Emerging bacterial infectious diseases/pathogens vectored by human lice.

Human lice have always been a major public health concern due to their vector capacity for louse-borne infectious diseases, like trench fever, louse-borne relapsing fever, and epidemic fever, which are caused by Bartonella quintana, Borrelia recurrentis, and Rickettsia prowazekii, respectively. Those diseases are currently re-emerging in the regions of poor hygiene, social poverty, or wars with life-threatening consequences. These louse-borne diseases have also caused outbreaks among populations in jails and refugee camps. In addition, antibodies and DNAs to those pathogens have been steadily detected in homeless populations. Importantly, more bacterial pathogens have been detected in human lice, and some have been transmitted by human lice in laboratories. Here, we provide a comprehensive review and update on louse-borne infectious diseases/bacterial pathogens.

Zoonotic vector-borne bacteria in wild rodents and associated ectoparasites from Tunisia.

Wild rodents are considered as potential carriers of several zoonotic vector-borne bacteria but their epidemiology is poorly understood in Tunisia. A total of 305 biological samples (100 spleens, 100 livers, 100 kidneys, and 5 pooled ectoparasites (Xenopsylla cheopis, Laelaps echidninus, Ornithonyssus sp., Hoplopleura sp. and eggs of the rat fleas)) were collected from 100 wild rodents from three Tunisian governorates. Molecular screening was performed to reveal infections with main vector-borne bacteria. Captured rodents belonged to three rodent genera and species including Rattus rattus (n = 51, 51%), Meriones shawi (n = 24, 24%) and Mus musculus (n = 25, 25%). Examined rodents were found to be heavily infested by the rat flea X. cheopis (n = 32, 47%) and the rat mite L. echidninus (n = 22, 32.3%). However, the rat mite Ornithonyssus sp. (n = 13, 19.1%) and the rat lice Hoplopleura sp. (n = 1, 1.5%) were rarely identified. Based on 16S rRNA and msp4 genes, infection with Anaplasmataceae bacteria was detected in six specimens of R. rattus and one M. shawi. Pathogenic A. phagocytophilum (n = 1), A. phagocytophilum-like 1 (Anaplasma sp. Japan) (n = 1), and A. ovis (n = 5) were identified. On the basis of ompB, ompA and gltA genes, infection with Rickettsia spp. was identified in three specimens of R. rattus and one of M. shawi. Five Rickettsia species of the spotted fever group, corresponding to R. monacensis, R. helvetica, R. massiliae, R. africae, and R. aeschlimannii, were detected in mixed infections. Bartonella henselae DNA was also found in two R. rattus, based on rpoB partial sequences. All revealed Anaplasma, Rickettsia and Bartonella bacteria were detected in spleen samples. Ehrlichia, Coxiella and Borrelia spp. were not identified in any of the tested samples. In Tunisia, this is the first report indicating infections with Anaplasma, Rickettsia and Bartonella spp. in wild rodents, particularly present alongside domestic livestock and human. This represents a serious risk of potential bacterial transmission. Thus, controlling rodent population in animal herds, residential areas and sensitizing local people to this risk seem absolutely necessary.

Rickettsia-host interaction: strategies of intracytosolic host colonization.

Bacterial infection is a highly complex biological process involving a dynamic interaction between the invading microorganism and the host. Specifically, intracellular pathogens seize control over the host cellular processes including membrane dynamics, actin cytoskeleton, phosphoinositide metabolism, intracellular trafficking and immune defense mechanisms to promote their host colonization. To accomplish such challenging tasks, virulent bacteria deploy unique species-specific secreted effectors to evade and/or subvert cellular defense surveillance mechanisms to establish a replication niche. However, despite superficially similar infection strategies, diverse Rickettsia species utilize different effector repertoires to promote host colonization. This review will discuss our current understandings on how different Rickettsia species deploy their effector arsenal to manipulate host cellular processes to promote their intracytosolic life within the mammalian host.

The role of louse-transmitted diseases in historical plague pandemics.

The rodent-murine ectoparasite-human model of plague transmission does not correspond with historical details around plague pandemics in Europe. New analysis of ancient genomes reveal that Yersinia pestis was unable to be transmitted by rat fleas until around 4000 Before Present, which challenges the rodent-murine ectoparasite-human model of plague transmission and historical details around plague pandemics in Europe. In this Review, we summarise data regarding Y pestis transmission by human lice in the context of genomic evolution and co-transmission of other major epidemic deadly pathogens throughout human history, with the aim of broadening our view of plague transmission. Experimental models support the efficiency of human lice as plague vectors through infected faeces, which suggest that Y pestis could be a louse-borne disease, similar to Borrelia recurrentis, Rickettsia prowazekii, and Bartonella quintana. Studies have shown that louse-borne outbreaks often involve multiple pathogens, and several cases of co-transmission of Y pestis and B quintana have been reported. Furthermore, an exclusive louse-borne bacterium, namely B recurrentis, was found to be circulating in northern Europe during the second plague pandemic (14th-18th century). Current data make it possible to attribute large historical pandemics to multiple bacteria, and suggests that human lice probably played a preponderant role in the interhuman transmission of plague and pathogen co-transmission during previous large epidemics, including plague pandemics.

Wolbachia: A tool for livestock ectoparasite control.

Ectoparasites and livestock-associated insects are a major concern throughout the world because of their economic and welfare impacts. Effective control is challenging and relies mainly on the use of chemical insecticides and acaricides. Wolbachia, an arthropod and nematode-infecting, maternally-transmitted endosymbiont is currently of widespread interest for use in novel strategies for the control of a range of arthropod-vectored human diseases and plant pests but to date has received only limited consideration for use in the control of diseases of veterinary concern. Here, we review the currently available information on Wolbachia in veterinary ectoparasites and disease vectors, consider the feasibility for use of Wolbachia in the control of livestock pests and diseases and highlight critical issues which need further investigation.

Screening of ectoparasites from domesticated dogs for bacterial pathogens in Vientiane, Lao PDR.

Arthropod-borne diseases are widespread worldwide and are a complex interaction between animals, humans and ectoparasites. The understanding of the diversity and epidemiology of organisms transmitted by arthropod vectors, and the role of hosts and vectors in transmission of infections remain limited in Lao PDR. What knowledge does exist is primarily focused on more rural regions of the country. This study screened ectoparasites from domestic dogs in Vientiane city for the presence of bacterial pathogens of zoonotic importance. A total of 3,511 arthropod vectors were collected from 112 dogs. Vectors collected were Rhipicephalus sanguineus ticks, Ctenocephalides felis felis and Ctenocephalides felis orientis fleas and Heterodoxus spiniger lice. A sub-sample of vectors from each dog was analysed by PCR to identify the potential bacteria. From 129 vector pools, Rickettsia spp. was detected in 6.7% (7/105) pools of ticks, 86.4% (19/22) pools of fleas and both pools of lice. Sequencing analysis confirmed Rickettsia felis in 13 flea pools and one louse pool and Rickettsia asembonensis in six flea pools. Anaplasmataceae was identified in 14.3% (15/105) tick pools and 100% (22/22) flea pools. Sequencing revealed the presence of Anaplasma platys in ticks and Wolbachia pipientis in fleas. Leptospira spp. was detected in one tick and one louse pool, and Brucella spp. was detected in 12.4% (13/105) tick pools. All samples were negative for Bartonella spp., Coxiella burnetii and Borrelia burgdorferi. This is the first study providing evidence of R. asembonensis in fleas in Laos. Results from this study show arthropods are potential vectors to transmit zoonotic infection in Vientiane city, suggesting humans are at risk of zoonotic infections in the city.

Molecular Evidence of Bacteria in Clothes Lice Collected from Homeless People Living in Shelters in Marseille.

We sought to evidence the presence of emerging bacterial pathogens in clothes lice collected from sheltered homeless individuals from Marseille, France. During the 2013-2018 period, a total of 507 lice were collected from 37 individuals and were processed for molecular analysis. We reported a low prevalence of Bartonella quintana DNA carriage (1.2%). No louse tested positive for Rickettsia sp., Rickettsia prowazekii, Borrelia sp., Anaplasma sp., Yersinia Pestis, or Coxiella burnetii. A comparison with studies conducted before 2013 showed a 17.5-fold reduction in the rate of B. quintana DNA positivity. By contrast, a high prevalence of Acinetobacter species DNA carriage (40.8%), mostly A. baumannii (32.9%), was observed, tending to increase over time. In addition, we detected Acinetobacter ursingii DNA in clothes lice for the first time. Genotypic characterization and antimicrobial susceptibility testing of A. baumannii isolates from clothes lice are needed to assess whether these A. baumannii strains present in lice are similar to those responsible for human infections and harbor mechanisms of resistance against antibiotics.

Low occurrence of Bartonella in synanthropic mammals and associated ectoparasites in peri-urban areas from Central-Western and Southern Brazil.

Worldwide, Bartonella species are known to infect a wide range of mammalian and arthropod hosts, including humans. The current study aimed to investigate the prevalence of Bartonella spp. in synanthropic mammals captured in peri-urban areas from Central-Western and Southern Brazil and their ectoparasites. For this aim, 160 mammals belonging to four species, and 218 associated arthropods were sampled. DNA was extracted and subjected to different Bartonella screening assays. Additionally, blood samples from 48 small rodents were submitted to liquid BAPGM culture followed by qPCR assay and solid culture. Two out of 55 Rattus captured in Santa Catarina state were PCR-positive for Bartonella when targeting the nuoG, 16S, and ITS loci. Sequences showed high homology with Bartonella coopersplainsensis. Conversely, all 48 small rodents, 14 capybaras and 43 opossum DNA samples from animals trapped in Mato Grosso do Sul were Bartonella negative in the HRM real time PCR assays targeting the ITS locus and gltA gene. Additionally, all mammal-associated ectoparasites showed negativity results based on HRM real time PCR assays. The present study showed, for the first time, the occurrence of B. coopersplainsensis in Brazil, shedding some light on the distribution of rats-related Bartonella in South America. In addition, the majority of rodents and marsupials were negative for Bartonella spp. Since B. coopersplainsensis reservoirs - Rattus spp. - are widely dispersed around the globe, their zoonotic potential should be further investigated.

Molecular Survey of Rickettsia spp., Anaplasma spp., Ehrlichia spp., Bartonella spp., and Borrelia spp. in Fleas and Lice in Ethiopia.

Bacterial arthropod-borne pathogens can often cause fever in Africa, but rural laboratories in these settings are usually too basic to provide a precise picture of their epidemiological impact. Our aim was to determine the prevalence of bacterial pathogens in fleas and lice in a rural area of southeast Ethiopia. Between July and November 2013, we extracted DNA from 91 fleas (Ctenocephalides felis [n = 50; 54.9%], Pulex irritans [n = 37; 40.1%], and C. canis [n = 4; 4.4%] and 30 lice (Pediculus humanus capitis [n = 16; 53.3%] and Pediculus humanus humanus [n = 14; 46.7%]), using two quantitative PCR (qPCR) analyses to look for bacteria from the genera: Anaplasma, Bartonella, Borrelia, Coxiella, Ehrlichia, Francisella, and Rickettsia. Of the 91 fleas analyzed, pathogens were present in 79 (86.8%), including Rickettsia felis (n = 41; 45%), Anaplasma platys (n = 40; 44.0%), Rickettsia monacensis (n = 2; 2.2%), Ehrlichia muris-like agent (n = 1; 1.1%), and Bartonella clarridgeiae (n = 1; 1.1%). P. irritans was the flea species most frequently infected with A. platys (67.7%), followed by C. felis (30.7%) (p < 0.001). Of the 30 lice identified, pathogens were present in 7 (23.3%): Bartonella quintana (n = 4; 16.7%), E. muris (n = 2, 6.7%), and Borrelia recurrentis (n = 1, 3.3%). Thus, in this rural area of Africa, fleas and lice can transmit parasitic pathogens to humans, causing febrile symptoms.

Molecular Survey for Pathogens and Markers of Permethrin Resistance in Human Head Lice (Phthiraptera: Pediculidae) from Madagascar.

Human infestation with head lice, Pediculus humanus capitis De Geer, is the most prevalent ectoparasitic condition in the modern world. The purpose of this study was to test human head lice from Madagascar for infection with 2 louse-borne bacteria, Bartonella quintana and Acinetobacter spp. including Acinetobacter baumannii, to assess the potential risk of exposure to these pathogens in rural populations experiencing head-louse pediculosis. A second aim was to determine the occurrence of a biomarker for permethrin resistance in head lice from 6 isolated human communities in Madagascar. Deoxyribonucleic acid (DNA) of B. quintana was detected using species-specific Fab3 gene TaqMan in 12.6% of lice from 4 villages. DNA of Acinetobacter spp. was detected using rpoB TaqMan in 42.1% of lice collected from all locations; 58.3% of rpoB-positive lice had the blaOXA51-like enzyme gene specific for A. baumannii. The kdr-resistant allele was detected in 70% of lice tested and was found in lice from each location. These results provide the first information regarding these combined characteristics of head-louse infestations in Madagascar. This approach can be applied to larger and broader surveys of lice from pediculosis capitis occurring in other geographic locations.

Insects and the Transmission of Bacterial Agents.

Arthropods are small invertebrate animals, among which some species are hematophagous. It is during their blood meal that they can transmit pathogenic microorganisms that they may be harboring to the vertebrate host that they parasitize, which in turn will potentially develop a vector-borne disease. The transmission may occur directly through their bite, but also through contaminated feces. Zoonotic diseases, diseases that can naturally be transmitted between humans and animals, are a considerable part of emerging diseases worldwide, and a major part of them are vector-borne. Research and public attention has long been focused on malaria and mosquito-borne arboviruses, and bacterial vector-borne diseases remains today a neglected field of medical entomology. Despite the emphasis on Lyme disease in recent decades, and despite the major outbreaks caused by bacteria in the last few centuries, this field has in fact been poorly explored and is therefore relatively poorly known, other than the most famous examples such as the plague and epidemic typhus outbreaks. Here we propose to review the state of knowledge of bacterial agents transmitted by arthropod vectors.

Pathogens in ectoparasites from free-ranging animals: Infection with Rickettsia asembonensis in ticks, and a potentially new species of Dipylidium in fleas and lice.

Vector-borne infections are persistent public health threats worldwide. In recent years, a number of mosquito-borne viruses have emerged or re-emerged to cause major disease outbreaks. Other vector-borne pathogens, however, remain understudied and much neglected especially in the developing regions of the world including Southeast Asia. In this study, the brown dog tick Rhipicephalus sanguineus sensu lato, cat louse Felicola subrostratus, and cat fleas Ctenocephalides felis and Ctenocephalides orientis collected from free-ranging cats and dogs in Malaysia were molecularly screened for the presence of Bartonella and Rickettsia bacteria, and Dipylidium tapeworm. Our results showed the presence of Bartonella clarridgeiea, Bartonella henselae (lineage Marseille and lineage Houston-1), and Rickettsia sp. in C. felis. We also detected Rickettsia asembonensis in C. orientis and R. sanguineus s.l. Additionally, this study provides the first documentation on a potentially new species of Dipylidium infecting F. subrostratus and C. felis. Our results highlight the role of ectoparasites from free-ranging animals including cats and dogs, in harboring multiple transmissible pathogens.

Molecular survey of Rickettsial organisms in ectoparasites from a dog shelter in Northern Mexico.

The objective of this study was to screen and identify rickettsial organisms in ectoparasites collected from dogs in a shelter in Gomez Palacio, Durango, Mexico. One hundred dogs were inspected for ectoparasites. All the dogs were parasitized with Rhipicephalus sanguineus ticks, three with Heterodoxus spiniger lice and one with Ctenocephalides felis fleas. DNA was extracted from the ectoparasites found on each dog, and PCR with the primers for the Anaplasmataceae 16S rRNA and citrate synthase gltA genes were performed. Eight DNA samples obtained from ticks, three from lice and one from fleas were positive to 16S rRNA. Only one sample from C. felis and one from H. spiniger were positive to gltA. Sequence analysis of amplified products from C. felis showed identity to Rickettsia felis, Wolbachia pipientis, and Wolbachia spp., while a sequence from H. spiniger showed identity to Wolbachia spp. Herein we report the molecular detection of R. felis, W. pipientis, and Wolbachia spp. in C. felis and H. spiniger in northern Mexico. These results contribute to the knowledge of the microorganisms present in ectoparasites from dogs in Mexico.

A Personal View of How Paleomicrobiology Aids Our Understanding of the Role of Lice in Plague Pandemics.

We have been involved in the field of paleomicrobiology since 1998, when we used dental pulp to identify Yersinia pestis as the causative agent of the great plague of Marseille (1720). We recently designed a specific technique, "suicide PCR," that can prevent contamination. A controversy arose between two teams, with one claiming that DNA must be altered to amplify it and the other group claiming that demographic data did not support the role of Y. pestis in the Black Death (i.e., the great plague of the Middle Ages). These controversies led us to evaluate other epidemiological models and to propose the body louse as the vector of this pandemic. This proposal was substantiated by experimental models, the recovery of Y. pestis from lice in the Congo, and the identification of epidemics involving both Y. pestis and Bartonella quintana (the agent of trench fever, transmitted by the body louse) in ancient corpses from mass graves. Paleomicrobiology has led to a re-evaluation of plague pandemics.

Rickettsia (Rickettsiales: Rickettsiaceae) Vector Biodiversity in High Altitude Atlantic Forest Fragments Within a Semiarid Climate: A New Endemic Area of Spotted-Fever in Brazil.

Rickettsioses are re-emerging vector-borne zoonoses with a global distribution. Recently, Rickettsia sp. strain Atlantic rainforest has been associated with new human spotted-fever (SF) cases in Brazil, featuring particular clinical signs: eschar formation and lymphadenopathy. These cases have been associated with the tick species, Amblyomma ovale From 2010 until 2015, the Brazilian Health Department confirmed 11 human SF cases in the Maciço de Baturité region, Ceará, Brazil. The present study reports the circulation of Rickettsia spp. in vectors from this entirely new endemic area for SF. A total of 1,727 ectoparasites were collected in this area from the environment, humans, and wild and domestic animals. Samples (n = 887) were screened by polymerase chain reaction (PCR), targeting the gltA and ompA rickettsial genes. Sequencing and phylogenetic analyses of gltA gene amplicons were carried out for 13 samples positive for both screening PCRs. Fragments of gltA and ompA from three samples were cloned, sequenced, and analyzed further. A. ovale and Rhipicephalus sanguineus specimens, collected from dogs, were found to be infected with Rickettsia sp. str. Atlantic rainforest, suggesting the importance of dogs in the epidemic cycle. Candidatus Rickettsia andeanae, Rickettsia felis, and Rickettsia bellii were also found infecting ticks and fleas in five municipalities, demonstrating the broad diversity of rickettsiae in circulation in the studied area. This study reports, for the first time, evidence of infection with Rickettsia sp. strain Atlantic rainforest in A. ovale and R. sanguineus in Ceará, and Ca. R. andeanae in an Atlantic rainforest environment of Brazil.

Comparative genomics reveals multiple pathways to mutualism for tick-borne pathogens.

BACKGROUND: Multiple important human and livestock pathogens employ ticks as their primary host vectors. It is not currently known whether this means of infecting a host arose once or many times during evolution. RESULTS: In order to address this question, we conducted a comparative genomics analysis on a set of bacterial pathogens from seven genera - Borrelia, Rickettsia, Anaplasma, Ehrlichia, Francisella, Coxiella, and Bartonella, including species from three different host vectors - ticks, lice, and fleas. The final set of 102 genomes used in the study encoded a total of 120,046 protein sequences. We found that no genes or metabolic pathways were present in all tick-borne bacteria. However, we found some genes and pathways were present in subsets of tick-transmitted organisms while absent from bacteria transmitted by lice or fleas. CONCLUSION: Our analysis suggests that the ability of pathogens to be transmitted by ticks arose multiple times over the course of evolution. To our knowledge, this is the most comprehensive study of tick transmissibility to date.

Differential associations of Borrelia species with European badgers (Meles meles) and raccoon dogs (Nyctereutes procyonoides) in western Poland.

European badgers and raccoon dogs and their associated ticks and lice were assayed for the presence of Lyme borreliosis and relapsing fever-group spirochete DNA in western Poland. Analyses of blood, ear-biopsy and liver samples revealed that 25% of 28 raccoon dogs and 12% of 34 badgers were PCR positive for borreliae. Borrelia garinii was the dominant species in raccoon dogs (62.5%), followed by B. afzelii (25%) and B. valaisiana (12.5%). PCR-positive badgers were infected only with B. afzelii. A total of 351 attached ticks was recovered from 23 (82%) of the raccoon dogs and 13 (38%) of the badgers. Using a nested PCR targeting the ITS2 fragments of Ixodes DNA, four Ixodes species were identified: I. ricinus, I. canisuga, I. hexagonus, and one provisionally named I. cf. kaiseri. Ixodes canisuga and I. ricinus prevailed on both host species. The highest infection prevalence was detected in I. ricinus, followed by I. canisuga and I. cf. kaiseri. Borrelia garinii and B. afzelii accounted for 61.6% and 30.1% of the infections detected in all PCR-positive ticks, respectively. Four other Borrelia species (B. burgdorferi sensu stricto, B. valaisiana, B. lusitaniae and B. miyamotoi) were detected only in I. ricinus from raccoon dogs. Moreover, Borrelia DNA, mostly B. garinii, was detected in 57 (81.4%) of 70 Trichodectes melis lice derived from 12 badgers. The detection of B. afzelii in one-half of PCR-positive biopsies reconfirms previous associations of this species with mammalian hosts, whereas the high prevalence of B. garinii in feeding lice and I. ricinus ticks (including larvae) demonstrates that both carnivores serve as hosts for B. garinii. The lack of B. garinii DNA in the tissues of badgers versus its prevalence in raccoon-dog biopsies, however, incriminates only the latter carnivore as a potential reservoir host.