Prevalence of babesiosis in bovines of India: a meta-analytical approach for 30 years (1990–2019)

Abstract Background India has a massive population of bovines, which makes the framework of the economy mainly relying on milk and meat production. Parasitic diseases such as babesiosis are detrimental to bovines by decreasing animal welfare and production efficiency. Aim Performing a meta-analysis of the prevalence of babesiosis over 30 years viz 1990 to 2019 within India to pool out individual studies from different country regions. Material and methods The studies were reviewed thoroughly to assess the quality, and it was done by following the preferred reporting items for systematic review and meta-analysis (PRISMA) and MOOSE protocols. The prevalence of babesiosis in cattle and buffaloes was calculated using meta-analysis tools using R-software and Q Statistics. Results The systematic review and meta-analysis performed on 47 studies among bovine, 48 studies among cattle, and 13 studies among buffaloes revealed the (pooled) prevalence of babesiosis in India as 10.9% (6.3%–18.2%; Q = 5132.03, d.f. = 46, P < 0.001), 11.9% (6.9%–19.8%; Q = 5060.2, d.f.=47, P < 0.001), and 6.0% (2.6%–13.2%; Q = 500.55, d.f.=12, P < 0.001), respectively, which provides a rather exact scenario of the prevalence of this haemoparasitic disease across the country. In addition, cattle were having higher risk of babesiosis than buffalo. Conclusion The findings from the meta-analysis showed that the disease is prevalent across the country, and that bovines are highly affected by it. Clinical relevance Appropriate prevention and control measures should be taken to mitigate this disease and enhance welfare and production performances of bovines.


Introduction
in india, since the ancient era, livestock has played a pivotal role in agriculture. for doubling the farmers' income, livestock has immense importance out of which the bovines, especially cattle and buffaloes, serve the key role to the economy among the livestock. india is the highest livestock owner with diversified genera of breeds of livestock and poultry, which have a pivotal role in the socio-economic development of rural households. the livestock and agriculture sectors are intrinsically linked to producing the consumables and ensuring the food security of the nation.
Several diseases cause a negative impact on livestock health and production as well as have high economical importance (perry and Grace 2009; Dhama et al. 2014). the consequences of animal diseases in livestock are detrimental and cause producers to lose in terms of production, resources, and maintenance. parasitic diseases of bovines like babesiosis, an infectious tick-borne haemoprotozoal disease caused by Babesia bigemina and Babesia bovis, can greatly affect the animal's health status leading to high economic losses and is among the most prevalent and costly tick-borne diseases (tBD's) of cattle worldwide (Jacob et al. 2020;He et al. 2021). other babesia species affecting bovids include B. orientalis, B. ovata, B. major, B. motasi, B. U sp. Kashi and B. venatorum. the disease is also termed as bovine babesiosis, piroplasmosis, texas fever, redwater fever, tick fever, or tristeza (Zaugg 2009). it was first detected by Babes in 1888. it is common in tropical and sub-tropical regions worldwide with relatively high morbidity and mortality rate, and efforts are being carried out with regards to prevention and control measures (Suarez and Noh 2011;Gohil et al. 2013;Jacob et al. 2020;He et al. 2021). the disease is mechanically transmitted by ticks, in bovines, mainly by the genera of Boophilus and Hyalomma spp. (ravindran et al. 2002).
Cattle acquire the infection by the introduction of the sporozoite stage of the parasite into the bloodstream from an infected tick during a blood meal (Barman et al. 2018). it has high economic importance as india annually loses around 57.2 million USD in the livestock sector due to this disease. in a case study conducted on an organized farm in Meghalaya in 2012, it has been reported that due to B. bigemina infection in a milch cross-bred cow, a total of 51.6 liters loss of milk and an economic loss worth 1032 rupees (12.92 US dollar) due to decrease in production for 30 days (Laha et al. 2012).
Meta-analysis is a statistical technique that combines the results of several related studies over a topic and offers more accurate and reliable information on the effects of certain factors and treatments. in simple language, meta-analysis can be said an analysis of analysis. Meta-analysis of the prevalence of babesiosis in bovine will be useful to obtain pooled estimates of summary estimates from the published studies. it will help to better understand the prevalence of the disease associated with various risk factors. therefore, the present study was carried out to estimate the prevalence of bovine babesiosis in india by performing a systematic review and meta-analysis compiling the data of 30 years (1990 to 2019).

Materials and methods
the systematic review of prevalence and risk factors of babesiosis in bovines was done from 1990 to 2019. Data collected from all the farms were clubbed with published studies to get a pooled estimate. published studies were collected from various journals, annual reports, and online search engines like pubMed, Science Direct, Google scholar, NCBi, J-Gate, Krishikosh, etc. the studies were reviewed thoroughly to assess the quality, and it was done by following the preferred reporting items for systematic review and meta-analysis (priSMA) and MooSe protocols. Accordingly, the inclusion and exclusion criteria for studies were prepared and shown in table 1. flow diagram of study selection for meta-analysis of babesiosis in bovine is shown in figure 1.
the prevalence of babesiosis in cattle and buffaloes was calculated using meta-analysis tools using r-software, with 48 published studies across india from 1990 to 2019 after screening and quality assessments. these again were subdivided into cattle and buffalo separately and subsequently 48 and 13 studies were included, respectively. the list of studies included in the meta-analysis of babesiosis is given in table 2.

Meta-analysis in cattle
Among the selected 48 published references, 56,748 cattle were considered for meta-analysis. following the quality assessment, the pooled prevalence was found to be 11.9% (95% Ci; 6.9; 19.8) with a significant Q statistics value (Q = 5060.2, d.f. = 47, P < 0.001). Variability between the studies was 4.3284 (tausquare), and the measure of heterogeneity was 99.5% (i 2 index). the forest plot (figure 2) represents the proportion of cattle affected by babesiosis per individual studies and the overall pooled estimate of the prevalence of the disease.

Meta-analysis in buffaloes
from 13 published literature, 5370 cattle were included for the following meta-analysis, after the quality assessment and the pooled prevalence was found 6.0% (95% Ci; 2.6; 13.2) with significant Q value (Q = 500.55, d.f.=12, P < 0.001), which stated that there was significant heterogeneity in between the 13 published studies. Variability between the
Variability between the studies was 2.0519 (tausquare) whereas the measure of heterogeneity was 99.6% (i 2 index). the forest plot (figure 4) represents the proportion of bovines affected by babesiosis per individual studies and the overall pooled estimate of the prevalence of the disease.

Identification of publication bias in meta-analysis of the prevalence of babesiosis
funnel plot techniques were used to identify the publication bias among the studies where the proportion of each study was plotted on the horizontal axis, while the standard error was on the vertical one. figures 5, 6, and 7 show the funnel plots for studies taken for babesiosis in cattle, buffaloes, and bovine, respectively, where only a few studies were inside the funnel. in contrast, most of the studies were scattered outside of it, which implied significant publication bias. in addition, the studies are distributed scattered throughout the graph, which implies they have different standard errors.

Discussion
the present meta-analysis was performed to review prevalence of babesiosis in cattle, buffaloes and bovine in last 30 years in order to consider maximum number of studies for better conclusions. Meta-analysis of the prevalence of babesiosis in cattle cited the pooled prevalence was 11.9% (6.9%-19.8%) which was related to the studies done by Ananda et al. (2009), who claimed the prevalence of babesiosis in cattle was about 12.1%. on the other hand, the meta-analysis in terms of buffaloes resulted that the pooled prevalence was 6.0% (2.6%-13.2%) which was found similar to the findings of Agrawal et al. (2003), who stated the prevalence was 7.4% along with other authors like Mishra et al. (1998); Sharma et al. (2013); Krishnamurthy et al. (2014) and Sharma et al. (2016) who also found similar results on the prevalence of babesiosis in buffaloes were 7.4%, 8%, 4.7%, and 7.9% respectively.
Meta-analysis of risk of babesiosis in cattle with respect to buffaloes was studied, which showed that cattle were having higher risk of babesiosis than buffalo. Similar findings were observed in many studies reported in india (Agrawal et al. 2003;Aulakh et al. 2005;Muraleedharan et al. 2005;Krishnamurthy et al. 2014;Kaur et al. 2016;Maharana et al. 2016).

Conclusion
the systematic review and meta-analysis analysed 47 studies among bovine, 48 studies among cattle, and 13 studies among buffaloes to estimate the prevalence of Babesiosis in india. the findings indicate a pooled prevalence of 10.9% (6.3%-18.2%), 11.9% (6.9%-19.8%), and 6.0% (2.6%-13.2%) in bovine, cattle and buffaloes, respectively. the climatic conditions, topography of the country enhance the growth and transmission of the vector, ultimately affecting the occurrence of the disease. the findings from the meta-analysis showed that the disease is prevalent across the country, and the bovines are highly affected by it. So, to mitigate the disease, appropriate prevention and control measures should be taken to safeguard bovine health and enhance production.

Availability of data and material
the data that support the findings of this study are available from the corresponding author upon reasonable request.