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RESEARCH ARTICLE
Year : 2022 | Volume
: 59
| Issue : 1 | Page : 79-85
Kyasanur forest disease and climatic attributes in India
Poonam Singh1, Prakash Kumar2, Ramesh C Dhiman1
1 Centre of Excellence for Climate Change and Vector borne Diseases, ICMR-National Institute of Malaria Research, New Delhi, India
2 Directorate of Health & FW Services, Ananda Rao Circle, Bangalore, Karnataka, India
Correspondence Address:
Ramesh C Dhiman
Environmental Epidemiology Division, ICMR–National Institute of Malaria Research, Sector-8, Dwarka, New Delhi 110077
India
Source of Support: None, Conflict of Interest: None
CheckDOI: 10.4103/0972-9062.331408
Background & objectives: In India, Kyasanur Forest Disease has been reported from the states of Karnataka, Kerala, Goa, and Maharashtra. The relationship between climatic factors and transmission of KFD remains untouched, therefore, the present study was undertaken.
Methods: Based on the occurrence of cases, Shivamogga district (Karnataka) and Wayanad district in Kerala and northern Goa (Goa state) were selected for the study. Data on the incidence of KFD and climate factors were collected from concerned authorities. To determine the relationship between dependent and independent variables, spearman’s correlation was calculated for monthly as well as with lag months.
Results: KFD cases and temperature (°C) were found significantly correlated up to 1 months’ lag period (p<0.05) while with precipitation relationship was found negatively significant for 0-3 months’ lag. The range of suitable temperature for KFD in Shivamogga, Goa and Wayanad was found as 20-31°C, 25-29°C and 27-31°C respectively. The cumulative precipitation during transmission months (November–May) ranged from <150-500mm, while in non-transmission months (June-October) from >1100-2400mm.
Interpretation & conclusion: The analysis of three sites revealed that with the increase in temperature, the intensity of KFD transmission decreases as corroborated by the seasonal fluctuations in Shivamogga, Goa and Wayanad. High precipitation from June to October rovides suitable ecology to tick vector and sets in transmission season from November to May when cumulative precipitation is <500 mm.
Keywords: Kyasanur Forest Disease; Temperature; Precipitation; Climate; India
In recent years, the impact of climate change has been extensively studied and found responsible for affecting the public health scenario worldwide. Climate change affects the development of vectors, their survival alters the distribution[1] and emergence and re-emergence of vector-borne diseases (VBDs)[2]. Tick-borne diseases are also highly sensitive to climate change[3] affecting the biology of ticks and epidemiology of tick borne diseases[4].
In India, Kyasanur Forest disease (KFD), a tick-borne disease, was reported for the first time from Shivamogga (Karnataka) in the year 1957[5]. The disease is caused by KFD virus (Family Flaviviridae and genus Flavivirus)[6],[7] and transmitted mainly by the bites of Haemaphysalis spinigera[8]. Apart from Haemaphysalis spinigera, other species like H. turturis, H. papuanakinneari, H. wellingtoni, H. kyasanurensis and even Ornithodoros crossi were also found naturally infected as well as transmitted infection in laboratory-based experiments[9],[10]. The disease can also be transmitted through aerosols and handling virus-infected material in the laboratory[11]. The life cycle of tick has four stages, i.e. egg, larva, nymph, and adult of which only larvae and nymph transmit KFD virus. Ticks feed on a variety of hosts i.e., cattle, monkeys and birds etc. including human beings. The maximum density of larvae and nymphs are found from December–May (transmission season of KFD), while the adult ticks are found mainly during rainy season i.e., July–September[12]. Approximately 400–500 KFD cases occur in India annually[13]. In addition to erstwhile endemic areas of Karnataka[14], KFD outbreaks have been reported from the states of Kerala[15],[16], Maharashtra[17],[18] and Goa[19] during 2014–2016 [Table 1].
The studies undertaken so far have confined mainly to investigation of outbreaks but the role of climatic factors, which play crucial role in transmission of VBDs[20],[21],[22] still remain unexplored. The understanding of climatic determinants will help in characterizing the KFD endemic areas, defining transmission and non-transmission seasons and will pave the way for early warning of outbreaks Therefore, the present study was undertaken to find out the role of climatic factors in characterizing the KFD endemic areas in southern India.
Material & MethodsKFD incidence data
Monthly incidence of KFD from representative districts of different states was collected from State Programme Officers of Karnataka, Kerala, and Goa. Since Shivamogga district (Karnataka) is endemic for KFD since long, the data for the period of January 2011 to December 2018 were collected. In the states of Kerala and Goa (North & South), where KFD emerged since 2014 only, data were collected for the period of 2014 to 2016 and 2015 to 2017 respectively. Sindhudurg district (Maharashtra) also reported 130 cases from December 2015 to July 2016[17]. But, owing to non-availability of data, analysis was not done in respect of Sindhudurg districts. The study sites are shown in [Figure 1].
Figure 1: Districts reporting Kyasanur Forest Disease in India. Boundaries of states are shown on the map.Climate data
Monthly observed climatic data i.e., temperature (°C) and relative humidity (RH %) from 2011 to 2016 were procured from Indian Meteorological Department (IMD), Pune. In addition to this, monthly precipitation data were downloaded from the IMD precipitation data portal (http://hydro.imd.gov.in/hydrometweb/ (S(tmkcnc45of34t1z4h03b3q45))/landing.aspx) which provides average precipitation of a district based on average of 4-5 rain gauzes in a district. In respect of Wayanad district, data of temperature was not available from IMD; therefore, the data of adjoining districts, i.e., Kozhikode and Kannur was used by taking average values of both the districts (Kozhikode and Kannur fall in the same landscape of Western Ghats in the country).
Data analysis
All the data were entered, calculated and analyzed using Microsoft Excel and SPSS 17.4 software. Correlation and cross-correlation was also employed for analyzing the lag effect# of climatic parameters i.e. temperature and precipitation on KFD occurrence using spearman rho. The lag (L) effect of climatic parameters on occurrence of KFD cases was calculated up to five months (L1-L5). The p-value of <0.05 was considered statistically significant. The ranges of suitable temperature and precipitation were determined based on occurrence of KFD cases in respect of each site.
ResultsAssociation between KFD cases and climatic parameters in Shivamogga district
In Shivamogga district, the annual trend of KFD cases (2011–2018) shows that starting from the month of January cases are present which reach to peak up in the month of March. Thereafter, start declining gradually and by June/July, the cases reach to almost zero and the same trend continues until October [Figure 2]. Reoccurrence of the cases started from the month of November. Overall, the transmission of KFD in Shivamogga district has been observed up to a maximum of seven months i.e., November–May.
Figure 2: Monthly trend of KFD cases in Shivamogga, Karnataka (2011–2019). The annual trend shows that the peak of KFD occurs in the month of March and starts declining gradually and reach to almost zero by June/July. From the month of November, cases started re-occurring[Figure 3] shows the annual trend of KFD cases and temperature from 2011–2016. The analysis revealed that the average annual temperature in Shivamogga district ranged from 20–31°C. The precipitation starts from the month of February/March and reaches to peak in the month of July and ceases by November/December. It has been observed that during the transmission season of KFD (i.e., November–May), the amount of monthly precipitation never reaches >250 mm [Figure 3]. With the increase in precipitation from April month onwards, cases start declining [Figure 4]. With the reduction in precipitation from the month of September onwards, the KFD cases starts appearing until the month of May and rarely in the month of June. In other words, it can be stated that after the cessation of precipitation, the transmission of KFD commences from November and continues till the month of May. Further, analysis revealed that during peak transmission months, i.e., from January-March, monthly precipitation amount was <50mm. In 2014, district Shivamogga witnessed an outbreak of KFD resulting in overall 147 cases of which maximum cases (n=71) occurred in the month of March [Figure 4].
Figure 3: Annual occurrence of KFD cases and temperature (°C) in Shivamogga (Karnataka) (2011-2016). The average annual temperature in Shivamogga district ranged from 20–31°C. The highest peak of KFD cases was recorded at average temperature of 38°C. (Avg_T= average temperature, MMAX_T= Mean maximum Temperature, MMIN_T= Mean minimum Temperature).
Figure 4: Time series plot of KFD cases and precipitation (mm) in Shivamogga (2011–2018).Association between KFD cases and climatic parameters in Wayanad and Goa
In Wayanad district (Kerala), KFD was reported in the year 2014 with first case in the month of March. Later on, in 2015, an outbreak occurred with 102 confirmed cases. Similar to Shivamogga, in Wayanad district also, cases reach to peak in the month of February (n=37) and come down to zero by June. After cessation of rains in October/November, the cases start emerging from November/December. No KFD cases occurred during rainy season i.e., from June to October [Figure 5]. In Wayanad reoccurrence of the cases started from the month of December. The transmission season lasts for 7–8 months (November/ December to May/June).
Figure 5: Time series plot of KFD Cases and Climatic parameters i.e., Temperature (°C) and Precipitation (mm) in Wayanad district, Kerala (2013-2016). (Avg_T= average temperature, Mmax_T= Mean maximum Temperature, Mmin_T= Mean minimum Temperature).At Goa also, KFD was first reported in the month of March 2015 with 36 total cases followed by the outbreak in the year 2016 (n= 285) and 73 cases in 2017 [Figure 6]. The occurrence of KFD at both the places followed the seasonal pattern of transmission similar to Shivamogga i.e., November/December–May. Further, in respect of climatic parameters, the analysis revealed that the average annual temperature ranged from 25–31°C in Wayanad and 25–30°C in Goa. During transmission months (November/December–May), the minimum temperature is 27°C/25°C and maximum 31°C/29°C in Wayanad/Goa and cumulative precipitation was found <500mm and <150mm in Wayanad and Goa, respectively. The cumulative precipitation during the non-transmission months (June to October) was found >1100mm and > 2400mm at Wayanad and Goa respectively.
Figure 6: Time series plot of KFD cases and climatic parameters i.e., Temperature (°C) and Precipitation (mm) in Goa (2014-2017). (Avg_T= average temperature, Mmax_T= Mean maximum Temperature, Mmin_T= Mean minimum Temperature).Statistical analysis
To understand the association completely, two tailed correlation (r) analysis was carried using spearman rho. The correlation was calculated for month-to-month association and up to five months lag [Table 2]. The results revealed that KFD cases have significant positive correlation with temperature (p <0.05) in Shivamogga (r =0.339**[1]) and Wayanad (r =0.618**), while in respect of Goa (r= -0.046, p >0.05) no correlation was found [Table 2]. The lag effect of temperature in terms of correlation coefficient revealed significant association up to one/two months lag; Shivamogga Lag (L1)= -0.334**, and Wayanad Lag (L1)= -0.565**, Lag (L2)= -0.420**. At Goa, the significant correlation appeared at fifth month (Lag 5= 0.509**). After one or two months, lag effect of temperature appears insignificant. As regards the relationship between KFD and precipitation, a significant (p <0.05) negative correlation (r) was found in respect of all the three sites (Shivamogga=-0.488**, Goa=- 0.626** and Wayanad = -315*), which remained significant up to three months lag (L1-L3) [Table 2]. Significant correlation (r) was found up to three months i.e. in Shivamogga Lag (L1)= -0.623**, Lag (L2)= -0.613**, Lag (L3)= -0.385**; in Goa Lag (L1)= - 0.682**, Lag (L2) = -0.652**, Lag (L3) = -0.395*; in Wayanad Lag (L1) = -0.504**, Lag (L2) = -0.574**, Lag (L3)= -0.451**. Fourth month onwards, the correlation remains insignificant except at Shivamogga (L5= 0.325**) [Table 2].
Table 2: Cross-Correlation between temperature, precipitation and KFD cases at Shivamogga (Karnataka), Wayanad (Kerala) and GoaDetermination of climate suitability range for KFD
After understanding the relationship between climatic parameters and KFD cases, a visual analysis was carried out. Of three study sites, in Shivamogga, the suitable range of temperature was found 20–31°C while the cumulative precipitation of <250 mm during transmission months (November–May) and >1300mm during non-transmission months (June-October). On the other hand, in Wayanad it was found that the suitable temperature ranged from 27–31°C and cumulative precipitation of <500 mm in transmission months and >1100mm in non-transmission months. In respect of Goa, during the transmission months the temperature ranged from 25–29°C and cumulative precipitation of <150mm while >2400mm in non-transmission months. Considering the climatic suitability of three sites, it can be deduced that the suitable temperature for transmission of KFD ranged from 20–31°C while the cumulative precipitation during transmission months was <500mm[1]. On the other hand, during non-transmission months i.e., June-October, the cumulative precipitation for all the three sites was >1100mm[2][Table 3].
DiscussionThe result of three sites studied in the present study revealed that with the increase in temperature, the intensity of KFD transmission decreases as corroborated by the seasonal fluctuations in Shivamogga, Goa and Wayanad. The cumulative precipitation during transmission season (November to May) has been found ranging from 150 to 500mm reflecting that transmission does not occur during high precipitation months.
The findings of the present study have brought out the importance of cumulative precipitation >1100 mm from June to October, during which transmission does not take place across all the three studied sites. At Goa site (newly established focus), the cumulative precipitation during non-transmission season was highest (>2400 mm) followed by >1300 mm and >1100 mm in Shivamogga and Wayanad sites, respectively. If we Look at the calender year, it appears that KFD cases occur before precipitation, but it is not so as the KFD cases start occurring with cessation of rainy season i.e., in November/December and continues further till May next year. It indicates that heavy precipitation of >1100mm is essential for sustenance of deciduous forest wherein a constant availability of foliage on the ground is required[12]. During the rainy season, the ticks breed profusely in the soil under the foliage[23]. With the cessation of rains in October, the newly hatched larvae seek hosts like monkeys, shrews, squirrels, and birds etc., for blood meal, which are found in forest. Monkeys (Macaca radiata and Presbytis entellus) have been reported as major reservoir host for KFD and they have also been reported to come closer to human habitation after cessation of precipitation i.e., November month onwards[24],[25]. The KFD cases are reported usually after death of monkeys, resulting in dropping-off of larvae and nymphs, which ultimately attack man. It may be explained by the observation of the lag period in precipitation and occurrence of KFD cases. The variation in temperature and precipitation between the three sites indicate that lower temperature with higher precipitation experienced in Shivamogga district during non-transmission months is related with higher endemicity of KFD[26].
The literature search on the impact of climatic factors on vector survival and development revealed the crucial role of temperature and relative humidity individually or in combination. In Haemaphysalis longicornis[20] oviposition, egg hatching and moulting of larva to nymph did not occur at lower temperature i.e., 12°C[21] while the temperature of 40°C has been determined as the upper threshold for development of tick. Studies have proved the important role of relative humidity alone in the development of ticks as at <75% RH, eggs did not hatch, engorged larvae did not moult to the nymphs and all ticks died within 14 days, kept at the constant temperature of 30°C[20],[21]. Bhatt 1979[27] found the temperature range from 18–35°C crucial for development of ticks. Based on laboratory experiments carried out at 18–35°C temperature and 80–90% relative humidity[27], it has been found that the lifespan of Haemaphysalis spinigera is approx. 276, 320 and up to 350 days in larva, nymph and adult stage respectively. It suggests that vector is technically available in all seasons in a year, but remained hidden under the foliage during rainy season. Considering 18–35°C, ambient temperature for Haemaphysalis spinigera, all three sites are climatically suitable throughout the year for the development and availability of vector. It is corroborated by the identification of upper suitability range of temperature across all KFD reported areas only up to 31°C.
It is also apparent that precipitation of >1100 mm during non-transmission season is also essential for KFD transmission. The reason of high precipitation i.e., >2400 mm during non-transmission season in Goa needs to be analysed in the context of terrain modelling: may be the water is not stagnating otherwise it should be in the range of other two sites (1100 to 1300 mm). As per reported cases, the transmission season of KFD varies from 6–8 months (six in Shivamogga while eight in Goa and Wayanad). The reason of difference in transmission period may be attributed to forest cover/ months of precipitation, which can be explained further by bioclimatic models[28].
Customarily, death of monkeys is the only signal for imminent threat of KFD, which may depend on the efforts of forest staff to detect and report monkey deaths. Rajagopalan et al. (1968)[12], and Sreenivasan et al. (1986)[29], reported epizootic cycle of transmission through longitudinal availability of tick’s species and wild monkeys. However, the exact time of onset of outbreaks is not known. Longitudinal studies are required on monitoring of ticks density, importance of transovarian/trans-stadial transmission[30] and critical precipitation to determine the exact onset of transmission of KFD in new foci for early warning. Periodic surveys for the presence of antibodies in man/ monkeys should be undertaken for pre-warning of the threat of KFD. The findings of this work elucidate the importance of climatic parameters in the transmission of KFD transmission which are basically related with suitable ecological conditions for breeding, survival and continuation of life cycle of tick vector.
The data of precipitation used for the study districts was average of multiple-point locations within a district. Since there is lot of variability in precipitation patterns within a district depending upon altitude, more particularly for Shivamogga district, it is desirable that analysis with sub-district level monthly precipitation would be helpful for refining early warning of occurrence of KFD cases. In view of projected scenarios of climate change, decadal variations in the identified cut-off of temperature and precipitation may be observed.
ConclusionThe study highlights the relationship between KFD and climatic parameters in erstwhile endemic district, Shivamogga (Karnataka) and in newly established foci i.e., Wayanad (Kerala) and Goa. It defines suitable monthly temperature ranging from 20–31°C in Shivamogga, 27–31°C in Wayanad and 25–29°C in Goa. The disease does not occur in rainy months and the transmission season in all the study sites was confined to November-May. It was found that the cumulative precipitation of <500 mm in transmission months (November to May) and >1100 mm in non-transmission months (June to October) is essential across all the three studied sites. The study also suggests the development of a climate-based alert system for health system just after cessation of precipitation in southern states.
AcknowledgementsThe authors acknowledge the Climate Change Programme, SPLICE, Department of Science & Technology (DST), Govt. of India for financial support. Thanks to the State Programme Officers of Kerala, Goa, and Karnataka state for sharing epidemiological data of KFD. Authors also acknowledge the Virus Diagnostic Laboratory, Shivamogga for their support during the field activities.
Conflict of interest: None
References
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