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The M. unguiculatus plague focus of the Inner Mongolian Plateau was first confirmed in 1954 (14–15) and is located on the Ulanqab Plateau, in desert grassland on the Ordos Plateau, and in grassland on the Chahar Hills, which are all located at an altitude of more than 1,000 meters. The plague focus is distributed in more than 30 counties in Inner Mongolia, Ningxia, Shaanxi, and Hebei provinces(6). The M. unguiculatus are a species of Mongolian gerbils that are widely distributed in Inner Mongolia and are the representative dominant species in the desert steppe. In nature, they are distributed in one of three patterns: island, banded, and dispersed distributions. In its densest distribution areas, M. unguiculatus can account for up to 79.8% of all rodents species (7). Mongolian gerbils exhibit no hibernation period and are active all year round, resulting in a lack of significant seasonality in plague cases in humans. However, because the life span of M. unguiculatus is only 1–1.5 years, the effect of interanimal immunity caused by plague epidemics among animals is not clear, which is the main characteristic of M. unguiculatus-dependent plague. The main vector insects in this focus are Nosopsyllus laeviceps kuzenkovi, Xenopsylla conformis conformis, and Neopsylla pleskei orientalis (7). The peak season for fleas in M. unguiculatus is the warm season, and the peak season for fleas in the nest is the cold season; thus, fleas infected with plague can exist all year round, especially in winter. The infected fleas have a strong affinity for human blood and can carry Y. pestis throughout the winter. Unlike marmots, which live for more than 10 years, M. unguiculatus have a shorter lifespan, meaning that frequent host renewal occurs during epidemics, which leads to a much weaker immune barrier established during epidemics than in other rodents. The maximum titer of serum antibody in M. unguiculatus was 1∶2,560 under laboratory conditions. However, the serum positive rate was 10%, and the antibody titer was 1∶10,240 for M. unguiculatus caught in an area suffering from recurrent plague epidemics (7). It is precisely because of these characteristics in this focus that the epidemic regularity and epidemic intensity of the M. unguiculatus plague are difficult to predict, making the formulation and implementation of prevention and control measures somewhat difficult.
There was a positive significant correlation between the density of M. unguiculatus and the nocturnal rodent capture rate (r=0.670, p<0.05); a significant correlation between the IHA positive rate of M. unguiculatus and the nocturnal rodent capture rate (r=0.344, p<0.05). Thus, it is suspected that there was an indirect correlation between the density of M. unguiculatus and the IHA positive rate of M. unguiculatus. It is inferred that the density of M. unguiculatus was higher, and the IHA positive rate of M. unguiculatus was higher within a certain range. However, there was a significant negative correlation between the density of M. unguiculatus and the percentage of hosts infested with fleas (r=–0.361, p<0.05), which suggests that an increase in the percentage of hosts infested with fleas would increase the exposure of M. unguiculatus to infected fleas, thereby increasing the probability of plague infection of M. unguiculatus and decreasing the density of M. unguiculatus. This conclusion is consistent with the surveillance data in Southwest China from 2000 to 2015, in which the rat density decreased and the flea rate increased simultaneously (22). Moreover, the density of M. unguiculatus increased in 1984 and 1985 and then dropped in 1986 and 1987.
Surprisingly, plague in humans also occurred in 1986 and 1987 (Figure 1A and 1C). It can be hypothesized that as the density of rats increases, the contact between rats will increase, and the plague will spread among animals. The increase in dead rats caused by the plague reduced the density of rats, which may provide a prerequisite for the occurrence of plague in humans. This thinking is consistent with another study that used rat density as an important parameter in plague prediction models (23).
There was a significant negative correlation between the IHA positive rate of M. unguiculatus and the percentage of hosts infested with fleas (r=−0.337, p<0.05), and a significant negative correlation between the IHA positive rate of M. unguiculatus and the percentage of nests infested with fleas (r=−0.348, p<0.05). These seemingly paradoxical results may stem from the following reasons. The IHA positive rate came from live M. unguiculatus, while the percentage of hosts infested with fleas and the percentage of nests infested with fleas increased, causing the risk of plague infection of M. unguiculatus to increase and the death of infected M. unguiculatus to increase. However, those who survived were often healthy, so the percentage of hosts infested with fleas and the percentage of nests infested with fleas increased, and the IHA positive rate of M. unguiculatus decreased (Figure 3). Therefore, it is necessary to simultaneously conduct pathogenic surveillance, serological surveillance, and vector index analysis of gerbils to accurately reflect the prevalence of plague among local animals.
From 1950 to 1959, the number of cases of plague in Inner Mongolia was relatively high, while the number of cases in the M. unguiculatus plague focus of the Inner Mongolian Plateau was not. The cases of plague appeared and disappeared alternately after 1960 in the M. unguiculatus plague focus of the Inner Mongolian Plateau (Figure 1 and Figure 2). A large number of studies have confirmed that plague foci have alternating periods of rest and activity (22–24). In Inner Mongolia, the M. unguiculatus plague focus of the Inner Mongolian Plateau has alternating periods of rest and activity, while other plague foci of Inner Mongolia are in a resting state. Therefore, this suggests that the target of plague prevention strategies should be the M. unguiculatus plague focus of the Inner Mongolian Plateau. Combined with the data of Y. Pestis isolates, it can be concluded that a large number of isolates can still be detected in the environment and in hosts when the plague focus is at rest, indicating that the plague is still epidemic among animals. In the initial stage of plague prevention and control (1950–1959), the prevention and control of plague and the economy in China were both weak points, and the plague caused by M. unguiculatus was generally mild in human patients, so attention was focused on severe patients. After the 1950s in Inner Mongolia, there were only sporadic cases of the plague in the M. unguiculatus plague focus of the Inner Mongolian Plateau, and the expansion of the plague focus due to land desertification may also have been the reason for the sporadic and increasing cases in this focus. In the plague eradication stage (1960–1979), it was believed that unilateral eradication of the host would eradicate the plague, so intensive rodent extermination efforts were carried out in the plague focus. Although such measures cannot eradicate the plague, the reduction of the host could reduce the risk of the spread of plague to some extent. This may explain the high detection rate of plague in animals in the 1970s but with relatively few human cases. In the plague surveillance stage (1980–1999), China gradually formed a plague surveillance system, and the prevention and control measures were more targeted. At this stage, as during the previous stage, the plague in humans was still sporadic, and the plague in animals continued to be epidemic. In the comprehensive prevention and control stage under the emergency system (2000–2019), the emergency system was added on the basis of surveillance, and more timely and effective measures could be taken to prevent and control the plague. Interestingly, unlike the previous two stages in which the spatial distribution of the plague in humans was relatively dispersed, the cases in the comprehensive prevention and control stage were distributed in four adjacent counties. In 2019, a simultaneous rise in plague cases in humans and plague cases in animals appeared. Therefore, it should be noted that the plague in this focus is excessively active and shows a great risk of transmission.
Plague prevention and control in the Inner Mongolia Autonomous Region of China remain a critical issue. The M. sibirica plague focus of the Hulun Buir plateau, which presents a potential risk of reactivation, has not experienced an epidemic of plague in animals and humans for nearly a hundred years. The S. dauricus plague focus of the Song-Liao Plain, which is in a resting stage, presents a possibility of outbreaks at any time due to an extremely low plague prevalence among animals (22). With the serious desertification of grasslands in recent years, the M. unguiculatus plague focus of the Inner Mongolian Plateau, where enzootic and plague in humans are currently prevalent, has been expanding; and the threat to people has been increasing. Although enzootic plague is continuously prevalent in the M. brandti plague focus of the Xilin Gol League plateau, it has not posed any threat to human beings. With the evolution of the strains, the risk of human infection still exists. Therefore, the comprehensive prevention and control of the Inner Mongolian plague should focus on the M. unguiculatus plague focus of the Inner Mongolian Plateau.
In addition, the Inner Mongolia Autonomous Region is also in danger of importing plague cases from abroad. There are active natural foci in neighboring Mongolia and Russia. The two countries share a border with Inner Mongolia that stretches more than 4,000 kilometers and presents dozens of interchanging ports. In addition, many adjacent areas are natural plague foci that are active or resting for many years. Most of the border lines are not separated by natural barriers. The natural foci are connected as a whole, and enzootic plague can spread among animals (25–29). From 2019 to 2020, more than 20 suspected sporadic cases of plague in humans were reported in natural marmot plague foci in Mongolia (13). This shows that the Mongolian marmot plague is extremely active in Mongolia, and these foci are connected with the M. sibirica plague focus of the Hulun Buir Plateau. Although the M. sibirica plague focus of the Hulun Buir Plateau has been resting for nearly a hundred years, it previously caused disasters in northeast China (9-12). The M. sibirica plague focus of the Hulun Buir Plateau presents potential danger of reactivation. Therefore, there is a double risk of plague resurgence in the M. sibirica plague focus of the Hulun Buir Plateau and the plague epidemic in the M. unguiculatus plague focus of the Inner Mongolian Plateau, which greatly increases the difficulty of local prevention and control.
To prevent and control the resurgence of plague in the M. sibirica plague focus of the Hulun Buir plateau, it seems necessary to do health education on forbidding the flaying and eating of marmots. In the natural plague foci of marmots in China and Mongolia, the plague in humans is mainly contracted through wounds when flaying and eating infected marmots (30–31). Few cases have been caused by the consumption of raw marmot meat, which were eventually followed by septicemic plague or pneumonic plague (32). Unlike the marmot plague foci, human cases in other plague natural foci were mostly caused by fleabites (22). However, it should be noted that in the vast grazing region, due to special methods of food storage, infected rats may occasionally directly contaminate food, and domestic cats might also contaminate food (dried meat, cheese, etc.) by eating infected rats together with food stored by herdsmen. Then, herdsmen eating contaminated raw food could cause enteric plague. For example, the first case of pneumonic plague among herdsmen in Inner Mongolia in 2019 is likely to have developed from enteric plague because the earliest symptoms of this case occurred acutely in the abdomen (16). Therefore, in M. unguiculatus plague foci, attention should be paid to not only the carriage status in fleas but also the possibility of plague spreading through the digestive tract. In the M. unguiculatus plague focus of the Inner Mongolian Plateau, in addition to the traditional dissemination of health information about plague prevention, it is also necessary to promote knowledge about healthy eating habits among herdsmen.
Our study addressed the epidemic and distribution characteristics both of human and plague in animals from 1950 to 2019. We found that the plague occurring in the M. unguiculatus plague focus of the Inner Mongolian was sporadic. In recent years, cases have been gradually confined to the four neighboring counties, and reported cases are on the rise. It is necessary to be vigilant against possible outbreaks of plague in humans in this epidemic area. In addition, we predict that the trend of rodent density will first rise and then fall and be a prerequisite for the occurrence of plague in humans in the M. unguiculatus plague focus of the Inner Mongolian Plateau. The threat of plague resurgence in the M. sibirica plague focus of the Hulun Buir Plateau, coupled with the sporadic plague that occurred in the M. unguiculatus plague focus of the Inner Mongolian Plateau, has posed a new challenge to the control of plague in Inner Mongolia.
Funding: This work was supported by National Major Science and Technology Projects of China (2018ZX10713-003-002, 2018ZX10713-001-002).
Acknowledgment: American Journal Experts (Sub ID YNR9ZR12).
Figure 1.Distribution over time of plague in humans and animals in the Inner Mongolian Autonomous Region.
(A) Distribution over time of plague in humans in the Inner Mongolian Autonomous Region from 1950 to 2019. (B) Distribution characteristics of Yersinia pestis isolates detected in the Inner Mongolia Autonomous Region from 1950 to 2019. (C) Distribution characteristics of pathogenic and serological detection results of plague hosts in the Inner Mongolia Autonomous Region from 1981 to 2019.Figure 2.Spatial distribution of the Meriones unguiculatus plague focus on the Inner Mongolian Plateau from 1950 to 2019.
Year County Number of cases 1954 Hangjinhou 8 1970 Sunitezuo 1 1970 Wulatezhong 1 1972 Shangdu 1 1986 Wulateqian 2 1987 Etuokeqian 2 1991 Siziwang 1 2004 Suniteyou 1 2019 Sunitezuo 2 2019 Siziwang 1 2019 Xianghuang 1 Table 1. Distribution of plague cases in humans in the natural plague focus of Meriones unguiculatus on the Inner Mongolian Plateau from 1950 to 2019.
Item The third stage (1981–1999) The fourth stage (1999–2019) Total (1981–2019) Investigation area of M. unguiculatus (ha) 20,788.95 26,533.00 47,321.95 Density of M. Unguiculatus (/ha) 4.50 3.49 3.93 Nocturnal rodent capture rate (%) 4.55 3.43 3.98 Percentage of hosts infested with fleas (%) 23.04 27.83 25.56 The host-flea index 0.57 0.76 0.67 Percentage of the passage of burrows infested with nomadic fleas (%) 2.39 11.53 6.96 The index of nomadic fleas at the passage of burrows 0.09 0.24 0.16 Percentage of nests infested with fleas (%) 55.79 59.81 57.91 The nest-flea index 8.40 8.22 8.31 M. Unguiculatus positive rate (%) 1.15 0.55 0.87 Flea positive rate (%) 2.15 1.61 1.88 Indirect hemagglutination assay positive rate of M. unguiculatus (%) 1.39 0.42 1.06 Table 2. The epidemiological characteristics of host (Meriones unguiculatus) and vector surveillance in the Inner Mongolian Autonomous Region from 1981 to 2019.
Figure 3.Correlation analysis scatter plot and chi-squared test results of plague-related factors among animals in the natural plague focus of Meriones unguiculatus (M. unguiculatus) on the Inner Mongolian Plateau.
(A) The positive rate of M. unguiculatus and the positive rate of the flea group. (B) Density of M. unguiculatus and the nocturnal rodent capture rate. (C) Density of M. unguiculatus and the percentage of hosts infested with fleas. (D) IHA positive rate of M. unguiculatus and the nocturnal rodent capture rate. (E) Indirect Hemagglutination Assay (IHA) positive rate of M. unguiculatus and the percentage of hosts infested with fleas. (F) IHA positive rate of M. unguiculatus and the percentage of nests infested with fleas.Factor b χ2 p Intercept 0.140 64.717 <0.000 Density of M. unguiculatus (/ha) –0.001 3.237 0.072 Nocturnal rodent capture rate 0.076 0.628 0.428 Percentage of hosts infested with fleas (%) –0.019 0.771 0.380 The host-flea index –0.011 5.394 0.020 Percentage of nests infested with fleas (%) –0.241 46.991 <0.000 The nest-flea index 0.003 46.320 <0.000 Percentage of the passage of burrows infested with nomadic fleas (%) –0.192 11.680 0.001 The index of nomadic fleas at the passage of burrows 0.055 4.576 0.032 Table 3. Generalized linear model parameters of the indirect hemagglutination assay (IHA) positive rate of Meriones unguiculatus (M. unguiculatus) in the plague natural focus of M. unguiculatus on the Inner Mongolian Plateau.
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