Climate Change and Vibrio in the Chesapeake Bay

Vibrio bacteria are natural constituents of various marine, estuarine, and aquatic ecosystems, forming part of the natural microbiome of extratropical oceans, bays, and rivers (Semenza 2021).The genus Vibrio includes over 100 species of gram-negative rod-shaped bacteria, about a dozen of which have been shown to cause infections in humans (Baker-Austin et al. 2017). Pathogenic Vibrios include the well-known V. cholerae, which causes cholera, as well as V. vulnificus and V. parahaemolyticus. While V. cholerae prefers near-freshwater environments, both V. vulnificus and V. parahaemolyticus thrive in warm, low-salinity marine and estuarine environments such as the Chesapeake Bay (Semenza 2021).

Vibrio bacteria can survive and reproduce independently in water, or they can associate with a variety of biotic and abiotic particulates such as plankton, algae, and sediment (Semenza 2021). This makes it more likely for filter feeders, such as oysters and other shellfish, to accumulate and host Vibrio bacteria in their tissues (Semenza 2021).

The general term for any form of Vibrio infection is vibriosis. Vibriosis can occur through exposure of open cuts, abrasions, or other wounds to contaminated water, or through consumption of raw or undercooked contaminated seafood, especially filter-feeding oysters (Semenza 2021).

V. parahaemolyticus causes of the most common form of seafood-associated food poisoning (Baker-Austin et al. 2017). It is estimated that there are more than 34,000 annual cases of V. parahaemolyticus infection in the U.S. alone, leading to an estimated $40 million in associated economic costs, although these numbers are likely artificially low due to underreporting (Muhling et al. 2017). Infection with V. parahaemolyticus primarily occurs through consumption of contaminated seafood, and usually results in acute gastroenteritis—abdominal cramps, nausea, headaches, diarrhea, fever, and chills—and is generally self-limiting, resolving within a few days of the onset of symptoms (Baker-Austin et al. 2017). While seafood-associated infections are usually mild, infections caused through exposure of open wounds are considered more serious than seafood-associated infections, and often require intervention with antibiotics (Baker-Austin et al. 2017).

Although much rarer than V. parahaemolyticus infections, V. vulnificus infections are significantly more lethal. Although there are, on average, currently only about 100-300 cases per year reported in the U.S., they are responsible for 95% of seafood consumption-linked fatalities (Baker-Austin et al. 2017). The overwhelming majority of these cases occur in men with preexisting health conditions, particularly alcohol-associated liver cirrhosis, although the mechanisms behind these trends are still being studied (Baker-Austin et al. 2017).

Consumption of V. vulnificus-contaminated seafood, particularly raw oysters, can lead to severe, fulminant systemic infection, including fever, chills, nausea, and hypotensive septic shock (Jones and Oliver 2009). Seafood-associated V. vulnificus infections have an average mortality rate exceeding 50% (Jones and Oliver 2009). While the mortality rate for wound-associated infections is less than that of seafood-associated infections, it is still incredibly high at around 25% (Jones and Oliver 2009). Despite the low number of cases, these high mortality rates lead to an estimated economic cost of around $320 million annually in the U.S. (Muhling et al. 2017).

Over the past several decades, both V. parahaemolyticus and V. vulnificus infections have been increasing in the U.S. Of all the major food-borne bacterial pathogens, including Salmonella, Listeria, E. coli, and Campylobacter, only Vibrio infections are on the rise (Baker-Austin et al. 2017). It is difficult to know the exact rate of increase for V. parahaemolyticus infections, as many mild cases go unreported. For V. vulnificus, the Centers for Disease Control and Prevention reported a 78% increase in cases between 1996 and 2006 (Jones and Oliver 2009).

While much of Vibrio bacteria's pathogenesis remains poorly understood, it is well-known that all types of Vibrio bacteria are incredibly dependent upon and responsive to their environment. Vibrios have some of the fastest known replication times in the known bacterial world—about 8-9 minutes if the conditions are right (Baker-Austin et al. 2017). This rapid replication time allows them to quickly take advantage of favorable environmental conditions, leading to increased risk of outbreaks. During periods of unfavorable environmental conditions, the bacteria enter a dormant state, ready to take advantage of the next favorable spell (Semenza 2021).

Vibrio abundance and spatial extent is mainly dependent on water temperature and salinity (Semenza 2021). It has been shown that the optimal temperatures for several Vibrio species are around 37-39˚C, which is significantly higher than currently observed water temperatures in regions where Vibrios are endemic, suggesting that an increase in temperature contains great potential for an increase in Vibrio abundance (Muhling et al. 2017). Currently, the vast majority of cases occur in the summer months, when temperatures are higher and more people engage in activities that could expose them to contaminated water or seafood (Semenza 2021). Increased temperatures, therefore, could also extend the length of the high-risk season (Muhling et al. 2017). Salinity could also change in a warmer world, as evaporation and precipitation patterns change. V. parahaemolyticus has been shown to have the widest range of acceptable salinity, from approximately 5-30 psu (practical salinity unit), while V. vulnificus prefers near-fresh to about 24 psu, but is most common between 8 and 16 psu (Muhling et al. 2017).

Climate-influenced changes in water temperature, salinity, and turbidity will all impact the abundance, seasonality, and spatial extent of different Vibrio species (Semenza 2021). These changes will interact with changes in oyster and other seafood populations, recreational behaviors, sea level rise, and extreme weather events to produce new geographies of Vibrio exposure and infection under climate change (Semenza 2021). Due to the multifaceted and complex nature of the relationships amongst these various human and environmental factors, each at-risk region must be examined and modeled in its own context in order to obtain the best understanding of how climate change might affect Vibrio in that particular region, and to adopt the most appropriate adaptive actions.

Records show that the Bay's water temperature has warmed faster during the past two centuries than at any point in the previous two millennia (Hinson et al. 2021). There have been elevated rates of warming in the summer, averaging about 0.04 ± 0.01˚C per year, which is largely attributed to atmospheric warming (Hinson et al. 2021). These trends are problematic due to the potential for increased Vibrio abundance, among other reasons.

Vibrio occurrence and abundance increases linearly with water temperatures above 15˚C, with ideal temperatures being 37-39˚C (Jacobs et al. 2014). Given that the Bay's current water temperature reaches its peak in August with maximums around 29˚C, potential warming will maintain summer temperatures within Vibrio's preferred range and bring the water temperature closer to Vibrio's ideal. Warming will also likely extend the season of Vibrio risk, which currently peaks in the summer, into the late spring and early fall (Muhling et al. 2017).

Shown above on the left is the projected change in summer V. vulnificus occurrence in the Chesapeake Bay under two different warming scenarios, and above on the right is the projected change in summer V. parahaemolyticus occurrence in Chesapeake Bay oysters under the same two warming scenarios. All four models demonstrate a marked increase in the risk of Vibrio occurrence, but more so under the higher warming scenario.

While the links between increasing temperature and increasing Vibrio abundance are clear and the fact that the Bay's water temperatures are warming is overwhelmingly agreed upon, the impact of salinity change on Vibrio dynamics is more nuanced.

Salinity could change due to changes in freshwater inputs and outputs, since the rate of inputs and outputs of marine water from the ocean are relatively stable. Projections of future precipitation patterns for the Bay region and its watershed are uncertain (Muhling et al. 2017). Some models show strong increases in precipitation and therefore freshwater inputs, which would move high-risk areas downstream and down-Bay, since both V. vulnificus and V. parahaemolyticus prefer brackish environments over near-fresh environments (Muhling et al. 2017). On the other hand, some models project minimal changes in precipitation which, when combined with increased evaporation due to increased temperatures, could lead to an increase in salinity throughout the Bay and move high-risk areas upstream and up-Bay (Muhling et al. 2017). Below, retrospective predictions show the difference in the geographic ranges of V. vulnificus probability of occurrence in high-precipitation and low-precipitation years. In the wet year, the risk of occurrence shifts south, closer to the mouth, while in the dry year, the risk shifts north and closer to the headwaters of tributaries.

V. parahaemolyticus and V. vulnificus will respond differently to changes in salinity due to differences in their preferred salinity ranges. V. parahaemolyticus has the widest range of salinity tolerance, from approximately 5-30 psu (practical salinity unit) (Jacobs et al. 2014). Due to this wide tolerance, models anticipate the climate-driven increase in V. parahaemolyticus occurrence both in the water and in oysters to be relatively spatially uniform across the Bay (Jacobs et al. 2014). V. vulnificus, on the other hand, prefers a narrower range of salinities, occurring most commonly between 8 and 16 psu with an estimated ideal of 11.5 (Jacobs et al. 2014). This narrower range creates the potential for spatially localized "hot spots" of V. vulnificus abundance, which shift according to streamflow (Jacobs et al. 2014). Climate-driven increases in V. vulnificus occurrence and abundance will likely be most pronounced in moderate salinity zones, such as the Mid Bay, Upper Bay, Patuxent River, and Rappahannock River (Jacobs et al. 2014).

Further research into the impacts of climate change on the Bay's salinity is necessary, but it is important to note that regardless of the true outcomes, any change in salinity will impact the geographic range of Vibrio risk.

The main environmental determinants of Vibrio occurrence, abundance, and geographic distribution are water temperature and salinity, both of which will be impacted by climate change, but the abundance of microbiota such as plankton and algae also plays a role (Jacobs et al. 2014). Because Vibrios are flexible and adaptive bacteria, they often choose to associate with plankton and algae in addition to surviving independently (Jacobs et al. 2014). In a 2014 study, Jacobs et al. measured this using the Secchi depth test of turbidity, a proxy for water clarity that can indicate the amount of plankton and algae in the water. They found that more highly turbid waters (Secchi depth <1 m) contained 78% of the samples they took that tested positive for V. vulnificus, and that inclusion of turbidity in their model of V. vulnificus occurrence prediction improved model fit (Jacobs et al. 2014).

In a warmer world, they may be more plankton and algae in Chesapeake Bay waters. While the availability of nutrients such as carbon, nitrogen, and phosphorus are the primary factors that limit the growth of algae, temperature is another variable (Metcalf and Souza 2021). Many species of algae have an optimum growth temperature around 30˚C, which is slightly warmer than current maximum Bay temperatures (Metcalf and Souza 2021). Additionally, climate-driven changes in precipitation and weather may increase the runoff of nutrient-polluted water into the Bay, an issue that is already well-documented and which could increase the availability of these nutrients and therefore the growth of Vibrio-hosting microbiota (Metcalf and Souza 2021).

Overall, the degree of increase in V. parahaemolyticus and V. vulnificus occurrence and abundance in the Chesapeake Bay will depend on the degree of warming and other variables mentioned previously. Occurrence and abundance of both species is anticipated to increase under all climate models. For V. parahaemolyticus, mean concentrations in oysters were predicted to increase by 1.5 times under the more conservative MRI model, and more than 3 times under the CM3 model (Muhling et al. 2017). Its range, however, was not expected to expand much given that it is already tolerant to environmental conditions throughout most of the Bay (Muhling et al. 2017). For V. vulnificus, the Mid Bay is anticipated to have the greatest increase in probability of occurrence, from a 47.3% chance in the 1970-1999 summer peak seasons to a 71.7% chance by 2071-2100 summer peak seasons (Muhling et al. 2017). The Patuxent River is anticipated to remain the highest risk zone, however, with probability of occurrence increasing from 64.6% to 84.2% (Muhling et al. 2017).

It is evident that both V. parahaemolyticus and V. vulnificus occurrence and abundance will increase in the Chesapeake Bay under climate change. Increased occurrence and abundance, however, does not directly translate into increased rates of infection—human exposure to Vibrio-contaminated water or shellfish is also involved. Human interaction with the Bay's water and shellfish may change over time, due to both climate-related and other reasons, influencing rates of infection.

One of the main routes of human exposure to both V. parahaemolyticus and V. vulnificus is consumption of raw or undercooked oysters. Models that predict an increase in the proportion of Vibrio-infected oysters in the Bay under climate change usually do not, however, account for the impact that climate change and other environmental changes may have on the oysters themselves. Centuries of overharvesting, pollution, and disease have contributed to an unprecedented decline in oyster populations in the Bay (Chesapeake Bay Foundation 2022). In Maryland, the oyster population has declined from about 600 million market-size oysters in 1999 to about 400 million in 2020 (Chesapeake Bay Foundation 2022). If these trends continue, Vibrio exposure from consumption of contaminated raw and undercooked oysters may decline even while Vibrio abundance rises, although banking on further environmental degradation to help lessen the impacts of other forms of environmental degradation is not a good adaptation solution.

For wound-associated infections, exposure occurs via contact of an open wound with contaminated water. Recreation is one of the main ways that people are exposed to the waters of the Chesapeake Bay. Any link between climate change and the number of people exposing themselves to the water via recreational activities would be indirect at best, but it is conceivable that, in a warmer world with longer warm-weather seasons and more extreme heat waves, more people may seek activities in and on the water to cool off or to simply enjoy a longer summer. The more direct impact on recreation, however, would likely come from increasing populations around the Bay and, therefore, more people recreating in it. This could, however, be offset by fears of degrading water quality or other factors. How recreation on the Bay will change over time is uncertain—it is simply important to note that recreation is one avenue of exposure and, therefore should be taken into consideration when anticipating future rates of Vibrio infections.

Another possible way that people could become exposed to contaminated water is if the water comes to them. Sea levels are rising everywhere, but they are rising especially fast in the Chesapeake Bay, because the land around the Bay is sinking due to ongoing natural geologic processes known as subsidence (Fincham and Brainard 2014). Scientists anticipate that relative sea level rise in Maryland may reach 1.4 feet by 2050, and somewhere between 3.7 and 5.7 feet by 2100 (Fincham and Brainard 2014). The effects of sea level rise are even more obvious when storms occur, because the high tides and storm surges that accompany hurricanes and other extreme weather are exacerbated by the higher water (Fincham and Brainard 2014).

Many regions around the Bay, but especially Annapolis, MD, the Hampton Roads area of Virginia, and the Eastern Shore are already familiar with frequent coastal flooding events. If these events become more common and more extreme, more people may inadvertently become exposed to Vibrio-contaminated water, potentially resulting in higher rates of infection.

While antibiotic resistance does not impact rates of infection for Vibrios, it could impact the severity of vibriosis and the rates of mortality. Antibiotic resistance is increasingly common and, while most Vibrios are susceptible to commonly used antibiotics, the early signs of resistance are emerging (Dutta et al. 2021). Recent studies have shown that some V. vulnificus bacteria have become resistant to ampicillin, tetracycline, aztreonam, streptomycin, gentamicin, and tobramycin (Dutta et al. 2021). This is especially concerning given the mortality rate of V. vulnificus infections if allowed to progress to primary septicemia. The source of emerging antibiotic resistance in Vibrios is still unknown, but possibilities include horizontal gene transfer from other pathogens, especially those found in the effluent of wastewater treatment plants (Dutta et al. 2021).

Given that climate change is already occurring and will continue to occur to some degree regardless of emissions reductions, the most immediate adaptation that can be undertaken to prevent and reduce Vibrio infections from the Chesapeake Bay is environmental monitoring. The  ECDC Vibrio Map Viewer  is one such example of environmental monitoring aimed at predicting Vibrio risk, but it is calibrated to the Baltic Region of Northern Europe, so a Chesapeake Bay-specific monitoring system is necessary (Semenza 2021).. Environmental monitoring of water temperature, salinity, and other variables is already ongoing in the Bay, both through NOAA buoys and other research. Interpreting these data through the lens of Vibrio risk and communicating it in a way that is easy for the public to understand and act upon could reduce Vibrio infections in the future by providing the public with the information necessary to avoid exposure during high-risk periods.

It is unlikely that locals to the Chesapeake Bay region will stop consuming oysters, or stop consuming them raw. However, new fishery regulations could help reduce the risk. Currently, both Maryland and Virginia regulations require oysters to be delivered by certain times of day and to be refrigerated within a certain number of hours, depending on the month (Muhling et al. 2017). An adjustment of these regulations to accommodate a warmer world with higher Vibrio risk could help reduce the amount of contaminated oysters that end up on someone's plate.

Additionally, it is worth exploring the feasibility of regulations that aim to prevent the operation of the fishery during high-risk Vibrio periods. These may be unrealistic given the dependence of local economies on the fishery, but if they are required to keep people safe, they may be necessary. Randomized testing of oyster catches for Vibrios could also help identify contaminated regions or catches, but could be unduly expensive.

There are many ways to prevent the further development of antibiotic resistance, both generally and in Vibrios specifically. Careful following of antibiotic use best practices by both medical professionals and patients is key. Ideally, antibiotics should not be prescribed or overprescribed when they are not necessary, and alternative therapeutics should be developed and considered as a treatment option for mild bacterial infections (Dutta et al. 2021). Considering the potential role of wastewater effluents in the emergence of antibiotic resistance in Vibrios, patients should ensure that their extra antibiotics do not find their way into municipal wastewater systems (Dutta et al. 2021). Robust surveillance for emerging antibiotic resistance in Vibrios should be established and maintained (Dutta et al. 2021).

At the end of the day, adapting to a Chesapeake Bay with higher Vibrio risk may largely fall on individuals' abilities to protect themselves. The easiest ways are avoiding consumption of raw oysters and other shellfish and avoiding swimming or other water-related activities with open wounds and during high-risk periods. For some, these measures may be nearly impossible to follow—many people make their livelihoods on the waters of the Chesapeake Bay, and it would be difficult for them to avoid exposure to the water. In their case, knowledge of the symptoms and careful self-monitoring combined with early treatment could prevent serious illness.

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