Impact of Human Activities on Zoonotic Infection Transmissions: History
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Contributor:
Michelle Marie Esposito
,
Sara Turku
,
Leora Lehrfield
,
Ayat Shoman

As humans expand their territories across more and more regions of the planet, activities such as deforestation, urbanization, tourism, wildlife exploitation, and climate change can have drastic consequences for animal movements and animal–human interactions. These events, especially climate change, can also affect the arthropod vectors that are associated with the animals in these scenarios. As the COVID-19 pandemic and other various significant outbreaks throughout the centuries have demonstrated, when animal patterns and human interactions change, so does the exposure of humans to zoonotic pathogens potentially carried by wildlife.

  • zoonoses
  • emerging
  • climate change
  • urbanization
  • deforestation
  • wildlife exploitation

1. Introduction

Human activities, such as urbanization, deforestation, wildlife exploitation, and tourism, as well as the global climate changes that have occurred from mankind’s inhabitation of the planet, not only change the landscapes of nature but also serve as driving forces of zoonotic disease emergences, thereby increasing the prevalence of already known zoonoses [1]. Various animals and arthropod reservoirs have been linked to the connection between human-related factors and the emergence of diseases, including rodents, birds, pigs, cows, bats, primates, camels, mosquitoes, ticks, and fleas [1][2]. It is important to study the various causes of emerging zoonoses, as these diseases account for more than 60% of infectious diseases encountered by humans and can create worldwide devastation as seen during the COVID-19 pandemic [3][4]. As mankind becomes more aware of the threats of pandemics, such as the plague, Spanish flu, and SARS-CoV-2, it is of great interest to better characterize ways to minimize activities that increase reservoirs or human–animal contact [3].

2. Urbanization

With urbanization comes a variety of connected activities that will be further discussed in this review, such as habitat destruction, pollution, climate change, and human exploitation of animals, all of which have been linked to a significant loss of biodiversity and increased risks of zoonotic exposures [5]. With the West Nile virus and Lyme disease as models, it has been demonstrated that areas with less urbanization or anthropogenic activities that retain high biodiversity subsequently have pathogen vectors feeding on a wider range of hosts that end up as poorer reservoirs for the pathogens, yielding a reduced prevalence of zoonotic emergences [5]. When biodiversity is low, however, the pathogen vectors can feed on select primary reservoirs that dominate and increase the spread of diseases [5]. Some taxa prone to zoonotic reservoirs have been found to preferentially thrive in human-dominated landscapes, whereas non-reservoirs have been found to dominate less-disturbed landscapes [6]. Ultimately, urbanization is a major driver of decreased biodiversity, as some animals have difficulty adapting to the changing environment [7]. The changed environment also contributes to some other animals being more attracted to migration into urban habitats, as these locations provide new robust food sources and protective shelters [7]. This, in turn, leads to an increase in the population of these animals as they thrive in the resource-rich urban location, which subsequently increases potential interactions with humans, and exposure of humans to the parasites or pathogens carried by these wild animals [7]. For instance, rodents, bats, Carnivora (such as dogs and cats), Cetartiodactyla (such as hooved mammals), and primates are major reservoirs of zoonotic pathogens and have all been pushed into increased human contact through urbanized landscapes or urban practices [7]. However, it should be noted that in some cases, the opposite pattern is observed in which increased biodiversity is associated with a greater prevalence of disease through a higher diversity of potential hosts to carry pathogens [8]. Urbanization, however, tends to reduce human contact with the biodiverse forest habitats in these scenarios, and thus, more studies have demonstrated the previously mentioned correlation between lower biodiversity and higher zoonotic emergences [8]. Furthermore, some studies attribute urbanization to reduced disease through increased sanitation processes, increased medical care, public health initiatives such as arthropod spraying, and improved pest reduction indoors [8].
While many pathogens and reservoirs exist, one category with significant consequences from urbanization is parasites [9][10]. In many developing countries, urbanization has included a strain that leads to insufficient water/food supplies, sanitation, garbage removal, health care, and hygiene, leading to prime conditions for parasitic contaminations or transmissions [9][11]. In one study on Sri Lankan macaques of three subspecies in urban, suburban, and wild populations, twenty gastrointestinal parasite genera were analyzed, including protozoans, cestodes, nematodes, trematodes, and acanthocephalans [10]. The results demonstrated that in all subsets of species analyzed, macaques of urban and suburban populations exhibited greater parasitic prevalence, ova and cyst counts, and species richness in comparison to samples from the wild populations [10]. Not only were the data of parasitic robustness in these macaques valuable for understanding anthropogenic impacts, but so were the observational findings of modified daily activities, ranging patterns, and food/water selection of the macaques in urban sites compared to the wild sites [10]. The forms of urbanization can also impact risk levels, as multiple helminth-infected samples of urban sites were obtained in religious or archaeological sites of the region where many pilgrims and tourists walk barefoot and are more susceptible to soil-transmitted zoonoses [10]. In addition to soil-transmission zoonoses, protozoan-infected samples were found in urban sites where macaques were seen bathing and drinking from shared water sources of humans, which increases oral route transmission risks [10]. Even burrowing mite parasites have been found to have an increased prevalence in larger urban regions rather than in wild habitats [12]. For instance, in Estonia, a higher percentage of sarcoptic mange from the parasitic mite, S. scabiei, was found in larger urban towns than in wild habitats [12]. It is believed that more urban locations promote the increased presence of zoonotic infected wildlife, as the infected animals require a larger amount of energy; thus, they flock towards the increased food, warmth, and shelter of urban environments [12].

3. Deforestation

Deforestation modifies wildlife communities, and thus increasing zoonotic spillover potential is a growing area of concern [13]. The increase in zoonotic outbreaks, majorly in tropical lands, has been in part connected to human population growth from 1990 to 2016 [14]. To help reduce the risk of the emergence and spread of zoonotic pathogens, it would be of great value to encourage the redirection of wildlife hosts to alternate forested lands when they have lost habitat space in a deforested region [13]. The regeneration and reparation of forested lands can reduce the transmission potential of zoonoses while also benefiting the ecosystem as a whole [13]. New studies have shown that viruses are more likely to be transmitted from animals to humans if they are around disturbed ecosystems, which include deforested lands [14]. These outbreaks can lead to an increase in zoonotic pandemics as well. In 2013, the Ebola outbreak emerged after an eighteen-month-old child became ill while playing near a tree and died shortly thereafter [15]. The World Health Organization reported that the Ebola outbreak may have been caused by deforestation, which caused bats to infest the child’s village [16]. Large portions of the bats’ biological environment were destroyed due to deforestation, forcing them to infiltrate the village [17]. Another example is the coronavirus, SARS-CoV-2, which originated in an animal, most likely a bat, and then spread globally causing a pandemic that killed millions of infected patients [18][19]. The rising increase in deforestation causes ecological landscape disruptions, loss of biodiversity, and displaced wildlife migrations to local communities, all of which are associated with increases in zoonotic transmissions [20].

4. Tourism and Zoos

As mankind has become more advanced in traveling technologies, the movement of people in large numbers across greater spans of land each day has vastly increased exposure amongst humans, as well as with animals [21]. Furthermore, the exploration of mankind across new locations also creates opportunities for recreational experiences that increase human contact with animals. Interestingly, when people think of animals in contact with humans, sometimes the animals seen around homes on a daily basis, such as birds, domestic pets, and rodents come to mind. In some cases, however, more exotic animals have also come into contact with humans and have increased zoonotic risks in recent years, such as South African lions that are bred on farms for commercial uses, including tourism [22]. On these farms, interactive tourism activities, including petting of the cubs, as well as other uses of these captive lions, such as slaughtering them for trophy hunting or medicinal purposes, have increased direct contact and zoonotic risks with big game animals previously kept rather separated from human interactions [22]. Lions in zoos also present zoonotic dangers. Even though the public may not be directly interacting with them, zookeepers and volunteers caring for them are known to obtain zoonotic infections. For instance, a zookeeper caring for a lion cub in 2015 contracted dermatophytosis from the animal transferring pathogenic fungi to the caregiver [22]. As the potential for the spread of disease from human activities becomes more acknowledged, it can shine a spotlight on the need for increased large-scale surveillance of potential emerging zoonoses. The benefits have already become apparent in studies, such as the first large-scale surveillance of zoonotic flaviviruses in European zoo mammals across a seventeen-year timespan [23]. In this study, West Nile virus, Usutu virus, and tick-borne encephalitis virus exposure were found in zoo mammals [23]. The benefit of surveillance of zoo animals for zoonotic transmission became apparent in that study when they looked at the time span data and noted that Anti-West Nile Virus antibodies were detected in the sample of zoo animals at least one year prior to the first outbreaks that were reported in humans in that region [23].
One aspect of tourism and zoo life that promotes the risks of zoonoses is the concept of petting zoos [24]. Interestingly, petting zoos and tourist parks create a zoonotic risk factor that is similar to one of the driving factors of deforestation, which is the relocation of animals normally in high canopy locations to suddenly being at ground level, and thus in closer proximity to humans [25][26][27]. These types of attractions have placed humans in direct contact with animals through petting and feeding, including the now popular way of taking close selfies with animals [24][27]. While some zoos or tourist sites, such as Gunung Leuser National Park in Indonesia, try to minimize the risks with strict rule sets, such as minimum distance restrictions, studies have shown a major lack of compliance [27]. The desire of people trying to obtain the best social media posts has encouraged a blatant disregard for the rules, including Instagram posts of visitors feeding animals that are not meant to be fed, having direct contact, or having proximity less than the minimum restrictions [27]. It should be noted that the increased spread of wildlife selfies is not simply restricted to parks or zoos, but has become the norm in tourist trips out in the wild in general as well [28]. In one study by the World Animal Protection Organization, an analysis of approximately 34 billion images posted on Instagram from a sample of 700 million people found tens of thousands of wildlife selfies [28]. This shocking discovery has led to the organization developing ecotourist pledges to abstain from baiting or restraining animals for selfies as well as the creation of Instagram pages dedicated to educating the public on animal wildlife [28]. Additionally, Instagram has even added a pop-up feature that appears to demonstrate warnings of illegal wildlife trade if anyone searches for wildlife selfies [28]. Although mankind’s obsession with social media has created some zoonotic risks and unpleasant behaviors towards animals, it should be noted that these platforms have also benefited conservation efforts and helped promote better public opinions towards wildlife in general when used in an appropriate manner [28]. While many of these initiatives aim to protect the welfare and rights of animals, it should be noted that they also subsequently help reduce zoonotic risks by decreasing public interactions with many animals. As public opinion has become more aware of the issues surrounding animal-based tourist attractions, companies such as TripAdvisor have stepped forward to stop the sales of tickets for circuses or other entertainment attractions that include cruelty to animals and direct exposure of humans to wildlife [28].

5. Wildlife Exploitation and Trade

After Dr. Fauci called COVID-19 a “direct result” of wet markets, scrutiny of the wildlife trade emphasized that tighter biosecurity and more controlled regulations are needed than they were before the pandemic [29][30]. The confirmation of countless mammals as hosts for zoonotic diseases in several studies has already highlighted the need for stricter surveillance and more sanitary conditions [31][32]. In the past, the Center for Disease Control and Prevention (CDC) restricted the importation of Gambian pouched rats during the monkeypox pandemic, and the Chinese government ordered the mass killing of tens of thousands of infected civets following the SARS outbreak [32][33]. PREDICT, a project of USAID’s Emerging Pandemic Threats program, discovered more than a thousand new viruses in mammals mostly from Asia, Africa, and a few from Latin America [34]. Countries with slaughterhouse inspection in place detects about two-thirds of bovine tuberculosis outbreaks and cities with firm hygiene and animal storage rules, such as Hong Kong, show lower transmission rates of zoonotic pathogens [35][36]. In 2017, the CDC organized the first “One Health” workshop with the US Departments of Agriculture and Interior to address zoonoses, prioritizing influenza, salmonellosis, West Nile Virus, plague, emerging coronaviruses (SARS and MERS), rabies, brucellosis, and Lyme diseases [20]. In an attempt to control human exposure to zoonotic pathogens while maintaining steady wildlife trade, several protocols have been suggested and instituted by the World Health Organization, World Organization for Animal Health, and United Nations Environment Programme, including sanitation, disinfection, prohibition of overnight poultry storage, use of protective equipment, and tracing [31][36]. Ensuing the COVID-19 outbreak, the Chinese and Vietnamese governments prohibited the trade and consumption of wild animals [37][38]. Infectious disease researchers argue that the risks of wildlife trade are becoming increasingly abundant and severe, and the better way to diminish them than regulating the trade is to dissolve it [29]. Patrolling trade is difficult because of poor records, mislabeled species, and the heavy influence of illegal operations on legal ones [29]. Terminating illegal wildlife trade is an issue that so-called developing countries—often the source of illegal bushmeat for food and exotic live animals for pets—and developed countries, such as those in the EU that import animals, alike need to tackle [39].
However, banning the trade will strip thousands of their livelihoods or drive it underground, so strict regulations while maintaining steady trade need to be executed and research aiming to prevent future outbreaks must address deeper-rooted issues of poverty and health [34]. A more effective and favored strategy than illegalizing trade would be to prioritize surveillance, restriction, and sanitary and quantitative control of pathogen and animal taxa known to be prevalent and most infectious in the largest markets first and foremost [29][31][32][34]. Analyzing the dynamics and processes of trading networks—including the animals’ handlers at each step, countries of origin, methods of breeding (wild-caught and captive-bred), grouping during maintenance, transportation, and trade (how many and with which species)—helps ensure protocol observance, better understand and hypothesize zoonotic transmission, and guide new regulations to aid in disease eradication [20][32][36][40]. Additional control includes clear labeling of meat as domestic so as not to disguise any as exotic, which is often illegal [30]; separation between animals of different species and origin [36]; criminalization of trade that does not adhere to environmental rules [39]; tighter border control in the EU, which has reported hundreds of tons of bushmeat on Air France alone from Central and West Africa every year (likely an underestimate because of lax inspection) and Asian ports, which currently have free-trade zones [30][39]. Continuous detection of known pathogens is critical, e.g., Staphylococcus aureus in camels in Africa and bovine tuberculosis in birds and cattle [35][41][42]. Public health organizations, such as USAID’s Emerging Pandemic Threats program, have invested billions into disease tracking, analysis, and appropriate response [40][43]. Forensic laboratories and genomic technologies for animal body parts have been growing in the EU to identify illicit wildlife trade [39]. The One Health Initiative should educate farmers, vendors, importers, veterinarians, pet store employees, and animal consumers on the risks of zoonotic diseases and the application of safety and hygiene measures [32][33][34][44]. Under the One Health Initiative, which was formed in 2008 to align human, animal, and planetary health, experts in wildlife, ecology, public health, epidemiology, and sociology should collaborate on research and legislative measures to minimize zoonotic transmission and educate farmers, vendors, importers, veterinarians, pet store employees, and animal consumers on the risks of these diseases and the application of safety and hygiene measures [20][32][33][34][44]. More needed than ever for the welfare of humans and animals alike is thorough screening and legislation, which can be implemented while maintaining steady wildlife trade and exploitation, to not only combat already-existing zoonotic diseases but also to prevent future outbreaks.

6. Climate Change

Finally, it is of interest to briefly mention the connection between zoonotic infections, vector-borne transmissions, and climate change. Although climate change is more of an environmental factor than the other factors discussed in this review, climate change has become a topic of growing concern as more evidence is revealed of the large increases in greenhouse gases due to human activity [45]. These increases have led to abnormal changes in the climate, which has, in turn, affected the occurrence of zoonotic diseases [45]. Changes in global temperatures can alter the number of vectors, transmission cycles, and contact between species, which affects the emergence of zoonotic diseases [45]. If vectors mature faster and last longer throughout the year, for instance, or habitats lose their favorability as precipitation or protection diminishes, then human exposure levels expand consequentially (Figure 2).
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Figure 2. Climate change is more than just temperature change. As temperature, precipitation, humidity, and climate patterns become more disrupted, vector and animal patterns become modified in ways that increase human exposure to infectious diseases.
The impact of climate change on zoonotic and vector-borne transmissions is most obviously seen with arthropod vectors, which are sensitive to changes in temperature [46]. Mosquitoes show a rise in activity and reproduction when temperatures increase, leading to an increase in vectors [46]. Additionally, the pathogens using mosquitoes as hosts reach maturity faster. In Italy, there was an association between an outbreak of the chikungunya virus, which is spread by mosquitoes, and a higher temperature in the area due to climate change [46][47]. The same effects are seen for ticks and sandflies, and ticks will begin biting earlier than usual in the year and for a larger gap in time [46]. For example, Crimean-Congo hemorrhagic fever (CCHF) is caused by a virus transmitted by ticks, and there was an outbreak of CCHF in Turkey that was correlated with a warmer spring in the country a year earlier [48]. The same observation was made for the Ixodes ricinus tick in Sweden, which is a vector for Lyme borreliosis and tick-borne encephalitis (TBE) [49]. Sweden’s climate has become warmer since the 1980s, which has caused the population density of ticks to rise and extend northward [49]. This has been related to the growing incidence of TBE in Sweden [49]. The spread of disease by way of rodents will also increase as temperature increases, causing there to be less snowfall, which rodents use for protection [46]. This will cause rodents to enter human housing, leading to higher chances of transmission between humans and rodents [46][50]. For similar reasons, the risk of rabies in Alaska would increase [51]. This is because foxes usually spread rabies to dogs, which then infect humans, and a decline in sea ice because of climate change could lead to more interactions between foxes and dogs, as foxes lose parts of their habitat [51]. Cryptosporidiosis and giardiasis could also become issues in Alaska, as they are usually transmitted via ingestion of water contaminated with animal feces and human feces, respectively [51]. The change in climate could cause animals with the disease to move into areas north where humans have not been exposed to yet, and it increases rain and the moisture of the soil, which could heighten the survival chance of pathogens [51]. This effect was also seen in China as Oncomelania hupensis, a type of snail that acts as a vector for Schistosomiasis, has spread out over its usual range into Northern China due to increasing temperatures [52]. Migratory birds will also shift north due to climate change, which may change the transmission pattern of the highly pathogenic avian influenza H5N1 [53]. Rising temperatures also pose a threat in that they might prompt mutations in pathogens that could increase their reproduction or survival rates [52]. In addition, with an increase in temperature, climate change can lead to very dry conditions in certain parts of the world, such as Arizona, U.S.A [54]. As the climate there has changed, there has been an association between the dry weather and the incidence of coccidiomycosis [54]. As observations have shown, the alterations in the number and population of species present in communities can lead to an increase in the spread of zoonotic disease-causing pathogens [55]. However, it could also lead to a decrease, as additional species in a community may not be viable host options, causing a decrease in the spread of pathogens [55].
One type of pathogen in particular that can have increased transmission due to changes in climate is foodborne pathogens [56]. This is because the optimal temperature for the majority of foodborne pathogens is around 37 °C, so as temperatures warm, these pathogens’ growth rate increases [57]. Additionally, some pathogens, such as Listeria monocytogenes, are inhibited by freezing events and climate change will lessen the frequency of these events [57]. As a result, there will be an increase in pathogen populations in habitats that did not have issues before because of inhibitory freezing events [57]. Moreover, in the European Union, there was a positive correlation between the possibility of contracting campylobacteriosis and the mean weekly temperature [56]. There has also been a correlation between increases in salmonellosis notifications and weekly temperature increases for temperatures above 5 °C [56].
Furthermore, the increasing temperatures due to climate change have not only affected outbreaks directly but also indirectly by causing an increase in heavy rainfall [56]. This has been correlated with breakouts of waterborne norovirus, as increasing precipitation causes wastewater overflow to taint aquatic habitats [56]. In addition, the impact of heavy rainfall was observed after the 2015–2016 El Nino-Southern Oscillation (ENSO) event [58]. It has caused major rises in precipitation in different parts of the world and led to higher incidences of plague in Colorado and cholera in Tanzania due to that [58]. The rise in cholera could be because an increase in flooding would lead to more water contamination and this added stress on aquatic environments may make them more vulnerable to infection [58]. Climate change has also caused early winters in Northern Europe to become rainier, which is associated with a rise in the transmission of Puumala orthohantavirus (PUUV) in bank voles [59]. This could lead to a rise in the risk of transmission to humans [59]. The exact mechanism for this is not known, but some possibilities are that the change in winter has modified host behavior or physiology, or increased the period of time the pathogens persist in the environment [59]. An example of this is the outbreak of nephropathia epidemica, which was caused by PUUV in Sweden in 2007 [59]. In the autumn before the outbreak, there was a higher number of voles, and then a very rainy winter where many voles began infesting houses, likely leading to the jump in cases of nephropathia epidemica [59]. Also, in Kenya, there was an increase in Aedes aegypti mosquito eggs and adults during months with higher-than-normal rain [60]. These mosquitoes are vectors for dengue fever, so the increase in rain could present a concern for a potentially higher risk of the disease [60]. Another facet to the issue of global warming is not only that it will push species further inland to human habitats, but that it will also expose pathogens that were frozen [47][61]. In Yakutia, Russia there have been outbreaks of anthrax in areas near burial sites that are thought to be caused by the pathogen surviving in permafrost soils [61].
The importance of climate change’s impact on the emergence of zoonotic diseases has multiplied in recent years as the world has become more aware of the dangers of increased zoonotic transmissions through experiences such as the COVID-19 pandemic [62][63]. It has been suggested that COVID-19 was spread from a seafood market in Wuhan, China, and it has been recorded that wild animals can be hosts for SARS-CoV-related coronaviruses [62][64]. While no direct links have yet been made between climate change and COVID-19 emergence, it is an area that is currently seeing hypotheses developed. Ultimately, it is believed that climate change will lead to further intrusion into existing habitats for animals and more interactions with humans, which can lead to more zoonotic infections [62].

This entry is adapted from the peer-reviewed paper 10.3390/ani13101646

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