Our research systematically illustrated the wide prevalence and phylogenetic relationship of Babesia in reservoir host species in Fujian Province, Southeast China. Infections of B. microti parasites were observed in four cities and eight sampling sites in Fujian Province (Fig. 1, Table 1). Babesia microti has been reported in small mammals in Beijing [3], Henan [37], Yunnan [35], and Taiwan [29]. Babesia microti infections was also previously reported in the Wuyi Mountain area, Fujian [44]; however, the epidemiological features of Babesia remain unclear in the other cities in Fujian. In this study, the prevalence of B. microti in rodents (3.96%) followed the low prevalence described in Yunnan (4.31% [31] and 2.40% [35]), and the Dapan Mountains of Zhejiang (1.30%) [45]. However, the positive infection rates of B. microti in R. tanezumi in Yunnan (2.70%) and Dapan Mountains (5.56%) were higher than in our research (0.61%). Our study showed that the high prevalence of B. microti in N. confucianus in Fujian (17.02%) was similar to that found in the Dapan Mountains of Zhejiang (20.0%). This suggested that N. confucianus may be superior reservoir hosts in Southeast China [35]. The high prevalence of B. microti infection in rodents in Ningde and Sanming in this survey strongly supports the hypothesis that these surveillance points are major natural foci for human babesiosis. Furthermore, the results call for close monitoring of B. microti transmissions in Ningde and Sanming, while the epidemic of B. microti in other cities should not be ignored. It should be noted that the B. microti infection rates were zero in Putian, Quanzhou, Zhangzhou, and Longyan, which may be attributed to a lack of samples and rodent habitats (Table 4). The prevalence of B. microti varied from district to district. Although both Fuzhou and Quanzhou are adjacent to Sanming, the B. microti infection rates were lower than 5.00% for both, while Sanming had the highest infection rate. This may be attributed to the distribution and density of the reservoir host species.
Interestingly, the infection rate of Babesia in Xiapu District, Ningde City, was 15.79%, which may provide a novel link to the first human case of babesiosis in Fujian [46]. The patient, who was diagnosed with a B. microti infection, lived and worked in a village in Xiapu, Ningde, which was surrounded by abundant shrubs and forests. Our study revealed that the prevalence of B. microti in rodents from shrubs (11.18%), irrigated cropland (4.70%), and forests (4.55%) was significantly higher than in the residential areas (0.99%), suggesting that ecological habitat types played an important role in the spread of B. microti. Furthermore, B. microti would be able to live and reproduce in the wild, which is likely related to the habitat and density of the tick vector [35]. Similar results have been reported in Yunnan [35] and Beijing [3]. The prevalence of B. microti in small mammals in Yunnan from the forest (3.37%) and agricultural areas (1.79%) was significantly higher than in residential areas (0.93%). In Beijing, the positive rate of B. microti from different habitats was shrubs (27.4%), broad-leaved forests (23%), cropland (16%), mixed forests (8.4%), and residential areas (7.2%). It has been reported that forests are an essential risk factor for Babesia infection in Thailand, Cambodia, Lao PDR, and China (Yunnan and Heilongjiang) [32, 35, 36]. Considering that forest areas are burdened with tick-transmitting pathogens, people who work in or travel to forests should take appropriate protective measures. Both Babesia and Plasmodium are intraerythrocytic protozoans and elicit similar inflammatory responses with similar clinical symptoms, which allows them to be easily misdiagnosed [47]. In summary, doctors should pay attention to human babesiosis, while public health agencies should urgently formulate prevention and control measures. Our study found that the prevalence of B. microti in adult rodents (4.53%) was significantly higher than in pubertal rodents (1.10%), which was similar to other studies in Yunnan (2.69% (adult) and 0.37% (pubertal)) [35] and Beijing (13.3% (adult) and 6.2% (pubertal)) [3].
Our study revealed that all the collected Babesia parasites were B. microti from rodents in Fujian Province. This conclusion can be drawn from the abundance of samples detected, which was similar to previous findings in Yunnan [31, 35], Taiwan [29], and Beijing [3]. Phylogenetic analysis suggested that B. microti in this survey shared high homology with those in Zhejiang Province, where a confirmed human babesiosis case was reported in Hangzhou in 2002 following kidney transplantation [44]. Surprisingly, no water buffaloes were infected with Babesia bovis or Babesia orientalis. This varied in comparison to other studies [48, 49], which might be due to insufficient samples and a single sampling location. In addition, both domestic goats and domestic pigs were infected with Babesia spp. We detected B. canis vogeli from the blood of domestic dogs for the first time and the sequence shares high homology with B. canis vogeli from Côte d’Ivoire (GenBank MK495837.1). The prevalence of B. canis in dogs has been previously documented in Henan province [50].
Ovine babesiosis is a tick-borne disease in goats, sheep, and cattle, posing a huge threat to the livestock industry [51–53]. Although the infection rate of ovine babesiosis is extremely low in this study, relevant institutions should pay more attention and strengthen quarantine measures for early detection and treatment. Babesia infection can also be transmitted through blood transfusion when the infected individual is asymptomatic or in the latent period of the infection [30]. Therefore, it is necessary to test Babesia infection in donors when evaluating the risk of blood transfusion. In the future, we will investigate the prevalence of Babesia in different ticks and blood donors to provide scientific evidence for preventing and controlling babesiosis epidemics.
There are limitations to this study. A nested PCR approach was used to investigate the rates of Babesia parasites in mammals in some reports [31, 32]. A large number of samples (n = 1,562) with a high risk of contamination were part of this study, therefore the nested PCR method was not used. Our study showed that the prevalence of B. microti was higher in northern Fujian (Sanming, Nanping, Ningde, and Fuzhou) than in southern Fujian (Putian, Quanzhou, Zhangzhou, and Longyan), which could be due to altitude, as northern Fujian (495 meter) has a higher average altitude than southern Fujian (411 meter). A study in southern Norway has shown that ticks exist at an altitude much higher than previously, with an increased risk of infection of mammals with tick-borne diseases [54]. It was reported that altitude is a risk factor associated with Babesia infections [3, 35]; however, altitude was not taken into account in this study. With the development of the economy and the improvement of living standards in China, the number of domesticated dogs and cats has increased, resulting in B. vogeli cases in dogs and cats [4, 50, 55]. Therefore, it is necessary to monitor Babesia infections in domestic dogs and cats.