INTRODUCTION

Peste des petits ruminants (PPR) is a highly contagious viral disease of sheep and goats (1). The World Organization for Animal Health has identified PPR as a remarkable and economically important worldwide viral disease of small ruminants associated with high morbidity and mortality (2,3). This particular disease had a course of per acute, acute or may be chronic and its fatality rate may be very high (4). Clinically, manifestations of this disease include severe pyrexia, oculo-nasal discharges, necrotizing and erosive stomatitis, enteritis, and pneumonia. PPR virus (PPRV), is genetically grouped into four lineages (I, II, III, and IV) based on partial sequence analysis of the fusion (F) gene and N gene (5,6). PPR is a member of morbillivirus genus of paramyxoviridae family. The disease was first described in 1942 in the Ivory Coast of West Africa and was later reported in other parts of the world (6). Episodes associated with PPR are usually occur inside India, Nepal, Bangladesh, Pakistan, Bhutan and Afghanistan (5,7,8,9,10). In Asia, PPR was first reported in Pakistan in early 1990s on the bases of clinical and epidemiological observations (11) and it was confirmed through laboratory assays by Amjad et al in 1996 (6). The morbidity rate can reach levels of 80-90% in naïve herds and mortality rate varies from 50% to 80% (9). In non-endemic areas mortality and morbidity rates may range depending upon sensitive population and in severe cases can reach up to 90% and 100%, respectively. Superinfections with other bacterial, viral or parasitic agents may increase mortality up to 100% (12).

Information on prevalence of PPR disease is available from a number of countries in which the disease has been reported such as Asian countries (13,14). However, the pattern of PPR disease, prevalence and underlying risk factors in Chaharmahal and Bakhtiari province of Iran has not been analyzed before. Also, no systematic study of PPRV infection has been done in small ruminants from Iran. The clinical prevalence of PPR among ruminants could be of epidemiological significance, and data about PPR outbreaks are necessary for effective disease management. Therefore, the current study was performed to analyze baseline data to determine the PPR prevalence of PPR in Chaharmahal and Bakhtiari province of Iran over a period of 6 years.

MATERIALS AND METHODS

Data collection. This research was a cross-sectional study that was performed during the years 2009 to 2015. In this study, data of PPR cases were recorded by veterinary centers in Chaharmahal and Bakhtiari Province and data were collected during 2009 to 2014. Veterinary centers in Iran used ELISA test using monoclonal antibodies (MAb) raised to the N protein for diagnosing PPR disease in addition to clinical symptoms. Several homologous PPR vaccines are available in Iran, being cell culture-attenuated strains of natural PPRV. Although transmission of the live attenuated PPR vaccine strain in the field cannot be completely ruled out, there is currently no evidence for vaccine strain transmission either in the field or through experimental infection studies (15). All animals at the various locations are monitored for 12 weeks post-vaccination both by regular weekly visits and with the aid of the local veterinarian for evidence of PPR or any other illness in any of the experimental animals. In this study, the simultaneous presence of a positive result in the ELISA test with clinical signs of the disease was necessary for considering an animal as a PPR case. Then all of information contains location of outbreaks (latitude and longitude), time of occurrence (month, season and year), host species of sick animals, social and political divisions of locations, type of herds, the total number of farms, the number of examined and affected animals and the number of dead patients recorded. Animals tested during the period of this study included cattle, sheep and goat. The cities where the disease monitored included Koohrang, Borujen, Shahrekord, Kiar, Ardal, Farsan, Ben and Lordegan.

Chaharmahal and Bakhtiari province generally has a cold and dry climate. Although in winter, there is a high rainfall especially in Kouhrang city. In the study more than two hundred villages that were suspected for PPRV infection was surveyed.

Statistical analysis. Data were classified using Microsoft Excel 2010 and were analyzed using IBM SPSS version 22. For all of analyses Chi-square test was selected.

Spatial modeling. Spatial modeling was performed using GIS software. Physiographic information, distance from water sources and sanitation and distance from urban residential areas were used for modeling. Maps describing the pattern of disease distribution was made and interpreted.

RESULTS

Out of 2231475 animals, 911145 were checked from 2009 to 2014. The results of this study showed that the overall prevalence of PPR was 1.37 % (12518). The spatial distribution of morbidity rates was 0.94% in Farsan, 0.64% in Kiar, 1.65% in Lordegan, 1.76% in Ardal, 1.375% in Ben, 0.95% in Shahrekord, 1.03% in Borujen and 2.42% in Kouhrang cities. However, with spatial modeling, the main hotspot of PPR was observed in Borujen (morbidity rate: 1.03%), However, two other hotspot were found in Ardal and Naghan (morbidity rates: 1.76% and 4.3% respectively). With chi-square test there wasn’t a statistically significant difference between morbidity rates in different cities (p<0.05)

Distribution of disease in different types of herds is shown in figure 1. The prevalence of PPR in dairy- Beef cattle farms (25%) was higher than other farms. The PPR infection rate reported in goats was 1.69% and it was higher than sheep (1.32%). With chi-square test a statistically significant difference obtained between PPR prevalence in different types of animal farms (p<0.05) (Figures 1 and 2).

PPR prevalence from 2009 to 2014 was 2.1%, 2.59%, 0.7%, 0.49%, 1.08%, 1.73% respectively. Seasonal distribution of PPR infection was 2.6% in the spring, 1.55% in the summer, 0.32 per% in the autumn and 1.73% in the winter, respectively. The means of morbidity percentage in different months has been variable of almost 0.17% in August to 3.8% in March. The results of monthly distribution of the PPR have been shown in figure 3.

Based on the results of spatial modeling, in Chaharmahal and Bakhtiari province, the most severity of disease has been observed in Borujrn town of the city Borujen. Two other hotspots of disease have been existed in Ardal and Naghan. The risk of PPR disease in more than fifty percent of the province is less than 30% (Figure 4).

DISCUSSION

Peste des petits ruminants (PPR) is usually extremely contagious as well as morbillivirus disease affecting sheep and goats (16). For effective control of PPR, a full understanding of the disease epidemiology is obligatory. PPR eradication depends on rapid and precise diagnosis, and using of fast control measures. Due to the massive economic effects of PPR, it is absolutely essential to perform epidemiological surveys of this disease. In Iran, several PPR outbreaks were not accurately recorded due to inadequate animal disease reporting and surveillance systems. Measuring the clinical prevalence of PPR in different geographical areas of may be helpful for organizing disease control strategies and can be useful for determining the true infection rate. Longitudinal survey of PPR in Iran has not been performed

The present study has provided introductory information about confirmed PPR outbreaks or infection among sheep and goats in Iran between 2009 and 2014. Current vaccination programs are being accomplished in Iran which will alter PPR epidemiology, particularly distribution of the disease. Sheep and goats are the natural host of PPRV and goats are more susceptible than sheep (17). In this study, greater PPR positivity was observed in samples from goats than sheep. Soundararajan et al (18) also showed a higher mortality rate among infected goats than sheep in a large organized farm. However, higher seroprevalence in sheep as compared to goats has been observed in some other studies (13,19,20,21,22) Although sheep and goats may not vary significantly in qualifications of disease incidence but a higher mortality rate in PPRV infected goats than in sheep has been established (23).

Based on difference in the virulence of field strains from both species, sheep might have greater innate resistance to clinical development of the disease than goats. This hypothesis appears to be supported by data previously collected during several outbreaks of PPR. It is also possible that the PPRV prefers goat over sheep when both of these natural hosts are reared connectedly. Higher recovery rate in sheep leads to longevity as a result of which a higher population of sheep shows PPRV positivity than goats (13). Moreover, due to higher productivity rate of goats, herd is quickly replaced by young ones which are more susceptible to PPRV (11). Findings in present study are in agreement with Balamurugan et al (24) and Rashid et al (25) who found a lower PPRV prevalence in sheep than goats (24,25).

The reported prevalence of PPR in goats at present study was 1.37% and was in opposite with the results higher prevalence reported by Al–Dubaib (26), Islam et al (27), Rahman et al (28), Sarker and Islam (29), Swai et al (30), Ozkul et al (28) and Singh et al (12) who reported 50.27% and 20.57% in Bangladesh, 55% in Black Bangle goat(BAU), 55.1% seroprevalence in Saudi Arabia, 49.5% seroprevalence in Tanzania, 15.36% seroprevalence in Pakistan, 20% in Turkey and 32.4% in India (21,28,32,33,34). This variation might be due to different geographical location, research time, and different management actions.

In Chaharmahal and Bakhtiari province, goats are reared mostly by nomads. These animals are free-range or pasture-grazed and receive minimum veterinary care, which may further augment the chances of acquiring PPR infection. During the lean period, the animals are flocked from one place to another and animal movement and climatic factors that favor the survival and spread of the virus might predispose temporal occurrence of PPR outbreaks. Trading small ruminants at market places, where animals from different areas are brought into close contact with one another, also promotes PPRV transmission (13).

When prevalence were analyzed according to geographic region, high positivity was observed in animals from Farsan (1.41%) and Kiar (1.12%) compared to other towns. Using chi-square test there weren’t significant differences between infection levels in different cities studied, as well as in different types of animals (p>0.05).

Since 1995, a number of PPR outbreaks have been reported in different provinces of Iran with variable morbidity and mortality rates (7). Nargesi et al (31) reported that PPR prevalence in Mash-had province of Iran was 59.52% in 2012, from these positive samples 72.09% were belonged to sheep and 27.91% were belonged to goat (34).

In a survey performed by Shadmanesh et al in 2014 (30), PPR prevalence in Eghlid City of Iran was compered between goat and sheep. The highest prevalence rate in the flock of sheep was in the Haji-Abad area (25%) and lowest contamination rate was in Jadval-Now area (3.45%). In flocks of goats, the highest contamination rate was in Bidsobhan area (45%) and lowest contamination rate was in Sharad-Eigder area (2.5%). They interpreted that high density of the flocks in some regions, the neglect of hygiene, quarantine, and migratory herds (herds of nomads) in these areas are causes of more contamination (33).

Differences in disease prevalence could be due to the sample size, animal movements and nutritional deficiencies (21). Little nutrition may increase disease incidence due decreased immune resistance. Since relatively few numbers of samples from some towns were tested, differences in PPR prevalence among sheep and goats from these various towns may not be significant. Low rates of positivity recorded in Ben and Kouhrang towns in sheep and goats. This could be due to small sample sizes, surrounded movement of the animals.

Spatial modeling of PPR in Iran has not been reported. This study showed the average distance of the nearest PPR cluster to the center of each province was 160 km and none of the PPR hotspots were located in the provincial centers. Interpretation of spatial modeling is different from interpretation of the results of statistical analysis. As the map shows, one of the main hotspot of the PPR is Borujen and the disease is seen within 200 kilometers away from this city and the incidence decreased with increasing distance.

The situation is likewise Ardal and Naghan. This distribution pattern is dependent on issues such as animal husbandry systems, knowledge of animal farmers, humidity, rainfall and temperature in these areas is as well as the possibility of further distribution of the disease by animal movements (33).

This study indicated that the prevalence of PPR in Chaharmahal and Bakhtiari was 1.37% from 2009 to 2014. During these years, incidence of PPR disease in Chaharmahal and Bakhtiari had chaotic process. Earlier studies (7) indicated that the disease is distributed, which could likely be ascribed to agro-climatic conditions, socio-economic factors, and migration patterns of small ruminants. PPR outbreaks among sheep and goats in Iran can occur at any time of the year, but are most common during the wet (February and May) or dry (April and October) months in Chaharmahal and Bakhtiari province (21). Rainy season is more susceptible to occurrence of the disease as compared with dry season (34). When the temporal distribution of PPR outbreaks was analyzed in the current study, increased numbers of outbreaks occurred during the winter and spring seasons. These results are in coordination with study performed by Sarker and Islam (2011) who observed higher prevalence in winter season (13). This could be due to limited availability of feed during a part of theses seasons, close contact, inhalation of aerosol produced by sneezing and coughing of infected animals, direct contact with ocular, nasal, oral secretions, feces, fomites such as bedding, water and feed troughs (31). However, Taylor (33) believed that increased PPR rate might be due to the increased introduction of sensitive young animals to the flocks rather than a seasonal surge in viral activity. This researcher also reported that PPR is mostly observed during the wet season. Moreover, Wosu (31,32) found that disease incidence peaks during the dry season rather than the rainy season. Inclement dry cold weather during October coupled with poor nutrition over this period promotes the spread of PPR.

The prevalence of PPR in dairy- Beef cattle farms (25%) was higher than other farms. The high potential for cross-species transmission of PPRV from small ruminants to cattle in areas where these species live in close proximity suggests that monitoring such livestock communities would be useful for detecting any changes in the apparent pathogenicity of PPRV, including the possible emergence of PPR as a disease in cattle populations. The incidence of PPR in rural farms was higher (1.42%) than urban farms (0.92%). This variation may be due to poor management of traditional herders. The difference between the rate of disease in different livestock systems evaluated by chi-square analysis and there was a statistically significant difference (p<0.05).

National eradication strategy can only be based on latest data on prevalence of PPR in various parts of Iran. The present study was carried out to determine current prevalence of the disease in small ruminants in various districts of Chaharmahal and Bakhtiari province. Our findings provide evidence of widespread PPR endemicity in Chaharmahal and Bakhtiari that may be due to variations in husbandry practices in different geographical regions, agro-climatic conditions, and animal migration. Vaccination against PPR has been practiced in Iran to control the disease (6). Currently available PPR vaccines and preventive strategies against PPR in Chaharmahal and Bakhtiari, especially in hotspots are very important and have been recommended for a collaborative nation-wide control programs.

Acknowledgments

This study was conducted in as a research project (No.: 170/1) of the faculty of veterinary medicine, Shahrekord University.The authors are thankful for the financial support of Shahrekord University.

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Author notes

a.mokhtari@alumni.ut.ac.ir

IR