Molecular Evidence of Spotted Fever Group Rickettsiae in Ticks and Fleas Collected from Some Wild and Domestic Animals in Different Biotopes in Algeria
-
Assia Beneldjouzi
,
Ismail Lafri
,
Amel Djerbouh
,
Safia Nekhili
,
Lydia Hamrioui
,
Nacer Eddine Messahel
,
Zoubir Harrat
,
Naouel Eddaikra
,
Idir Bitam
Abstract
Background: Emergent vector-borne diseases have gained significant attention in recent years due to their increasing prevalence and impact on public health. With its vast geographic and ecological diversity, Algeria has limited available data on the distribution and prevalence of neglected vector-borne diseases. This study aimed to inventory hematophagous ectoparasites, including ticks and fleas, collected from domestic and wild animals such as dogs, hedgehogs, cattle, and rodents across diverse biotopes in northwestern Algeria (Mascara, Oran, Tlemcen, Sidi Bel Abbes, Mostaganem, Tiaret, and Ain Temouchent) and southern Algeria (Laghouat).
Methods: A total of 984 arthropods, comprising 609 ticks and 375 fleas, were collected from domestic and wild animals. Among these, 193 ticks and 105 fleas underwent molecular screening for Rickettsia spp. using gltA and ompA gene-specific primers.
Results: The minimum infection rate (MIR) for Rickettsia spp. was estimated at 6.37%, assuming one positive individual per pool. Quantitative PCR revealed the presence of Rickettsia massiliae in 1/68 (1.47%) of Rhipicephalus sanguineus ticks and Rickettsia felis in 7/48 (14.58%) of Ctenocephalides felis fleas. Additionally, a novel strain of Rickettsia sp. was identified in Rhipicephalus sanguineus and Rhipicephalus turanicus.
Conclusion: This study expands the understanding of tick- and flea-borne Rickettsia species in Algeria, highlighting the diverse range of ectoparasite-borne pathogens associated with domestic and wild animals. The findings underscore the importance of continued surveillance and molecular characterization to address the public health risks posed by these pathogens.
1. Blanton LS (2019) The Rickettsioses: A practical update. Infect Dis Clin North Am. 33: 213–229.
2. Bitam I (2012) Vectors of rickettsiae in Africa. Ticks Tick Borne Dis. 3(5–6): 382–386.
3. Oteo JA, Portillo A (2012) Tick-borne rick¬ettsioses in Europe. Ticks Tick Borne Dis. 3(5–6): 271–278.
4. Chisu V, Leulmi H, Masala G, Piredda M, Foxi C, Parola P (2017) Detection of Rick¬ettsia hoogstraalii, Rickettsia helvetica, Rick¬ettsia massiliae, Rickettsia slovaca and Rickettsia aeschlimannii in ticks from Sar¬dinia, Italy. Ticks Tick Borne Dis. 8(3): 347–352.
5. Portillo A, Santibáñez S, García-Álvarez L, Palomar AM (2015) Rickettsioses in Europe. Microbes Infect. 17(11–12): 834–838.
6. Zhang YY, SunYQ, Chen JJ, Teng AY, Wang T, Li H, Hay SI, Fan LQ, Yang Y, Liu W (2023) Mapping the global distri-bution of spotted fever group rickettsiae: a systematic review with modelling anal-ysis. Lancet. 5: 5–15.
7. Villa L, Zanzani SA, Mortarino LM, Gaz-zonis AL, Olivieri E, Manfredi MT (2022) Molecular prevalence of selected tick-borne pathogens in Dermacentor re-tic¬u¬latus collected in a natural park in Ita-ly. Pathogens. 11(8): 887.
8. Walker DH (1996) Rickettsiae. In: Baron S, (eds): Medical Microbiology. 4th edi-tion. Galveston (TX): University of Tex¬as Medical Branch at Galveston; Chapter 38. Available at: https://www.ncbi.nlm.nih.gov/books/NBK7624/.
9. Rovery C, Raoult D (2008) Rickettsioses. In: Bessis D, Springer (Eds.) Manifesta-tions dermatologiques des maladies in-fectieuses. Paris, pp. 10–26.
10. Abdad MY, Abdallah RA, Fournier PE, Stenos J, Vasoo S (2018) A concise re-view of the epidemiology and diagnos-tics of Rickettsioses: Rickettsia and Ori-entia spp. J Clin Microbiol. 56(8): 1110–1128.
11. Bitam I, Kernif T, Harrat Z, Parola P, Ra-oult D (2009) First detection of Rickett-sia aeschlimannii in Hyalomma ae-gyptium from Algeria. Clin Microbiol Infect. 5: 253–254.
12. Beaucournu JC, Menier K (1998) The genus Ctenocephalides Stiles and Collins, 1930 (Siphonaptera, Pulicidae). Parasite. 5: 3–16.
13. Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier PE, Raoult D (2013) Update on tick-borne rickettsioses around the world: a geo¬graphic approach. Clin Microbiol Rev. 26(4): 657–702.
14. Bouattour A (2002) Clé dichotomique et identification des tiques (Acari: Ixodi-dae) parasites du bétail au Maghreb. Arch Inst Pasteur Tunis. 79(1–4): 43–50.
15. Piotrowski M and Rymaszewska A (2020) Expansion of tick-borne Rickettsioses in the World. Microorganisms. 8: 1–28.
16. Eldin C, Parola P (2020) Rickettsioses, Rev. Prat. French. PMID: 32877141. 70 (02): 201–205.
17. Parola P, Raoult D (2001) Ticks and tick-borne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis. 32(6): 897–928.
18. Gage KL, Burkot TR, Eisen RJ, Hayes EB (2008) Climate and vector borne diseas¬es. Am J Prev Med. 35: 436–450.
19. Bitam I, Parola P, Matsumoto K, Jrolain M, Baziz B., Boubidi SC, Harrat Z, Bel-kaid M, Raoult D (2006) First molecular detection of R. conorii, R. aeschli-mannii, and R. massiliae in ticks from Algeria. Ann NY Acad Sci. 1078: 368–372.
20. Kernif T, Socolovschi C, Bitam I, Raoult D, Parola P (2012) Vector-borne rick-ettsioses in north Africa. Infect Dis Clin North Am. 26: 455–478.
21. Dib L, Bitam I, Bensouilah M, Parola P, Raoult D (2009) First description of Rickettsia monacensis in Ixodes ricinus in Algeria. Clin Microbiol Infect. 15(2): 261–262.
22. Kernif T, Djerbouh A, Mediannikov O, Ayach B, Rolain JM, Raoult D, Bitam I (2012) Rickettsia africae in Hyalomma dromedarii ticks from sub-Saharan Al-geria. Ticks Tick Borne Dis. 3(5–6): 377–379.
23. Bitam I, Parola P, De La Cruz KD, Matsu¬moto K, Baziz B, Rolain J M, Belkaid M, Raoult D (2006) First molecular de¬tection of Rickettsia felis in fleas from Algeria. Am J Trop Med Hyg. 74(4): 532–535.
24. Bitam I, Baziz B, Kernif T, Harrat Z, Pa-rola P, Raoult D (2009) Molecular detec¬tion of Rickettsia typhi and Rickett-sia felis in fleas from Algeria. Clin Mi-crobiol Infect. 15(2): 255–256.
25. Relevé épidémiologique mensuel 2000, vol. VI. INSP Algérie.
26. Relevé épidémiologique mensuel 2001, vol. VI. INSP Algérie.
27. Relevé épidémiologique mensuel 2002, vol. VI. INSP Algérie.
28. Relevé épidémiologique mensuel 1994, vol. VI. INSP Algérie.
29. Relevé épidémiologique mensuel 1995, vol. VI. INSP Algérie.
30. Beaucournu JC, Launay H (1990) Les puces (Siphonaptera) de France et du Bassin méditerranéen occidental. Faune de France, second ed., Paris.
31. Kumsa B, Parola P, Raoult D, So¬colovschi C (2014) Molecular detection of Rickett-sia felis and Bartonella henselae in dog and cat fleas in Central Oromia, Ethio-pia. Am J Trop Med Hyg. 90(3): 457–462.
32. Socolovschi C, Kernif T, Raoult D, Parola P (2010) Borrelia, Rickettsia, and Ehr-lichia species in bat ticks, France. Emerg Infect Dis. 18 (12): 1966–1975.
33. Leulmi H, Socolovschi C, Laudisoit A, Houemenou G, Davoust B, Bitam I, Ra-oult D, Parola P (2014) Detection of Rick¬ettsia felis, Rickettsia typhi, Bar-tonel¬la species and Yersinia pestis in fleas (Siphonaptera) from Africa. PLoS Negl Trop Dis. 8(10): e3152.
34. Magesa1 WS, Haji1 I, Kinimi E, Nzala-wahe1 JS, Kazwala R (2023) Distribu-tion and molecular identification of ix-odid ticks infesting cattle in Kilombero and Iringa Districts, Tanzania. BMC Vet Res. 19: 121.
35. Dantas-Torres F, Otranto D (2022) Rhip-icephalus sanguineus (Brown dog tick). Trends Parasitol. 38(11): 993–994.
36. Dantas-Torres F, Latrofa LS, Annoscia G, Giannelli A, Parisi A, Otranto D (2013) Morphological and genetic diversity of Rhipicephalus sanguineus sensu lato from the new and old worlds. Parasite Vec¬tors. 6: 213.
37. Hornok S, Kováts D, Horváth G, Kontschán J, Farkas R (2020) Checklist of the hard tick (Acari: Ixodidae) fauna of Hungary with emphasis on host-associations and the emergence of Rhipicephalus san¬guineus. Exp Appl Acarol. 80(3): 311–328.
38. Aouadi N, Benkacimi L, Zan Diarra A, Laroche M, Bérenger JM, Bitam I, Pa-rola P (2022) Microorganisms associ¬ated with the North African hedgehog Atelerix algirus and its parasitizing ar-thropods in Algeria. Comp Immunol Mi-crobiol Infect Dis. 80: 101726.
39. Djerbouh A, Lafri I, Kechemir-Issad N, Bitam I (2018) Endo- and ectoparasites (Ixodidae) of camels (Camelus drome-darius) from Southern Algeria. Live-stock Res Rural Dev. 30(8): 141.
40. Li-Ping G, Su-Hua J, Dan L, Shi-Wei W, Chuang-fu C, Yuan-Zhi W (2016) Emerg¬ing spotted fever group rickettsiae in ticks, northwestern. Ticks Tick Borne Dis. 7(6): 1146–1150.
41. Derradj L, Kohil K (2021) Identification and incidence of hard tick species dur-ing summer season 2019 in Jijel Prov¬ince (northeastern Algeria). J Parasit Dis. 45 (1): 211–217.
42. Bouchama B, Dik B, Benia F, Mouffok C (2020) Parasitologie dynamique saison-nière des tiques (Acari: Ixodidae) para-sites des bovins dans la région semi-aride de la wilaya de sétif algérie. Bull Soc Zool Fr. 145(2): 71–81.
43. Boulkaboul A (2003) Parasitisme des tiques (Ixodidae) des bovins à Tiaret, Algé¬rie. Revue d’élevage et de méde-cine vé¬térinaire des pays tropicaux. 56(3): 157–162.
44. Yousfi-monod R, Aeschlimann A (1986) Recherches Sur Les Tiques (Acarina, Ixodi¬dae), Parasites De Bovidés Dans L’ouest Algérien. I - Inventaire systéma-tique et dynamique saisonnière. Ann Parasitol Hum Comp. 61(3): 341–358.
45. Cascio A, Torina A, Valenzise M, Blanda V, Camarda N, Bombaci S, Iaria C, Deluca F, Wasniewska M (2013) Scalp eschar and neck lymphadenopathy caused by Rickettsia massiliae. Emerg Infect Dis. 19(5): 836–837.
46. Vitale G, Mansueto S, Rolain JM, Raoult D (2006) Rickettsia massiliae: first iso-lation from the blood of a patient. Emerg Infect Dis. 12(1): 174–175.
47. Parola P, Socolovschi C, Jeanjean L, Bitam I, Fournier PE, Sotto A, Labauge P, Ra¬oult D (2008) Warmer weather linked to tick attack and emergence of severe rick¬ettsioses. PloS Negl Trop Dis. 2(11): e338.
48. Sadeddine R, Zan Diarra A, Laroche M, Mediannikov O, Righi S, Benakhla A, Dahmana H, Raoult D, Parola P (2020) Molecular identification of protozoal and bacterial organisms in domestic an-imals and their infesting ticks from north-eastern Algeria. Ticks Tick Borne Dis. 11(2): 101330.
49. La Scola B, Meconi S, Fenollar F, Rolain JM, Roux V, Raoult D (2002) Emended description of Rickettsia felis (Bouyer et al. 2001), a temperature-dependent cul-tured bacterium. Int J Syst Evol Micro-biol. 52(6): 2035–2041.
50. Parola P (2011) Rickettsia felis: from a rare disease in the USA to a common cause of fever in sub-Saharan Africa. Clin Microbiol Infect. 17(7): 996–1000.
51. Socolovschi C, Pages F, Raoult D (2012) Rickettsia felis in Aedes albopictus mos-quitoes, Libreville, Gabon. Emerg Infect Dis. 18(10): 1687–1689.
52. Mouffok N (2007). Profil clinico-épidémiologique de la fièvre boutonneuse méditerranéenne dans une région de l'ouest algérien. Thèse de Doctorat en Sciences Médicales, Faculté de Médecine, Université d'Oran, Algérie.
53. Gehrke FS, Gazeta GS, Souza ER, Ribeiro A, Marrelli MT, Schumaker TT (2009) Rickettsia rickettsii, Rickettsia felis and Rickettsia sp. TwKM03 infecting Rhip-icephalus sanguineus and Cten-ocephalides felis collected from dogs in a Brazilian potted fever focus in the State of Rio De Janeiro, Brazil. Clin Microbiol Infect. 15 (l 2): 267–268.
54. Abramowicz KF, Wekesa JW, Nwadike CN, Zambrano ML, Karpathy SE, Cecil D, Burns J, Hu R, Eremeeva ME (2012) Rickettsia felis in cat fleas, Cten-ocephalides felis parasitizing opossums, San Bernardino County, California. Med Vet Entomol. 26(4): 458–562.
55. Ramírez-Hernández A, Montoya V, Mar-tínez A, Pérez JE, Mercado M, De La Ossa A, Vélez C, Estrada G, Correan MI, Duque L (2013) Molecular detec-tion of Rickettsia felis in different flea species from Caldas, Colombia. Am J Trop Med Hyg. 89(3): 453–459.
56. Tsai KH, Lu HY, Huang JH, Wang PJ, Wang HC, Huang CG, Wu WJ, Shu PY (2009) Rickettsia felis in cat fleas in Taiwan. Vector Borne Zoonotic Dis. 9 (5): 561–563.
57. Zavala-Velazquez JE, Zavala-Castro JE, Vadosolis I, Ruiz-Sosa J, Moron C, Bouyer D, Walker D (2002) Identifica-tion of Ctenocephalides felis fleas as a host of Rickettsia felis, the agent of a spotted fever rickettsiosis in Yucatan, Mexico. Vector Borne Zoonotic Dis. 2 (2): 69–75.
58. Troyo A, Álvarez D, Taylor L, Abdalla G, Calderón-Arguedas O, Zambrano ML, Dasch GA, Lindblade K, Hun L, Ere Meeva ME (2012) Rickettsia felis in Ctenocephalides felis from Guatemala and Costa Rica. Am J Trop Med Hyg. 86(6): 1054–1056.
59. Venzal JM, Pérez‐Martínez L, Felix ML, Portillo A, Blanco JR, Oteo JA (2006) Prevalence of Rickettsia felis in Cten-ocephalides felis and Ctenocephalides canis from Uruguay. Ann N Y Acad Sci. 1078: 305– 308.
60. Bessas A, Leulmi H, Bitam I, Zaidi S, Ait-Oudhia K, Raoult D, Parola P (2016) Mo¬lecular evidence of vector-borne patho¬gens in dogs and cats and their ectopara¬sites in Algiers, Algeria. Comp Immu¬nol Microbiol Infect Dis. 45: 23–28.
61. Kernif T, Aissi M, Doumandji SE, Chomel BB, Raoult D, Bitam I (2010) Molecular evidence of Bartonella infec-tion in do¬mestic dogs from Algeria, North Africa, by polymerase chain reac-tion (PCR). Am J Trop Med Hyg. 83(2): 298–300.
2. Bitam I (2012) Vectors of rickettsiae in Africa. Ticks Tick Borne Dis. 3(5–6): 382–386.
3. Oteo JA, Portillo A (2012) Tick-borne rick¬ettsioses in Europe. Ticks Tick Borne Dis. 3(5–6): 271–278.
4. Chisu V, Leulmi H, Masala G, Piredda M, Foxi C, Parola P (2017) Detection of Rick¬ettsia hoogstraalii, Rickettsia helvetica, Rick¬ettsia massiliae, Rickettsia slovaca and Rickettsia aeschlimannii in ticks from Sar¬dinia, Italy. Ticks Tick Borne Dis. 8(3): 347–352.
5. Portillo A, Santibáñez S, García-Álvarez L, Palomar AM (2015) Rickettsioses in Europe. Microbes Infect. 17(11–12): 834–838.
6. Zhang YY, SunYQ, Chen JJ, Teng AY, Wang T, Li H, Hay SI, Fan LQ, Yang Y, Liu W (2023) Mapping the global distri-bution of spotted fever group rickettsiae: a systematic review with modelling anal-ysis. Lancet. 5: 5–15.
7. Villa L, Zanzani SA, Mortarino LM, Gaz-zonis AL, Olivieri E, Manfredi MT (2022) Molecular prevalence of selected tick-borne pathogens in Dermacentor re-tic¬u¬latus collected in a natural park in Ita-ly. Pathogens. 11(8): 887.
8. Walker DH (1996) Rickettsiae. In: Baron S, (eds): Medical Microbiology. 4th edi-tion. Galveston (TX): University of Tex¬as Medical Branch at Galveston; Chapter 38. Available at: https://www.ncbi.nlm.nih.gov/books/NBK7624/.
9. Rovery C, Raoult D (2008) Rickettsioses. In: Bessis D, Springer (Eds.) Manifesta-tions dermatologiques des maladies in-fectieuses. Paris, pp. 10–26.
10. Abdad MY, Abdallah RA, Fournier PE, Stenos J, Vasoo S (2018) A concise re-view of the epidemiology and diagnos-tics of Rickettsioses: Rickettsia and Ori-entia spp. J Clin Microbiol. 56(8): 1110–1128.
11. Bitam I, Kernif T, Harrat Z, Parola P, Ra-oult D (2009) First detection of Rickett-sia aeschlimannii in Hyalomma ae-gyptium from Algeria. Clin Microbiol Infect. 5: 253–254.
12. Beaucournu JC, Menier K (1998) The genus Ctenocephalides Stiles and Collins, 1930 (Siphonaptera, Pulicidae). Parasite. 5: 3–16.
13. Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier PE, Raoult D (2013) Update on tick-borne rickettsioses around the world: a geo¬graphic approach. Clin Microbiol Rev. 26(4): 657–702.
14. Bouattour A (2002) Clé dichotomique et identification des tiques (Acari: Ixodi-dae) parasites du bétail au Maghreb. Arch Inst Pasteur Tunis. 79(1–4): 43–50.
15. Piotrowski M and Rymaszewska A (2020) Expansion of tick-borne Rickettsioses in the World. Microorganisms. 8: 1–28.
16. Eldin C, Parola P (2020) Rickettsioses, Rev. Prat. French. PMID: 32877141. 70 (02): 201–205.
17. Parola P, Raoult D (2001) Ticks and tick-borne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis. 32(6): 897–928.
18. Gage KL, Burkot TR, Eisen RJ, Hayes EB (2008) Climate and vector borne diseas¬es. Am J Prev Med. 35: 436–450.
19. Bitam I, Parola P, Matsumoto K, Jrolain M, Baziz B., Boubidi SC, Harrat Z, Bel-kaid M, Raoult D (2006) First molecular detection of R. conorii, R. aeschli-mannii, and R. massiliae in ticks from Algeria. Ann NY Acad Sci. 1078: 368–372.
20. Kernif T, Socolovschi C, Bitam I, Raoult D, Parola P (2012) Vector-borne rick-ettsioses in north Africa. Infect Dis Clin North Am. 26: 455–478.
21. Dib L, Bitam I, Bensouilah M, Parola P, Raoult D (2009) First description of Rickettsia monacensis in Ixodes ricinus in Algeria. Clin Microbiol Infect. 15(2): 261–262.
22. Kernif T, Djerbouh A, Mediannikov O, Ayach B, Rolain JM, Raoult D, Bitam I (2012) Rickettsia africae in Hyalomma dromedarii ticks from sub-Saharan Al-geria. Ticks Tick Borne Dis. 3(5–6): 377–379.
23. Bitam I, Parola P, De La Cruz KD, Matsu¬moto K, Baziz B, Rolain J M, Belkaid M, Raoult D (2006) First molecular de¬tection of Rickettsia felis in fleas from Algeria. Am J Trop Med Hyg. 74(4): 532–535.
24. Bitam I, Baziz B, Kernif T, Harrat Z, Pa-rola P, Raoult D (2009) Molecular detec¬tion of Rickettsia typhi and Rickett-sia felis in fleas from Algeria. Clin Mi-crobiol Infect. 15(2): 255–256.
25. Relevé épidémiologique mensuel 2000, vol. VI. INSP Algérie.
26. Relevé épidémiologique mensuel 2001, vol. VI. INSP Algérie.
27. Relevé épidémiologique mensuel 2002, vol. VI. INSP Algérie.
28. Relevé épidémiologique mensuel 1994, vol. VI. INSP Algérie.
29. Relevé épidémiologique mensuel 1995, vol. VI. INSP Algérie.
30. Beaucournu JC, Launay H (1990) Les puces (Siphonaptera) de France et du Bassin méditerranéen occidental. Faune de France, second ed., Paris.
31. Kumsa B, Parola P, Raoult D, So¬colovschi C (2014) Molecular detection of Rickett-sia felis and Bartonella henselae in dog and cat fleas in Central Oromia, Ethio-pia. Am J Trop Med Hyg. 90(3): 457–462.
32. Socolovschi C, Kernif T, Raoult D, Parola P (2010) Borrelia, Rickettsia, and Ehr-lichia species in bat ticks, France. Emerg Infect Dis. 18 (12): 1966–1975.
33. Leulmi H, Socolovschi C, Laudisoit A, Houemenou G, Davoust B, Bitam I, Ra-oult D, Parola P (2014) Detection of Rick¬ettsia felis, Rickettsia typhi, Bar-tonel¬la species and Yersinia pestis in fleas (Siphonaptera) from Africa. PLoS Negl Trop Dis. 8(10): e3152.
34. Magesa1 WS, Haji1 I, Kinimi E, Nzala-wahe1 JS, Kazwala R (2023) Distribu-tion and molecular identification of ix-odid ticks infesting cattle in Kilombero and Iringa Districts, Tanzania. BMC Vet Res. 19: 121.
35. Dantas-Torres F, Otranto D (2022) Rhip-icephalus sanguineus (Brown dog tick). Trends Parasitol. 38(11): 993–994.
36. Dantas-Torres F, Latrofa LS, Annoscia G, Giannelli A, Parisi A, Otranto D (2013) Morphological and genetic diversity of Rhipicephalus sanguineus sensu lato from the new and old worlds. Parasite Vec¬tors. 6: 213.
37. Hornok S, Kováts D, Horváth G, Kontschán J, Farkas R (2020) Checklist of the hard tick (Acari: Ixodidae) fauna of Hungary with emphasis on host-associations and the emergence of Rhipicephalus san¬guineus. Exp Appl Acarol. 80(3): 311–328.
38. Aouadi N, Benkacimi L, Zan Diarra A, Laroche M, Bérenger JM, Bitam I, Pa-rola P (2022) Microorganisms associ¬ated with the North African hedgehog Atelerix algirus and its parasitizing ar-thropods in Algeria. Comp Immunol Mi-crobiol Infect Dis. 80: 101726.
39. Djerbouh A, Lafri I, Kechemir-Issad N, Bitam I (2018) Endo- and ectoparasites (Ixodidae) of camels (Camelus drome-darius) from Southern Algeria. Live-stock Res Rural Dev. 30(8): 141.
40. Li-Ping G, Su-Hua J, Dan L, Shi-Wei W, Chuang-fu C, Yuan-Zhi W (2016) Emerg¬ing spotted fever group rickettsiae in ticks, northwestern. Ticks Tick Borne Dis. 7(6): 1146–1150.
41. Derradj L, Kohil K (2021) Identification and incidence of hard tick species dur-ing summer season 2019 in Jijel Prov¬ince (northeastern Algeria). J Parasit Dis. 45 (1): 211–217.
42. Bouchama B, Dik B, Benia F, Mouffok C (2020) Parasitologie dynamique saison-nière des tiques (Acari: Ixodidae) para-sites des bovins dans la région semi-aride de la wilaya de sétif algérie. Bull Soc Zool Fr. 145(2): 71–81.
43. Boulkaboul A (2003) Parasitisme des tiques (Ixodidae) des bovins à Tiaret, Algé¬rie. Revue d’élevage et de méde-cine vé¬térinaire des pays tropicaux. 56(3): 157–162.
44. Yousfi-monod R, Aeschlimann A (1986) Recherches Sur Les Tiques (Acarina, Ixodi¬dae), Parasites De Bovidés Dans L’ouest Algérien. I - Inventaire systéma-tique et dynamique saisonnière. Ann Parasitol Hum Comp. 61(3): 341–358.
45. Cascio A, Torina A, Valenzise M, Blanda V, Camarda N, Bombaci S, Iaria C, Deluca F, Wasniewska M (2013) Scalp eschar and neck lymphadenopathy caused by Rickettsia massiliae. Emerg Infect Dis. 19(5): 836–837.
46. Vitale G, Mansueto S, Rolain JM, Raoult D (2006) Rickettsia massiliae: first iso-lation from the blood of a patient. Emerg Infect Dis. 12(1): 174–175.
47. Parola P, Socolovschi C, Jeanjean L, Bitam I, Fournier PE, Sotto A, Labauge P, Ra¬oult D (2008) Warmer weather linked to tick attack and emergence of severe rick¬ettsioses. PloS Negl Trop Dis. 2(11): e338.
48. Sadeddine R, Zan Diarra A, Laroche M, Mediannikov O, Righi S, Benakhla A, Dahmana H, Raoult D, Parola P (2020) Molecular identification of protozoal and bacterial organisms in domestic an-imals and their infesting ticks from north-eastern Algeria. Ticks Tick Borne Dis. 11(2): 101330.
49. La Scola B, Meconi S, Fenollar F, Rolain JM, Roux V, Raoult D (2002) Emended description of Rickettsia felis (Bouyer et al. 2001), a temperature-dependent cul-tured bacterium. Int J Syst Evol Micro-biol. 52(6): 2035–2041.
50. Parola P (2011) Rickettsia felis: from a rare disease in the USA to a common cause of fever in sub-Saharan Africa. Clin Microbiol Infect. 17(7): 996–1000.
51. Socolovschi C, Pages F, Raoult D (2012) Rickettsia felis in Aedes albopictus mos-quitoes, Libreville, Gabon. Emerg Infect Dis. 18(10): 1687–1689.
52. Mouffok N (2007). Profil clinico-épidémiologique de la fièvre boutonneuse méditerranéenne dans une région de l'ouest algérien. Thèse de Doctorat en Sciences Médicales, Faculté de Médecine, Université d'Oran, Algérie.
53. Gehrke FS, Gazeta GS, Souza ER, Ribeiro A, Marrelli MT, Schumaker TT (2009) Rickettsia rickettsii, Rickettsia felis and Rickettsia sp. TwKM03 infecting Rhip-icephalus sanguineus and Cten-ocephalides felis collected from dogs in a Brazilian potted fever focus in the State of Rio De Janeiro, Brazil. Clin Microbiol Infect. 15 (l 2): 267–268.
54. Abramowicz KF, Wekesa JW, Nwadike CN, Zambrano ML, Karpathy SE, Cecil D, Burns J, Hu R, Eremeeva ME (2012) Rickettsia felis in cat fleas, Cten-ocephalides felis parasitizing opossums, San Bernardino County, California. Med Vet Entomol. 26(4): 458–562.
55. Ramírez-Hernández A, Montoya V, Mar-tínez A, Pérez JE, Mercado M, De La Ossa A, Vélez C, Estrada G, Correan MI, Duque L (2013) Molecular detec-tion of Rickettsia felis in different flea species from Caldas, Colombia. Am J Trop Med Hyg. 89(3): 453–459.
56. Tsai KH, Lu HY, Huang JH, Wang PJ, Wang HC, Huang CG, Wu WJ, Shu PY (2009) Rickettsia felis in cat fleas in Taiwan. Vector Borne Zoonotic Dis. 9 (5): 561–563.
57. Zavala-Velazquez JE, Zavala-Castro JE, Vadosolis I, Ruiz-Sosa J, Moron C, Bouyer D, Walker D (2002) Identifica-tion of Ctenocephalides felis fleas as a host of Rickettsia felis, the agent of a spotted fever rickettsiosis in Yucatan, Mexico. Vector Borne Zoonotic Dis. 2 (2): 69–75.
58. Troyo A, Álvarez D, Taylor L, Abdalla G, Calderón-Arguedas O, Zambrano ML, Dasch GA, Lindblade K, Hun L, Ere Meeva ME (2012) Rickettsia felis in Ctenocephalides felis from Guatemala and Costa Rica. Am J Trop Med Hyg. 86(6): 1054–1056.
59. Venzal JM, Pérez‐Martínez L, Felix ML, Portillo A, Blanco JR, Oteo JA (2006) Prevalence of Rickettsia felis in Cten-ocephalides felis and Ctenocephalides canis from Uruguay. Ann N Y Acad Sci. 1078: 305– 308.
60. Bessas A, Leulmi H, Bitam I, Zaidi S, Ait-Oudhia K, Raoult D, Parola P (2016) Mo¬lecular evidence of vector-borne patho¬gens in dogs and cats and their ectopara¬sites in Algiers, Algeria. Comp Immu¬nol Microbiol Infect Dis. 45: 23–28.
61. Kernif T, Aissi M, Doumandji SE, Chomel BB, Raoult D, Bitam I (2010) Molecular evidence of Bartonella infec-tion in do¬mestic dogs from Algeria, North Africa, by polymerase chain reac-tion (PCR). Am J Trop Med Hyg. 83(2): 298–300.
| Files | ||
| Issue | Articles In Press | |
| Section | Original Article | |
| Keywords | ||
| Algeria; Molecular detection; Spotted fever group rickettsiae; Ectoparasites | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Beneldjouzi A, Lafri I, Djerbouh A, Nekhili S, Hamrioui L, Eddine Messahel N, Harrat Z, Eddaikra N, Bitam I. Molecular Evidence of Spotted Fever Group Rickettsiae in Ticks and Fleas Collected from Some Wild and Domestic Animals in Different Biotopes in Algeria. J Arthropod Borne Dis. 2025;.
