By combining spatial-temporal and phylogenetic data of MPXV, we mapped the global distribution of MPXV infections in humans and animals, defined populations at risk by zoonotic transmission or travel-related infections, thereby providing a robust framework for assessing its global impact. Since its introduction in 1970, a total of 49 432 human cases of MPXV infections have been reported, primarily in Central Africa and Western Africa till 2022, with occasional travel-related cases in other countries and animal trade-related outbreak in the United States, 2003. The current outbreaks associated with the West African clade have milder disease severity and resulted in less fatalities, however, remained as a severe concern when taking into account the marginally increased Rt from 2000–2009 to the recent decade, indicating an elevated transmissibility. The international connectivity by airline traffic posed another severe concern, many Europe countries especially those in West Europe have a high risk of travel-related infections both from endemic and current epidemic countries, and three cities (Chongqing, Beijing and Guangzhou) in China have reported five MPXV cases [26], indicating that more attention should be paid to the spillover and human-to-human transmission, and if it continuously spreads, it will be a shock to the vulnerable global health system during the COVID-19 pandemic [27].
BRT models revealed that ecological niche of MPXV was significantly associated with four ecoclimatic factors such as annual precipitation, min temperature of coldest month, isothermality, and annual mean temperature, and three reservoirs-related factors including predicted distributions of Graphiurus crassicaudatus and Graphiurus crassicaudatus, and richness of Rodentia. Ecoclimatic factors could lead to increased MPXV infections in humans from zoonotic transmission, because the drought in forested areas may compel sylvan mammals that carry MPXV to disperse to non-forested areas such as human settlements for food, which could contribute to a rise in MPXV infections in humans from zoonotic transmission. This climatic-driven zoonotic spillover potentially generated by human activities such as deforestation, combined with agricultural activities and hunting in forests, may contribute to the spread of monkeypox in endemic areas [28, 29].
Ecological drivers are part of the complex interrelationship between humans, animals, and the environment during zoonotic transmission of MPXV. Four rodent reservoirs were used to build the model, two of which (Graphiurus crassicaudatus and Graphiurus crassicaudatus) were included in the final model, revealing a highly correlation with the zoonotic niche of MPXV [17, 28]. Our study indicates that researches about rodents should not be ignored due to the vital roles of rodents in many zoonotic diseases e.g., Lassa fever and human infection with hantaviruses that have persistent threats to global health [29, 30]. There remains a hypothetical risk of human-to-animal transmission, which deserves attention to those areas with highly suitable environment for MPXV occurrence outside Africa projected by our models for avoiding the colonization of the virus in animals. Our model predicted potential ecological niche of the MPXV throughout Congo Basin and Western Africa, including parts of the DRC, Nigeria, Congo, Côte d'Ivoire, as well as some areas without reported cases, e.g., Ethiopia, Kenya, and Guinea. Some areas are lack of efficient surveillance network of MPXV infection in animals or clinical patients, in where underreporting due to limited field investigations or laboratory identification might contribute to its continuous transmission among humans, until outbreaks were noticed [31]. The international community could consider to allocate resources to strengthen surveillance, laboratory tests, case investigation and contact tracing, clinical management, vaccinations and immunization, and risk communication in these countries.
The unprecedented and unexpected outbreaks outside Africa since May 2022, have attracted the focus of global public health systems and have been issued as a public health emergency of international concern (PHEIC) by WHO [6, 32]. According to our updated estimates of the transmissibility, the effective reproduction number is greater than 1 in Europe since May, indicating a probable increase of its transmissibility. For countries at a higher-imported risk, e.g., the United Kingdom,3,33 the United States [33], South Africa [34], and Saudi Arabia [35], measures to increase the sensitivity of case detection are helpful for the control of the disease. As global routine measures of prevention and control of the COVID-19 pandemic were made, the demand for gatherings is increasing day by day. Although the role of MSM transmission in the spread of monkeypox cannot be ruled out at present [14, 36–38], clustered cases may occur in any group that has been in close contact in a large-scale gathering event. The continuous 2022-monkeypox outbreaks revealed significant gaps in understanding the mechanisms of viral transmission and continuously changing epidemiological characteristics of the disease, and a more integrated approach to epidemic preparedness is long overdue.
The study is subject to several limitations. Firstly, due to the weak medical and health conditions in some countries of Africa, the epidemic status of monkeypox may be underreported in Africa. In addition, although smallpox had been eliminated in the world and the smallpox vaccine had been stopped in the 1980s [39], good cross immunizations between smallpox and monkeypox viruses has been reported, we did not consider the susceptibility of populations to monkeypox in the analysis of interregional transmission of MPXV, which might overestimate the risk of interregional transmission.