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Microbiologie & Sciences Humaines

Equipe n°12: Idir Bitam, CR

UNITE DE RECHERCHE SUR LES MALADIES BACTERIENNES VECTORISEES EN ALGERIE

 

 

1. Team composition

 

  1. Idir BITAM (MCF, Alger, HDR)
  2. Slim BENYACOUB (PU, Alger)
  3. Nadjet MOUFFOK (PU, Oran)

 

2. Achievements

Scientific output

This team has been included in URMITE in the context of the « Jeunes Équipes Associées à l’IRD » (JEAI) program designed to promote and strengthen new research teams in developing countries through partnership with IRD research units. After having been trained by Philippe Parola and obtained his PhD degree at Aix-Marseille university, Idir Bitam created the JEAI MALBAVECT (2011-2014), a unique research team in entomology in Algeria. Then in 2014, this team was established as the main partner of the REMEDIER (for REsearch 
for MEDiterranean Infections that are Emerging or Reemerging) program that has been granted by the A*MIDEX (n° ANR-11-IDEX-0001-02) funded by the Investissements d’Avenir French Government. In this context and beside the creation of a doctoral program at Université des Sciences et de la Technologie Houari Boumedien in Algiers, Idir Bitam has been appointed as invited Associate Professor at Aix-Marseille University in 2015 and 2016. The accomplishments of the team are described below.

 

  1. Palgue

                The history of infectious diseases raised the plague as one of the most devastating for human beings. Far too often considered an ancient disease, the frequent resurgence of the plague has led to consider it as a reemerging disease in Madagascar, Algeria, Libya, and Congo.

                In Algeria, we found Yersinia pestis in 18/237 (8%) rodents of five species, including Apodemus sylvaticus, previously undescribed as pestiferous; and disclosed three new plague foci by using PCR sequencing of pla, glpD and rpoB genes. Multiple spacer typing confirmed a new Orientalis variant. Rodent survey should be reinforced in this country hosting reemerging plague.(1)

                The genetic factors associated with the pathogenicity of Yersinia pestis, the causative agent of the plague, involve the acquisition of the pPCP1 plasmid that promotes host invasion through the expression of the virulence factor Pla. The surveillance of plague foci after the 2003 outbreak in Algeria resulted in a positive detection of the specific pla gene of Y. pestis in rodents. However, the phenotypic characterization of the isolate identified a Citrobacter koseri. The comparative genomics of our sequenced C. koseri URMITE genome revealed a mosaic gene structure resulting from the lifestyle of our isolate and provided evidence for gene exchanges with different enteric bacteria. The most striking was the acquisition of a continuous 2 kb genomic fragment containing the virulence factor Pla of the Y. pestis pPCP1 plasmid; however, the subcutaneous injection of the CKU strain in mice did not produce any pathogenic effect. Our findings demonstrate that fast molecular detection of plague using solely the pla gene is unsuitable and should rather require Y. pestis gene marker combinations. We also suggest that the evolutionary force that might govern the expression of pathogenicity can occur through the acquisition of virulence genes but could also require the loss or the inactivation of resident genes such as antivirulence genes.(2)

 

 2. Rickettsial agents

                In 2012, we have detected by qPCR vector-associated bacteria in stray dogs and cats and their ectoparasites from Algiers. 18/117 (15.38%) dogs and 2/107 (1.87%) cats were positive for at least one vector-borne agent. Coxiella burnetii and Bartonella henselae were identified in 1/117 (0.85%) dog individually. Ehrlichia canis DNA was detected in 17/117 (14.52%) dogs. 1/107 (0.93%) cat was positive to C. burnetii and another 1/107 (0.93%) to B. henselae. DNA of Rickettsia massiliae, Rickettsia conorii and E. canis was detected in Rhipicephalus sanguineus. Cat fleas were infected with Rickettsia felis, B. henselae and Bartonella clarridgeiae. B. vinsonii subsp. berkhoffii was identified in Xenopsylla cheopis collected from dogs. The findings of this study indicate that dogs and cats from Algeria are exposed to multiple tick and flea-borne pathogens. (3)

                In 2013, using real-time PCR, standard PCR and sequencing, the presence of Bartonella spp., Rickettsia spp., Borrelia spp. and Coxiella burnetii was evaluated in 268/1626 ticks, 136 fleas, 11 Nycteribiidae flies and 16 spleens of domestic and/or wild animals from the El Tarf and Souk Ahras areas. For the first time in Algeria, Bartonella tamiae was detected in 12/19 (63.2 %) Ixodes vespertilionis ticks, 8/11 (72.7 %) Nycteribiidae spp. flies and in 6/10 (60 %) bat spleens (Chiroptera spp.). DNA from Coxiella burnetii, the agent of Q fever, was also identified in 3/19 (15.8 %) I. vespertilionis from bats. Rickettsia slovaca, the agent of tick-borne lymphadenopathy, was detected in 1/1 (100 %) Haemaphysalis punctata and 2/3 (66.7 %) Dermacentor marginatus ticks collected from two boars (Sus scrofa algira) respectively. Ri. massiliae, an agent of spotted fever, was detected in 38/94 (40.4 %) Rhipicephalus sanguineus sensu lato collected from cattle, sheep, dogs, boars and jackals. DNA of Ri. aeschlimannii was detected in 6/20 (30 %) Hyalomma anatolicum excavatum and 6/20 (30 %) Hy. scupense from cattle. Finally, Ri. felis, an emerging rickettsial pathogen, was detected in 80/110 (72.7 %) Archaeopsylla erinacei and 2/2 (100 %) Ctenocephalides felis of hedgehogs (Atelerix algirus). In this study, we expanded knowledge about the repertoire of ticks and flea-borne bacteria present in ectoparasites and/or tissues of domestic and wild animals in Algeria. (4)

                From 2012 to 2014, we conducted field surveys in 4 distinct areas of Algeria. We investigated the occurrence of soft ticks in rodent burrows and yellow-legged gull (Larus michahellis) nests in 10 study sites and collected 154 soft ticks. Molecular identification revealed the occurrence of two different soft tick genera and five species, including Carios capensis in yellow-legged gull nests and Ornithodoros occidentalis, Ornithodoros rupestris, Ornithodoros sonrai, Ornithodoros erraticus in rodent burrows. Rickettsial DNA was detected in 41/154, corresponding to a global detection rate of 26.6%. Sequences of the citrate synthase (gltA) gene suggest that this agent is a novel spotted fever group Rickettsia. For the first time in Algeria, we characterize a novel Rickettsia species by molecular means in soft ticks. (6)

                We collected ticks from camels in 4 regions of southern Algeria (El Oued, Bechar, Ghardia, and Adrar) from February to October in 2008 and in April of 2011. A total of 307 ticks representing multiple species (including Hyalomma dromedarii, H. marginatum rufipes, H. impeltatum, and H. impressum), was tested for the presence of spotted fever group rickettsia DNA using gltA real-time quantitative PCR (qPCR). The presence of Rickettsia aeschlimannii was confirmed with a new qPCR using species-specific primers and Taqman probes based on the sca2 genes. The R. aeschlimannii sequence was further confirmed by detecting the gltA and outer membrane protein (ompA) genes in H. m. rufipes, H. impeltatum, and H. dromedarii ticks. These findings represent the first report of the detection of R. aeschlimannii in ticks collected from camels from southern Algeria. (19)

                From December 2011 to march 2012, a study was carried out using Ixodes ricinus ticks collected from cattle from Tizi-Ouzou and Dermacentor marginatus ticks collected from the vegetation of the Blida region, a tourist site, both regions situated in northern Algeria. The results of real-time quantitative PCR (qPCR) specific for a partial sequence of the citrate synthase gene (gltA) indicate that Rickettsia spp. were present in 11/23 (48%) and 4/9 (44%) of the examined ticks from Tizi-Ouzou and Blida, respectively. The sequences of Rickettsia helvetica and Ri. monacensis were found in I. ricinus ticks using gltA primers. In addition, Ri. slovaca was detected based on the sequences of the gltA and the outer membrane protein (OmpA) genes in D. marginatus ticks. DNA sequencing to identify the species revealed for the first time the presence of Ri. helvetica in I. ricinus ticks and Ri. slovaca in D. marginatus ticks from Algeria and confirmed the presence of Ri. monacensis. (20)

                From November 2011 to March 2012, We report here the detection of Rickettsia africae, the agent responsible for African tick-bite fever, by amplification of fragments of gltA and ompA genes and multi-spacer typing from Hyalomma dromedarii ticks collected from the camel Camelus dromedarius in the Adrar and Béchar region (sub-Saharan Algeria). To date, R. africae has been associated mainly with Amblyomma spp. The role of H. dromedarii in the epidemiology of R. africae requires further investigation. (22)

                In 2011, we have conducted the experimental study about relationship between the Rickettsia and its tick vector is still poorly understood one century after the first description of Mediterranean spotted fever. Colonies of R. conorii conorii-infected and non-infected ticks were established under laboratory conditions. Gimenez staining and electron microscopy on the ovaries of infected ticks indicated heavy rickettsial infection. The transovarial transmission of R. conorii conorii in naturally infected Rh. sanguineus ticks was 100% at eleven generations, and the filial infection rate was up to 99% according to molecular analyses. No differences in life cycle duration were observed between infected and non-infected ticks held at 25°C, but the average weight of engorged females and eggs was significantly lower in infected ticks than in non-infected ticks. The eggs, larvae and unfed nymphs of infected and non-infected ticks could not tolerate low (4°C) or high (37°C) temperatures or long starvation periods. R. conorii conorii-infected engorged nymphs that were exposed to a low or high temperature for one month experienced higher mortality when they were transferred to 25°C than non-infected ticks after similar exposure. High mortality was observed in infected adults that were maintained for one month at a low or high temperature after tick-feeding on rabbits. These preliminary results suggest that infected quiescent ticks may not survive the winter and may help explain the low prevalence of infected Rh. sanguineus in nature. Further investigations on the influence of extrinsic factors on diapaused R. conorii-infected and non-infected ticks are required. (24)

                In 2011, we report the molecular detection of several Bartonella species in 44 (21.5%) of 204 fleas from Algeria collected from 26 rodents and 7 hedgehogs. Bartonella elizabethae and B. clarridgeiae were detected in the fleas collected on hedgehogs. Bartonella tribocorum and B. elizabethae were detected in fleas collected from rats and mice, and sequences similar to an unnamed Bartonella sp. detected in rodents from China were detected in rats as well as a genotype of Bartonella closely related to Bartonella rochalimae detected in fleas collected on brown rats (Rattus norvegicus).(27)

                In 2011, we report for the first time the presence of Phlebotomus mascittii and the female of Phlebotomus chadlii in Algeria. These two species were collected during an entomological study conducted in endemic visceral leishmaniasis focus from the north part of the country, Kabylia.(28)

                In August 2010, during an entomological programme targeting sandflies, in the region of Larbaa-Nath-Iraten, Wilaya of Tizi-Ouzou (Algeria), a female Aedes albopictus was trapped alive and partially engorged. To our knowledge, this is the first report of Ae. albopictus in Algeria and more widely in the Maghreb. (29)

 

3. Borrelia and other arthropod borne bacteria

 

                From January 2011 to July 2012, we have detected B. garinii, a cause of Lyme disease, in Algeria in I. ricinus ticks by using a standard PCR and sequencing methods. We also confirmed the presence of R. monacensis in this country. B. garinii is the most neurotropic of the genospecies of B. burgdorferi sensu lato; it causes meningopolyneuritis and, rarely, encephalomyelitis. Clinicians need to be aware of the prevalence of this bacterium in Algeria. Our results help clarify the epidemiology of B. garinii in Algeria. R. monacensis is an agent of tickborne diseases that was detected in Algeria in 2009. The few cases that have been described were characterized by influenza-like symptoms, fever, an inoculation eschar, and a generalized rash.(13)

                Relapsing fever is the most frequent bacterial disease in Africa. Four main vector / pathogen complexes are classically recognized, with the louse Pediculus humanus acting as vector for B. recurrentis and the soft ticks Ornithodoros sonrai, O. erraticus and O. moubata acting as vectors for Borrelia crocidurae, B. hispanica and B. duttonii, respectively. Our aim was to investigate the epidemiology of the disease in West, North and Central Africa. We conducted field surveys in 17 African countries and in Spain. We investigated the occurrence of Ornithodoros ticks in rodent burrows in 282 study sites. We collected 1,629 small mammals that may act as reservoir for Borrelia infections. Using molecular methods we studied genetic diversity among Ornithodoros ticks and Borrelia infections in ticks and small mammals. Of 9,870 burrows investigated, 1,196 (12.1%) were inhabited by Ornithodoros ticks. In West Africa, the southern and eastern limits of the vectors and Borrelia infections in ticks and small mammals were 13°N and 01°E, respectively. Molecular studies revealed the occurrence of nine different Ornithodoros species, including five species new for science, with six of them harboring Borrelia infections. Only B. crocidurae was found in West Africa and three Borrelia species were identified in North Africa: B. crocidurae, B. hispanica, and B. merionesi (17).

                Members of the Chlamydiales order are obligate intracellular bacteria that replicate within eukaryotic cells of different origins including humans, animals, and amoebae. Many of these bacteria are pathogens or emerging pathogens of both humans and animals, but their true diversity is largely underestimated, and their ecology remains to be investigated. In 2012, we have analyzed the prevalence of Chlamydial DNA in ticks and fleas. Considering their potential threat on human health, it is important to expand our knowledge on the diversity of Chlamydiae, but also to define the host range colonized by these bacteria. Thus, using a new pan-Chlamydiales PCR, we analyzed the prevalence of Chlamydiales DNA in ticks and fleas, which are important vectors of several viral and bacterial infectious diseases. To conduct this study, 1340 Ixodes ricinus ticks prepared in 192 pools were collected in Switzerland and 55 other ticks belonging to different tick species and 97 fleas belonging to different flea species were harvested in Algeria. In Switzerland, the prevalence of Chlamydiales DNA in the 192 pools was equal to 28.1% (54/192) which represents an estimated prevalence in the 1340 individual ticks of between 4.0% and 28.4%. The pan-Chlamydiales qPCR was positive for 45% (25/55) of tick samples collected in Algeria. The sequencing of the positive qPCR amplicons revealed a high diversity of Chlamydiales species. Most of them belonged to the Rhabdochlamydiaceae and Parachlamydiaceae families. Thus, ticks may carry Chlamydiales and should thus be considered as possible vectors for Chlamydiales propagation to both humans and animals.(15)

 

4. The use of MALDI TOF in medical entomology

 

Phlebotomine sand flies

                This work was conducted in collaboration with team 5. Sand flies were captured in four sites in north Algeria. A subset was morphologically and genetically identified. Six species were found in these areas and a total of 28 stored frozen specimens were used for the creation of the reference spectrum database. The relevance of this original method for sand fly identification was validated by two successive blind tests including the morphological identification of 80 new specimens which were stored at -80°C, and 292 unknown specimens, including engorged specimens, which were preserved under different conditions. Intra-species reproducibility and inter-species specificity of the protein profiles were obtained, allowing us to distinguish specimens at the gender level. Querying of the sand fly database using the MS spectra from the blind test groups revealed concordant results between morphological and MALDI-TOF MS identification. However, MS identification results were less efficient for specimens which were engorged or stored in alcohol. Identification of 362 phlebotomine sand flies, captured at four Algerian sites, by MALDI-TOF MS, revealed that the subgenus Larroussius was predominant at all the study sites, except for in M'sila where P. (Phlebotomus) papatasi was the only sand fly species detected. The present study highlights the application of MALDI-TOF MS for monitoring sand fly fauna captured in the field. The low cost, reliability and rapidity of MALDI-TOF MS analyses opens up new ways in the management of phlebotomine sand fly-borne diseases.(5)

 

Fleas

                MALDI-TOF/MS was used as a tool for identifying flea vectors. We measured the MS spectra from 38 flea specimens of 5 species including Ctenocephalides felis, Ctenocephalides canis, Archaeopsylla erinacei, Xenopsylla cheopis and Stenoponia tripectinata. A blind test performed with 24 specimens from species included in a library spectral database confirmed that MALDI-TOF/MS is an effective tool for discriminating flea species. Although fresh and 70% ethanol-conserved samples subjected to MALDI-TOF/MS in blind tests were correctly classified, only MS spectra of quality from fresh specimens were sufficient for accurate and significant identification. A cluster analysis highlighted that the MALDI Biotyper can be used for studying the phylogeny of fleas. (14)

 

5. Other arthropod studies

                Pediculus humanus L. (Psocodea: Pediculidae) can be characterized into three deeply divergent lineages (clades) based on mitochondrial DNA. Clade A consists of both head lice and clothing lice and is distributed worldwide. Clade B consists of head lice only and is mainly found in North and Central America, and in western Europe and Australia. Clade C, which consists only of head lice, is found in Ethiopia, Nepal and Senegal. Twenty-six head lice collected from pupils at different elementary schools in two localities in Algiers (Algeria) were analysed using molecular methods for genotyping lice (cytochrome b and the multi-spacer typing (MST) method. For the first time, we found clade B head lice in Africa living in sympatry with clade A head lice. The phylogenetic analysis of the concatenated sequences of these populations of head lice showed that clade A and clade B head lice had recombined, suggesting that interbreeding occurs when lice live in sympatry.(11)

 

                We have recorded 23 species of hard ticks 10 species of soft ticks, and 16 species fleas and 13 species of human lice and animals was conducted in Algeria, It has also carried out an inventory of 24 species of Phlebotomus vectors of leishmaniasis and Phlebovirus and Bartonella bacilliformis. A total of 3 families, 7 genera and 17 species were collected, including the first report of Culex territanslarvae captured at an altitude of 1750 m and the confirmation of the presence of Aedes albopictus(Dengue, Chikungunya and other arboviruses vector) in Algeria and the Maghreb, based on a second capture in this country.(30)

 

                During our fields works and in order to contribute to the knowledge of arthropod fauna in Algeria, other arthropods have been identified. We collected 159 mites, belonging to Mesostigmata, Uropodina 150 and Sejidae, Sejina 9. We also found 2 pseudoscorpions, 1 chewing louse (Mallophaga,Laemobothriidae) and, for the first time in nests of white storks, the flea Ctenocephalides felis(4 specimens). The remainder were ant heads, beetle heads of Carabidae and Histeridae, immature Anthocorisbugs (Heteroptera) and woodlice (Isopoda) (31)

 

6. Micromammals collection     

                Mammal studies have been conducted to complete entomological studies. The rodents were collected from areas where plague cases were reported during the Algeria plague outbreak in 2003; at Kehailia (35°29′N, 0°32′E) and Benaouali (near Zaghloul, (35°33′N, 0°21′E) in the area of Oran and Mascara, ≈450 km West of the capital, Algiers. Rodents were captured inside human residences and from peridomestic areas by using BTS (Besancon Technique Service, INRA, Montpellier, France), Sherman Trap (H.P. Sherman Traps, Tallahassee, FL, USA) and the flooding technique (Blanc and Baltazard, 1945; Pollitzer, 1953). The rodents trapped belong to Rattus rattus, Rattus norvegicus, and Mus spretus species.

 

7. Clinical studies in rickettsiology

            In 2011-2016, we have participated in various clinical studies (32-35) including the innovative use of swabbing eschars for the diagnosis of Mediterranean spotted fever, the description of R. felis in patients with fever of unknown origin, and the description of a new Borrelia pathogenic for humans.

 

 

URMITE  - Team 12: Vector borne bacterial diseases in Maghreb PUBLICATIONS 2011-2016

 

Refrences Indexed in Pub Med:

 

1: Malek MA, Bitam I, Drancourt M. Plague in Arab Maghreb, 1940-2015: A Review. Front Public Health. 2016 Jun 3;4:112. 

 

2: Armougom F, Bitam I, Croce O, Merhej V, Barassi L, Nguyen TT, La Scola B, Raoult D. Genomic Insights into a New Citrobacterkoseri Strain Revealed Gene Exchanges with the Virulence-Associated Yersinia pestis pPCP1 Plasmid. Front Microbiol. 2016 Mar 16;7:340. doi: 10.3389/fmicb.2016.00340. eCollection 2016. PubMed PMID: 27014253; PubMed Central PMCID: PMC4793686.

 

3: Bessas A, Leulmi H, Bitam I, Zaidi S, Ait-Oudhia K, Raoult D, Parola P. Molecular evidence of vector-borne pathogens in dogs and cats and their ectoparasites in Algiers, Algeria. Comp ImmunolMicrobiol Infect Dis. 2016 Apr;45:23-8. doi: .1016/j.cimid.2016.01.002. Epub 2016 Jan 23. PubMed PMID:27012917.

 

4: Leulmi H, Aouadi A, Bitam I, Bessas A, Benakhla A, Raoult D, Parola P. Detection of Bartonellatamiae, Coxiellaburnetii and rickettsiae in arthropods and tissues from wild and domestic animals in northeastern Algeria. Parasit Vectors. 2016 Jan 20;9:27. doi: 10.1186/s13071-016-1316-9. PubMed PMID: 26791781; PubMed Central PMCID: PMC4721140.

 

5: Lafri I, Almeras L, Bitam I, Caputo A, Yssouf A, Forestier CL, Izri A, Raoult D, Parola P. Identification of Algerian Field-Caught Phlebotomine Sand Fly Vectors by MALDI-TOF MS. PLoSNegl Trop Dis. 2016 Jan 15;10(1):e0004351. doi: 10.1371/journal.pntd.0004351. eCollection 2016 Jan. PubMed PMID: 26771833; PubMed Central PMCID: PMC4714931.

 

6: Lafri I, Leulmi H, Baziz-Neffah F, Lalout R, Mohamed C, Mohamed K, Parola P, Bitam I. Detection of a novel Rickettsia sp. in soft ticks (Acari: Argasidae) in Algeria. Microbes Infect. 2015 Nov-Dec;17(11-12):859-61. doi: 10.1016/j.micinf.2015.09.010. Epub 2015 Sep 25. PubMed PMID: 26408401.

 

7: Leulmi H, Bitam I, Berenger JM, Lepidi H, Rolain JM, Almeras L, Raoult D, Parola P. Correction: Competence of Cimexlectularius Bed Bugs for the Transmission of Bartonellaquintana, the Agent of Trench Fever.PLoSNegl Trop Dis. 2015 Jun 15;9(6):e0003871. doi: 10.1371/journal.pntd.0003871. eCollection 2015 Jun. PubMed PMID: 26075401; PubMed Central PMCID: PMC4468256.

 

8: Leulmi H, Bitam I, Berenger JM, Lepidi H, Rolain JM, Almeras L, Raoult D, Parola P. Competence of Cimexlectularius Bed Bugs for the Transmission of Bartonellaquintana, the Agent of Trench Fever.PLoSNegl Trop Dis. 2015 May 22;9(5):e0003789. doi: 10.1371/journal.pntd.0003789. eCollection 2015 May. Erratum in: PLoSNegl Trop Dis. 2015 Jun;9(6):e0003871. PubMed PMID: 26000974; PubMed Central PMCID: PMC4441494.

 

9: Malek MA, Hammani A, Beneldjouzi A, Bitam I. Enzootic plague foci, Algeria. New Microbes New Infect. 2014 Dec 4;4:13-6. doi: 10.1016/j.nmni.2014.11.003. eCollection 2015 Mar. PubMed PMID: 25834736; PubMed Central PMCID: PMC4354914.

 

10: Kernif T, Stafford K, Coles GC, Bitam I, Papa K, Chiaroni J, Raoult D, Parola P. Responses of artificially reared cat fleasCtenocephalidesfelisfelis (Bouché, 1835) to different mammalian bloods.Med Vet Entomol. 2015 Jun;29(2):171-7. doi: 10.1111/mve.12100. Epub 2015 Jan 21. PubMed PMID: 25604709.

 

11: Boutellis A, Bitam I, Fekir K, Mana N, Raoult D. Evidence that clade A and clade B head lice live in sympatry and recombine in Algeria. Med Vet Entomol. 2015 Mar;29(1):94-8. doi: 10.1111/mve.12058. Epub 2014 Oct 25. PubMed PMID: 25346378.

 

12: Leulmi H, Socolovschi C, Laudisoit A, Houemenou G, Davoust B, Bitam I, Raoult D, Parola P. Detection of Rickettsia felis, Rickettsia typhi, Bartonella Species and Yersinia pestis in Fleas (Siphonaptera) from Africa. PLoSNegl Trop Dis. 2014 Oct 9;8(10):e3152. doi: 10.1371/journal.pntd.0003152. eCollection 2014 Oct. PubMed PMID: 25299702; PubMed Central PMCID: PMC4191943.

 

13: Benredjem W, Leulmi H, Bitam I, Raoult D, Parola P. Borrelia garinii and Rickettsia monacensis in Ixodesricinus ticks, Algeria. Emerg Infect Dis. 2014 Oct;20(10):1776-7. doi: 10.3201/eid2010.140265. PubMed PMID: 25272139; PubMed Central PMCID: PMC4193170.

 

14: Yssouf A, Socolovschi C, Leulmi H, Kernif T, Bitam I, Audoly G, Almeras L, Raoult D, Parola P. Identification of flea species using MALDI-TOF/MS. Comp ImmunolMicrobiol Infect Dis. 2014 May;37(3):153-7. doi: 10.1016/j.cimid.2014.05.002. Epub 2014 May 17. PubMed PMID: 24878069.

 

15: Croxatto A, Rieille N, Kernif T, Bitam I, Aeby S, Péter O, Greub G. Presence ofChlamydiales DNA in ticks and fleas suggests that ticks are carriers of Chlamydiae. Ticks Tick Borne Dis. 2014 Jun;5(4):359-65. doi: 10.1016/j.ttbdis.2013.11.009. Epub 2014 Mar 31. PubMed PMID: 24698831.

 

16: Kernif T, Leulmi H, Socolovschi C, Berenger JM, Lepidi H, Bitam I, Rolain JM, Raoult D, Parola P. Acquisition and excretion of Bartonellaquintana by the cat flea, Ctenocephalidesfelisfelis. Mol Ecol. 2014 Mar;23(5):1204-12. doi: 10.1111/mec.12663. Epub 2014 Feb 20. PubMed PMID: 24400877.

 

17: Trape JF, Diatta G, Arnathau C, Bitam I, Sarih M, Belghyti D, Bouattour A, Elguero E, Vial L, Mané Y, Baldé C, Prugnolle F, Chauvancy G, Mahé G, Granjon L, Duplantier JM, Durand P, Renaud F. The epidemiology and geographic distribution of relapsing fever borreliosis in West and North Africa, with a review of the Ornithodoros erraticus complex (Acari: Ixodida).PLoS One. 2013 Nov

4;8(11):e78473. doi: 10.1371/journal.pone.0078473. eCollection 2013. Erratum in: PLoS One. 2014;9(1). doi:10.1371/annotation/20b57909-df52-4073-a93f-a6689f84389d.Pugnolle, Franck [corrected to Prugnolle, Franck]. PubMed PMID: 24223812; PubMed Central PMCID: PMC3817255.

 

18: Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T,Abdad MY, Stenos J, Bitam I, Fournier PE, Raoult D. Update on tick-borne rickettsioses around the world: a geographic approach. ClinMicrobiol Rev. 2013Oct;26(4):657-702. doi: 10.1128/CMR.00032-13. Review. Erratum in: ClinMicrobiolRev. 2014 Jan;27(1):166. PubMed PMID: 24092850; PubMed Central PMCID: PMC3811236.

 

19: Djerbouh A, Kernif T, Beneldjouzi A, Socolovschi C, Kechemir N, Parola P,Raoult D, Bitam I. The first molecular detection of Rickettsia aeschlimannii inthe ticks of camels from southern Algeria. Ticks Tick Borne Dis. 2012Dec;3(5-6):374-6. doi: 10.1016/j.ttbdis.2012.10.014. Epub 2012 Oct 22. PubMedPMID: 23168055.

 

20: Kernif T, Messaoudene D, Ouahioune S, Parola P, Raoult D, Bitam I. Spotted fever group rickettsiae identified in Dermacentormarginatus and Ixodesricinus ticks in Algeria. Ticks Tick Borne Dis. 2012 Dec;3(5-6):380-1. doi:10.1016/j.ttbdis.2012.10.012. Epub 2012 Oct 22. PubMed PMID: 23168054.

 

21: Bitam I. Vectors of rickettsiae in Africa. Ticks Tick Borne Dis. 2012Dec;3(5-6):382-6. doi: 10.1016/j.ttbdis.2012.10.011. Epub 2012 Oct 23. Review.PubMed PMID: 23168053.

 

22: Kernif T, Djerbouh A, Mediannikov O, Ayach B, Rolain JM, Raoult D, Parola P, Bitam I. Rickettsia africae in Hyalommadromedarii ticks from sub-Saharan Algeria. Ticks Tick Borne Dis. 2012 Dec;3(5-6):377-9. doi:10.1016/j.ttbdis.2012.10.013. Epub 2012 Oct 22. PubMed PMID: 23164496.

 

23: Raoult D, Mouffok N, Bitam I, Piarroux R, Drancourt M. Plague: history and contemporary analysis. J Infect. 2013 Jan;66(1):18-26. doi:10.1016/j.jinf.2012.09.010. Epub 2012 Oct 3. Review. PubMed PMID: 23041039.

 

24: Socolovschi C, Gaudart J, Bitam I, Huynh TP, Raoult D, Parola P. Why are there so few Rickettsia conoriiconorii-infected Rhipicephalussanguineus ticks in the wild? PLoSNegl Trop Dis. 2012;6(6):e1697. doi:10.1371/journal.pntd.0001697. Epub 2012 Jun 19. PubMed PMID: 22724035; PubMedCentral PMCID: PMC3378603.

 

25: Kernif T, Socolovschi C, Bitam I, Raoult D, Parola P. Vector-borne rickettsioses in North Africa. Infect Dis Clin North Am. 2012 Jun;26(2):455-78.doi: 10.1016/j.idc.2012.03.007. PubMed PMID: 22632649.

 

26: Drali R, Benkouiten S, Badiaga S, Bitam I, Rolain JM, Brouqui P. Detection of a knockdown resistance mutation associated with permethrin resistance in the body lousePediculushumanuscorporis by use of melting curve analysis genotyping. J ClinMicrobiol. 2012 Jul;50(7):2229-33. doi: 10.1128/JCM.00808-12. Epub 2012 May 9. PubMed PMID: 22573588; PubMed Central PMCID: PMC3405629.

 

27: Bitam I, Rolain JM, Nicolas V, Tsai YL, Parola P, Gundi VA, Chomel BB, Raoult D. A multi-gene analysis of diversity of Bartonella detected in fleas from Algeria. Comp ImmunolMicrobiol Infect Dis. 2012 Jan;35(1):71-6. doi:10.1016/j.cimid.2011.11.002. Epub 2011 Dec 5. PubMed PMID: 22153359.

 

28: Berdjane-Brouk Z, Charrel RN, B itam I, Hamrioui B, Izri A. Record of Phlebotomus (Transphlebotomus) mascittiiGrassi, 1908 and Phlebotomus (Larroussius) chadliiRioux, Juminer&Gibily, 1966 female in Algeria. Parasite. 2011 Nov;18(4):337-9. PubMed PMID: 22091465; PubMed Central PMCID: PMC3677593.

 

29: Izri A, Bitam I, Charrel RN. First entomological documentation of Aedes (Stegomyia) albopictus (Skuse, 1894) in lgeria.ClinMicrobiol Infect. 2011 Jul;17(7):1116-8. doi: 10.1111/j.1469-0691.2010.03443.x. Epub 2011 Jan 20. PubMedPMID: 21435096.

 

30: Lafri I, Bitam I, Beneldjouzi A, Benmahdi MH. Bull. AN INVENTORY OF MOSQUITOES (DIPTERA: CULICIDAE) IN ALGERIA.Soc. zool. Fr., 2014, 139(1-4) : 255-261.

 

31: Aicha Beya MAMMERIA, Idir BITAM, Amina BOUTELLIS, Tahar KERNIF. FIRST ACCOUNT OF ARTHROPODS IN THE NEST OF THE WHITE STORK, CICONIA CICONIA,IN ALGERIA, INCLUDING THE FLEA CTENOPHALIDES FELIS. Bull. Soc. zool. Fr., 2014, 139(1-4) : 199-213.

 

32: Fotso Fotso A, Angelakis E, Mouffok N, Drancourt M, Raoult D. Blood-Borne Candidatus Borrelia algerica in a Patient with prolonged Fever in Oran, Algeria.  Am J Trop Med Hyg. 2015 Nov;93(5):1070-3. doi: 10.4269/ajtmh.15-0124. Epub 2015 Sep 28. PubMed PMID: 26416117; PubMed Central PMCID: PMC4703269.

 

33: Angelakis E, Mediannikov O, Socolovschi C, Mouffok N, Bassene H, Tall A, Niangaly H, Doumbo O, Znazen A, Sarih M, Sokhna C, Raoult D. Coxiella burnetii-positive PCR in febrile patients in rural and urban Africa. Int J Infect Dis. 2014 Nov;28:107-10. doi: 10.1016/j.ijid.2014.05.029. Epub 2014 Sep 19. PubMed PMID: 25245003.

 

34: Mediannikov O, Socolovschi C, Edouard S, Fenollar F, Mouffok N, Bassene H, Diatta G, Tall A, Niangaly H, Doumbo O, Lekana-Douki JB, Znazen A, Sarih M, Ratmanov P, Richet H, Ndiath MO, Sokhna C, Parola P, Raoult D. Common epidemiology of Rickettsia felis infection and malaria, Africa. Emerg Infect Dis. 2013 Nov;19(11):1775-83. doi: 10.3201/eid1911.130361. PubMed PMID: 24188709;

PubMed Central PMCID: PMC3837673.

 

35: Mouffok N, Socolovschi C, Benabdellah A, Renvoise A, Parola P, Raoult D. Diagnosis of rickettsioses from eschar swab samples, Algeria. Emerg Infect Dis. 2011 Oct;17(10):1968-9. doi: 10.3201/eid1710.110332. PubMed PMID: 22000389;

 

 


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