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Detailed Infestation Spectrums About Biological Stages of Hard Ticks (Acari: Ixodida: Ixodidae) in Humans: A Systematic Review and Meta-Analysis

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Abstract

Purpose

A comprehensive systematic meta-analysis review which deals with the degrees and trends of human infestation by biological stages of ticks, the degrees and trends of human infestation by biological stages of ticks in rural and urban areas, the infestation scale of tick attachment sites in body parts of humans, and the degrees of tick infestation in human age groups is critical. Therefore, this systematic meta-analysis review summarizes the above-detailed human infestation spectrums about biological stages of hard ticks.

Methods

After a preliminary review from 605 papers representing areas of the study objectives, 96 were selected for detailed human infestation spectrums of biological stages of hard ticks.

Results

In general, the results suggest that the adult ticks, and mostly females attack humans more than larval and nymphalid ones, and adult males, respectively. Unlike the trends of human infestation by larval and nymphalid stages of ticks, and the adult, male and female ticks which exhibited approximately a sharply decreasing trend, the global trend of human infestation by hard ticks exhibited approximately a sharply increasing trend over time. Ticks attack humans more in rural area than urban area. Also, the trends of human tick infestation in rural and urban areas exhibit, respectively, a sharp increase and decrease trends over time.

Conclusions

The majority of ticks mostly attach to human body trunk and extremity than head and neck, and genital area. Ticks attack human age groups of 0–9, 20–39, and 40–59 years more than those aged between 10 and 19 or older than 60 years.

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References

  1. Akhlagh A, Salehzadeh A, Zahirnia AH, Davari B (2019) 10-year trends in epidemiology, diagnosis, and treatment of cutaneous Leishmaniasis in Hamadan Province, West of Iran (2007–2016). Front Public Health 7:27. https://doi.org/10.3389/fpubh.2019.0002

    Article  PubMed  PubMed Central  Google Scholar 

  2. Andersson MO, Marga G, Banu T, Dobler G, Chitimia-Dobler L (2018) Tick-borne pathogens in tick species infesting humans in Sibiu County, central Romania. Parasitol Res 117:1591–1597

    Article  PubMed  Google Scholar 

  3. Bakirci S, Aysul N, Bilgic HB, Hacilarlioglu S, Eren H, Karagenc T (2019) Tick bites on humans in southwestern region of Turkey: species diversity. Turkiye Parazitol Derg 43:30–35

    Article  PubMed  Google Scholar 

  4. Bakirci S, Aysul N, Eren H, Unlu A, Karagenc T (2014) Diversity of ticks biting humans in Aydın province of Turkey. Ank Univ Vet Fak Derg 61:93–98

    Article  Google Scholar 

  5. Barker SC, Walker AR (2014) Ticks of Australia. The species that infest domestic animals and humans. Zootaxa 3816:1–144

    Article  Google Scholar 

  6. Beyhan YE, Mungan M, Babur C (2016) The species of ticks bites on human and their seasonal distribution in Ankara, Turkey. Ankara Univ Vet Fak Derg 63:115–119

    Article  Google Scholar 

  7. Brahma RK, Dixit V, Sangwan AK, Doley R (2014) Identification and characterization of Rhipicephalus (Boophilus) microplus and Haemaphysalis bispinosa ticks (Acari: Ixodidae) of North East India by ITS2 and 16S rDNA sequences and morphological analysis. Exp Appl Acarol 62:253–265

    Article  PubMed  Google Scholar 

  8. Briciu VT, Titilincu A, Tatulescu DF, Carstina D, Lefkaditis M, Mihalca AD (2011) First survey on hard ticks (Ixodidae) collected from humans in Romania: possible risks for tick-borne diseases. Exp Appl Acarol 54:199–204

    Article  CAS  PubMed  Google Scholar 

  9. Bursalı A, Keskin A, Keskin A, Kul Köprülü T, Tekin Ş (2017) Investigation of the presence of rickettsiae in ticks parasitizing humans in Corum Region. Turk Bull Hyg Exp Biol 74:293–298

    Article  Google Scholar 

  10. Bursali A, Tekin S, Keskin A, Ekici M, Dundar E (2011) Species diversity of Ixodid Ticks feeding on humans in Amasya, Turkey: seasonal abundance and presence of crimean-congo hemorrhagic fever virus. J Med Entomol 48:85–93

    Article  CAS  PubMed  Google Scholar 

  11. Bursali A, Tekin S, Keskin A, Ekici M, Dundar E (2014) Species diversity of Ixodid ticks feeding on humans in Amasya, Turkey: seasonal abundance and presence of Crimean-Congo hemorrhagic fever virus. J Med Entomol 48:85–93

    Article  Google Scholar 

  12. Cakabay T, Gokdogan O, Kocyigit M (2016) Human otoacariasis: demographic and clinical outcomes in patients with ear-canal ticks and a review of literature. J Otol 11:111–117

    Article  PubMed  PubMed Central  Google Scholar 

  13. Campbell BS, Bowles DE (1994) Human tick bite records in a United States air force population, 1989–1992: implications for tick-borne disease risk. J Wilderness Med 5:405–412

    Article  Google Scholar 

  14. Chan, W.-H., & Kaufman, P.E. (2008). Featured creatures: Dermacentor variabilis (Say) (Arachnida: Ixodida: Ixodidae) http://entnemdept.ufl.edu/creatures/urban/medical/american_dog_tick.htm

  15. Davari B, Alam FN, Nasirian H, Nazari M, Abdigoudarzi M, Salehzadeh A (2017) Seasonal distribution and faunistic of ticks in the Alashtar county (Lorestan Province) Iran. Pan Afr Med J 27:1–16

    Article  Google Scholar 

  16. Davari B, Hassanvand A, Nasirian H, Ghiasian S, Salehzadeh A, Nazari M (2017) Comparison of cockroach fungal contamination in the clinical and non-clinical environments from Iran. J Entomol Acarol Res 49:109–115

    Article  Google Scholar 

  17. Davari B, Kashani S, Nasirian H, Nazari M, Salehzadeh A (2018) The efficacy of MaxForce and Avion gel baits containing fipronil, clothianidin and indoxacarb against the German cockroach (Blattella germanica). Entomol Res 48:459–465

    Article  CAS  Google Scholar 

  18. de la Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE (2008) Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci 13:6938–6946

    Article  PubMed  Google Scholar 

  19. Estrada-Peña A, Jongejan F (1999) Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol 23:685–715

    Article  PubMed  Google Scholar 

  20. Farahi A, Ebrahimzade E, Nabian S, Hanafi-Bojd AA, Akbarzadeh K, Bahonar A (2016) Temporal and spatial distribution and species diversity of hard ticks (Acari: Ixodidae) in the eastern region of caspian sea. Acta Trop 164:1–9

    Article  PubMed  Google Scholar 

  21. Faulde MK, Rutenfranz M, Hepke J, Rogge M, Görner A, Keth A (2014) Human tick infestation pattern, tick-bite rate, and associated Borrelia burgdorferi s.l. infection risk during occupational tick exposure at the Seedorf military training area, northwestern Germany. Ticks Tick-borne Dis 5:594–599

    Article  PubMed  Google Scholar 

  22. Felz MW, Durden LA (1999) Attachment sites of four tick species (Acari: Ixodidae) parasitizing humans in Georgia and South Carolina. J Med Entomol 36:361–364

    Article  CAS  PubMed  Google Scholar 

  23. Gargili A, Kar S, Yilmazer N, Cerit C, Sonmez G, Sahin F, Alp H, Vatansever Z (2010) Evaluation of ticks biting humans in Thrace province, Turkey. Kafkas Univ Vet Fak Derg 16:141–146

    Google Scholar 

  24. Gargili A, Kar S, Yilmazer N, Ergonul O, Vatansever Z (2011) Different abundances of human-biting ticks in two neighboring provinces in Turkey. Kafkas Univ Vet Fak Derg 17:93–97

    Google Scholar 

  25. Gargili A, Palomar AM, Midilli K, Portillo A, Kar S, Oteo JA (2012) Rickettsia species in ticks removed from humans in Istanbul, Turkey. Vector Borne Zoonotic Dis 12:938–941

    Article  PubMed  PubMed Central  Google Scholar 

  26. Ghosh S, Azhahianambi P, de la Fuente J (2006) Control of ticks of ruminants, with special emphasis on livestock farming systems in India: present and future possibilities for integrated control—a review. Exp Appl Acarol 40:49–66

    Article  CAS  PubMed  Google Scholar 

  27. González-Álvarez VH, de la Cruz-Ramos JM, Pérez-Muñoz R, Siller-Rodríguez QK, Ortega-Morales AI (2020) The brown dog tick infesting humans in North-Central Mexico: a tick-borne disease risk. Folia Entomológica Mexicana (Nueva Serie) 6:9–12

    Google Scholar 

  28. Guglielmone AA, Beati L, Barros-Battesti DM, Labruna MB, Nava S, Venzal JM, Mangold AJ, Szabó MPJ, Martins JR, González-Acuña D, Estrada-Peña A (2006) Ticks (Ixodidae) on humans in South America. Exp Appl Acarol 40:83–100

    Article  CAS  PubMed  Google Scholar 

  29. Guglielmone AA, Mangold AJ, Vinabal AE (1991) Ticks (Ixodidae) parasitizing humans in four provinces of north-western Argentina. Ann Trop Med Parasitol 85:539–542

    Article  CAS  PubMed  Google Scholar 

  30. Horak I, Fourie L, Heyne H, Walker JB, Needham G (2002) Ixodid ticks feeding on humans in South Africa: with notes on preferred hosts, geographic distribution, seasonal occurrence and transmission of pathogens. Exp Appl Acarol 27:113–136

    Article  CAS  PubMed  Google Scholar 

  31. Jameson LJ, Morgan PJ, Medlock JM, Watola G, Vaux AGC (2012) Importation of Hyalomma marginatum, vector of Crimean-Congo haemorrhagic fever virus, into the United Kingdom by migratory birds. Ticks Tick-borne Dis 3:95–99

    Article  PubMed  Google Scholar 

  32. Kar S, Dervis E, Akın A, Ergonul O, Gargili A (2013) Preferences of different tick species for human hosts in Turkey. Exp Appl Acarol 61:349–355

    Article  CAS  PubMed  Google Scholar 

  33. Kar S, Yilmazer N, Akyildiz G, Gargili A (2017) The human infesting ticks in the city of Istanbul and its vicinity with reference to a new species for Turkey. Syst Appl Acarol 22:2245–2256

    Google Scholar 

  34. Karaer Z, Guven E, Nalbantoglu S, Kar S, Orkun O, Ekdal K, Kocak A, Akcay A (2011) Ticks on humans in Ankara, Turkey. Exp Appl Acarol 54:85–91

    Article  PubMed  Google Scholar 

  35. Keskin A, Bulut YE, Keskin A, Bursali A (2017) Tick attachment sites in humans living in the Tokat province of Turkey. Turk Hij Den Biyol Derg 74:121–128

    Article  Google Scholar 

  36. Keskin A, Keskin A, Bursali A, Tekin S (2015) Ticks (Acari: Ixodida) parasitizing humans in Corum and Yozgat provinces, Turkey. Exp Appl Acarol 67:607–616

    Article  PubMed  Google Scholar 

  37. Khasnatinov MA, Liapunov AV, Manzarova EL, Kulakova NV, Petrova IV, Danchinova GA (2016) The diversity and prevalence of hard ticks attacking human hosts in Eastern Siberia (Russian Federation) with first description of invasion of non-endemic tick species. Parasitol Res 115:501–510

    Article  PubMed  Google Scholar 

  38. Ladonni H, Paksa A, Nasirian H, Doroudgar A, Abaie M (2013) Detection of Carbamat and organo phosphorus susceptibility levels in German cockroach in vivo. Toloo e Behdasht 40:95–105

    Google Scholar 

  39. Leblebicioglu H, Eroglu C, Erciyas-Yavuz K, Hokelek M, Acici M, Yilmaz H (2014) Role of migratory birds in spreading Crimean-Congo hemorrhagic fever, Turkey. Emerg Infect Dis 20:1331–1334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Leblebicioglu H, Ozaras R, Irmak H, Sencan I (2016) Crimean-Congo hemorrhagic fever in Turkey: current status and future challenges. Antiviral Res 126:21–34

    Article  CAS  PubMed  Google Scholar 

  41. Limoee M, Shayeghi M, Heidari J, Nasirian H, Ladonni H (2010) Susceptibility level of hospital-collected strains of German cockroach Blattella germanica (L.) to carbamate and organophosphorous insecticides using surface contact method in Tehran (2007–2008). J Kermanshah Univ Med Sci 13:337–343

    Google Scholar 

  42. Lotfollahzadeh S, Nikbakht Boroujeni GR, Mokhber Dezfouli MR, Bokaei S (2011) A serosurvey of Crimean-Congo haemorrhagic fever virus in dairy cattle in Iran. Zoonoses Public Health 58:54–59

    Article  CAS  PubMed  Google Scholar 

  43. Manfredi M, Dini V, Piacenza S, Genchi C (1999) Tick species parasitizing people in an area endemic for tick-borne diseases in north-western Italy. Parassitologia 41:555–560

    CAS  PubMed  Google Scholar 

  44. Moradi A, Zahirnia A, Alipour A, Eskandari Z (2009) The prevalence of Pediculosis capitis in primary school students in Bahar, Hamadan Province Iran. J Res Health Sci 9:45–49

    PubMed  Google Scholar 

  45. Nasirian H (2007) Duration of fipronil and imidacloprid gel baits toxicity against Blattella germanica strains of Iran. J Arthropod-Borne Dis 1:40–47

    Google Scholar 

  46. Nasirian H (2008) Rapid elimination of German Cockroach, Blattella germanica, by fipronil and imidacloprid gel baits. J Arthropod-Borne Dis 2:37–43

    Google Scholar 

  47. Nasirian H (2010) An overview of German cockroach, Blattella germanica, studies conducted in Iran. Pak J Biol Sci 13:1077–1084

    Article  CAS  PubMed  Google Scholar 

  48. Nasirian, H. (2013). Using insects for heavy metal contamination survey in Shadegan wetland. Thesis for fulfillment of the PhD Degree in Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences

  49. Nasirian H (2014) Evaluation of water quality and organic pollution of Shadegan and Hawr Al Azim wetlands by biological indices using insects. J Entomol Zool Stud 2:193–200

    Google Scholar 

  50. Nasirian H (2016) New aspects about Supella longipalpa (Blattaria: Blattellidae). Asian Pac J Trop Biomed 6:1065–1075

    Article  Google Scholar 

  51. Nasirian H (2017) Contamination of cockroaches (Insecta: Blattaria) to medically fungi: a systematic review and meta-analysis. J Med Mycol 27:427–448

    Article  CAS  Google Scholar 

  52. Nasirian H (2017) Infestation of cockroaches (Insecta: Blattaria) in the human dwelling environments: a systematic review and meta-analysis. Acta Trop 167:86–98

    Article  PubMed  Google Scholar 

  53. Nasirian H (2019) Contamination of cockroaches (Insecta: Blattaria) by medically important bacteriae: a systematic review and meta-analysis. J Med Entomol 56:1534–1554

    Article  PubMed  Google Scholar 

  54. Nasirian H (2019) Crimean-Congo hemorrhagic fever (CCHF) seroprevalence: a systematic review and meta-analysis. Acta Trop 196:102–120

    Article  PubMed  Google Scholar 

  55. Nasirian H (2019) Recent cockroach bacterial contamination trend in the human dwelling environments: a systematic review and meta-analysis. Bangladesh J Med Sci 18:540–545

    Article  Google Scholar 

  56. Nasirian H (2020) New aspects about Crimean-Congo hemorrhagic fever (CCHF) cases and associated fatality trends: a global systematic review and meta-analysis. Compar Immunol Microbiol Infect Dis 69:101429. https://doi.org/10.1016/j.cimid.102020.101429

    Article  Google Scholar 

  57. Nasirian H, Alimohammadi M, Kamandar M, Saikh Barahwie L, Mojadami Moghadam H, Sheikhi R, Asgari M, Hosseini SS, Farhani Ahmadi F (2015) Water quality evaluation of the Shadegan and Hawr Al Azim wetlands from Iran. Indian J Sci Res 6:11–24

    CAS  Google Scholar 

  58. Nasirian H, Irvine K (2017) Odonata larvae as a bioindicator of metal contamination in aquatic environments: application to ecologically important wetlands in Iran. Environ Monit Assess 189:436

    Article  PubMed  CAS  Google Scholar 

  59. Nasirian H, Irvine K, Sadeghi S, Mahvi A, Nazmara S (2016) Assessment of bed sediment metal contamination in the Shadegan and Hawr Al Azim wetlands, Iran. Environ Monit Assess 188:1–15

    Article  CAS  Google Scholar 

  60. Nasirian H, Ladoni H, Davari B, Shayeghi M, Ershadi Y, Reza M, Vatandoost H (2006) Effect of fipronil on permethrin sensitive and permethrin resistant strains of Blattella germanica. Sci J Kurd Univ Med Sci 11:33–41

    Google Scholar 

  61. Nasirian H, Ladonni H, Aboulhassani M, Limoee M (2011) Susceptibility of field populations of Blattella germanica (Blattaria: Blattellidae) to spinosad. Pak J Biol Sci 14:862–868

    Article  CAS  PubMed  Google Scholar 

  62. Nasirian H, Ladonni H, Shayeghi M, Soleimani-Ahmadi M (2009) Iranian non-responding contact method German cockroach permethrin resistance strains resulting from field pressure pyrethroid spraying. Pak J Biol Sci 12:643–647

    Article  CAS  PubMed  Google Scholar 

  63. Nasirian H, Ladonni H, Shayeghi M, Vatandoost H, Rassi Y, Ershadi MY, Rafinejad J, Basseri H (2006) Duration of fipronil WHO glass jar method toxicity against susceptible and feral German Cockroach strains. Pak J Biol Sci 9:1955–1959

    Article  CAS  Google Scholar 

  64. Nasirian H, Ladonni H, Shayeghi M, Vatandoost H, Yaghoobi-Ershadi M, Rassi Y, Abolhassani M, Abaei M (2006) Comparison of permethrin and fipronil toxicity against German cockroach (Dictyoptera: Blattellidae) strains. Iran J Public Health 35:63–67

    CAS  Google Scholar 

  65. Nasirian H, Ladonni H, Vatandoost H (2006) Duration of fipronil topical application toxicity in Blattella germanica field population strains. Pak J Biol Sci 9:800–804

    Article  CAS  Google Scholar 

  66. Nasirian H, Ladonni H, Vatandoost H, Shayeghei M, Poudat A (2006) Laboratory performance of 0.05% fipronil and 2.15% imidacloprid gel baits against German cockroaches. Blattella germanica Hormozgan Med J 10:24–25

    Google Scholar 

  67. Nasirian H, Mahvi AH, Hosseini M, Vazirianzadeh B, Sadeghi SM, Nazmara S (2013) Study on the heavy metal bioconcentrations of the Shadegan international wetland mosquitofish, Gambusia affinis, by inductively coupled plasma technique. J Environ Health Sci Eng 11:22

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Nasirian H, Nazmara S, Mahvi AH, Hosseini M, Shiri L, Vazirianzadeh B (2015) Assessment of some heavy metals in the Shadegan and Hawr Al Hawizea wetland waters from Iran. Indian J Sci Technol 8:1–9

    Article  CAS  Google Scholar 

  69. Nasirian H, Sadeghi SMT, Vazirianzadeh B, Moosa-Kazemi SH (2014) New record of Aedes vittatus and Culiseta subochrea (Diptera: Culicidae) and their distribution from Shadegan Wetland, South Western Iran. J Entomol Zool Stud 2:271–275

    Google Scholar 

  70. Nasirian H, Salehzadeh A (2019) Control of cockroaches (Blattaria) in sewers: a practical approach systematic review. J Med Entomol 56:181–191

    Article  CAS  PubMed  Google Scholar 

  71. Nasirian H, Salehzadeh A (2019) Effect of seasonality on the population density of wetland aquatic insects: a case study of the Hawr Al Azim and Shadegan wetlands, Iran. Vet World 12:584–592

    Article  PubMed  PubMed Central  Google Scholar 

  72. Nasirian H, Vazirianzadeh B, Taghi Sadeghi SM, Nazmara S (2014b) Culiseta subochrea as a bioindicator of metal contamination in Shadegan International Wetland, Iran (Diptera: Culicidae). J Insect Sci 14:258. https://doi.org/10.1093/jisesa/ieu120

    Article  PubMed  PubMed Central  Google Scholar 

  73. Nava S, Caparros JA, Mangold AJ, Guglielmone AA (2006) Ticks (Acari: Ixodida: Argasidae, Ixodidae) infesting humans in Northwestern Cordoba Province, Argentina. Medicina (B Aires) 66:225–228

    Google Scholar 

  74. Nazari M, Alipourian Motlagh B, Nasirian H (2016) Toxicity of cypermethrin and chlorpyrifos against German cockroach [Blattella germanica (Blattaria: Blattellidae)] strains from Hamadan, Iran. Pak J Biol Sci 19:259–264

    Article  PubMed  CAS  Google Scholar 

  75. Otranto D, Dantas-Torres F, Giannelli A, Latrofa MS, Cascio A, Cazzin S, Ravagnan S, Montarsi F, Zanzani SA, Manfredi MT, Capelli G (2014) Ticks infesting humans in Italy and associated pathogens. Parasit Vectors 7:328

    Article  PubMed  PubMed Central  Google Scholar 

  76. Över L, İnceboz T, Yapar N, Bakirci S, Günay T, Akisü Ç (2012) Investigation of the cases presenting to Dokuz Eylul University hospital with tick bites. Turkiye Parazitol Derg 36:75–81

    Article  PubMed  Google Scholar 

  77. Paksa A, Ladonni H, Nasirian H (2011) Detection of malathion and chlorpyrifos resistance mechanism in German cockroaches (Blattella germanica, Insecta: Blattodea: Blattellidae) using piperonyl butoxide and tributyl phosphorotrithioate. Bimonthly J Hormozgan Univ Med Sci 15:243–253

    CAS  Google Scholar 

  78. Paksa A, Ladonni H, Nasirian H (2012) Comparison of PBO and DEF effects on creating bendiocarb and carbaryl insecticide resistance in German cockroach. Sci J Kurd Univ Med Sci 17:91–101

    Google Scholar 

  79. Papa A, Xanthopoulou K, Kotriotsiou T, Papaioakim M, Sotiraki S, Chaligiannis I, Maltezos E (2016) Rickettsia species in human-parasitizing ticks in Greece. Trans R Soc Trop Med Hyg 110:299–304

    Article  PubMed  PubMed Central  Google Scholar 

  80. Piggott JJ, Townsend CR, Matthaei CD (2015) Climate warming and agricultural stressors interact to determine stream macroinvertebrate community dynamics. Glob Change Biol 21:1887–1906

    Article  Google Scholar 

  81. Poudat A, Nasirian H (2007) Prevalence of pediculosis and scabies in the prisoners of Bandar Abbas, Hormozgan province, Iran. Pak J Biol Sci 10:3967–3969

    Article  CAS  PubMed  Google Scholar 

  82. Ramos VN, Osava CF, Piovezan U, Szabó MP (2014) Ticks on humans in the Pantanal wetlands, Brazil. Ticks Tick-borne Dis 5:497–499

    Article  PubMed  Google Scholar 

  83. Rodríguez-Vivas RI, Apanaskevich DA, Ojeda-Chi MM, Trinidad-Martínez I, Reyes-Novelo E, Esteve-Gassent MD, Pérez de León AA (2016) Ticks collected from humans, domestic animals, and wildlife in Yucatan, Mexico. Vet Parasitol 215:106–113

    Article  PubMed  Google Scholar 

  84. Sajid MS, Kausar A, Iqbal A, Abbas H, Iqbal Z, Jones MK (2018) An insight into the ecobiology, vector significance and control of Hyalomma ticks (Acari: Ixodidae): a review. Acta Trop 187:229–239

    Article  CAS  PubMed  Google Scholar 

  85. Sanei Dehkordi A, Salim Abadi Y, Nasirian H, Hazratian T, Gorouhi MA, Yousefi S, Paksa A (2017) Synergists action of piperonyl butoxide and S, S, S-tributyl phosphorotrithioate on toxicity of carbamate insecticides against Blattella germanica. Asian Pac J Trop Med 10:981–986

    Article  CAS  PubMed  Google Scholar 

  86. Schapheer C, Sandoval G, Villagra CA (2018) Pest cockroaches may overcome environmental restriction due to anthropization. J Med Entomol. https://doi.org/10.1093/jme/tjy1090

    Article  PubMed  Google Scholar 

  87. Shayeghi M, Piazak N, Gollampuor A, Nasirian H, Abolhassani M (2016) Tick-borne relapsing fever in Sabzevar (Khorasan Razavy province), North-Eastern Iran. Bangladesh J Med Sci 15:551–555

    Article  Google Scholar 

  88. Soleimani-Ahmadi M, Nasirian H, Gheshmi AN, Ershadi MY (2009) Human extensive head skin myiasis. Iran J Public Health 38:134–138

    Google Scholar 

  89. Sutherst RW (2004) Global change and human vulnerability to vector-borne diseases. Clin Microbiol Rev 17:136–173

    Article  PubMed  PubMed Central  Google Scholar 

  90. Telmadarraiy Z, Nasirian H, Vatandoost H, Abuolhassani M, Tavakoli M, Zarei Z, Banafshi O, Rafinejad J, Salarielac S, Faghihi F (2007) Comparative susceptibility of cypermethrin in Ornithodoros lahorensis Neuman and Argas persicus Oken (Acari: Argasidae) field populations. Pak J Biol Sci 10:4315–4318

    Article  CAS  PubMed  Google Scholar 

  91. Valente JD, Silva PW, Arzua M, Barros-Battesti DM, Martins TF, Silva AM, Vieira TS, Labruna MB, Vieira RF (2020) Records of ticks (Acari: Ixodidae) on humans and distribution of spotted-fever cases and its tick vectors in Paraná State, southern Brazil. Ticks Tick-borne Dis 11:101510. https://doi.org/10.1016/j.ttbdis.102020.101510

    Article  PubMed  Google Scholar 

  92. Wilhelmsson P, Lindblom P, Fryland L, Nyman D, Jaenson TG, Forsberg P, Lindgren P-E (2013) Ixodes ricinus ticks removed from humans in Northern Europe: seasonal pattern of infestation, attachment sites and duration of feeding. Parasite Vectors 6:362

    Article  Google Scholar 

  93. Zahirnia A, Boroomand M, Nasirian H, Salehzadeh A, Soleimani-Asl S (2019) Comparing cytotoxicity of propoxur and Nepeta crispa (Lamiales: Lamiaceae) essential oil against invertebrate (Sf9) and vertebrate (L929) cell lines. Vet World 12:1698–1706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Zahirnia A, Boroomand M, Nasirian H, Soleimani-Asl S, Salehzadeh A, Dastan D (2019) The cytotoxicity of malathion and essential oil of Nepeta crispa (lamiales: lamiaceae) against vertebrate and invertebrate cell lines. Pan Af Med J 33:285. https://doi.org/10.11604/pamj.12019.11633.11285.18776

    Article  Google Scholar 

  95. Zahirnia A, Moradi A, Norozi NA, Bathaii SJN, Erfani H, Moradi A (2009) Epidemiological survey of cutaneous Leishmaniasis in Hamadan province (2002–2007). Avicenna J Clin Med 16:43–47

    Google Scholar 

  96. Zahirnia AH, Bordbar A, Ebrahimi S, Spotin A, Mohammadi S, Ghafari SM, Ahmadvand S, Jabbari N, Esmaeili Rastaghi AR, Parvizi P (2018) Predominance of Leishmania major and rare occurrence of Leishmania tropica with haplotype variability at the center of Iran. Braz J Infect Dis 22:278–287

    Article  PubMed  Google Scholar 

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This work did not receive any technical or financial support from any institution and was done by the authors at their own personal expense.

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Nasirian, H., Zahirnia, A. Detailed Infestation Spectrums About Biological Stages of Hard Ticks (Acari: Ixodida: Ixodidae) in Humans: A Systematic Review and Meta-Analysis. Acta Parasit. 66, 770–796 (2021). https://doi.org/10.1007/s11686-021-00362-y

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  • DOI: https://doi.org/10.1007/s11686-021-00362-y

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