Abstract
The rickettsial pathogen Orientia tsutsugamushi, causing scrub typhus, has been implicated as a major cause of acute encephalitis syndrome (AES) in many places in India including Gorakhpur district of Uttar Pradesh. Seasonal abundance of the principal vector mite of the pathogen, Leptotrombidium deliense, its animal hosts, and prevalence of infection on them are important attributes in the assessment of outbreaks of the disease. Hence, these aspects were investigated, seasonally, in rural villages of Gorakhpur district, where peak incidence of AES cases were reported. A total of 903 animals (rodents/shrews) was collected using 6484 Sherman traps in eight study villages (14% overall trap rate). A sum of 5526 trombiculid mites comprising 12 species was collected from 676 live rodents/shrews screened. Suncus murinus, the Asian house shrew was the predominant species (67%). Among trombiculids, the principal vector mite, L. deliense, was predominant (64.7%) and its infestation index (i.e., average number of chiggers per host animal) was 5.3. The L. deliense infestation index was higher during July to November with a peak in October. Out of 401 animal sera samples screened, 68% were positive for antibodies against O. tsutsugamushi. Of 465 blood samples tested by nested PCR, seven were positive for the 56 kDa gene of O. tsutsugamushi. In conventional PCR, 41 out of 265 samples were positive for the 60 kDa groEL gene of O. tsutsugamushi. Among the 5526 mite samples, tested as 352 pools through nested PCR, four pools were positive for 56 kDa gene. Phylogenetic analysis of 56 and 60 kDa genes confirmed circulation of Karp and TA678 (rodents) and TA678 (mite) serotypes of O. tsutsugamushi in Gorakhpur. Peak incidence of AES in Gorakhpur district occurs during the rainy season (July–October), coinciding with the peak abundance of L. deliense. These results indicate involvement of L. deliense as the vector mite transmitting the scrub typhus pathogen O. tsutsugamushi to humans in the rural areas of Gorakhpur district, India.
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References
Agarwal VC (2000) Taxonomic studies on Indian muridae and hystricidae (Mammalia: Rodentia). Records of the Zoological Survey of India, Occasional Paper No. 180, Kolkata, pp 1–177
Bal M, Mohanta MP, Sahu S et al (2019) Profile of pediatric scrub typhus in Odisha, India. Indian Pediatr 56:304–306
Bhalwar R, Tilak R, Rao M, Tilak VW (2003) Surveillance of scrub typhus in the fringe areas around Pune: potential for transmission does exist. Med J Armed Forces India 59(2):117–120. https://doi.org/10.1016/S0377-1237(03)80054-0
Bhatt GC, Bondre VP, Sapkal GN et al (2012) Changing clinico-laboratory profile of encephalitis patients in the eastern Uttar Pradesh region of India. Trop Dr 42:106–108
Bhattacharya D, Mittal V, Gupta N et al (2009) Scrub typhus and other rickettsiosis. CD Alert 13:1–8
Bhopdhornangkul B, Meeyai AC, Wongwit W, Limpanont Y, Iamsirithaworn S, Laosiritaworn Y, Tantrakarnapa K (2021) Non-linear effect of different humidity types on scrub typhus occurrence in endemic provinces Thailand. Heliyon 7:e06095. https://doi.org/10.1016/j.heliyon.2021.e06095
Burgdorfer W, Varma MGR (1967) Trans-stadial and transovarial development of disease agents in arthropods. Annu Rev Entomol 12:347–376
Candasamy S, Ayyanar E, Paily K et al (2016) Abundance & distribution of trombiculid mites & Orientia tsutsugamushi, the vectors & pathogen of scrub typhus in rodents & shrews collected from Puducherry & Tamil Nadu, India. Indian J Med Res 144:893
Chaisiri K, Gill AC, Stekolnikov AA et al (2019) Ecological and microbiological diversity of chigger mites, including vectors of scrub typhus, on small mammals across stratified habitats in Thailand. Anim Microbiome 1(1):18. https://doi.org/10.1186/s42523-019-0019-x
Davis GE, Austrian RC, Bell EJ (1947) Observations on tsutsugamushi disease (scrub typhus) in Assam and Burma. The recovery of strains of Rickettsia orientalis. Am J Hyg 46:268–286
Devine J (2003) A review of scrub typhus management in 2000–2001 and implications for soldiers. J Rural Remote Environ Health 2:14–20
Fernandes SSJ, Kulkarni SM (2003) Studies on the trombiculid mite fauna of India. Records of the Zoological Survey of India, Occasional Paper No.212, Kolkata, pp 1–539
Fletcher W, Lesslar JE, Lewthwaite R (1928) The ætiology of the tsutsugamushi disease and tropical typhus in the Federated Malay States: a preliminary note. Trans R Soc Trop Med Hyg 22:161–174
Frances SP, Watcharapichat P, Phulsuksombati D, Tanskul P (1999) Occurrence of Orientia tsutsugamushi in chiggers (Acari: Trombiculidae) and small animals in an orchard near Bangkok, Thailand. J Med Entomol 36:449–453
Heaslip WG (1941) Tsutsugamushi fever in North Queensland, Australia. Med J Aust 1:380–392
Jain P, Prakash S, Tripathi PK et al (2018) Emergence of Orientia tsutsugamushi as an important cause of acute encephalitis syndrome in India. PLoS Negl Trop Dis 12:e0006346
Kakkar M, Rogawski ET, Abbas SS et al (2013) Acute encephalitis syndrome surveillance, Kushinagar District, Uttar Pradesh, India, 2011–2012. Emerg Infect Dis 19:1361
Kalra SL (1952) Natural history of typhus fevers in India. Indian J Med Sci 6:569–575
Kelly DJ, Richards AL, Temenak J et al (2002) The past and present threat of rickettsial diseases to military medicine and international public health. Clin Infect Dis 34:S145–S169
Khan SA, Dutta P, Khan AM et al (2012) Re-emergence of scrub typhus in northeast India. Int J Infect Dis 16:e889–e890
Khan SA, Bora T, Laskar B et al (2017) Scrub typhus leading to acute encephalitis syndrome, Assam. India Emerg Infect Dis 23:148
Koh GCKW, Maude RJ, Paris DH, Newton PN, Blacksell SD (2010) Review: diagnosis of scrub typhus. Am J Trop Med Hyg 82(3):368–370
Kumar K, Saxena VK, Thomas TG, Lal S (2004) Outbreak investigation of scrub typhus in Himachal Pradesh (India). J Commun Dis 36:277–283
Lee J-H, Park H-S, Jang W-J et al (2003) Differentiation of rickettsiae by groEL gene analysis. J Clin Microbiol 41:2952–2960
Lee HI, Shim SK, Song BG et al (2011) Detection of Orientia tsutsugamushi, the causative agent of scrub typhus, in a novel mite species, Eushoengastia koreaensis, in Korea. Vector-Borne Zoonotic Dis 11:209–214
Luo L, Guo Z, Lei Z, Hu Q, Chen M, Chen F et al (2020) Epidemiology of tsutsugamushi disease and its relationship with meteorological factors in Xiamen city, China. PLoS Negl Trop Dis 14(10):e0008772. https://doi.org/10.1371/journal.pntd.0008772
Lv Y, Guo XG, Jin DC, Fan R, Zhao CF, Zhang ZW, Mao KY, Song WY, Dong WG, Qian TJ, Yang ZH (2021) Distribution and host selection of the chigger mite vector of scrub typhus, Leptotrombidium deliense, in southwest China. Int J Acarol 47(3):233–241. https://doi.org/10.1080/01647954.2021.1890210
Mehta DR (1937) Studies on typhus in the Simla Hills. Part VIII. Ectoparasites of rats and shrews with special reference to their possible rôle in the transmission of typhus. Indian J Med Res 25:353–365
Mittal M, Thangaraj JWV, Rose W et al (2017) Scrub typhus as a cause of acute encephalitis syndrome, Gorakhpur, Uttar Pradesh. India Emerg Infect Dis 23:1414
Murhekar MV, Mittal M, Prakash JAJ et al (2016) Acute encephalitis syndrome in Gorakhpur, Uttar Pradesh, India-Role of scrub typhus. J Infect 73:623–626
Narvencar KP, Rodrigues S, Nevrekar RP et al (2012) Scrub typhus in patients reporting with acute febrile illness at a tertiary health care institution in Goa. Indian J Med Res 136:1020
National Vector Borne Disease Control Programme (NVBDCP), Government of India. Annual Report 2014–15. Details of AES/JE Cases and Deaths from 2009–2015; 2015. Available from: http://www.nvbdcp.gov.in/Doc/je-aes-cd-March17.pdf. Accessed August 18 2020
Oaks JSC, Ridgway RL, Shirai A, Twartz JC 1983 Scrub typhus. United States Army Medical Research Unit, Institute for Medical Research, Malaysia; Bulletin No. 21:1–107
Olson JG, Bourgeois AL, Fang RC (1982) Population indices of chiggers (Leptotrombidium deliense) and incidence of scrub typhus in Chinese military personnel, Pescadores Islands of Taiwan. Trans R Soc Trop Med Hyg 76:85–88
Padbidri VS, Kulkarni SM, Joshi MV et al (1980) Murine rickettsiosis along the Western Ghats of Maharashtra State, India. Indian J Med Res 71:721–724
Park S-W, Ha N-Y, Ryu B et al (2015) Urbanization of scrub typhus disease in South Korea. PLoS Negl Trop Dis 9:e0003814
Rahelinirina S, Rajerison M, Telfer S, Savin C, Carniel E, Duplantier JM (2017) The Asian house shrew Suncus murinus as a reservoir and source of human outbreaks of plague in Madagascar. PLoS Negl Trop Dis 11(11):e0006072. https://doi.org/10.1371/journal.pntd.0006072 (PMID:29155827;PMCID:PMC5714386)
Ramyasree A, Kalawat U, Rani N, Chaudhury A (2015) Seroprevalence of Scrub typhus at a tertiary care hospital in Andhra Pradesh. Indian J Med Microbiol 33:68
Ranjan P, Gore M, Selvaraju S et al (2014) Changes in acute encephalitis syndrome incidence after introduction of Japanese encephalitis vaccine in a region of India. J Infect 69:200–202
Rapmund G (1984) Rickettsial diseases of the Far East: new perspectives. The University of Chicago Press, Chicago
Rodkvamtook W, Gaywee J, Kanjanavanit S et al (2013) Scrub typhus outbreak, northern Thailand, 2006–2007. Emerg Infect Dis 19:774
Rose W, Kang G, Verghese VP et al (2019) Risk factors for acquisition of scrub typhus in children admitted to a tertiary centre and its surrounding districts in South India: a case control study. BMC Infect Dis 19:1–8
Sadanandane C, Jambulingam P, Paily KP et al (2018) Occurrence of Orientia tsutsugamushi, the etiological agent of scrub typhus in animal hosts and mite vectors in areas reporting human cases of acute encephalitis syndrome in the Gorakhpur region of Uttar Pradesh, India. Vector-Borne Zoonotic Dis 18:539–547
Sankhyan N, Saptharishi LG, Sasidaran K et al (2014) Clinical profile of scrub typhus in children and its association with hemophagocytic lymphohistiocytosis. Indian Pediatr 51:651–653
Saxena VK (1983) On the presence of Leptotrombidium (L) deliense in district Bastar, Madhya Pradesh. J Commun Dis 15:290–291
Saxena VK (1989) Chigger mite infestation of small mammals in a feral biotope of a public park area of South Delhi. J Commun Dis 21:360–364
Sethi S, Prasad A, Biswal M et al (2014) Outbreak of scrub typhus in North India: a re-emerging epidemic. Trop Dr 44:156–159
Sharma AK (2013) Eco-entomological investigation in scrub typhus affected area of Thiruvananthapuram, Kerala (India) and their control/containment measures. Int J Curr Microbiol Appl Sci 2:43–49
Sharma AK, Kumar K (2014) Entomological surveillance for rodent and their ectoparasites with special reference to potential of scrub typhus at Kolkata Port Trust (KPT), Kolkata (India). Arch Adv Biosci 5:2–6
Sharma PK, Ramakrishnan R, Hutin YJF et al (2009) Scrub typhus in Darjeeling, India: opportunities for simple, practical prevention measures. Trans R Soc Trop Med Hyg 103:1153–1158
Sharma N, Biswal M, Kumar A et al (2016) Scrub typhus in a tertiary care hospital in North India. Am J Trop Med Hyg 95:447–451
Sinha P, Gupta S, Dawra R, Rijhawan P (2014) Recent outbreak of scrub typhus in North Western part of India. Indian J Med Microbiol 32:247
Steele JH, Stoenner H, Kaplan W, Torten M (1980) CRC handbook series in zoonoses. Sect A: bacterial, rickettsial, and mycotic diseases. CRC Press, Boca Raton
Stephen S, Sangeetha B, Ambroise S et al (2015) Outbreak of scrub typhus in Puducherry & Tamil Nadu during cooler months. Indian J Med Res 142:591
Tilak R, Kunwar R, Wankhade UB, Tilak VW (2011) Emergence of Schoengastiella ligula as the vector of scrub typhus outbreak in Darjeeling: has Leptotrombidium deliense been replaced? Indian J Public Health 55:92
Varghese GM, Raj D, Francis MR et al (2016) Epidemiology & risk factors of scrub typhus in south India. Indian J Med Res 144:76
Varma RN (1969) Prevalence of Leptotrombidium deliense, the scrub typhus vector, in the eastern Himalayas. Nature 222:984–985
Varma RN, Mahadevan B (1973) The bionomics and vector potential of the scrub typhus vector Leptotrombidium (L.) deliense and other trom-biculid populations in Eastern Himalayas, India. Indian J Med Sci 27:900–919
Vivekanandan M, Mani A, Priya YS et al (2010) Outbreak of scrub typhus in Pondicherry. J Assoc Physicians India 58:24–28
Walker DH (2016) Scrub typhus-scientific neglect, ever-widening impact. N Engl J Med 375:913–915
Wangrangsimakul T, Elliott I, Nedsuwan S, Kumlert R, Hinjoy S, Chaisiri K et al (2020) The estimated burden of scrub typhus in Thailand from national surveillance data (2003–2018). PLoS Negl Trop Dis 14(4):e0008233. https://doi.org/10.1371/journal.pntd.0008233
Watt G, Parola P (2003) Scrub typhus and tropical rickettsioses. Curr Opin Infect Dis 16:429–436
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This work was supported by Indian Council of Medical Research (IN), Ministry of Health and Family Welfare, Government of India.
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Sadanandane, C., Elango, A., Panneer, D. et al. Seasonal abundance of Leptotrombidium deliense, the vector of scrub typhus, in areas reporting acute encephalitis syndrome in Gorakhpur district, Uttar Pradesh, India. Exp Appl Acarol 84, 795–808 (2021). https://doi.org/10.1007/s10493-021-00650-2
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DOI: https://doi.org/10.1007/s10493-021-00650-2