Sea temperature influences accumulation of tetrodotoxin in British bivalve shellfish.

Tetrodotoxin (TTX), a potent neurotoxin mostly associated with pufferfish poisoning, is also found in bivalve shellfish. Recent studies into this emerging food safety threat reported TTX in a few, mainly estuarine, shellfish production areas in some European countries, including the United Kingdom. A pattern in occurrences has started to emerge, however the role of temperature on TTX has not been investigated in detail. Therefore, we conducted a large systematic TTX screening study, encompassing over 3500 bivalve samples collected throughout 2016 from 155 shellfish monitoring sites along the coast of Great Britain. Overall, we found that only 1.1 % of tested samples contained TTX above the reporting limit of 2 µg/kg whole shellfish flesh and these samples all originated from ten shellfish production sites in southern England. Subsequent continuous monitoring of selected areas over a five-year period showed a potential seasonal TTX accumulation in bivalves, starting in June when water temperatures reached around 15 °C. For the first time, satellite-derived data were also applied to investigate temperature differences between sites with and without confirmed presence of TTX in 2016. Although average annual temperatures were similar in both groups, daily mean values were higher in summer and lower in winter at sites where TTX was found. Here, temperature also increased significantly faster during late spring and early summer, the critical period for TTX. Our study supports the hypothesis that temperature is one of the key triggers of events leading to TTX accumulation in European bivalves. However, other factors are also likely to play an important role, including the presence or absence of a de novo biological source, which remains elusive.

A new generation of real-time environmental monitoring systems to study the impact of El Niño on disease dynamics.

Global warming is drastically altering weather patterns, accentuating the frequency and strength of global events such as the El Niño Southern Oscillation. This alteration is driving the spread of diseases sensitive to climate such as diarrheal diseases. Environmental monitoring through remote sensing, in combination with data from epidemiological surveillance programs, is facilitating the study of infectious disease dynamics associated with El Niño. This integrative approach can inform the development of strategies for mitigating the impact of these diseases on public health. Here, we discuss some of the achievements of this approach in the management, control, and prevention of infectious diseases linked to El Niño.

Climate warming and increasing Vibrio vulnificus infections in North America.

Vibrio vulnificus is an opportunistic bacterial pathogen, occurring in warm low-salinity waters. V. vulnificus wound infections due to seawater exposure are infrequent but mortality rates are high (~ 18%). Seawater bacterial concentrations are increasing but changing disease pattern assessments or climate change projections are rare. Here, using a 30-year database of V. vulnificus cases for the Eastern USA, changing disease distribution was assessed. An ecological niche model was developed, trained and validated to identify links to oceanographic and climate data. This model was used to predict future disease distribution using data simulated by seven Global Climate Models (GCMs) which belong to the newest Coupled Model Intercomparison Project (CMIP6). Risk was estimated by calculating the total population within 200 km of the disease distribution. Predictions were generated for different "pathways" of global socioeconomic development which incorporate projections of greenhouse gas emissions and demographic change. In Eastern USA between 1988 and 2018, V. vulnificus wound infections increased eightfold (10-80 cases p.a.) and the northern case limit shifted northwards 48 km p.a. By 2041-2060, V. vulnificus infections may expand their current range to encompass major population centres around New York (40.7°N). Combined with a growing and increasingly elderly population, annual case numbers may double. By 2081-2100 V. vulnificus infections may be present in every Eastern USA State under medium-to-high future emissions and warming. The projected expansion of V. vulnificus wound infections stresses the need for increased individual and public health awareness in these areas.

Tracking the impacts of climate change on human health via indicators: lessons from the Lancet Countdown.

BACKGROUND: In the past decades, climate change has been impacting human lives and health via extreme weather and climate events and alterations in labour capacity, food security, and the prevalence and geographical distribution of infectious diseases across the globe. Climate change and health indicators (CCHIs) are workable tools designed to capture the complex set of interdependent interactions through which climate change is affecting human health. Since 2015, a novel sub-set of CCHIs, focusing on climate change impacts, exposures, and vulnerability indicators (CCIEVIs) has been developed, refined, and integrated by Working Group 1 of the "Lancet Countdown: Tracking Progress on Health and Climate Change", an international collaboration across disciplines that include climate, geography, epidemiology, occupation health, and economics. DISCUSSION: This research in practice article is a reflective narrative documenting how we have developed CCIEVIs as a discrete set of quantifiable indicators that are updated annually to provide the most recent picture of climate change's impacts on human health. In our experience, the main challenge was to define globally relevant indicators that also have local relevance and as such can support decision making across multiple spatial scales. We found a hazard, exposure, and vulnerability framework to be effective in this regard. We here describe how we used such a framework to define CCIEVIs based on both data availability and the indicators' relevance to climate change and human health. We also report on how CCIEVIs have been improved and added to, detailing the underlying data and methods, and in doing so provide the defining quality criteria for Lancet Countdown CCIEVIs. CONCLUSIONS: Our experience shows that CCIEVIs can effectively contribute to a world-wide monitoring system that aims to track, communicate, and harness evidence on climate-induced health impacts towards effective intervention strategies. An ongoing challenge is how to improve CCIEVIs so that the description of the linkages between climate change and human health can become more and more comprehensive.

Future scenarios of risk of Vibrio infections in a warming planet: a global mapping study.

BACKGROUND: Infections caused by non-cholera Vibrio species have undergone a global expansion over the past few decades reaching new areas of the world that were previously considered adverse for these organisms. The geographical extent of the expansion has not been uniform, and some areas have shown a rapid increase in infections. METHODS: We applied a new generation of models combining climate, population, and socioeconomic projections to map future scenarios of distribution and season suitability for pathogenic Vibrio. We used the Coupled Model Intercomparison Project 6 framework. Three datasets were used: Geophysical Fluid Dynamics Laboratory's CM4.0 sea surface temperature and sea surface salinity; the coastline length dataset from the World Resources Institute; and Inter-Sectoral Impact Model Intercomparison Project 2b annual global population data. Future projections were used up to the year 2100 and historical simulations from 1850 to 2014. We also project human population at risk under different shared socioeconomic pathways worldwide. FINDINGS: Projections showed that coastal areas suitable for Vibrio could cover 38 000 km of new coastal areas by 2100 under the most unfavourable scenario with an expansion rate of season suitability in these regions of around 1 month every 30 years. Population at risk in suitable regions almost doubled from 1980 to 2020 (from 610 million to 1100 million under the scenario of medium challenges to mitigation and adaptation, shared socioeconomic pathway 2-4.5), although the increment will be more moderate in the future and stabilises after 2050 at 1300 million. Finally, we provide the first global estimate for Vibrio infections, with values around half a million of cases worldwide in 2020. INTERPRETATION: Our projections anticipated an expansion of both the temporal and spatial disease burden for Vibrio infections, in particular at high latitudes of the northern hemisphere. However, the largest extent occurred from 1980 to 2020 and a more moderate increase is expected for the future. The most positive outcome is that the projections showed that Vibrio morbidity will remain relatively stable over the coming decades. FUNDING: NOAA Atlantic Oceanographic and Meteorological Laboratory and NOAA OceanWatch, and by the University of Miami's Cooperative Institute for Marine and Atmospheric Studies.

The new tools revolutionizing Vibrio science.

As microbiologists we live in exciting times. A variety of technical and conceptual developments, particularly in the last decade have revolutionized the field of microbiology, redrawing the landscape, and entirely redefining what is possible. Perhaps this paradigm shift is no more apparent than in the study of vibrios. The family Vibrionaceae are almost unique as a group of bacteria to study in microbiology: they are genomically, phylogenetically and functionally diverse yet a distinct group of environmental bacteria encompassing important human and animal pathogens as well as non-pathogenic species such as ecologically critical symbionts. Sensitive to physiochemical stimuli, they are among the fasting replicating bacteria studied, capable of responding almost immediately to favourable environmental conditions such as those afforded by climate warming. Characterized by an unusual double chromosome and frequently carrying numerous cryptic plasmids - their genomes are often pockmarked with insertion elements, transposons, prophages and integrases - paying testament to past genomic promiscuity. With a strong affinity for environmental niches in freshwater and marine systems, they are among the most numerous bacteria present in our oceans, coasts and freshwater environments. As such they offer something for almost anyone interested in microbiology and represent an excellent example of field of microbiology that has benefitted hugely by advances across a gamut of disciplines - not just microbiological - but encompassing genomics, genetics, oceanography, ecological, earth observations sciences and data visualization, among others. We will briefly outline some of the most exciting, innovative and translational scientific advances that are currently being applied to these ecologically, environmentally and clinically important bacteria.

Enduring Lagrangian coherence of a Loop Current ring assessed using independent observations.

Ocean flows are routinely inferred from low-resolution satellite altimetry measurements of sea surface height assuming a geostrophic balance. Recent nonlinear dynamical systems techniques have revealed that surface currents derived from altimetry can support mesoscale eddies with material boundaries that do not filament for many months, thereby representing effective transport mechanisms. However, the long-range Lagrangian coherence assessed for mesoscale eddy boundaries detected from altimetry is constrained by the impossibility of current altimeters to resolve ageostrophic submesoscale motions. These may act to prevent Lagrangian coherence from manifesting in the rigorous form described by the nonlinear dynamical systems theories. Here we use a combination of satellite ocean color and surface drifter trajectory data, rarely available simultaneously over an extended period of time, to provide observational evidence for the enduring Lagrangian coherence of a Loop Current ring detected from altimetry. We also seek indications of this behavior in the flow produced by a data-assimilative system which demonstrated ability to reproduce observed relative dispersion statistics down into the marginally submesoscale range. However, the simulated flow, total surface and subsurface or subsampled emulating altimetry, is not found to support the long-lasting Lagrangian coherence that characterizes the observed ring. This highlights the importance of the Lagrangian metrics produced by the nonlinear dynamical systems tools employed here in assessing model performance.

Epidemic Dynamics of Vibrio parahaemolyticus Illness in a Hotspot of Disease Emergence, Galicia, Spain.

Galicia in northwestern Spain has been considered a hotspot for Vibrio parahaemolyticus infections. Infections abruptly emerged in 1998 and, over the next 15 years, were associated with large outbreaks caused by strains belonging to a single clone. We report a recent transition in the epidemiologic pattern in which cases throughout the region have been linked to different and unrelated strains. Global genome-wide phylogenetic analysis revealed that most of the pathogenic strains isolated from infections were associated with globally diverse isolates, indicating frequent episodic introductions from disparate and remote sources. Moreover, we identified that the 2 major switches in the epidemic dynamics of V. parahaemolyticus in the regions, the emergence of cases and an epidemiologic shift in 2015-2016, were associated with the rise of sea surface temperature in coastal areas of Galicia. This association may represent a fundamental contributing factor in the emergence of illness linked to these introduced pathogenic strains.

Genomic Variation and Evolution of Vibrio parahaemolyticus ST36 over the Course of a Transcontinental Epidemic Expansion.

Vibrio parahaemolyticus is the leading cause of seafood-related infections with illnesses undergoing a geographic expansion. In this process of expansion, the most fundamental change has been the transition from infections caused by local strains to the surge of pandemic clonal types. Pandemic clone sequence type 3 (ST3) was the only example of transcontinental spreading until 2012, when ST36 was detected outside the region where it is endemic in the U.S. Pacific Northwest causing infections along the U.S. northeast coast and Spain. Here, we used genome-wide analyses to reconstruct the evolutionary history of the V. parahaemolyticus ST36 clone over the course of its geographic expansion during the previous 25 years. The origin of this lineage was estimated to be in ~1985. By 1995, a new variant emerged in the region and quickly replaced the old clone, which has not been detected since 2000. The new Pacific Northwest (PNW) lineage was responsible for the first cases associated with this clone outside the Pacific Northwest region. After several introductions into the northeast coast, the new PNW clone differentiated into a highly dynamic group that continues to cause illness on the northeast coast of the United States. Surprisingly, the strains detected in Europe in 2012 diverged from this ancestral group around 2000 and have conserved genetic features present only in the old PNW lineage. Recombination was identified as the major driver of diversification, with some preliminary observations suggesting a trend toward a more specialized lifestyle, which may represent a critical element in the expansion of epidemics under scenarios of coastal warming.IMPORTANCEVibrio parahaemolyticus and Vibrio cholerae represent the only two instances of pandemic expansions of human pathogens originating in the marine environment. However, while the current pandemic of V. cholerae emerged more than 50 years ago, the global expansion of V. parahaemolyticus is a recent phenomenon. These modern expansions provide an exceptional opportunity to study the evolutionary process of these pathogens at first hand and gain an understanding of the mechanisms shaping the epidemic dynamics of these diseases, in particular, the emergence, dispersal, and successful introduction in new regions facilitating global spreading of infections. In this study, we used genomic analysis to examine the evolutionary divergence that has occurred over the course of the most recent transcontinental expansion of a pathogenic Vibrio, the spreading of the V. parahaemolyticus sequence type 36 clone from the region where it is endemic on the Pacific coast of North America to the east coast of the United States and finally to the west coast of Europe.

Environmental Suitability of Vibrio Infections in a Warming Climate: An Early Warning System.

BACKGROUND: Some Vibrio spp. are pathogenic and ubiquitous in marine waters with low to moderate salinity and thrive with elevated sea surface temperature (SST). OBJECTIVES: Our objective was to monitor and project the suitability of marine conditions for Vibrio infections under climate change scenarios. METHODS: The European Centre for Disease Prevention and Control (ECDC) developed a platform (the ECDC Vibrio Map Viewer) to monitor the environmental suitability of coastal waters for Vibrio spp. using remotely sensed SST and salinity. A case-crossover study of Swedish cases was conducted to ascertain the relationship between SST and Vibrio infection through a conditional logistic regression. Climate change projections for Vibrio infections were developed for Representative Concentration Pathway (RCP) 4.5 and RCP 8.5. RESULTS: The ECDC Vibrio Map Viewer detected environmentally suitable areas for Vibrio spp. in the Baltic Sea in July 2014 that were accompanied by a spike in cases and one death in Sweden. The estimated exposure-response relationship for Vibrio infections at a threshold of 16°C revealed a relative risk (RR)=1.14 (95% CI: 1.02, 1.27; p=0.024) for a lag of 2 wk; the estimated risk increased successively beyond this SST threshold. Climate change projections for SST under the RCP 4.5 and RCP 8.5 scenarios indicate a marked upward trend during the summer months and an increase in the relative risk of these infections in the coming decades. CONCLUSIONS: This platform can serve as an early warning system as the risk of further Vibrio infections increases in the 21st century due to climate change. https://doi.org/10.1289/EHP2198.

Non-Cholera Vibrios: The Microbial Barometer of Climate Change.

There is a growing interest in the role of climate change in driving the spread of waterborne infectious diseases, such as those caused by bacterial pathogens. One particular group of pathogenic bacteria - vibrios - are a globally important cause of diseases in humans and aquatic animals. These Gram-negative bacteria, including the species Vibrio vulnificus, Vibrio parahaemolyticus and Vibrio cholerae, grow in warm, low-salinity waters, and their abundance in the natural environment mirrors ambient environmental temperatures. In a rapidly warming marine environment, there are greater numbers of human infections, and most notably outbreaks linked to extreme weather events such as heatwaves in temperate regions such as Northern Europe. Because the growth of pathogenic vibrios in the natural environment is largely dictated by temperature, we argue that this group of pathogens represents an important and tangible barometer of climate change in marine systems. We provide a number of specific examples of the impacts of climate change on this group of bacteria and their associated diseases, and discuss advanced strategies to improve our understanding of these emerging waterborne diseases through the integration of microbiological, genomic, epidemiological, climatic, and ocean sciences.

Heat Wave-Associated Vibriosis, Sweden and Finland, 2014.

During summer 2014, a total of 89 Vibrio infections were reported in Sweden and Finland, substantially more yearly infections than previously have been reported in northern Europe. Infections were spread across most coastal counties of Sweden and Finland, but unusually, numerous infections were reported in subarctic regions; cases were reported as far north as 65°N, ≈100 miles (160 km) from the Arctic Circle. Most infections were caused by non-O1/O139 V. cholerae (70 cases, corresponding to 77% of the total, all strains were negative for the cholera toxin gene). An extreme heat wave in northern Scandinavia during summer 2014 led to unprecedented high sea surface temperatures, which appear to have been responsible for the emergence of Vibrio bacteria at these latitudes. The emergence of vibriosis in high-latitude regions requires improved diagnostic detection and clinical awareness of these emerging pathogens.

Epidemiological investigation of a foodborne outbreak in Spain associated with U.S. West Coast genotypes of Vibrio parahaemolyticus.

We describe an outbreak of seafood-associated Vibrio parahaemolyticus in Galicia, Spain in on 18th of August 2012 affecting 100 of the 114 passengers travelling on a food banquet cruise boat. Epidemiological information from 65 people was available from follow-on interviews, of which 51 cases showed symptoms of illness. The food items identified through the questionnaires as the most probable source of the infections was shrimp. This product was unique in showing a statistically significant and the highest OR with a value of 7.59 (1.52-37.71). All the nine strains isolated from stool samples were identified as V. parahaemolyticus, seven were positive for both virulence markers tdh and trh, a single strain was positive for trh only and the remaining strain tested negative for both trh and tdh. This is the largest foodborne Vibrio outbreak reported in Europe linked to domestically processed seafood. Moreover, this is the first instance of strains possessing both tdh+ and trh+ being implicated in an outbreak in Europe and that a combination of strains represent several pathogenicity groups and belonging to different genetic variants were isolated from a single outbreak. Clinical isolates were associated with a novel genetic variant of V. parahaemolyticus never detected before in Europe. Further analyses demonstrated that the outbreak isolates showed indistinguishable genetic profiles with hyper-virulent strains from the Pacific Northwest, USA, suggesting a recent transcontinental spread of these strains.

Dissipative inertial transport patterns near coherent Lagrangian eddies in the ocean.

Recent developments in dynamical systems theory have revealed long-lived and coherent Lagrangian (i.e., material) eddies in incompressible, satellite-derived surface ocean velocity fields. Paradoxically, observed drifting buoys and floating matter tend to create dissipative-looking patterns near oceanic eddies, which appear to be inconsistent with the conservative fluid particle patterns created by coherent Lagrangian eddies. Here, we show that inclusion of inertial effects (i.e., those produced by the buoyancy and size finiteness of an object) in a rotating two-dimensional incompressible flow context resolves this paradox. Specifically, we obtain that anticyclonic coherent Lagrangian eddies attract (repel) negatively (positively) buoyant finite-size particles, while cyclonic coherent Lagrangian eddies attract (repel) positively (negatively) buoyant finite-size particles. We show how these results explain dissipative-looking satellite-tracked surface drifter and subsurface float trajectories, as well as satellite-derived Sargassum distributions.

Origins and colonization history of pandemic Vibrio parahaemolyticus in South America.

The dynamics of dissemination of the environmental human pathogen Vibrio parahaemolyticus are uncertain. The O3:K6 clone was restricted to Asia until its detection along the Peruvian coasts and in northern Chile in 1997 in phase with the arrival of El Niño waters. A subsequent emergence of O3:K6 strains was detected in austral Chile in 2004. The origin of these 1997 and 2004 population radiations has not yet been conclusively determined. Multiple loci VNTR analysis using seven polymorphic loci was carried out with a number of representative strains from Asia, Peru and Chile to determine their genetic characteristics and population structure. Asian and Chilean subpopulations were the most genetically distant groups with an intermediate subpopulation in Peru. Population structure inferred from a minimum-spanning tree and Bayesian analysis divided the populations into two genetically distinct groups, consistent with the epidemic dynamics of the O3:K6 clone in South America. One group comprised strains from the original Asiatic population and strains arriving in Peru and Chile in 1997. The second group included the remaining Peruvian Strains and Chilean strains obtained from Puerto Montt in 2004. The analysis of the arrival of the O3:K6 clone at the Pacific coasts of South America has provided novel insights linking the origin of the invasion in 1997 to Asian populations and describing the successful establishment of the O3:K6 populations, first in Peru and subsequently in the South of Chile owing to a possible radiation of Peruvian populations.

Emergence of Asiatic Vibrio diseases in South America in phase with El Niño.

BACKGROUND: The seventh pandemic of Vibrio cholerae unexpectedly reached the coast of Peru in 1991, causing an explosive emergence of infections throughout the American continents. The origin and routes of dissemination are as yet unknown. A new Vibrio epidemic arose in 1997 in South America (northern Chile) when the pandemic clone of Vibrio parahaemolyticus was for the fist time detected outside of Asia. These 2 cases were concurrent with 2 episodes of El Niño. METHODS: We carried out a survey of records of V. parahaemolyticus infection and of strains existing in the Instituto Nacional de Salud of Peru between 1994 and 2005. Association between the El Niño event and the V. parahaemolyticus disease was analyzed through generalized additive models applied to time-series data with negative binomial response, selecting some oceanographic factors distinctive of the movement of the El Niño waters. RESULTS: Epidemiologic data and laboratory investigations of the strains showed that V. parahaemolyticus infections caused by the pandemic clone emerged in the coasts of Peru linked to the 1997 El Niño episode. The epidemic dissemination of this clone matched the expansion and dynamics of the poleward propagation and the receding of the El Niño waters. This pattern was similar to previously reported onset of cholera epidemic in 1991. CONCLUSIONS: These findings identify the El Niño episodes as a reliable vehicle for the introduction and propagation of Vibrio pathogens in South America. The movement of oceanic waters seems to be one of the driving forces of the spread of Vibrio diseases.

Environmental determinants of the occurrence and distribution of Vibrio parahaemolyticus in the rias of Galicia, Spain.

Infections associated with Vibrio parahaemolyticus on the coast of Galicia (in northwestern Spain) were reported to be linked to large outbreaks of illness during 1999 and 2000. Little information is available about the ecological factors that influence the emergence of V. parahaemolyticus infections in this temperate region. We carried out a 3-year study to investigate the occurrence and distribution of V. parahaemolyticus at 26 sites located in the four main rias of Galicia in association with environmental and oceanographic variables. V. parahaemolyticus was detected in all the areas investigated and throughout the complete period of study with an overall incidence of 12.5%. Salinity was the primary factor governing the temporal and spatial distribution of V. parahaemolyticus, whereas seawater temperature had a secondary effect and only modulated the abundance in periods and areas of reduced salinities. Higher occurrence of V. parahaemolyticus was observed during periods of lower salinity in autumn, with a total of 61 positive samples (18%) and a mean density of 1,234 most probable number/100 g. V. parahaemolyticus was primarily detected in areas of reduced salinity close to freshwater discharge points, where it was found in up to 45% of the samples. Characterization of the isolates obtained from the study resulted in the first identification of two pathogenic tdh-positive strains of V. parahaemolyticus recovered from the marine environment in Galicia. These isolates showed serotypes identical to and DNA profiles indistinguishable from those of the clinical clone of V. parahaemolyticus dominant in infections in Spain in the last 10 years.