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Plague is a zoonotic disease caused by Yersinia pestis (Y. pestis), with rodents serving as reservoir hosts and fleas as vectors (1). Humans can contract plague through exposure to infected rodents, their fleas, or other infected humans. Historically, 3 plague pandemics have resulted in significant human casualties (2). Plague continues to pose a public health problem in Asia and globally (3-4).
Inner Mongolia Autonomous Region, in northern China, has the greatest longitudinal span of any provincial-level administrative division (PLAD). Annual rainfall ranges from 50 to 450 mm, and monthly average temperatures range from −28.6 to 27.3 ℃. This diverse geography supports various rodent species and their fleas, creating four natural plague foci (5). From 2019 to 2023, the Inner Mongolia Autonomous Region reported a cumulative total of 14 human plague cases. Therefore, systematic ecological monitoring of rodent hosts and vector fleas, along with scientific data analysis, is imperative to guide local plague prevention and control efforts.
This study summarizes rodent and ectoparasitic flea data from 12 regions in Inner Mongolia from 2013 to 2021. A spatiotemporal analysis of the flea index on predominant rodent species was conducted. Based on cluster analysis, different preventative measures were proposed for geographical areas with varying plague surveillance characteristics. This study provides a basis for the reasonable allocation of surveillance resources and effective plague prevention and control.
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Plague data from Inner Mongolia from 2013 to 2021 were obtained from the National Plague Surveillance System. Plague surveillance was performed in regions in Inner Mongolia, including parasitism rate, plague cases, host density, flea index, and rate of positive fleas.
Surveillance was conducted primarily in accordance with the National Plague Surveillance Program (6) in both plague-focus and non-focus counties using fixed and mobile sites for comprehensive animal plague monitoring. Stratified sampling, representing 0.5% of habitats, was implemented. Captured rodents were individually bagged, anesthetized with ether, and examined for fleas using a fine brush in a white porcelain basin. The collected fleas were classified and counted.
The flea infestation rate was calculated as the proportion of rodents with fleas relative to the total number of rodents inspected. The host-flea index was calculated by dividing the total number of fleas by the number of rodents inspected.
Fleas were tested for Y. pestis using the stomach pumping method. Fleas from the same host, species, and location were grouped (10–20 fleas per group) for testing. All procedures adhered to the Determination for natural plague foci and plague epizootics (7).
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Flea indices for different rodent species were analyzed using the Kruskal-Wallis H test and Dunn’s test for multiple group comparisons. The Mann-Kendall test was used to analyze trends in the interannual variations of the flea indices. Hierarchical cluster analysis was used to cluster the surveillance data and determine plague risk zones. Statistical analyses were performed in R 4.2.2 (R Foundation for Statistical Computing, Vienna, Austria). A two-tailed test was conducted with a significance level of 0.05.
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From 2013 to 2021, 134,181 rodents belonging to 28 species were captured in Inner Mongolia. Of these, 42,216 were infested with fleas, yielding an average flea parasitism rate of 31.46%. A total of 143,958 fleas were captured, with a flea index of 1.07. The predominant rodent species were the Mongolian gerbil Meriones unguiculatus (M. unguiculatus) (44.04%) and the Daurian ground squirrel Spermophilus dauricus (S. dauricus) (36.65%). S. dauricus exhibited a higher flea parasitism rate (38.82%) and flea index (1.49) than M. unguiculatus (24.80% and 0.64, respectively). Rodent population and parasitic status are shown in Table 1.
Species Number of rodents Number of rodents parasitized by fleas Flea parasitism
rate (%)Number of fleas Flea index Meriones unguiculatus 59,096 14,656 24.80 37,937 0.64 Spermophilus dauricus 49,171 19,089 38.82 73,176 1.49 Microtus brandti 8,374 2,748 32.82 6,930 0.83 Meriones meridianus 3,835 1,091 28.45 3,190 0.83 Cricetulus barabensis 3,423 826 24.13 1,644 0.48 Allactaga sibirica 2,905 1,091 37.56 3,685 1.27 Rhombomys opimus 1,566 1,165 74.39 12,890 8.23 Phodopus roborovskii 1,287 131 10.18 275 0.21 Dipus sagitta 1,023 308 30.11 762 0.74 Phodopus sungarus 640 220 34.38 616 0.96 Cricetulus migratorius 543 249 45.86 819 1.51 Spermophilus erythrogenys 497 209 42.05 664 1.34 Lagurus luteus 456 147 32.24 492 1.08 Mus musculus 357 9 2.52 37 0.10 Cricetulus eversmanni 309 100 32.36 365 1.18 Marmota bobak 193 33 17.10 76 0.39 Spermophilus alaschanicus 125 76 60.80 137 1.10 Euchoreues uaso 117 16 13.68 84 0.72 Rattus norvegicus 116 9 7.76 15 0.13 Marmota himalayana 74 33 44.59 132 1.78 Myospalax aspalax 25 1 4.00 11 0.44 Eutamias sibiricus 18 0 0.00 0 0.00 Scirtopoda telum 17 6 35.29 18 1.06 Microtus gregalis 7 1 14.29 0 0.00 Cardiocranius paradoxu 3 0 0.00 0 0.00 Apodemus agrarius 2 0 0.00 0 0.00 Cricetulus triton 1 1 100.00 2 2.00 Salpingotus kozlovi 1 1 100.00 1 1.00 Total 134,181 42,216 31.46 143,958 1.07 Table 1. The rodent host and flea vector surveillance in Inner Mongolia, 2013–2021.
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The Mann-Kendall test indicated that the total flea index, as well as the flea indices of M. unguiculatus, S. dauricus, and other rodents, all exhibited a declining trend (
Supplementary Table S1 ). However, the decreasing trend in the flea index for the two predominant rodent species was not significant (P>0.05). The distribution of flea indices among M. unguiculatus, S. dauricus, and other rodents was not identical (H=20.38, P<0.001) according to the Kruskal-Wallis H test (Supplementary Table S2 ). Pairwise comparisons using Dunn’s test revealed a statistically significant difference in flea indices between M. unguiculatus and S. dauricus (P<0.001). Figure 1 shows that M. unguiculatus was recorded throughout the year. Two seasonal peaks occurred, in May and October, while the peak flea index occurred in August. S. dauricus was detected only from March to December, with the highest numbers in May, and the flea index was higher in March and November. Other rodents showed higher numbers in May and September, with peak flea indices occurring in March and October.
Figure 1.Seasonal trends in rodent numbers and flea indices in Inner Mongolia, 2013–2021.
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Geographically, M. unguiculatus was the predominant species in Wuhai, Ulanqab, Hohhot, Bayan Nur, Baotou, and Erdos, while S. dauricus was more common in Chifeng, Tongliao, Hulun Buir, and Hinggan League. Both rodent species had a high proportion in the Xilingol League, but Meriones meridianus was more frequent in the Alxa League, as shown in Figure 2.
Figure 2.Rodent species composition in regions of Inner Mongolia during 2013–2021.
Overall, Erdos and Wuhai had relatively high cumulative flea indices in M. unguiculatus from 2013 to 2021, as shown in
Supplementary Table S3 . The Kruskal-Wallis H test indicated a significant overall difference among the regions (H=25.75, P<0.001). Pairwise comparisons revealed that the flea index in Erdos was significantly higher than that in Hohhot (P<0.01), and the flea index in Wuhai was significantly higher than that in Hohhot and Ulanqab (P<0.05), as shown inSupplementary Table S4 .Similarly, Xilingol League consistently exhibited a high flea index from 2013 to 2021, as shown in
Supplementary Table S5 . The Kruskal-Wallis H test revealed a significant overall difference among the regions (H=29.88, P<0.001). Pairwise comparisons indicated that the flea index in Xilingol League was significantly higher than that in Chifeng, Hinggan League, Hulun Buir, and Tongliao (P<0.01), as shown inSupplementary Table S6 . For the specific spatial distribution year by year, see attachedSupplementary Tables S3 andS5 . -
After clustering based on parasitism rate, flea index, flea positive detection rate, number of plague cases, and host density, 12 regions were grouped into 3 categories (Figure 3). Xilingol League and Bayan Nur clustered together, characterized by high flea indices (1.57 and 1.52) and the highest number of plague cases (3 and 2). The 3 regions represented by Erdos were characterized by a high parasitism rate and high rodent density. The remaining 7 regions were characterized by low flea parasitism rates and minimal positive flea detection rates.
Figure 3.Cluster analysis of host-vector-pathogen-plague cases in the Inner Mongolia, 2013–2021.
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In the current study, 28 rodent species were detected. The predominant species, M. unguiculatus and S. dauricus, accounted for approximately 80%. Despite the greater number of M. unguiculatus, S. dauricus exhibited a higher flea parasitism rate and flea index. This difference may be partly attributable to the larger size of S. dauricus compared to M. unguiculatus. Furthermore, M. unguiculatus, being social rodents with close intergroup social connections (8), likely reduce flea parasitism through mutual grooming.
This study analyzed the temporal trends of flea indices on annual and monthly scales. Annually, the observed decline in flea indices for the two predominant rodent species may be attributed to the implementation of ongoing and effective human flea control measures. For instance, following a series of rodent and flea control interventions in plague-endemic areas, such as the significant reduction in rodent density and flea parasitism rates observed in the M. unguiculatus habitats in 2021, there has been a notable decrease in these indicators (9). The Monthly lag effect of the rodent population and flea index may play a positive role in local plague prevention and control. Therefore, some studies used the flea index to predict outbreaks of rodent plague (10). However, due to the flea index’s instability, the predictive accuracy of many studies was limited (11). This suggests that flea and rodent control efforts in early spring and late summer may yield better results in preventing and controlling plague in Inner Mongolia.
This study showed that S. dauricus predominated in the eastern Xilingol League, while M. unguiculatus was more common in the west (excluding the Alxa League). However, both species coexisted in the Xilingol League. The total flea index of M. unguiculatus in Erdos and Wuhai was higher than in other cities in previous years. This is likely because most counties in these 2 cities are located within natural plague foci for M. unguiculatus and have a long history as plague-endemic areas (12). This plague focus is primarily centered on the Ordos and Ulanqab Plateaus, and recent research has confirmed the continued plague prevalence in the Ordos Plateau region (13). This study showed that the geographic center of the flea index changed dynamically. In 2015, Bayan Nur had the highest flea index, while in 2018, the Xilingol League had the highest. Both areas have reported human plague cases in recent years (14). This further underscores the close relationship between the flea index and plague occurrence.
Over the past several years, the flea index of S. dauricus in the Xilingol League has remained consistently high, surpassing neighboring areas and peaking at 4.69 in 2014. Quantitative analysis indicates that sustaining the spread of Y. pestis requires more than 3.9 Xenopsylla cheopis fleas per host rodent (15). Previous studies have divided this natural plague focus into the Songliao Plain and Chaha Hills regions (16). Consequently, a high flea index may signal a risk of a local plague outbreak. If rodent plague occurs, the elevated flea index increases the likelihood of spreading to other animal populations and spillover into humans, raising the risk of a plague epidemic. Additionally, this study showed that the flea indices for both M. unguiculatus and S. dauricus in this area have been consistently high, posing significant challenges for local plague prevention and control.
Regional collaboration is effective for controlling epidemics. This study classified the 12 regions of Inner Mongolia into three zones based on cluster analysis and plague surveillance indicators, recommending customized control measures for each zone. Zone A (many plague cases and a high flea index) should enhance grassroots capacity for detecting human plague, preventing its spread to larger cities, and implementing effective flea eradication measures. Zone B (high parasitic flea rate and rodent density) should intensify rodent density management and implement rodent eradication measures. Zone C (low parasitic flea and positive rates) should regularize monitoring efforts and health education to maintain a low plague risk.
Our study had some limitations. Due to variations in rodent and flea control measures across PLADs, and fluctuations in plague incidence among rodents, flea-to-host ratios may shift, introducing bias. Given the limited availability of relevant plague monitoring indicators, the resulting risk zone classifications may not be as comprehensive as desired.
In this study, we described the rodent and flea species composition in the Inner Mongolia Autonomous Region from 2013 to 2021. We primarily identified the flea parasitism status of two predominant rodent species, analyzed the spatiotemporal characteristics of the host and ectoparasite, and delineated plague risk areas based on plague surveillance data. These studies can provide valuable information for developing strategies and policies to prevent and control plague outbreaks in the Inner Mongolia Autonomous Region.
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We gratefully acknowledge the Chinese Center for Disease Control and Prevention for their legitimate software support and administrative assistance. We also thank Steven Su for his invaluable assistance in the language review of this manuscript.
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Surveillance Data
Statistical Analysis
Rodent Species and Flea Parasitism Status
Temporal Distribution Analysis
Spatial Distribution Analysis
Classification of Risk Zones
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