|DR. S D GAUR MEMORIAL AWARD FOR ENVIRONMENT BASED ORIGINAL RESEARCH ARTICLE
|Year : 2017 | Volume
| Issue : 3 | Page : 174-181
Zoonotic surveillance for rickettsiae in rodents and mapping of vectors of rickettsial diseases in India: A multi-centric study
Rina Tilak1, Rajesh Kunwar2, PK Tyagi3, Anurag Khera4, RK Joshi4, Urmila B Wankhade5
1 Scientist “G”, Department of Community Medicine, Armed Forces Medical College, Pune, Maharashtra, India
2 Epidemiologist, AFMS, Pune, Maharashtra, India
3 Public Health Specialist, AFMS, Pune, Maharashtra, India
4 Reader, Department of Community Medicine, Armed Forces Medical College, Pune, Maharashtra, India
5 Junior Scientific Assistant, Department of Community Medicine, Armed Forces Medical College, Pune, Maharashtra, India
|Date of Web Publication||15-Sep-2017|
Department of Community Medicine, Armed Forces Medical College, Sholapur Road, Wanowrie, Pune - 411 040, Maharashtra
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Background: The global resurgence of rickettsial diseases and their potential to impact the fitness of military personnel and inflict widespread casualties amongst civil populations has emerged as a major cause of public health concern. Absence of surveillance system, lack of awareness amongst medical fraternity to rickettsial activity along with the difficulty in diagnosis because of their protean clinical manifestations are reasons for the outbreaks of these diseases. Objectives: To determine rickettsial activity amongst rodents and study vector diversity, abundance and their distribution to enable mapping of rickettsial hotspots. Methods: Zoonotic surveillance was undertaken in six selected study areas in India - Jammu, Akhnoor, Rajouri-Poonch, Udhampur-Nagrota, Dehradun and Pune. Weil–Felix test was used for rickettsial sero-surveillance amongst rodents and standard identification keys were used for mapping vector diversity and database preparation. Results: Serological findings revealed positivity to all the three rickettsial antigens (OXK, OX19 and OX2) in Jammu, OX19 in Dehradun and OXK and OX2 positivity in Udhampur-Nagrota belt. The vector database records presence of 16 species of trombiculid mites from three important genera - Leptotrombidium, Schoengastiella and Gahrliepia with ticks from five genera and 8 species of fleas from four genera. Mite fauna of study sites has been enriched with addition of new records of mite species (five mite species at Pune, two at Akhnoor with one mite species each at Jammu and Dehradun). Conclusion: The study reveals rickettsial activity amongst rodents at Jammu, Dehradun and Udhampur-Nagrota belt. The results correlate well with the presence of vectors of scrub and tick typhus and corroborate the occurrence of outbreaks of these diseases in the respective areas.
Keywords: Rickettsial diseases, rickettsial sero-surveillance, scrub typhus, tick typhus, vector mapping
|How to cite this article:|
Tilak R, Kunwar R, Tyagi P K, Khera A, Joshi R K, Wankhade UB. Zoonotic surveillance for rickettsiae in rodents and mapping of vectors of rickettsial diseases in India: A multi-centric study. Indian J Public Health 2017;61:174-81
|How to cite this URL:|
Tilak R, Kunwar R, Tyagi P K, Khera A, Joshi R K, Wankhade UB. Zoonotic surveillance for rickettsiae in rodents and mapping of vectors of rickettsial diseases in India: A multi-centric study. Indian J Public Health [serial online] 2017 [cited 2020 Apr 5];61:174-81. Available from: http://www.ijph.in/text.asp?2017/61/3/174/214811
| Introduction|| |
One of the most notable diseases affecting troops which had a higher mortality rate than any other infectious disease in World War II in the China-Burma-India area of operations was the rickettsial disease - scrub typhus. During the war, scrub typhus left a trail of sick soldiers in all the areas where allied soldiers were sent to contest the advances of the Japanese Army and in some areas, more than one of every four men died due to the disease.
Scrub typhus has a world-wide distribution with special activity over a triangular area bound by Japan in the East, India in the West and Australia in the South. The disease is endemic in Asia and remains an important public health problem.,,, In India, scrub typhus came into prominence as a war disease especially in the eastern regions and thereafter a series of outbreaks were reported from various parts of the country,,,,,,, as also from the Armed Forces.,,,,, The Armed Forces personnel are at special risk of contracting scrub typhus due to exigencies of services, when the troops are deployed in the mite endemic areas for exercise or during war.
Worldwide, ticks are one of the primary vectors of human disease, second only to mosquitoes. The presence of tick borne rickettsioses in Southern India, Maharashtra and in the Himalayan belt has been well documented.,,, The outbreak of tick typhus in Himachal Pradesh has brought into sharp focus the existence of Indian tick typhus in this region of India., Tick borne rickettsioses are undoubtedly a re-emerging entity and the Indian medical fraternity needs to consider its widespread presence and potential to cause outbreaks in hitherto naïve areas.
The study was planned to determine rickettsial activity amongst rodents and study the trombiculid mite, tick and flea diversity, abundance and their distribution in selected study areas to enable mapping of rickettsial hotspots.
| Materials and Methods|| |
Place of study
The study was conducted in six selected areas of India viz., Pune, Dehradun, Akhnoor, Jammu, Udhampur-Nagrota belt and Rajouri-Poonch sector. These areas were selected keeping in mind their reported endemicity for rickettsial diseases in the past or reported outbreaks of mite/tick borne diseases in the last decade.
The vectors targeted in the present study were the trombiculid mites, ticks and fleas-the known vectors of the common rickettsial diseases prevalent in India viz., scrub, tick and endemic typhus.
Live rodent capture and processing
The rodent surveys were undertaken in mite active seasons, i.e., immediately after monsoons (September–October) and late winter (February–March). Live rodent capture was undertaken using Sherman traps in forested/camp/fringe areas, whereas Wonder traps were used in peri-domestic areas. The duly numbered and tagged baited traps were laid in suspected mite islands before dusk and retrieved before dawn for laboratory processing. Each rodent was anaesthetized and blood collected by direct heart puncture method for serological studies.
The rodents were subjected to ectoparasite screening in the following order and all samples transported to nodal centre Pune for identification and preparation of vector database:
- Flea: Using a flea comb, the fleas were sampled and placed in 70% alcohol vials for identification
- Tick: The rodent was checked for tick infestation on the ear, tail, and anal area and skin underneath the fur. If found infested, the tick was removed and immediately transferred to 70% alcohol vial for subsequent identification using standard keys for genera
- Mite: The rodent/shrew ear and rump were examined for mite attachment under stereomicroscope. If found positive, the ear pinna and rump skin was cut and transferred to alcohol vial. If the number of mites sampled from a rodent was <50, all mites were mounted in Hoyer's media or else if number exceeded 50, only 10% of the mites were mounted for identification. The mites were identified using phase contrast microscope following the standard key as given in “trombiculids of India” by Stan Fernandez.
The sera samples were subjected to serological testing by Weil–Felix procedure. The test was performed at the respective study sites; duplicate sera samples (10% of the total sera samples) were sent to Pune for standardization of testing procedure and confirmation of result.
| Results|| |
Trap positivity and Rodent infestation rate
A total of 397 rodents were trapped from all the study sites. The trap positivity ranged from 6.7 to 19.02, with the highest recorded at Pune and lowest at Udhampur-Nagrota [Table 1]. The rodent infestation rate was, however, highest in Jammu (50%) followed by Pune with nearly 34% of the trapped rodents positive for ectoparasites. The rodents trapped from Udhampur-Nagrota and Rajouri-Poonch sector were found free of tick, mite or any other ectoparasite infestation.
|Table 1: Ectoparasite diversity, composition and abundance in study areas|
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The various ectoparasite indices are presented in [Table 1]. The overall chigger infestation rate was 9.57%, with maximum at Pune (23.28%). A very high chigger index of 180.74 was recorded at Pune with chigger indices of 33, 17 and 3 recorded at Dehradun, Jammu and Akhnoor respectively. The highest flea index of 0.28 was recorded from Jammu and also maximum tick collections were made from Jammu, with a tick infestation rate of 40%. Dehradun and Pune recorded 12.84 and 13.79% tick infestation rate respectively with no ectoparasites collected from the rodents at Akhnoor, Udhampur-Nagrota and Rajouri-Poonch.
Ectoparasite diversity and composition
All captured rodents in Akhnoor were found majorly infested with mites, whereas the other three study areas viz., Pune, Dehradun and Jammu were found to be rich in ectoparasite diversity with infestation ranging from trombiculid mites to ticks and fleas [Table 1].
The maximum collection of trombiculid mites was from Pune which contributed nearly 97% of the total mite infestation. Jammu recorded the second highest yield of trombiculid mites, which was as low as about 2% of the total mite collection, whereas all the rodents trapped at Akhnoor were found to be infested with trombiculid mites with just one flea specimen.
Trombiculid mite abundance and distribution
The mite species abundance and distribution was found to be unique to each study area. The trombiculid mites sampled were further grouped as Trombiculinae (Leptotrombidium species) or Gahrliepiinae (other than Leptotrombidium viz. Schoengastiella, Gahrliepia etc.). All the trombiculid mites from Akhnoor as well as a high percentage (84.1%) of mites collected at Jammu and Pune (70.9%) were Gahrliepiinae making Gahrliepiinae the most abundant trombiculid mite distributed in our country. Dehradun however recorded maximum collection (90.5%) of Trombiculinae amongst the mites collected at Dehradun.
Trombiculid mite diversity
The trombiculid mites were identified and database was prepared for the study areas. Trombiculid mites were recorded from only four out of the six study areas. The trombiculid mite species diversity and abundance at the study areas is presented as under:
Pune recorded a total of five trombiculinae species with six from Schoengastiella and one species of Gahrliepia [Figure 1]. The most abundant trombiculid mite species from Pune were Schoengastiella species, with Leptotrombidium sinhgarhense being the next abundant species amongst the Leptotrombidium genus followed by Leptotrombidium kulkarnii. Amongst Schoengastiella species, Schoengastiella ceylonica was the most abundant constituting 28.27% of the mites with Schoengastiella ligula comprising about 22% of the total collection.
|Figure 1: Trombiculid mite diversity and abundance at Pune. *G - Gahrliepia, S - Schoengastiella, L – Leptotrombidium.|
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A total of three trombiculid mites species were recorded from Dehradun as presented in [Figure 2], with the most abundant being Leptotrombidium spiletti (83%) followed by S. ligula, which constituted about 13% of the total collection.
|Figure 2: Trombiculid mite diversity and abundance at Dehradun. *S - Schoengastiella, L - Leptotrombidium.|
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The trombiculid mite species diversity of Jammu is presented in [Figure 3]. The presence of mite vector, Leptotrombidium deliense at Jammu is an important finding and needs to be discussed in conjunction with presence of rickettsial activity in the area as it is one of the most important vectors of scrub typhus the world over. Schoengastiella species were the most abundant and constituted about 80% of the total mite collection.
|Figure 3: Trombiculid mite diversity and abundance at Jammu. *S - Schoengastiella, L – Leptotrombidium.|
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The trombiculid mites from Akhnoor were essentially Schoengastiella species. The species of Schoengastiella recorded were ligula and uttarkashiensis with Schoengastiella uttarkashiensis being the most abundant (92.31%).
New records of mite species in study areas
The study results have enriched the mite fauna diversity of the study areas with new records of species. The results are presented as [Table 2]. As per the existing database of trombiculid mites of India, two Leptotrombidium species have been added to the mite database of Pune viz., Leptotrombidium bhattipadense and tithwalense whereas Leptotrombidium spilletti has been added to trombiculid mite database of Dehradun. A total of five Schoengastiella species have also been added new to the existing mite database of the study areas with three at Pune (S. uttarkashiensis, Schoengastiella homunguis, and Schoengastiella punctata), one at Jammu (Schoengastiella tarsala) and two at Akhnoor (S. uttarkashiensis, S. ligula).
The ticks were exclusively sampled from the rodents in all study areas, however at Pune besides the rodents, domestic animals like dogs, goats and buffaloes were additionally screened for ticks. The tick fauna of the study areas is presented in [Table 3].
A total of five genera of ticks were recorded from the various study areas. Four species of Haemaphysalis and two species of Boophilus were collected from domestic animals other than rodents. Ticks belonging to Boophilus genus were exclusively collected from buffaloes and goats as presented in the [Table 3].
Tick diversity and abundance
The tick abundance and species composition of the study areas is presented as under:
The ticks collected were from four tick genera, i.e., Haemaphysalis, Rhipicephalus, Hyalomma and Boophilus, with the maximum infestation recorded of Haemaphysalis species followed by Rhipicephalus. Haemaphysalis cornigera was the most abundant constituting about 29% of the total collection. Rhipicephalus sanguineus and Boophilus annulatus contributed about 12% each [Figure 4].
|Figure 4: Tick diversity and abundance at Pune. * Hae - Haemaphysalis, R - Rhipicepahalus, Hy - Hyalomma, B – Boophilus.|
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The ticks of Jammu belonged to three major genera of ticks viz., Haemaphysalis, Rhipicephalus and Hyalomma as presented in [Figure 5]. The most abundant tick was Hyalomma hussaini (48%) followed by Rhipicephalus haemaphysaloides and R. sanguineus (28% and 21% respectively).
|Figure 5: Tick diversity and abundance at Jammu. * Hae - Haemaphysalis, R - Rhipicepahalus, Hy - Hyalomma.|
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The tick diversity of Dehradun is presented in [Figure 6]. A total of four genera were recorded. R. sanguineus constituted nearly 70% of the total collection with an equal representation of the two Hyalomma and Haemaphysalis species (8.6% each). The presence of Ixodes is unique to this study area with Ixodes acutitarsus forming 13% of the total ticks collected from this study area.
|Figure 6: Tick diversity and abundance at Dehradun. * Hy - Hyalomma, R - Rhipicepahalus, Hae - Haemaphysalis, I - Ixodes.|
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Flea diversity amongst study areas
The study records presence of four species of Xenopsylla viz., astia, cheopis, gerbilli and nubicus in the study areas [Table 4]. The two important flea vectors of endemic typhus, i.e., Xenopsylla cheopis and Nosopsyllus fasciatus were recorded from Jammu. The study areas - Dehradun and Akhnoor also recorded presence of endemic typhus vector, Xenopsylla astia. The presence of X. cheopis was recorded from Pune as well.
Rickettsial sero-surveillance amongst rodents
The results of rickettsial sero-surveillance amongst rodents using Weil–Felix test is presented in [Table 5]. No rickettsial activity was evidenced at three study areas, i.e., Pune, Rajouri-Poonch and Akhnoor. Only three sera samples tested positive with Weil–Felix out of the 41 sera tested at Dehradun. The positive response to OX19 at Dehradun indicates likely endemic/tick typhus activity in the area. Jammu recorded maximum OXK positivity amongst all study areas with 15 positive sera followed by 12 sera positive for OX2 and 7 for OX19. The results indicate definite scrub typhus activity along with tick and endemic typhus activity in Jammu. The results of Udhampur-Nagrota also show scrub typhus and tick typhus activity with maximum positive sera against OX2 antigen (six samples).
Vector corroboration with serological results
Data presented in [Table 6], highlights the presence of rickettsial activity pertaining to the three important rickettsial diseases viz., scrub, tick and endemic typhus in Jammu. The presence of vectors of scrub typhus - L. deliense, tick typhus vectors - R. sanguineus, R. haemaphysaloides and H. hussaini and endemic typhus vectors - X. cheopis, X. astia and N. fasciatus clearly sets the stage for potential outbreaks of the three rickettsial diseases in Jammu. If we analyse the serological findings and presence of vector species at Dehradun, the potential of tick/endemic typhus outbreak exists in this area. The corroboration of vector and rickettsial activity could not be undertaken for Udhampur-Nagrota belt, although rickettsial activity for scrub and tick/endemic typhus is evidenced in this study area.
| Discussion|| |
The resurgence of rickettsial diseases in India and their potential to impact the fitness of Indian troops by causing morbidity and mortality especially due to scrub typhus has been well appreciated by the Indian Armed Forces and Health authorities. Scrub typhus, as of now, is best prevented by implementing personal protective measures and avoidance of man-vector contact in addition to prompt management of cases. It was in this background that the study was undertaken to determine rickettsial activity amongst rodents and map the vectors of rickettsial diseases, i.e., trombiculid mites, ticks and fleas in selected outbreak prone areas of India.
A total of six selected areas with known endemicity/recorded outbreaks - Jammu, Dehradun, Akhnoor, Rajouri-Poonch, Udhampur-Nagrota and Pune were selected for the study.
The trap positivity recorded in the study (6.7–16.03) is in the normal range of positivity recorded in other studies as well.,,,, The rodents from Udhampur-Nagrota and Rajouri-Poonch were not found infested with any ectoparasites; the reason for this ectoparasite absence could possibly be due to rodent trapping being undertaken primarily in peri-domestic areas due to perceived security threat to field workers due to ongoing low intensity conflict.
The diversity amongst ectoparasite was evidenced in Jammu, Dehradun and Pune, where trombiculid mites, ticks as well as fleas were sampled from the trapped rodents. The rodents of Akhnoor were found to be majorly infested with trombiculid mites. Amongst the study areas, Pune recorded maximum infestation of trombiculid mite (97%) followed by Jammu and Dehradun. Tick infestation amongst rodents was highest in Pune which constituted nearly 50% of the total ticks sampled from the study areas, possibly due to screening of additional animals at Pune. The least infestation amongst the ectoparasites was that of fleas, with greater species diversity at Jammu.
The maximum diversity amongst the trombiculid mites was recorded from Pune, with a total of five and six species of Leptotrombidium and Schoengastiella respectively, and a single species of Gahrliepia viz., punensis. Amongst the Leptotrombidium species, no vector species was recorded. The most abundant trombiculid mite at Pune was Schoengastiella with ceylonica species contributing the maximum followed by S. ligula, which has the potential to transmit scrub typhus., In Dehradun, the predominant species was L. spiletti (82.6%).
The presence of the most important Leptotrombidium vector species transmitting Scrub typhus throughout the endemic areas in the world, i.e., L. deliense at Jammu is an important finding. The rickettsial sero-surveillance results (OXK activity) along with the presence of the vector species completes the triad for scrub typhus outbreaks, which have been reported from Jammu. The role of S. ligula as a probable vector of scrub typhus at Jammu needs to be kept in mind as it was found to be the most abundant trombiculid mite at Jammu (46%) and it is known to have the potential to transmit scrub typhus., This aspect needs to be accorded due importance while estimating the risk of scrub typhus in areas with high abundance of S. ligula and also as a probable vector of scrub typhus in these areas.
The presence of vectors of tick and endemic typhus in Jammu and rickettsial activity amongst rodents for the same sets the stage for tick/endemic typhus outbreaks. It is worthwhile to note that although no outbreaks of tick/endemic typhus have been reported from Jammu, the possibility of it being missed due to low index of suspicion cannot be overlooked.
Pune records the presence of known vectors of the important rickettsial diseases in India, i.e., trombiculid mites, ticks and fleas, yet barring one report of an Indian tick typhus outbreak (unpublished report of Armed Forces Medical College [AFMC], Pune, India) and its reported occurrence as zoonoses, outbreaks of any other rickettsial diseases has so far been not been reported from Pune.
The serological findings of Dehradun are puzzling. One of the most intriguing findings however, from Dehradun, is the total absence of the trombiculid mite vector L. deliense, which has been reported earlier from the area. Dehradun has in the past reported outbreaks of Scrub typhus amongst Armed Forces personnel from Indian Military Academy, Dehradun, however, the current serological surveillance draws negative. This negative finding, whether is influenced by the choice of survey sites or change in ecology of the earlier known endemic areas or some other factor, needs further investigation. Whatever be the plausible reason, what is unquestionable is the need to undertake extensive surveys in Dehradun to search for the currently “elusive” vector of Scrub typhus and to determine whether it is still endemic for scrub typhus or not. Interestingly the sero surveillance findings of Dehradun record tick/endemic typhus activity along with the presence of vectors of both the rickettsial diseases, i.e., tick and endemic typhus. The possibility of occurrence of outbreaks of these two diseases at Dehradun thus cannot be ruled out.
Though no ectoparasites were recorded from Udhampur-Nagrota, rickettsial positivity (OXK and OX2) indicates presence of scrub and tick/endemic typhus as zoonoses. Further search for the vectors need to be carried out in this area to substantiate the rickettsial activity.
The rickettsial sero-surveillance results of Pune although are negative, nonetheless, it should be viewed with caution as the vectors of scrub typhus, tick typhus as well as endemic typhus are present in the area. The reported presence of tick borne zoonosis in Pune district  coupled with a record of an outbreak of tick typhus in Pune city (unpublished data of AFMC) necessitates heightened vigilance for the same at Pune. Any human negligence could prove disastrous for Pune, especially given its record of presence of vectors of tick typhus and its presence as zoonoses.
The addition of new records of trombiculid mites has enriched the mite fauna of the study areas. Two Leptotrombidium species (bhattipadense and tithwalense) along with three Schoengastiella species (uttarkashiensis, homunguis and punctata) at Pune are new records as per the mite fauna records of India. The addition of S. tarsala to Jammu mite fauna and L. spilletti to Dehradun has been a significant contribution of the study to the trombiculid mite database of India. The study also records the presence of two Schoengastiella species at Akhnoor. This is the first time that mite fauna of Akhnoor has been attempted and hence this is a very important addition to the mite database of India.
| Conclusion and Recommendations|| |
The study findings clearly indicate presence of rickettsial activity amongst rodents in three study areas viz., Jammu, Dehradun and Udhampur-Nagrota. The results also correlate well with the presence of known vectors of scrub and tick typhus, thus increasing the risk of rickettsial diseases outbreaks in these areas. The presence of fleas correlates beautifully with the Weil–Felix findings. The absence of scrub typhus vectors as well as Weil–Felix positivity to OXK in Dehradun is intriguing and needs further investigation. Pune, on the other hand appears to be sitting tight on a ticking time bomb, absolutely ready to explode at the slightest trigger from either reservoir entry in infested areas or human negligence.
Armed Forces troops proceeding on exercise to known endemic areas for long periods should be advocated chemoprophylaxis with doxycycline as an effective means to reduce morbidity and mortality due to rickettsial diseases. Mapping of mites and ticks in Udahampur-Nagrota and Rajouri-Poonch needs to be undertaken afresh so that information on vector species composition, diversity and abundance can be determined in this area. Efforts should be made to survey likely “mite islands” to yield meaningful information. Dehradun also needs to be surveyed extensively to determine whether the absence of the scrub typhus vector L. deliense in the survey records is an incidental finding or truly there have been ecological changes to cause disappearance of this vector mite from Dehradun.
There is a felt need to enhance the level of awareness about rickettsial diseases amongst medical personnel of Pune with a view to increase the index of suspicion when dealing with cases of fever of unknown origin. There is also a need to impart information about methods of prevention and symptoms of rickettsial diseases amongst the blissfully unaware general population of Pune to ensure prevention of morbidity and mortality due to these diseases in this area.
The serological test used in the present study, i.e., Weil–Felix, is an obsolete method in this era of technological advancement especially so as it yields false positives. The laboratory diagnostics needs improvement by replacing good old “Weil–Felix test” with more accurate, fast and reliable methods viz. immunofluorescence assay and polymerase chain reaction. An important step forward would be to determine the antigenic diversity of Orientia tsutsugamushi and map the circulating strains of O. tsutsugamushi to understand the clinical spectrum of scrub typhus in India. This would also pave the way for development of vaccine against scrub typhus especially targeted against the Indian strains.
It is recommended that further studies incorporating human sero-surveillance may be undertaken in the areas found positive for rickettsial activity in this study so that the accuracy with which prediction of risk can be made is more precise.
Financial support and sponsorship
Defence Research and Development Organization.
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]