{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,18]],"date-time":"2025-11-18T03:32:30Z","timestamp":1763436750625,"version":"3.37.3"},"reference-count":48,"publisher":"Oxford University Press (OUP)","issue":"9","license":[{"start":{"date-parts":[[2022,4,23]],"date-time":"2022-04-23T00:00:00Z","timestamp":1650672000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,9,10]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background<\/jats:title>\n                  <jats:p>Sand flies are of considerable public health importance in Pakistan because these insects are vectors of leishmaniasis. The current study explores the bionomics of sand flies, their spatial distribution pattern and cutaneous leishmaniasis-associated risk factors in District Mohmand, Khyber Pakhtunkhwa, Pakistan.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>Sand flies were collected from indoor and outdoor habitats in 69 villages of five tehsils in Mohmand during July\u2013October 2019. Risk factor data were recorded for 829 households in 94 villages.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>In total, 2065 sand flies were captured. Phlebotomus (Paraphlebotbmus) sergenti was the most abundant species. Relative density for P. sergenti and Phlebotomus papatasi was highest in Prang Ghar and lowest in Safi. Sand flies abundance peaked in August and September, corresponding to maximum relative humidity, temperature and rainfall. Relative density for P. sergenti and P. papatasi was highest in combined dwellings (indoor) and cattle corrals (outdoor). Phlebotomus sergenti and P. papatasi were abundant at an elevation of 283\u20131140 m on agricultural land and rangelands. Both species were recorded abundantly on Carbontites, Mesozoic and Indus suture Melange rock formations. Presence of domestic animals, ownership of pet dogs, presence of muddy dunes in the village, knowledge of sandflies and use of mosquitoes spray remained significant risk factors.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>The study reports sand fly bionomics in District Mohmand. Risk identified for cutaneous leishmaniasis are significant in strategising control methods for Health authorities can allocate localized control means to high-risk areas using these findings.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/trstmh\/trac025","type":"journal-article","created":{"date-parts":[[2022,3,21]],"date-time":"2022-03-21T12:14:54Z","timestamp":1647864894000},"page":"832-844","source":"Crossref","is-referenced-by-count":3,"title":["Bionomics of the unexplored sand flies fauna of District Mohmand, Khyber Pakhtunkhwa, Pakistan: assessing risk factors associated with cutaneous leishmaniasis"],"prefix":"10.1093","volume":"116","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5377-104X","authenticated-orcid":false,"given":"Khurshaid","family":"Khan","sequence":"first","affiliation":[{"name":"Department of Zoology, Abdul Wali Khan University Mardan , Mardan, 23200, Khyber Pakhtunkhwa, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Muhammad","family":"Sajjad","sequence":"additional","affiliation":[{"name":"Department of Zoology, Abdul Wali Khan University Mardan , Mardan, 23200, Khyber Pakhtunkhwa, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sobia","family":"Wahid","sequence":"additional","affiliation":[{"name":"Department of Zoology, University of Peshawar , Peshawar, 25120, Khyber Pakhtunkhwa, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Muhammad","family":"Gul","sequence":"additional","affiliation":[{"name":"Department of Zoology, Abdul Wali Khan University Mardan , Mardan, 23200, Khyber Pakhtunkhwa, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Luqman","family":"Khan","sequence":"additional","affiliation":[{"name":"Department of Zoology, Abdul Wali Khan University Mardan , Mardan, 23200, Khyber Pakhtunkhwa, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Haseen","family":"Ullah","sequence":"additional","affiliation":[{"name":"Department of Zoology, Abdul Wali Khan University Mardan , Mardan, 23200, Khyber Pakhtunkhwa, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yasin","family":"Rahman","sequence":"additional","affiliation":[{"name":"Department of Zoology, Abdul Wali Khan University Mardan , Mardan, 23200, Khyber Pakhtunkhwa, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dawood","family":"Khan","sequence":"additional","affiliation":[{"name":"Department of Zoology, Abdul Wali Khan University Mardan , Mardan, 23200, Khyber Pakhtunkhwa, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kashif","family":"Khan","sequence":"additional","affiliation":[{"name":"Department of Zoology, Abdul Wali Khan University Mardan , Mardan, 23200, Khyber Pakhtunkhwa, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Muhammad Younas","family":"Khan","sequence":"additional","affiliation":[{"name":"Department of Zoology, Abdul Wali Khan University Mardan , Mardan, 23200, Khyber Pakhtunkhwa, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Saqib","family":"Khan","sequence":"additional","affiliation":[{"name":"Department of Zoology, Abdul Wali Khan University Mardan , Mardan, 23200, Khyber Pakhtunkhwa, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Safeer Ullah","family":"Shah","sequence":"additional","affiliation":[{"name":"National Centre of Excellence in Geology University of Peshawar , Peshawar, 25120, Khyber Pakhtunkhwa, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2022,4,23]]},"reference":[{"issue":"2","key":"2022091101234686100_bib1","doi-asserted-by":"crossref","first-page":"e0192236","DOI":"10.1371\/journal.pone.0192236","article-title":"Risk factors for anthroponotic cutaneous leishmaniasis in unresponsive and responsive patients in a major focus, southeast of Iran","volume":"13","author":"Bamorovat","year":"2018","journal-title":"PloS One"},{"issue":"3","key":"2022091101234686100_bib2","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/j.actatropica.2010.08.013","article-title":"Phlebotomine sand fly population dynamics in a leishmaniasis endemic peri-urban area in southern Italy","volume":"116","author":"Tarallo","year":"2010","journal-title":"Acta Trop"},{"key":"2022091101234686100_bib3","first-page":"2","article-title":"A review on biology. Epidemiology and public health significance of leishmaniasis","volume":"4","author":"Dawit","year":"2013","journal-title":"J Bacteriol Parasitol"},{"issue":"10","key":"2022091101234686100_bib4","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1016\/j.apjtm.2016.06.021","article-title":"Worldwide risk factors in leishmaniasis","volume":"9","author":"Oryan","year":"2016","journal-title":"Asian Pacific J Trop Med"},{"issue":"5","key":"2022091101234686100_bib5","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1016\/j.cimid.2004.03.004","article-title":"Leishmaniasis: current situation and new perspectives","volume":"27","author":"Desjeux","year":"2004","journal-title":"Comp Immunol Microbiol Infect Dis"},{"issue":"5","key":"2022091101234686100_bib6","doi-asserted-by":"crossref","first-page":"966","DOI":"10.3201\/eid1005.030894","article-title":"Cutaneous leishmaniasis, northern Afghanistan","volume":"10","author":"Reithinger","year":"2004","journal-title":"Emerg Infect Dis"},{"issue":"9","key":"2022091101234686100_bib7","doi-asserted-by":"crossref","first-page":"2848","DOI":"10.1128\/JCM.00951-08","article-title":"Molecular diagnosis of old world cutaneous leishmaniasis and species identification by use of a reverse line blot hybridization assay","volume":"46","author":"Nasereddin","year":"2008","journal-title":"J Clin Microbiol"},{"issue":"2","key":"2022091101234686100_bib8","doi-asserted-by":"crossref","first-page":"261","DOI":"10.4269\/ajtmh.2006.75.261","article-title":"Multilocus enzyme electrophoresis and cytochrome b gene sequencing\u2013based identification of leishmania isolates from different foci of cutaneous leishmaniasis in Pakistan","volume":"75","author":"Marco","year":"2006","journal-title":"Am J Trop Med Hyg"},{"article-title":"Leishmaniasis: status of endemicity of cutaneous leishmaniasis","year":"2020","author":"WHO","key":"2022091101234686100_bib9"},{"issue":"2","key":"2022091101234686100_bib10","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/S0035-9203(99)90285-7","article-title":"An outbreak of cutaneous leishmaniasis in an Afghan refugee settlement in north-west Pakistan","volume":"93","author":"Rowland","year":"1999","journal-title":"Trans Royal Soc Trop Med Hyg"},{"issue":"1","key":"2022091101234686100_bib11","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/0035-9203(95)90644-4","article-title":"Leishmania infantum in the Himalayas","volume":"89","author":"Rab","year":"1995","journal-title":"Trans Royal Soc Trop Med Hyg"},{"key":"2022091101234686100_bib12","first-page":"7981","article-title":"Characterization of a leishmania tropica antigen that detects immune responses in desert storm viscerotropic leishmaniasis patients","volume-title":"Proc Nat Acad Sci","author":"Dillon","year":"1995"},{"key":"2022091101234686100_bib13","first-page":"425","article-title":"Natural and experimental evidence of viscerotropic infection caused by leishmania tropica from north Sinai, Egypt","volume":"44","author":"Doha","year":"2014","journal-title":"J Egypt Soc Parasitol"},{"issue":"9","key":"2022091101234686100_bib14","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1001\/archdermatol.2009.181","article-title":"Leishmania tropica\u2013induced cutaneous and presumptive concomitant viscerotropic leishmaniasis with prolonged incubation","volume":"145","author":"Weiss","year":"2009","journal-title":"Arch Dermatol"},{"issue":"5-6","key":"2022091101234686100_bib15","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1016\/j.ijmm.2007.07.015","article-title":"Zoonotic cutaneous leishmaniasis outbreak in Mazar-e Sharif, northern Afghanistan: an epidemiological evaluation","volume":"298","author":"Faulde","year":"2008","journal-title":"Int J Med Microbiol"},{"issue":"1","key":"2022091101234686100_bib16","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1111\/jvec.12200","article-title":"Spatial distribution of sand fly species (Psychodidae: phlebtominae), ecological niche, and climatic regionalization in zoonotic foci of cutaneous leishmaniasis, southwest of Iran","volume":"41","author":"Ebrahimi","year":"2016","journal-title":"J Vector Ecol"},{"issue":"7","key":"2022091101234686100_bib17","doi-asserted-by":"crossref","first-page":"850","DOI":"10.1590\/S0074-02762010000700002","article-title":"Bionomics of phlebotomine sand flies (Diptera: psychodidae) in the province of Al-Baha, Saudi Arabia","volume":"105","author":"Doha","year":"2010","journal-title":"Mem\u00f3rias do Instituto Oswaldo Cruz"},{"issue":"5","key":"2022091101234686100_bib18","doi-asserted-by":"crossref","first-page":"1432","DOI":"10.1093\/jme\/tjaa050","article-title":"Sand fly (Diptera: psychodidae) species diversity, habitat preferences, and ecological aspects of distribution in Bajaur District, Khyber Pakhtunkhwa, Pakistan","volume":"57","author":"Wahid","year":"2020","journal-title":"J Med Entomol"},{"issue":"5","key":"2022091101234686100_bib19","doi-asserted-by":"crossref","first-page":"1390","DOI":"10.1093\/jme\/tjx098","article-title":"Potential resting and breeding sites of sand flies (Diptera: psychodidae) and their habitat characteristics in leishmaniasis foci of Dir districts, Khyber Pakhtunkhwa, Pakistan","volume":"54","author":"Khan","year":"2017","journal-title":"J Med Entomol"},{"key":"2022091101234686100_bib20","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.actatropica.2016.01.011","article-title":"Species composition and activity patterns of sand flies (Psycodidae: phlebotomine) in four tehsils of Dir districts, Khyber Pakhtunkhwa, Pakistan","volume":"156","author":"Ali","year":"2016","journal-title":"Acta Trop"},{"issue":"3","key":"2022091101234686100_bib21","doi-asserted-by":"crossref","first-page":"626","DOI":"10.1093\/jme\/tjx246","article-title":"Geospatial and climatic patterns associated with the distribution of sand fly (Diptera: psychodidae) vectors of leishmaniasis in Pakistan","volume":"55","author":"Khan","year":"2018","journal-title":"J Med Entomol"},{"key":"2022091101234686100_bib22","first-page":"1","volume-title":"A brief introduction to leishmaniasis epidemiology. The leishmaniases: old neglected tropical diseases","author":"Gradoni","year":"2018"},{"key":"2022091101234686100_bib23","first-page":"72","article-title":"The frequency of old world cutaneous leishmaniasis in skin ulcers in Peshawar","volume":"21","author":"Rahman","year":"2009","journal-title":"J Ayub Med College Abbottabad"},{"issue":"3","key":"2022091101234686100_bib24","doi-asserted-by":"crossref","first-page":"e639","DOI":"10.1371\/journal.pntd.0000639","article-title":"Risk factors for anthroponotic cutaneous leishmaniasis at the household level in Kabul","volume":"4","author":"Reithinger","year":"2010","journal-title":"Afghanistan. PLoS Negl Trop Dis"},{"key":"2022091101234686100_bib25","first-page":"1681","article-title":"Leishmaniasis in refugee and local Pakistani populations","volume-title":"Emerging Infectious Diseases","author":"Brooker","year":"2004"},{"article-title":"The only option for cutaneous leishmaniasis treatment in Khyber Pakhtunkhwa","year":"2019","author":"Fronteres","key":"2022091101234686100_bib26"},{"key":"2022091101234686100_bib27","first-page":"9","article-title":"Disease mapping and risk assessment in veterinary parasitology: some case studies","volume":"47","author":"Cringoli","year":"2005","journal-title":"Parassitologia"},{"key":"2022091101234686100_bib28","first-page":"109","article-title":"Improments and techniques of mounting adult sand flies (Phlebotomine) for identification","volume":"43","author":"Aslamkhan","year":"2000","journal-title":"Boilogia"},{"key":"2022091101234686100_bib29","first-page":"217","article-title":"The phlebotomine sand flies (Diptera, psychodidae) of the Oriental region","volume":"37","author":"Lewis","year":"1978","journal-title":"Bull Brit Mus Nat Hist"},{"key":"2022091101234686100_bib30","first-page":"328","article-title":"Sandflies (D\u00edptera, psychodida\u00e9, phlebotominae) of eastern Afghanistan. Communication II. The genus sergentomyia, subgenus sergentomyia","volume":"43","author":"Artemiev","year":"1974","journal-title":"Meditsinskaya Parazitologiya i Parazitarnye Bolezni"},{"article-title":"Geological map of north Pakistan, 1: 650,000","year":"1996","author":"Searle","key":"2022091101234686100_bib31"},{"key":"2022091101234686100_bib32","article-title":"Control of the leishmaniases","author":"WHO","year":"2010","journal-title":"World Health Organization technical report series"},{"issue":"2","key":"2022091101234686100_bib33","doi-asserted-by":"crossref","first-page":"327","DOI":"10.2754\/avb200978020327","article-title":"Activity patterns of sand fly (Diptera: psychodidae) species and comparative performance of different traps in an endemic cutaneous leishmaniasis focus in Cukurova Plain, Southern Anatolia, Turkey","volume":"78","author":"Kasap","year":"2009","journal-title":"Acta Veterinaria Brno"},{"key":"2022091101234686100_bib34","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1756-3305-3-10","article-title":"Natural infection of the sand fly phlebotomus kazeruni by trypanosoma species in Pakistan","volume":"3","author":"Kato","year":"2010","journal-title":"Parasite Vector"},{"key":"2022091101234686100_bib35","first-page":"611","article-title":"Leishmaniasis in Pak-Afghan region","volume":"13","author":"Kakarsulemankhel","year":"2011","journal-title":"Int J Agric Biol"},{"issue":"5","key":"2022091101234686100_bib36","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1016\/0035-9203(94)90142-2","article-title":"The isolation of leishmania major from phlebotomus (Paraphlebotomus) caucasicus, in Isfahan Province, Islamic Republic of Iran","volume":"88","author":"Yaghoobi-Ershadi","year":"1994","journal-title":"Trans Royal Soc Trop Med Hyg"},{"issue":"4","key":"2022091101234686100_bib37","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/0001-706X(95)92834-3","article-title":"Leishmania major MON-26 isolated from naturally infected phlebotomus papatasi (Diptera: psychodidae) in Isfahan Province","volume":"59","author":"Yaghoobi-Ershadi","year":"1995","journal-title":"Iran. Acta Trop"},{"key":"2022091101234686100_bib38","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1111\/j.1365-3156.2008.02121.x","article-title":"Nested PCRs and sequencing of nuclear ITS-rDNA fragments detect three leishmania species of gerbils in sandflies from Iranian foci of zoonotic cutaneous leishmaniasis","volume":"13","author":"Parvizi","year":"2008","journal-title":"Trop Med Int Health"},{"issue":"5","key":"2022091101234686100_bib39","first-page":"1581","article-title":"First report of sand fly (Diptera: psycodidae: phlebotomine) immature males and various reproductive stages of females in upper and lower Dir districts, Khyber Pakhtunkhwa, Pakistan","volume":"48","author":"Khan","year":"2016","journal-title":"Pakistan J Zoology"},{"key":"2022091101234686100_bib40","doi-asserted-by":"crossref","first-page":"105147","DOI":"10.1016\/j.actatropica.2019.105147","article-title":"Habitat characterization of sand fly vectors of leishmaniasis in Khyber Pakhtunkhwa, Pakistan","volume":"199","author":"Khan","year":"2019","journal-title":"Acta Trop"},{"issue":"1","key":"2022091101234686100_bib41","doi-asserted-by":"crossref","first-page":"193","DOI":"10.4081\/gh.2014.16","article-title":"Ecological niche model of phlebotomus perniciosus, the main vector of canine leishmaniasis in north-eastern Italy","volume":"9","author":"Signorini","year":"2014","journal-title":"Geospatial Health"},{"issue":"1","key":"2022091101234686100_bib42","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.actatropica.2003.09.021","article-title":"Mapping the potential distribution of phlebotomus martini and p. orientalis (Diptera: psychodidae), vectors of kala-azar in East Africa by use of geographic information systems","volume":"90","author":"Gebre-Michael","year":"2004","journal-title":"Acta Trop"},{"issue":"2","key":"2022091101234686100_bib43","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1016\/S0035-9203(03)90111-8","article-title":"The prolonged epidemic of anthroponotic cutaneous leishmaniasis in Kabul, Afghanistan: bringing down the neighbourhood","volume":"97","author":"Reyburn","year":"2003","journal-title":"Trans Royal Soc Trop Med Hyg"},{"issue":"5","key":"2022091101234686100_bib44","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1645\/15-919","article-title":"Assessing incidence patterns and risk factors for cutaneous leishmaniasis in Peshawar region, Khyber Pakhtunkhwa, Pakistan","volume":"102","author":"Ullah","year":"2016","journal-title":"J Parasitol"},{"issue":"6","key":"2022091101234686100_bib45","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1016\/0035-9203(95)90409-3","article-title":"The role of dogs in the epidemiology of human visceral leishmaniasis in northern Pakistan","volume":"89","author":"Rab","year":"1995","journal-title":"Trans Royal Soc Trop Med Hyg"},{"key":"2022091101234686100_bib46","first-page":"5","article-title":"Kaal daana (cutaneous leishmaniasis) in south-west Pakistan: a preliminary study","volume":"28","author":"Kakarsulemankhel","year":"2004","journal-title":"T\u00fcrkiye Parazitoloji Dergisi"},{"key":"2022091101234686100_bib47","first-page":"134","article-title":"Cutaneous leishmaniasis in Baluchistan: reservoir host and sandfly vector in Uthal, Lasbella","volume":"36","author":"Rab","year":"1986","journal-title":"J Pak Med Assoc"},{"issue":"5","key":"2022091101234686100_bib48","doi-asserted-by":"crossref","first-page":"1106","DOI":"10.4269\/ajtmh.16-0343","article-title":"Cutaneous leishmaniasis in Khyber Pakhtunkhwa province of Pakistan: clinical diversity and species-level diagnosis","volume":"95","author":"Khan","year":"2016","journal-title":"Am J Trop Med Hyg"}],"container-title":["Transactions of The Royal Society of Tropical Medicine and Hygiene"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/trstmh\/article-pdf\/116\/9\/832\/45788072\/trac025.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/trstmh\/article-pdf\/116\/9\/832\/45788072\/trac025.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,11]],"date-time":"2022-09-11T01:25:05Z","timestamp":1662859505000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/trstmh\/article\/116\/9\/832\/6573291"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,23]]},"references-count":48,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,4,23]]},"published-print":{"date-parts":[[2022,9,10]]}},"URL":"https:\/\/doi.org\/10.1093\/trstmh\/trac025","relation":{},"ISSN":["0035-9203","1878-3503"],"issn-type":[{"type":"print","value":"0035-9203"},{"type":"electronic","value":"1878-3503"}],"subject":[],"published-other":{"date-parts":[[2022,9]]},"published":{"date-parts":[[2022,4,23]]}}}