Effects of Altitude on the Transmission of Alveolar Echinococcosis

Yuxia Zhang and Kong Yang*

Institute of Qinghai-Tibet Plateau, Southwest Minzu University, P.R. China

ABSTRACT

Alveolar echinococcosis is an important cestode diseases with a huge public health impact, it caused by larval of Echinococus multilocularis, whose life cycle requires a variety of canids and small mammals as hosts. The terminal hosts have received a lot of attention, while there are few studies on the distribution and abundance of intermediate hosts. A structural equation model was produced to demonstrate the effects of habitat factors on the distribution and abundance of intermediate hosts of E. multilocularis. Plateau pika (Ochotona curzoniae) act as the main intermediate hosts of E. multilocularis, whose effective cave density was 0.03/m2 to 0.32/m2, and it was negatively correlated with altitude at a high value (p = 0.010). Altitude regulates the distribution and abundance of plateau pika by influencing food resources and their fertility, which in turn affects the transmission of alveolar echinococcosis.

Article Information

Received 28 April 2021

Revised 05 June 2021

Accepted 25 June 2021

Available online 07 January 2022

(early access)

Published 19 July 2022

Authors’ Contributions

KY designed and directed the study. KY and YZ carried out investigations, analysed and wrote the manuscript.

Key words

Alveolar echinococcosis, Echinococus multilocularis, Intermediate hosts, Plateau pika, Ochotona curzoniae.

DOI: https://dx.doi.org/10.17582/journal.pjz/20210428030426

* Corresponding author: lx-yk@163.com

0030-9923/2022/0005-2485 $ 9.00/0

Copyright 2022 by the authors. Licensee Zoological Society of Pakistan.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Alveolar echinococcosis (AE) is a parasitic disease caused by larval of Echinococus multilocularis, whose life cycle requires a variety of canids and small mammals as hosts. As the lack of obvious symptoms in 60%-75% of the patients, the disease has a high mortality due to the delayed start of treatment (Belard et al., 2016). The one-year postoperative mortality of AE patients was higher than that of cystic echinococcosis, another important cestode diseases with a huge public health impact globally, and the 10-year mortality of untreated AE patients was 94% (Mengyuan et al., 2018). AE has been described as a kind of parasitic cancer, the most serious zoonosis in temperate and Arctic regions of the Northern Hemisphere, and one of the top ten parasitic diseases by the World Health Organization (Jenkins, 2001; Zhenghuan et al., 2008; Guoqiang et al., 2019).

In China, E. multilocularis is mainly seen in Tibet Plateau, where not only has a large number of mammals as hosts, but also has low temperatures as well as dry climatic conditions, which can help their eggs survive. As a result, the AE prevalence in Tibetan plateau was significantly higher than that in non-Tibetan plateau areas (Weiping et al., 2018; Sihui et al., 2020). Shiqu County, located on the southeastern margin of Tibet Plateau, is one of the most seriously endemic areas in the world, with the serological positive rate among residents was as high as 95.4% in 2008, and the morbidity rate was 12.09% in 2007-2013 (Deyou et al., 2008). Although humans are unsuited and dead-end intermediate hosts for E. multilocularis, people who live there suffer a lot.

Serve as a source of infection, the terminal hosts have received a lot of attention. Fox is a kind of main terminal hosts for E. multilocularis in Tibet Plateau. But in fact, the Tibetan fox has been listed as the second class in the List of Wildlife under Key State Protection of China (Ministry of Agriculture and Rural Affairs of the People’s Republic of China, 2021). In addition, there are many stray dogs and domestic dogs in the Tibetan Plateau act as terminal hosts. It has been found that the spread of infected dogs plays an important role in transmission of AE (Junli et al., 2017). Then, a comprehensive control of echinococcosis in Shiqu County has been launched by the Chinese government since 2015. On the one hand, stray dogs in large numbers have been captured or killed. On the other hand, the expelling parasite control for domestic dogs was strictly enforced monthly. By building a harmless treatment tank for dog feces, it was cut off that the channel of environmental pollution through E. multilocularis eggs from dog fecal (Mingzhong et al., 2017). Besides, there are more than 40 kinds of small mammals that act as intermediate hosts for E. multilocularis in China. The infection rate of genus Microtus was 0.1% and that of genus Ochotona was close to 10% (Tang et al., 2004; Zhenghuan et al., 2008). They also play an important role in transmission of AE. However, there are few studies on the distribution and abundance of intermediate hosts. Therefore, it would be necessary to analyze the relationship between intermediate hosts and habitat factors, which will help to clarify the distribution and abundance of intermediate hosts, and provide a theoretical basis for the AE prevention.

Materials and methods

The intermediate hosts density was determined by the block-open method. 32 sample sites were choosed at random in Shiqu County, Sichuan province, China.

The sample sites were 25 m×25 m squares, with an altitude of 3924 m to 4249 m. The number of blocked caves was 47 to 226 among 32 sample sites, which depended on the number of caves in the sites (Supplementary Table I). Some indicators were recorded the next day, including the number of effective caves, the intermediate hosts species, and the distances from the sample sites to rivers, roads and human settlements. Caves provide mall mammals with shelter and protection, thus the number of effective caves can represent their density to some extent.

Then a structural equation model (SEM) was constructed by Amos software to analyze the relationship between the number of effective caves and other factors.

Results

In our study, as shown in Supplementary Table I, the number of effective caves was 17 to 201 per sample sites. That is to say, the effective cave density of the intermediate hosts was 0.03/m2 to 0.32/m2. As for the species, the investigation found that all intermediate hosts were plateau pika except in one sample quadrat that had rodent mammals (Lasiopodomys fuscus), thus plateau pika is the main intermediate hosts for E. multilocularis in Shiqu County.

In addition, the distances from the sample sites to the rivers, roads and human settlements were 30 m to 3000 m, 10 m to 800 m, and 0.21 m to 3000 m, respectively. Our SEM fits well with the following parameters: p = 0.411, RMSEA = 0.029, CFI = 0.945, CHI/DF = 1.025 (Fig. 1), because a SEM is regarded to match the data when p > 0.05, RMSEA < 0.08, 0.9 < CFI < 1, 1 <CHI/DF <3 (1 <CHI/DF < 2 is better). The model shows that the number of effective caves was directly affected by altitude with standardization coefficients of -0.40 (p = 0.010), and 48% of the number of effective caves explained by this model.

Discussion

Since the terminal hosts were strictly controlled in Shiqu County, we need to think about the effects of intermediate hosts for E. multilocularis. In this study, plateau pika is the main intermediate hosts in Shiqu County. According to the literature (Shijie et al., 2018), the density of plateau pika (103.80/hm2) were higher than that of rodent (83.35/hm2), and AE infection rate of plateau pika (6.50%) were also higher than that of rodent (3.01%) in Shiqu County. Moreover, plateau pika was detected in 99% of Tibetan fox food and accounted for 53.7% of its stomach contents (Harris et al., 2014). As the plateau pika is preyed upon by the fox, E. multilocularis can develop from larval stage to adult worms which lay eggs, then becoming a source of infection. Therefore, plateau pika play an important role in the transmission of AE.

Plateau pika prefer some habitats, altitude and rivers are the main factors affecting their habitat selection (Ye et al., 2014). Our SEM indicated that the number of effective caves was negatively correlated with altitude at a statically significantly level. Plateau pika are more widely distributed at low altitudes, thus we speculated that the pika select habitats by depending on oxygen concentration and temperature. On the one hand, oxygen concentration affects the physiological structure in male and the foetuses number in female among pikas (Lian et al., 2014). Thus, the oxygen level, decreasing with altitude increases, regulates population quantity of this species. On the other hand, the temperature also decreasing with altitude increases. Plateau pika may fail to reproduce at low temperatures during the breeding season (Shengqing et al., 2015). Low temperature makes pikas consume a large amount of heat to resist the cold, which leads to an increasing demand for food resources- often limited and shortage supply at high altitude.

Conclusions

In Shiqu County, the main intermediate hosts are Plateau pika, whose distribution and abundance are regulated by altitude, and it is speculated that the pikas select habitats depending on temperature and oxygen concentration.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31070380), the Fundamental Research Funds for the Central Universities, Southwest Minzu University (2019XMJXPY07), funded by Science and Technology Department of Sichuan Province (2020YFH0107). In addition, the authors are most grateful to Hongqi Xie (Station master of Ganzi Grassland Workstation) for his support of this work.

Supplementary material

There is supplementary material associated with this article. Access the material online at: https://dx.doi.org/10.17582/journal.pjz/20210428030426

Statement of conflict of interest

The authors have no potential conflict of interest.

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