio [aOR] = 2.6, 95% confidence interval [CI] = 1.1-5.8), delayed (≥ 2 days) washing of clothing (aOR = 4.0, 95% CI = 1.6-9.6), and delayed (≥ 1 month) washing of beddings (aOR = 4.6, 95% CI = 2.0-11) were associated with illness, whereas having stayed in the rehabilitation camp for ≥ 6 months was protective (aOR = 0.20, 95% CI = 0.10-0.40). Stronger surveillance and improvements in hygiene could prevent future outbreaks.

A New Clade of African Body and Head Lice Infected by Bartonella quintana and Yersinia pestis-Democratic Republic of the Congo.

The human body louse is known as a vector for the transmission of three serious diseases-specifically, epidemic typhus, trench fever, and relapsing fever caused by Rickettsia prowazekii, Bartonella quintana, and Borrelia recurrentis, respectively-that have killed millions of people. It is also suspected in the transmission of a fourth pathogen, Yersinia pestis, which is the etiologic agent of plague. To date, human lice belonging to the genus Pediculus have been classified into three mitochondrial clades: A, B, and C. Here, we describe a fourth mitochondrial clade, Clade D, comprising head and body lice. Clade D may be a vector of B. quintana and Y. pestis, which is prevalent in a highly plague-endemic area near the Rethy Health District, Orientale Province, Democratic Republic of the Congo.

Competence of Cimex lectularius Bed Bugs for the Transmission of Bartonella quintana, the Agent of Trench Fever.

BACKGROUND: Bartonella quintana, the etiologic agent of trench fever and other human diseases, is transmitted by the feces of body lice. Recently, this bacterium has been detected in other arthropod families such as bed bugs, which begs the question of their involvement in B. quintana transmission. Although several infectious pathogens have been reported and are suggested to be transmitted by bed bugs, the evidence regarding their competence as vectors is unclear. METHODOLOGY/PRINCIPAL FINDINGS: Bed bugs at the adult and instar developmental stages were fed three successive human blood meals inoculated with B. quintana bacterium from day one (D1) to D5; subsequently they were fed with pathogen-free human blood until the end of the experiment. Bed bugs and feces were collected in time series, to evaluate their capacities to acquire, multiply and expel viable B. quintana using molecular biology, immunohistochemistry and cultures assays. B. quintana was detected molecularly in 100% of randomly selected experimentally infected bed bug specimens (D3). The monitoring of B. quintana in bed bug feces showed that the bacterium was detectable starting on the 3rd day post-infection (pi) and persisted until day 18±1 pi. Although immunohistochemistry assays localized the bacteria to the gastrointestinal bed bug gut, the detection of B. quintana in the first and second instar larva stages suggested a vertical non-transovarial transmission of the bacterium. CONCLUSION: The present work demonstrated for the first time that bed bugs can acquire, maintain for more than 2 weeks and release viable B. quintana organisms following a stercorarial shedding. We also observed the vertical transmission of the bacterium to their progeny. Although the biological role of bed bugs in the transmission of B. quintana under natural conditions has yet to be confirmed, the present work highlights the need to reconsider monitoring of these arthropods for the transmission of human pathogens.

Acquisition and excretion of Bartonella quintana by the cat flea, Ctenocephalides felis felis.

Bartonella quintana is transmitted by the infected faeces of body lice. Recently, this bacterium was detected in cat fleas (Ctenocephalides felis) and in two humans with chronic adenopathy whose only risk factor was contact with cat fleas. In this study, a total of 960 C. felis were divided into 12 groups (2 control groups and 10 infected groups) each containing 80 fleas. The fleas were fed B. quintana-inoculated human blood at different dilutions (≈3.6 × 10(4) - 8.4 × 10(9) bacteria) for 4 days via an artificial membrane. Subsequently, all flea groups were fed uninfected blood until day 13 postinfection (dpi). On day 3 pi, B. quintana was detected with two specific genes by quantitative PCR in 60-100% of randomly chosen fleas per dilution: 52% (26/50) in the infected fleas in Trial 1 and 90% (45/50) of the fleas in Trial 2. B. quintana was also identified by molecular and culture assays in flea faeces. The average number of B. quintana as determined by qPCR decreased until the 11th dpi and was absent in both trials at the 13th dpi. Bacteria were localized only in the flea gastrointestinal gut by specific immunohistochemistry. Our results indicate that cat fleas can acquire B. quintana by feeding and release viable organisms into their faeces. Therefore, fleas may play a role as vectors of trench fever or other clinical manifestations that are caused by B. quintana. However, the biological role of C. felis in the transmission of B. quintana under natural conditions is yet to be defined.

Differential gene expression in laboratory strains of human head and body lice when challenged with Bartonella quintana, a pathogenic bacterium.

Human head and body lice are obligatory hematophagous ectoparasites that belong to a single species, Pediculus humanus. Only body lice, however, are vectors of the infectious Gram-negative bacterium Bartonella quintana. Because of their near identical genomes, yet differential vector competence, head and body lice provide a unique model system to study the gain or loss of vector competence. Using our in vitro louse-rearing system, we infected head and body lice with blood containing B. quintana in order to detect both differences in the proliferation of B. quintana and transcriptional differences of immune-related genes in the lice. B. quintana proliferated rapidly in body lice at 6 days post-infection, but plateaued in head lice at 4 days post-infection. RNAseq and quantitative real-time PCR validation analyses determined gene expression differences. Eight immunoresponse genes were observed to be significantly different with many associated with the Toll pathway: Fibrinogen-like protein, Spaetzle, Defensin 1, Serpin, Scavenger receptor A and Apolipoporhrin 2. Our findings support the hypothesis that body lice, unlike head lice, fight infection from B. quintana only at the later stages of its proliferation.

Borrelia recurrentis in head lice, Ethiopia.

Since the 1800s, the only known vector of Borrelia recurrentis has been the body louse. In 2011, we found B. recurrentis DNA in 23% of head lice from patients with louse-borne relapsing fever in Ethiopia. Whether head lice can transmit these bacteria from one person to another remains to be determined.

Genetic diversity of Bartonella quintana in macaques suggests zoonotic origin of trench fever.

Bartonella quintana is a bacterium that causes a broad spectrum of diseases in humans including trench fever. Humans were previously considered to be the primary, if not the only, reservoir hosts for B. quintana. To identify the animal reservoir and extend our understanding of the ecological and evolutionary history of B. quintana, we examined blood samples from macaques and performed multilocus sequence typing (MLST) analysis. We demonstrated the prevalence of B. quintana infection was common in macaques from main primate centres in mainland China. Overall, 18.0% (59/328) of rhesus macaques and 12.7% (39/308) of cynomolgus macaques were found to be infected with B. quintana by blood culture and/or polymerase chain reaction. The infection was more frequently identified in juvenile and young monkeys compared with adult animals. In contrast with the relatively low level of sequence divergence of B. quintana reported in humans, our investigation revealed much higher genetic diversity in nonhuman primates. We identified 44 new nucleotide variable sites and 14 novel sequence types (STs) among the B. quintana isolates by MLST analysis. Some STs were found only in cynomolgus macaques, while some others were detected only in rhesus macaques, suggesting evidence of host-cospeciation, which were further confirmed by phylogenetic analysis and Splits decomposition analysis. Our findings suggest that trench fever may primarily be a zoonotic disease with macaques as the natural hosts.

Transmission and maintenance cycle of Bartonella quintana among rhesus macaques, China.

We detected Bartonella quintana in 48.6% of captive rhesus macaques from an animal facility in Beijing, China. Prevalence of infection increased over the period of observation. Our findings suggest that macaques may serve as reservoir hosts for B. quintana and that Pedicinus obtusus lice might act as efficient vectors.

Bartonella quintana in head lice from Sénégal.

Head and body lice are strict, obligate human ectoparasites with three mitochondrial clades (A, B, and C). Body lice have been implicated as vectors of human diseases, and as the principal vectors of epidemic typhus, relapsing fever, and Bartonella quintata-associated diseases (trench fever, bacillary angiomatosis, endocarditis, chronic bacteremia, and chronic lymphadenopathy). Using molecular methods (real-time and traditional PCR), we assessed the presence of Bartonella quintana DNA in black head lice collected from three locations in Sénégal. DNA from B. quintana was identified in 19 lice (6.93%) collected from 7 patients (7%) in Dakar. B. quintana-positive lice collected from three subjects were identified as clades C and A.

Human louse-transmitted infectious diseases.

Several of the infectious diseases associated with human lice are life-threatening, including epidemic typhus, relapsing fever, and trench fever, which are caused by Rickettsia prowazekii, Borrelia recurrentis, and Bartonella quintana, respectively. Although these diseases have been known for several centuries, they remain a major public health concern in populations living in poor-hygiene conditions because of war, social disruption, severe poverty, or gaps in public health management. Poor-hygiene conditions favour a higher prevalence of body lice, which are the main vectors for these diseases. Trench fever has been reported in both developing and developed countries in populations living in poor conditions, such as homeless individuals. In contrast, outbreaks of epidemic typhus and epidemic relapsing fever have occurred in jails and refugee camps in developing countries. However, reports of a significantly high seroprevalence for epidemic typhus and epidemic relapsing fever in the homeless populations of developed countries suggest that these populations remain at high risk for outbreaks of these diseases. Additionally, experimental laboratory studies have demonstrated that the body louse can transmit other emerging or re-emerging pathogens, such as Acinetobacter baumannii and Yersinia pestis. Therefore, a strict survey of louse-borne diseases and the implementation of efficient delousing strategies in these populations should be public health priorities.

Altitude-dependent Bartonella quintana genotype C in head lice, Ethiopia.

To determine the presence of Bartonella quintana in head and body lice from persons in different locations in Ethiopia, we used molecular methods. B. quintana was found in 19 (7%) genotype C head lice and in 76 (18%) genotype A body lice. B. quintana in head lice was positively linked to altitude (p = 0.014).