Crossing the Line: Human Disease and Climate Change Across Borders.

Author:Cat, Linh Anh
Position:SPECIAL REPORT

Introduction

Many fungi disperse through the air as spores (Ingold, 1953; Roper, Pepper, Brenner, & Pringle, 2008). The atmosphere harbors living spores of an untold number of fungal species (Blackwell, 2011) and continuously moves them between nations and human populations (Kellogg & Griffin, 2006). In fact, 1 [m.sup.3] of air can harbor thousands of fungal spores representing hundreds of species (Bianchi & Olabuenaga, 2006; Crawford et al., 2009; Hasnain, Fatima, Al-Frayh, & Al-Sedairy, 2005; Kasprzyk & Worek, 2006; Levetin, 1990; Mallo, Nitiu, & Gardella Sambeth, 2011; Oliveira, Ribeiro, Delgado, & Abreu, 2009; Pyrri & Kapsanaki-Gotsi, 2007; Quintero, Rivera-Mariani, & Bolanos-Rosero, 2010).

Fungi produce spores that are able to disperse and colonize a new territory, which--in the case of pathogenic fungi--can include humans. More than 300 known fungal species can infect humans, causing more than 1 million human deaths each year (Centers for Disease Control and Prevention [CDC], 2018). Many of these fungal diseases are airborne. The prevailing winds that entrain them are likely to shift direction and magnitude under climate change, threatening populations that have not been exposed previously--and therefore have not developed immunity (Yin, 2005).

Climate models predict changes in the region surrounding the U.S.-Mexico border (Karl, Melillo, & Peterson, 2009; Schoof, Pryor, & Surprenant, 2010). Within this century, mean annual temperatures are expected to increase by 2-5[degrees]C and droughts to become longer and more severe (Karl et al., 2009; Schoof et al., 2010). Environmental niches of many species are strongly influenced by climate, therefore their geographic ranges will likely shift accordingly (Whittaker, 1975). In fact, these shifts in ranges are expected to be particularly striking in the U.S.-Mexico border region, where water scarcity and high temperatures already limit the activities of many animals, plants, and microbes (Toberman, Freeman, Evans, Fenner, & Artz, 2008; Yuste et al., 2011). It would not be surprising if species follow their optimal climate envelope north or south across the border, depending in part on their ability to withstand heat or drought. A large-scale movement of diverse species would connect ecosystems in Mexico with those in the U.S., with consequences that can best be understood via collaborative research between the two nations.

Because many diseases are expected to become more prevalent under climate change (Lafferty, 2009), disease ecology recently has emerged as a crisis discipline. Disease ecology requires a multidisciplinary effort by researchers with diverse expertise, including health professionals, social scientists, microbiologists, and climate change scientists who must advance research rapidly to address the new challenges. Furthermore, as pathogens cross borders, international collaboration is required to effectively anticipate and mitigate outbreaks (Bebber, Ramotowski, & Gurr, 2013; Lafferty, 2009; Rohr et al., 2011).

We use a dimorphic fungus, Coccidioides spp. (Figure 1), as 1) a test case for determining what environmental factors influence the dispersal of fungal pathogens within the border region and 2) an example of how scientists, public health specialists, and medical professionals from the U.S. and Mexico can collaborate by leveraging shared knowledge.

Two fungal species, C. immitis and C. posadosii, cause valley fever. Valley fever has been monitored for the last several decades but recently this disease has become a "silent epidemic." In the Southwestern U.S., its annual incidence has increased rapidly from 6 cases per 100,000 people in 1995 to a peak of 42 per 100,000 people in 2011, a more than 6-fold increase (Figure 2) (CDC, 2012; Sondermeyer, Lee, Gilliss, Tabnak, & Vugia, 2013). By comparison, the incidence of new lung cancer cases was 57 per 100,000 in 2011 (U.S. Cancer Statistics Working Group, 2016). A similar increase was documented in Mexico, though more data are needed to continue tracking these trends in the present day (Baptista-Rosas & Riquelme, 2007). Valley fever is caused by inhalation of Coccidioides spores, and even one spore can cause disease (Huang, Bristow, Shafir, & Sorvillo, 2012).

The fungus resides in the soil of arid and semiarid ecosystems in the Southwestern U.S. and northern Mexico (Figure 3). Coccidioides mycelia grow after rainstorms and then forms spores during long dry periods (Lacy & Swatek, 1974). Spores can cause infection once wind lofts dusty soil into the air. Climate models predict increased drought length interrupted by heavier rainstorms in the Southwestern U.S., which should favor these growth and dispersal mechanisms (Schoof et al., 2010). Coccidioides is not dependent on host densities for infection, unlike other vectorborne diseases such as Zika virus or Chagas disease. Incidence rates in humans are correlated with climate and environmental factors (Gorris, Cat, Zender, Treseder, & Randerson, 2018); therefore, understanding the ecology of the causal agent is critical to forecasting outbreaks.

Much of the information regarding environmental preferences of Coccidioides was collected and analyzed in the 1950s and 1960s. It is vital that we revisit these ideas using current data and modern techniques because a lack of contemporary studies prevents informed decision making regarding disease surveillance, vaccine development, and outbreak preparedness. In addition, a binational survey of this fungus would be unprecedented.

Human Welfare Impacts of Valley Fever

Fungal dispersal has far-reaching effects on many aspects of human welfare, ranging from health to economic concerns (Fisher et al., 2012). Human disease, including valley fever, can lead to debilitation, loss of quality of life, and a large financial burden from medical costs (World Health Organization, 2003). Mostly, valley fever causes only mild flu-like symptoms but it can lead to chronic pneumonia or mortality in some patients, particularly those who are immunocompromised. In some cases, life-long medical treatment is required (Nguyen et al., 2013).

Valley fever treatment is particularly expensive, averaging $23,000-$29,000 per patient in the U.S. (Plevin, 2012); treatment of systemic valley fever that spreads throughout the body costs $680,000 per person for hospitalization and treatment (Pappagianis & Coccidioidomycosis Serology Laboratory, 2007). Currently there is no vaccine for valley fever in humans. A vaccine was proved successful for mice and will be available in coming years for dogs, which are more prone than humans to inhale the fungal spores due to their proximity to the ground (Narra et al., 2016). To determine future threats of valley fever on human welfare, we need to know the extent to which it overlaps with dense human populations.

There are three distinct endemic areas for valley fever in Mexico: the northern area near the U.S. border, the Pacific coast, and the Mexican central valley (Sifuentes-Osornio, Corzo-Leon, & Ponce-de-Leon, 2012). In California, the Central Valley is hyperendemic with parts of Southern California classified as endemic (CDC, 2012; Sifuentes-Osornio et al., 2012). In various parts of Mexico, skin testing using coccidioidin, an antigen, has revealed exposure to the fungus of 5-30% of the population (Sifuentes-Osornio et al., 2012).

In general, up to 40% of humans exposed to valley fever spores develop the disease. Less than 1% of these patients experience severe pneumonia, which mostly affects patients with associated risk factors such as HIV, diabetes mellitus, chemotherapy, transplantation, or third-trimester pregnancy (Sifuentes-Osornio et al., 2012). For these high-risk groups, mortality rates increase up to 90% (Sifuentes-Osornio et al., 2012). Inmates imprisoned in the Central Valley of California are especially vulnerable to valley fever because prisons are often built near Coccidioides spp. habitats (de Perio, Niemeier, & Burr, 2015; Pappagianis & Coccidioidomycosis Serology Laboratory, 2007). In addition, prison populations contain a disproportionately high number of African-American and Latino males who have a relatively high risk of valley fever infection (de Perio & Burr, 2014). Many people are incarcerated for minor crimes but leave their imprisonment with debilitating and expensive cases of valley fever, evidenced by prisoners showing higher rates of incidence compared with the population in neighboring cities (Pappagianis & Coccidioidomycosis Serology Laboratory, 2007).

Rates of valley fever infection have reached epidemic proportions in the border region near the states of California, Arizona, and Baja California, perhaps owing to shifts in drought severity, temperature, and dust loads (Park et al., 2005). Moreover, if climate and soil disturbance continue to change, endemic regions of valley fever could spread in the near future, potentially exposing a greater number of humans to the illness, including:

* 13 million people within the greater Los Angeles area (U.S. Census Bureau, n.d.),

* 1.3 million people in the area of Tijuana, Mexico (National Institute of Statistics and Geography, 2010)...

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