Dissemination of bloodmeal acquired Rickettsia felis in cat fleas, Ctenocephalides felis

Thepparit, Chutima; Hirunkanokpun, Supanee; Popov, Vsevolod L.; Foil, Lane D.; Macaluso, Kevin R.

doi:10.1186/1756-3305-6-149

Cited by 34 publications

(31 citation statements)

References 27 publications

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“…This pathway is also the main route of the transmission of Rickettsia typhi, the agent of murine typhus transmitted mainly by the rat flea Xenopsylla cheopis (24). The transmission by fleas of R. felis has been associated with the presence of the bacteria in salivary glands and excretion in the feces (10).…”

Section: Discussionmentioning

confidence: 99%

“…More specifically, the cat flea Ctenocephalides felis is the arthropod in which R. felis has been most frequently detected. To date, it is the sole confirmed biological vector of R. felis, with both horizontal and vertical transmission making this flea a potential reservoir for this bacterium (9)(10)(11). However, in some countries where R. felis appears to be highly prevalent, such as Senegal, neither cat fleas nor other arthropods have been implicated in its transmission (12).…”

Section: Constentinmentioning

confidence: 99%

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Transmission potential of Rickettsia felis infection by Anopheles gambiae mosquitoes

Dieme

Bechah

Socolovschi

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

131

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A growing number of recent reports have implicated Rickettsia felis as a human pathogen, paralleling the increasing detection of R. felis in arthropod hosts across the globe, primarily in fleas. Here Anopheles gambiae mosquitoes, the primary malarial vectors in subSaharan Africa, were fed with either blood meal infected with R. felis or infected cellular media administered in membrane feeding systems. In addition, a group of mosquitoes was fed on R. felisinfected BALB/c mice. The acquisition and persistence of R. felis in mosquitoes was demonstrated by quantitative PCR detection of the bacteria up to day 15 postinfection. R. felis was detected in mosquito feces up to day 14. Furthermore, R. felis was visualized by immunofluorescence in salivary glands, in and around the gut, and in the ovaries, although no vertical transmission was observed. R. felis was also found in the cotton used for sucrose feeding after the mosquitoes were fed infected blood. Natural bites from R. felisinfected An. gambiae were able to cause transient rickettsemias in mice, indicating that this mosquito species has the potential to be a vector of R. felis infection. This is particularly important given the recent report of high prevalence of R. felis infection in patients with "fever of unknown origin" in malaria-endemic areas.Rickettsia felis | spotted fever | Anopheles gambiae I n 2002, Rickettsia felis, an obligate intracellular bacterium that belongs to the spotted fever group of Rickettsia, was definitively described (1, 2). Over the past 2 decades, an increasing number of reports have implicated R. felis as a human pathogen, paralleling an increase in reports of the detection of R. felis in arthropod hosts throughout the world (1, 3).By 2011, more than 70 human cases of R. felis had been reported worldwide, including in Central and South America, Asia, northern Africa, and Europe (1). More cases have been published since then, including the first probable human cases in Australia (4). In sub-Saharan Africa, recent studies have challenged the importance of R. felis infection in patients with "fever of unknown origin," with this bacterium detected in up to 15% of such patients (5-7). In 2011, a potential R. felis primary infection, called "yaaf," was suspected in the case of an 8-mo-old girl in Senegal with polymorphous skin lesions similar to those seen in patients from Mexico (8). The epidemiologic and clinical picture of this emerging infection in Africa, including its potential vectors, is poorly understood, however.Various arthropods, but primarily fleas, have been associated with R. felis (1, 3). More specifically, the cat flea Ctenocephalides felis is the arthropod in which R. felis has been most frequently detected. To date, it is the sole confirmed biological vector of R. felis, with both horizontal and vertical transmission making this flea a potential reservoir for this bacterium (9-11). However, in some countries where R. felis appears to be highly prevalent, such as Senegal, neither cat fleas nor other arthropods have been...

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Section: Discussionmentioning

confidence: 99%

Section: Constentinmentioning

confidence: 99%

Transmission potential of Rickettsia felis infection by Anopheles gambiae mosquitoes

Dieme

Bechah

Socolovschi

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

131

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“…This is in accordance with the findings of previous studies showing the persistence and qualitative increase in bacteria in flea guts 9 days after an infected blood meal (19) and the replication of B. henselae within adult fleas at 6 to 8 days after feeding (20). The first decrease in bacterial DNA in the fleas was observed 2 days after the infected blood meal and may have been due to fleas clearing themselves of an excess of bacteria, as was suggested for C. felis and X. cheopis after a highly septicemic blood meal with Rickettsia felis (36) and Y. pestis, respectively (37,38). Then, the persistence of Bartonella DNA until the end of the study could be explained by several assumptions requiring further investigation: the formation of aggregates in the flea gut; attachment to an extracellular matrix, as shown for Y. pestis and B. schoenbuchensis, respectively (33,39); or sequestration in other flea tissues.…”

Section: Discussionmentioning

confidence: 87%

“…This could suggest the second hypothesis of migration of B. henselae from the digestive tract to the body cavity and/or other organs (for example, reproductive tissues, hemolymph, Malpighian tubules) in the second part of the flea life span. Similarly, R. felis has recently been shown to replicate in the digestive tract of C. felis in the first stage of infection, and then to migrate to the hemolymph, disseminating to the excretory system (Malpighian tubules, hindgut, and rectal ampulla) and reproductive tissues (36). At present, the survival of B. henselae in excreted feces is estimated to last for at least 3 days in the environment (20) and could be possible because of the aggregation of the bacteria in a biofilm on the surface of the feces, as suggested for B. quintana on louse feces (34).…”

Section: Discussionmentioning

confidence: 99%

Assessment of Persistence of Bartonella henselae in Ctenocephalides felis

Bouhsira

Franc

Boulouis

et al. 2013

Appl Environ Microbiol

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c Bartonella henselae (Rhizobiales: Bartonellaceae) is a Gram-negative fastidious bacterium of veterinary and zoonotic importance. The cat flea Ctenocephalides felis (Siphonaptera: Pulicidae) is the main recognized vector of B. henselae, and transmission among cats and humans occurs mainly through infected flea feces. The present study documents the use of a quantitative molecular approach to follow the daily kinetics of B. henselae within the cat flea and its excreted feces after exposure to infected blood for 48 h in an artificial membrane system. B. henselae DNA was detected in both fleas and feces for the entire life span of the fleas (i.e., 12 days) starting from 24 h after initiation of the blood meal. Bartonella henselae is a Gram-negative facultative intracellular bacterium of veterinary and zoonotic importance distributed worldwide (1). At present, its major competent vector is the cat flea, Ctenocephalides felis (2). Viable B. henselae or its DNA has also been detected in several other blood-feeding arthropods, such as ticks (Dermacentor spp., Ixodes spp.) (3-6) and biting flies (Haematobia spp., Stomoxys spp.) (7); however, no evidence of the role of these insects as competent vectors exists. Cats, particularly kittens, represent the major reservoir of B. henselae (8). Infected cats are usually asymptomatic but experience chronic recurring bacteremia (9). Clinical signs observed after experimental infection of cats include febrile illness, transient anemia, neurological dysfunction, and endocarditis (10-12).In humans, B. henselae is the causative agent of cat scratch disease (CSD), a syndrome characterized by a persistent regional lymphadenopathy that is usually self-limiting within 2 to 4 months in immunocompetent patients (13). However, infected immunocompromised individuals (such as those with AIDS or organ transplant recipients) can develop severe vasoproliferative tumors known as bacillary angiomatosis and bacillary peliosis (13,14,15).Although the prevalence of B. henselae infection in cats fluctuates significantly, the highest levels of infection occur in temperate regions where conditions are most favorable for the development of C. felis (1,16,17). The seroprevalence of antibodies against B. henselae in healthy cat populations ranges from 25 to 45% throughout the world (17). Nonetheless, in North America, where C. felis is endemic, seroprevalence was reported to reach up to more than 90% in some cat colonies (18). Fleas acquire B. henselae during their blood meal on highly bacteremic cats (16). Once in the arthropod vector, the bacterium seems to replicate within the gut and is then excreted in the feces (19,20). While transmission by flea saliva still requires further investigation (21), the exposure to infected flea feces appears to be the main route of infection for cats and, accidentally, humans (22-24). B. henselae can also be inoculated into the skin of a naive host via scratching or biting by a flea-contaminated carrier animal (16,20,25).Knowledge of the kinetics of B. henselae in C. f...

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“…Recently, R. felis has been shown to replicate in the cat fleas' digestive tract, migrate to the hemolymph and then disseminate through the excretory system (such as the Malpighian tubules, hindgut and rectal ampulla) and reproductive tissues (Thepparit et al . ). However, the method of Bartonella migration (e.g.…”

Section: Discussionmentioning

confidence: 97%

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

et al. 2014

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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.

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Dissemination of bloodmeal acquired Rickettsia felis in cat fleas, Ctenocephalides felis

Cited by 34 publications

References 27 publications

Transmission potential of Rickettsia felis infection by Anopheles gambiae mosquitoes

Transmission potential of Rickettsia felis infection by Anopheles gambiae mosquitoes

Assessment of Persistence of Bartonella henselae in Ctenocephalides felis

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

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