1. Introduction
Bovine paratuberculosis (PTB), also known as John’s disease, is a chronic gastrointestinal infectious disease of ruminants caused by
Mycobacterium avium subsp. paratuberculosis (MAP) [
1,
2]. PTB is classified as a Class B animal disease by the World Organization for Animal Health and as a Class II animal disease in China. Diagnostic approaches to PTB detection are different for dairy cows; large-scale bovine PTB is usually diagnosed by ELISA using blood or milk samples, and fecal samples are often used in small-scale PTB studies (fecal suspension followed by supernatant). MAP is a small Gram-positive bacillus that is resistant to cold, dryness, certain acidic environments, and ultraviolet radiation, which is widely prevalent around the world [
3]. MAP strains are divided into three subtypes, namely type I (sheep type), type II (cattle type), and type III (pigmented type), based on culture characteristics and pathogenicity; the bovine strain, in particular, infects not only cows but other species as well [
4,
5,
6]. In addition, it is an intracellular, parasitic acid-fast-staining-positive bacterium. The use of antibiotics to treat this only relieves clinical symptoms and does not completely eradicate the disease. Previous research indicated that cow farms suffered serious economic losses due to the fact that the incubation period of bovine PTB ranges from several months to several years, with the total annual economic loss per cow ranging between USD 21 and 79 in the US [
7]. Currently, no available treatment drugs and vaccines have been reported for this disease either.
Previous studies report that PTB infection is highly associated with health and fertility issues in dairy cows, particularly in their productivity, reproductive performance, lameness incidence, and lying behavior during peak lactation [
8,
9]. MAP infections have seriously damaged milk production, calving intervals, and milk fat/milk protein content in infected cows [
10,
11]. PTB is transmitted through the placental barrier to newborn calves either horizontally or vertically, thus increasing the risk of transmission and spreads in the herd [
12]. Therefore, the best way to eradicate the disease is to detect, isolate, and eliminate infectious dairy cows.
In recent years, PTB infection has become widely prevalent around the world, not only affecting domestic and wild ruminants globally but also affecting non-ruminants and carnivores, among others [
13,
14,
15]. Previous studies indicate that the true herd-level prevalence in dairy cattle herds is estimated to be 19.6%, 9.8%, 6.3%, 3.6%, 9.4%, and 18.4% in Hungary [
16], Brazil [
17], Chile [
18], Switzerland [
19], Italy [
20], and Spain [
21], respectively. For dairy animals in the USA, the prevalence of PTB infection has been reported to reach up to 5–10%, and it is 33% in herds [
22]. In addition, a report indicated that the PTB prevalence in infected cows increased with age and somatic cell count according to MAP test results, while milk yield, milk protein, and milking days are negatively correlated with MAP infection [
23]. Meanwhile, the incidence of PTB also exhibited an up-regulated trend in China [
24,
25].
Mycobacterium paratuberculosis avium subspecies is structurally similar to
Mycobacterium tuberculosis antigens and is prone to exhibit immune cross-reaction, so the discrimination method must be accurately grasped. Therefore, the study aims to investigate the correlation of MAP infection with the milk production performance, health status, and reproductive performance of dairy cows in Xi’an city (from 2021 to 2024), with the objective of providing data support for the clinical eradication and prevention strategies for bovine PTB.
4. Discussion
PTB has become widespread in dairy farms, causing serious damage to dairy cows’ milk production and making the adoption of prevention and control measures difficult. According to relevant reports in China, the PTB antibody prevalence in dairy cows was 9.25% in Beijing, 5.73% in Gansu, 17.44% in northern Xinjiang, 14.10–86.67% in Shandong and Ningxia, and 4.31% in Heilongjiang Province. The same results were discovered in Pakistan and Ecuador, which exhibited that the prevalence of PTB was 3.8% and 25%. The above results confirmed that PTB is prevalent in major dairy farming areas in China, and there are differences in various regions of each country around the world. An analysis of the survey data showed that the prevalence of bovine PTB in a farm from Xi’an city has dropped from 6.76% to 3.58% as a result of continuous monitoring and elimination over the past three years. In addition, a previous study reported that herd scales, the purchase of cattle from unknown MAP infection status, and different feeding methods for calves play an important role in the MAP positivity rate of an entire farm [
26]. Therefore, we can pay sufficient attention to preventing and controlling MAP infection, especially in areas where the prevalence of MAP among cattle herds is high.
Our results found that the PTB prevalence in dairy cows was gradually increased with the increase in parity, which was inconsistent with the results of Bates A in New Zealand, because it was higher in primiparous dairy cows than in multiparous dairy cows in two out of three years according to PTB prevalence statistics [
27]; the difference might be associated with the immune system and the increasing parturition number. The results also exhibited that the milk fat content increased from 3.61% to 4.11%, exceeding the national standard milk level at 4%. The milk protein content increased from 3.28% to 3.41%, the ratio of fat to protein in milk increased by 0.13%, the somatic cell count in milk decreased by 10.2 × 10
3 mL
−1, the somatic cell count in milk decreased by 0.52 × 10
3 mL
−1, the milk loss decreased by 0.38 kg, the peaked milk production increased by 0.11 kg, and the duration was extended by 1.87 days. The number of monthly diarrhea occurrences decreased from 18.75 to 10.33 cows, the number of artificial inseminations decreased by 0.32 cows, the number of monthly endometritis occurrences decreased by 0.16 cows, the calving interval decreased by 4.43 days, the pregnancy at the first service increased by 0.35%, and the number of monthly mastitis occurrences increased by 16.9 cows. The above results indicated that continuous monitoring and active elimination of PTB-antibody-positive cows not only had a positive effect on milk quality, but also significantly reduced the occurrence of some reproductive diseases, including endometritis and mastitis, which is consistent with the previous results [
28,
29,
30]. The change in daily milk yield was not obvious in the 2022–2023 year. Meanwhile, we speculated that the decrease in the 305-day milk yield, peak day, and lactation time of the herd may be correlated to the milking disinfectant products or the non-standard disinfection operations of milking workers [
31]. In addition, the monthly occurrence of mastitis and the trend of the milk protein rate are consistent, which may be associated with the increasing number of milking times for cows during the peaking lactation period to improve economic benefits in large-scale dairy farms, thereby increasing the mastitis infection rate by promoting the permeability of mammary epithelial cells and the blood–milk barrier, resulting in an increase in the milk protein rate. Meanwhile, the milk fat rate and milk protein rate of high-yielding dairy cows in actual measurements were reduced due to the influence of the “dilution effect” [
32]. Laszlo et al. reported that the somatic cell count in positive cow’s milk (35.8%) was higher than that of negative cows on average [
33], which is basically consistent with the results in our study showing that the somatic cell count in milk in the 2022–2024 year was higher (45.0%) than that in the 2023–2024 year. The annual increase in urea nitrogen in milk may be caused by the fact that breeders increased the protein content in the feed to improve milk quality, and in a previous study, it was confirmed that controlling the quality of milk consumed by calves cannot prevent the spread of MAP infection [
34]. Therefore, changing feed formulations with parity-specific protein levels could be considered to optimize protein utilization efficiency in future breeding programs.
Antibodies directed against MAP epitopes could be detected in milk and other specimens as well as in serum. Cattle that are infected with tuberculosis will continue to excrete bacteria through feces. Currently, the specific diagnostic method for quarantine monitoring of cattle herds is the tuberculin test, and there are no other diagnostic methods for relatively easy performance at a low cost. Mycobacterium PTB can also produce tuberculin, and the PTB test was conducted on tuberculosis-positive cattle from 2021 to 2024. The result showed that the repetition rate of tuberculosis and PTB-positive cattle numbers in the 2021–2022 year was 85.71%, and it completely overlapped with that in the 2022–2024 year, indicating the accuracy of the bovine PTB test. In addition, the monthly expenditure on veterinary drugs, vaccines, and medical consumables in the 2023–2024 year was less than that in the 2021–2022 year, and the monthly expenditure on diarrhea-related drugs decreased year by year. In an analysis of economic losses due to reduced milk production and reproductive performance associated with bovine PTB in Switzerland, the total annual loss of PTB-positive cows was USD 1.3 × 10
9 [
35]. It is worth pointing out that this finding was not attributed to the efficacy of diarrhea medications, but rather to preventing and controlling the disease through a combination of regular quarantine, isolation, and culling, as well as effective biosecurity management [
36]. It is worth noting that farms will need to continue to invest in regular tests and culling when eradicating bovine PTB through testing and culling alone. Therefore, the cost-effectiveness of a herd-scale testing and selective culling strategy is measured by the number of positive cows on a farm, maximizing the cost-saving investment. In public health contexts, bovine PTB (
Mycobacterium avium subspecies PTB) presents zoonotic transmission risks through the food chain, posing significant public health risks, including its potential association with human rheumatoid arthritis [
37,
38,
39]. Consequently, implementing comprehensive control strategies for bovine PTB not only serves as a prerequisite for ensuring sustainable dairy production systems but also represents a critical intervention for safeguarding public health security.
In summary, bovine PTB is a disease that seriously endangers the healthy breeding of dairy cows, and it is highly contagious and lacks available treatment drugs, thereby resulting in a significant reduction in dairy cow production. Meanwhile, the almost ineffective treatment costs will cause great economic losses for farms. Therefore, there is an urgent need to strictly control the spread of the disease by conducting quarantine, isolation, and elimination measures.