Prevention and Control of Infectious Diseases in Pigs

For the prevention and control of infectious diseases, it is imperative to know the transmission dynamics of the causative agents. Studies from other endemic states of India reveal that the majority of the human JE cases appear during monsoon and post-monsoon season (Kulkarni et al., 2018). And there are reports of the occurrence of human JE cases in epidemic proportion in certain geographical areas where previously very few human JE cases were reported which warrants an in-depth study on the dynamics of JEV circulation in amplifying host and vectors (Dwibedi et al.

, 2015). JEV multiplies in pigs before being transmitted to humans. And hence seroconversion of pigs to JEV is an indirect indication of JEV activity in a particular geographical area (Cha et al., 2015). JEV antibodies appear in pigs 2-3 weeks before the JEV is transmitted to humans (Daniels et al., 2002). Therefore, either by detecting the time of JEV infection of pigs/mosquitoes or the period of pig seroconversion, it is possible to avert human JE outbreaks by implementing suitable control measures.

Hence the present study was initiated to elucidate the dynamics of JEV circulation by detecting the time of introduction of JEV and the period of seroconversion in pigs in their natural farm condition in Goa state.

The time of infection of pigs with JEV in farm A and farm B was distinctly different. Such difference in the time of pigs getting infected with JEV in peri-urban and rural pig farms has been documented in earlier studies in Cambodia. The pigs in farm A were the first to get infected with JEV (15th March).

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In farm B the JEV infection of pigs started late but extended up to the first week of December when the fifth and last pig (47BD) was detected positive for JEV RNA.

In farm A, JEV RNA was detected in blood on more than one occasion in four pigs using real-time RT-PCR unlike in farm B where such a pattern was not observed. Since long-term studies on JEV persistence in naturally infected swine are not available and it is cited in literature that pigs become immune after initial infection (Geeverghese et al., 1994), at this point, we don’t have a solid reason to justify why the JEV RNA was detected multiple times in blood. The most plausible explanation could be the reintroduction/reinfection of the pigs. However to support this statement we don’t have corresponding virus isolation/detection studies from mosquitoes. Another possibility could be reactivation or rebound viremia after the initial infection.

It has been previously demonstrated that in the tonsils of experimentally inoculated pigs JEV persisted for a long duration (25 days) despite the presence of neutralizing antibodies (Ricklin et al., 2016). A similar phenomenon of coexistence of JEV and HI antibodies and neutralizing antibodies was recorded in swine (Scherer et al., 1959). On the contrary, some experiments have shown that pigs that were previously infected with either JEV, Murray Valley encephalitis virus (MVE), or Kunjin virus (KUN) did not produce viremia after secondary inoculation with JEV (Williams et al., 2001). Therefore we think that long-duration prospective studies in naturally infected pigs under field conditions are required to validate the results obtained in this study. The presence of JEV in oro-nasal swabs of experimentally infected pigs has been recently documented (Ricklin et al., 2016). In the present study, we were able to demonstrate JEV RNA in oro-nasal swabs of naturally infected pigs.

It is evident from the earlier studies that pigs infected either naturally or experimentally with JEV, seroconvert seven to ten days after infection (Geeverghese et al., 1987a, Ricklin et al., 2016). In the present study seroconversion of a farm pig, A occurred nearly two months earlier than farm B. Further, seroconversion was rapid in farm A as all the eight pigs got seroconverted within 53 days compared to farm B where seroconversion was protracted over 106 days. The peak period of seroconversion in farm A was April as six of the eight pigs got seroconverted as opposed to farm B where peak seroconversion was observed in September when three pigs out of eight got seroconverted. It was evident that the pattern of JEV circulation was distinctly different on both farms. The onset of seroconversion in pigs observed in farm A (April 2017) and farm B (June 2017) in the present study preceded the month of occurrence of the majority of human JE cases (July-August) reported in previous years 1982 and from 2011 to 2015 in the Goa state. A similar observation of pig seroconversion preceding the appearance of human JE cases has been documented previously in South India and Thailand (Geeverghese et al., 1987b, Gingrich et al., 1987).

In light of the result of our study, the seroconversion experiments in sentinel pigs in two JE endemic districts (Kolar and Mandya) of Karnataka state, India deserve a special mention at this juncture. In the Kolar district, maximum seroconversion of sentinel pigs to JEV occurred from October to December every year between 1980 – 1985 (Geeverghese et al., 1987b). On the contrary, in the Mandya district, the high seroconversion of the pig was observed during April and May in the years 1985 and 1986. These two distinct patterns of seroconversion period were attributed to the ecological differences between the two districts. Kolar district is relatively a dry area. However, the Mandya district has round-the-year irrigation for crops with perennial water bodies which support the population of married birds, the natural hosts of JEV (Geeverghese et al., 1991). In the Dibrugarh district of Assam, a northeastern state of India where every year several hundred human JE cases and deaths have been reported, the majority of the pigs have been shown to seroconvert between June and August with peak seroconversion recorded in July in the years 2009 and 2010 (Borah et al., 2013).

In Japan, since the 1960s every year pigs seroconvert to JEV in the summer season between June and September. In Badu and Moa islands of Torres Strait, pigs seroconverted late in February 1998 and by mid of March 1998, all the sentinel pigs were seroconverted.

In the Australian mainland, JEV activity started only in the middle of march 1998 and the seroconversion was gradual and extended for a longer period (Hanna et al., 1999). The recent sentinel pig experiment conducted in Kandal province, Cambodia has also documented the difference in the time of infection of pigs located in peri-urban and rural pig farms and cited probable reasons behind the difference (Di Francesco et al., 2018). There could be several reasons for the difference in the period of seroconversion in farm A and farm B in our experiment. Weather conditions, the existence of other JEV reservoir hosts, and cropping patterns prevailing in the vicinity of the farm could be some of them.

During the period of the study, paddy was cultivated around farm A and a large lake (Carambolim lake), and marshy areas existed near farm A which were visited by several species of water birds (Rahmani et al., 2016). Paddy fields and water bodies provide breeding grounds for vector mosquitoes and water birds are the reservoir hosts for JEV. We suspect probably these factors might be the drivers for the intense activity of JEV in farm A. Around farm B such ecology did not exist during the period of the study. From the present study, it was evident that the JEV circulation in pigs is distinctly different in both the farms located in two different districts.

In countries like Japan and South Korea seroconversion of pigs to JEV is being monitored regularly for the past several decades. Such monitoring is essential to identify the magnitude of the infection in pigs and to alert the public health authorities. In Goa state, although only a few human JE cases are reported (less than ten laboratories confirmed JE cases per year) in the past ten years the disease cannot be neglected because of the presence of amplifying hosts, the existence of breeding grounds for vector mosquitoes, movement of reservoir hosts and vectors, suitable weather and urbanization.

Our study suffers from certain drawbacks. First, the study could be conducted only for one year and may need to be repeated for a few more years to make sure the JEV circulation trend is consistent across the years. Second, the experiment was conducted on only two pig farms and hence results cannot be generalized to the entire state. Despite these drawbacks, we could document certain key findings in the JEV epidemiology in the state. The study was able to identify that during the study period the pigs got infected with JEV as early as March and extend till December and seroconversion occurred from April onwards. In earlier studies in Goa, it has been observed that the onset of human JE cases starts in May and continued till November, and peaks during August. Our study confirms that the appearance of human cases was preceded by JEV infection and seroconversion of pigs.

Prevention and control measures of human JE largely depend on improving the immunity of humans by vaccination, vector control to prevent transmission, and pig vaccination. However, shifting pigs away from the backyard to a distant place is operationally impractical and vaccination of susceptible piglets during each farrowing season is logistically demanding. Therefore, vector control and human vaccination are the other options for JE prevention. Strict vector control measures before and during the JEV transmission season are essential. It is encouraging that JE vaccination has already been implemented in the state and it is an effective strategy for preventing the human JE. Education of pig farmers and the general public about the role of pigs in JEV epidemiology is also important. Further, we think that regular surveillance of amplifying hosts and vectors should also be the part of JE prevention and control strategy in the state.