Food Research International 43 (2010) 1780–1790

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Food Research International

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Climate anomalies and the increasing risk of Vibrio parahaemolyticusand Vibrio vulnificus illnesses

Jaime Martinez-Urtaza a, John C. Bowers b, Joaquin Trinanes c, Angelo DePaola d,*

a Instituto de Acuicultura, Universidad de Santiago de Compostela, Campus Sur, 15782 Santiago de Compostela, Spainb Food and Drug Administration, Center for Food Safety and Applied Nutrition, College Park, MD, USAc Instituto de Investigaciones Tecnologicas, Universidad de Santiago de Compostela, Campus Sur, 15782 Santiago de Compostela, Spaind Food and Drug Administration, Gulf Coast Seafood Laboratory, Dauphin Island, AL, USA

a r t i c l e i n f o

Article history:Received 22 February 2010Accepted 6 April 2010

Keywords:V. parahaemolyticusV. vulnificusClimate anomaliesOutbreaks

0963-9969/$ - see front matter Published by Elsevierdoi:10.1016/j.foodres.2010.04.001

* Corresponding author. Address: FDA, Gulf CoaBox 158, Dauphin Island, AL 36528, USA. Tel.: +1 254477.

E-mail address: angelo.depaola@fda.hhs.gov (A. De

a b s t r a c t

We examined the potential influence of climate anomalies in expanding the geographical and seasonalrange of seafood-borne illnesses from Vibrio parahaemolyticus and Vibrio vulnificus. Archived climate datafrom areas of implicated seafood production were obtained from various sources, including in situ mon-itoring devices and satellite imagery. The geographical expansion of V. parahaemolyticus outbreaks intoPeru and Alaska corresponded closely with climate anomalies such as El Niño, which brought largemasses of abnormally warm water into these regions. Seasonal expansion of V. vulnificus illnesses asso-ciated with oysters harvested from the Gulf of Mexico in April and November correspond with warmerwater temperatures (>20 �C) recorded during these months since 1998. This retrospective review indi-cates that climate anomalies have already greatly expanded the risk area and season for vibrio illnessesand suggest that these events can be forecasted. Certainly, when similar circumstances occur in thefuture, adjustments in industry practices and regulatory policy should be considered, especially for sea-food that is consumed raw, such as bivalve mollusks.

Published by Elsevier Ltd.

1. Introduction

The effect of climate change on the dynamics of human infec-tion and disease attributed to Vibrio cholerae has been extensivelyinvestigated and is well documented (e.g., Lipp, Huq, & Colwell,2002; Matsuda et al., 2008; Rodo, Pascual, Fuchs, & Faruque,2002). Less attention has been focused on the impacts of climatechange on other pathogenic Vibrio spp. In this manuscript, we re-view the impact of climate change on the population dynamicsand epidemiology of Vibrio parahaemolyticus and Vibrio vulnificus.The transmission of V. parahaemolyticus and V. vulnificus infectionsare typically more closely associated with consumption of seafood,particularly molluscan shellfish than that of V. cholerae, which ismost often associated with fecal–oral route of infection.

The approach used in this paper was to review the epidemiolog-ical record for outbreaks and illnesses that occurred outside thenormal window of risk areas or seasons for V. parahaemolyticusand V. vulnificus infections and determine if these correspondedto unusually warm climate patterns or other climate anomalies.Archived data for time lapse satellite imagery and other ocean

Ltd.

st Seafood Laboratory, P.O.1 690 3367; fax: +1 251 694

Paola).

observing data systems were employed to recreate the climateconditions in areas and times of unexpected outbreaks and ill-nesses. This review also discusses some of the control measuresthat may help mitigate risk during episodes of climate anomalies.

1.1. Vibrio parahaemolyticus

V. parahaemolyticus is a halophilic bacterium that naturally oc-curs in marine environments of warm and temperate regions andis a leading cause of seafood- associated gastroenteritis worldwide.Illnesses are usually sporadic or associated with small outbreaks. V.parahaemolyticus infections usually result from ingestion of raw orimproperly cooked or re-contaminated seafood (Barker, Weaver,Morris, & Martin, 1975). V. parahaemolyticus has one of the shortestgeneration times of any bacterium (<10 min) with an optimumgrowth temperature of approximately 37 �C (Miles, Ross, Olley, &McMeekin, 1997). While V. parahaemolyticus can grow at tempera-tures <10 �C, the minimum seawater temperature associated withV. parahaemolyticus illnesses is 15 �C (McLaughlin et al., 2005). V.parahaemolyticus can overwinter in sediments and emerge in thespring in association with zooplankton (Kaneko & Colwell, 1975,1978). The salinity optimum for V. parahaemolyticus in oysters is�23 ppt although salinities ranging from 10 to 34 ppt were re-ported to support relatively high numbers in bivalve shellfish

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(Anonymous, 2005; Martinez-Urtaza et al., 2004; Zimmermanet al., 2007). V. parahaemolyticus strains recovered from humangastroenteritis cases typically carry the thermostabile direct hem-olysin (tdh) gene, the tdh-related hemolysin (trh) gene, or both.These virulence markers occur infrequently in strains isolated fromenvironmental sources and foods. Strains bearing tdh or trh genesrepresent less than 3% of all V. parahaemolyticus strains isolatedfrom the environment (DePaola, Kaysner, Bowers, & Cook, 2000).However, the relative abundance of pathogenic strains may be sub-stantially higher in some areas and during certain times of the year(Alam, Miyoshi, & Shinoda, 2003; Johnson et al., 2008; McLaughlinet al., 2005; Rodriguez-Castro et al., 2010). Virulence of V. parahae-molyticus is not well understood. In some areas with high densitiesof total and pathogenic V. parahaemolyticus, such as the Gulf ofMexico, fewer cases are reported than in areas with lower levels,such as the US Pacific Northwest and Alaska (McLaughlin et al.,2005; Zimmerman et al., 2007). Additionally, isolates from someof the most severe V. parahaemolyticus cases in the US lack boththe tdh and trh genes (Yu, Puhr, Bopp, Gerner-Smidt, & Painter,2006). Ecological interactions of V. parahaemolyticus with marinefauna, including bivalve mollusks, may influence infectivity butare largely unknown. Risk assessments for V. parahaemolyticus inoysters and other seafood were conducted by the US Food andDrug Administration (FDA-VPRA) (Anonymous, 2005) and the Foodand Agricultural Organization and World Health Organization(FAO/WHO-VPRA, in press).

In 1950, Fujino and coworkers in Japan identified a new bacte-rium as the causative agent of a large outbreak associated with theconsumption of a semi-dried fish product, shirasu (Fujino, 1974).Initially, the new species was named Pasteurella parahaemolyticus(Fujino et al., 1953) and later designated as Vibrio parahaemolyticusby the Subcommittee on Taxonomy of Vibrios of the InternationalCommittee on Systematic Bacteriology (Hugh & Sakauki, 1975).

Prior to the 1970’s, nearly all reported infections caused by V.parahaemolyticus were confined to Japan. Food-borne outbreaksattributed to this organism were primarily associated with fish,and represented 70% of food-related illnesses during summermonths (Joseph, Colwell, & Kaper, 1982). In the early 1970’s, V.parahaemolyticus illnesses were first recognized in the US duringwarmer months at a variety of locales including Atlantic, Pacificand Gulf States (Barker, 1974). The first well-documented outbreakof V. parahaemolyticus in the US was in Maryland in 1971, and wasassociated with consumption of cross-contaminated crab products(Dadisman, Nelson, Molenda, & Carber, 1972). Serotypes of V. para-haemolyticus strains isolated from patients and suspect foods in theUS differed from those isolated in Japan (Fishbein, Wentz, Landry,& MacEachern, 1974).

Unlike V. cholerae, person to person transmission of V. parahae-molyticus has not been reported and foodborne illnesses arenearly always associated with seafood consumption (Josephet al., 1982). Throughout the 1970’s, sporadic cases and outbreaksof V. parahaemolyticus were reported in Europe, Africa, New Zea-land, and most of the Asian countries (Joseph et al., 1982). V.parahaemolyticus causes a mild illness that rarely needs medicalassistance. Most of the cases are not brought to the attention ofpublic health departments so illnesses are underreported. TheUS Centers for Disease Control and Prevention (CDC) estimatesthat only one in twenty V. parahaemolyticus cases is reported(Mead et al., 1999). V. parahaemolyticus is recognized as a primarycause of bacterial gastroenteritis associated with seafood con-sumption in many areas of the world, including Japan (Anony-mous, 1999), Taiwan (Wong et al., 2000), and the US (Danielset al., 2000b). Infections caused by V. parahaemolyticus are gener-ally associated with diverse serotypes and genetic groups ende-mic to certain coastal areas of seafood production (Johnsonet al., 2008).

In 1996, there was a sharp increase in V. parahaemolyticus casesassociated with the serotype O3:K6 in Calcutta, India. Moleculartyping placed these isolates into a single homogenous group withvirulence traits (tdh positive, trh negative) clearly differentiatedfrom other O3:K6 strains recovered before this epidemic (Okudaet al., 1997). The clonal clustering of the strains and their distinc-tive genetic characteristics, led to this group being named a ‘‘newO3:K6 clone” (Chowdhury et al., 2000a; Okuda et al., 1997). V.parahaemolyticus illnesses from the new O3:K6 clone spreadthroughout most Southeast Asian countries within a year (Okudaet al., 1997). In 1997, the new O3:K6 clone spread beyond Asiafor the first time to Peru, causing illnesses in June of that year(Martinez-Urtaza et al., 2008). It spread to Chile later in 1997(Gonzalez-Escalona et al., 2005). However, more than a decadehad passed before a retrospective study recognized that these ill-nesses were associated with this clone. In 1998, a large V. parahae-molyticus outbreak occurred in the US, and was associated withconsumption of raw oysters from Galveston Bay, Texas (Danielset al., 2000a). Molecular typing indicated that the clinical isolateswere the same as the new O3:K6 clone from Asia (Matsumotoet al., 2000). This was the first definitive evidence of a V. parahae-molyticus pandemic, and the term ‘‘pandemic clone” was coined.The pandemic clone has since been reported in many countriesincluding Russia (Nair et al., 2007), France (Quilici, Robert-Pillot,Picart, & Fournier, 2005), Spain (Martinez-Urtaza et al., 2005),Mozambique (Ansaruzzaman et al., 2005), and Italy (Ottavianiet al., 2008). Within a few years of its emergence, some strainsbelonging to the new O3:K6 clonal group began to seroconvertbut were otherwise genetically indistinguishable by most subtyp-ing methods (Chowdhury et al., 2000b). Thus, this clonal groupwas renamed a ‘‘clonal complex” (Gonzalez-Escalona et al., 2008)and most authors now refer to this as the pandemic clonalcomplex.

Probably the most important change in the epidemiology of V.parahaemolyticus in recent years has been the global spread ofinfections to areas such as Chile and Alaska where this pathogenwas rarely reported or was absent. The recent global spread of V.parahaemolyticus has often been associated with much larger out-breaks than have occurred in the past. The emergence of V. para-haemolyticus outbreaks in Chile (Gonzalez-Escalona et al., 2005),Peru (Martinez-Urtaza et al., 2008), Texas (Daniels et al., 2000a),Spain (Martinez-Urtaza et al., 2005), and Madagascar (Ansaruzz-aman et al., 2005) were largely associated with the pandemic clo-nal complex. However the emergence of large outbreaks is not anexclusive feature related to pandemic strains. Other large V. para-haemolyticus outbreaks associated with strains of a single serotypeor an array of diverse serotypes were reported in different regionsof the world. Three of the most important epidemic expansions re-lated to non-pandemic strains occurred on the Pacific Coast of theUS in 1997 (mainly O4:K12 strains; CDC, 1998), in the Northwestof Spain in 1999 (O4:K11 strains; Martinez-Urtaza et al., 2004),and in Alaska in 2004 (O6:K18 strains; McLaughlin et al., 2005).Some of the strains associated with the outbreaks in the US PacificNorthwest and Spain persisted regionally for at least a few decades(Gonzalez-Escalona et al., 2008), but were not reported in other re-gions of the world.

The origins and routes of dissemination of pathogenic V. para-haemolyticus strains responsible for the large outbreaks are a con-troversial issue. The dissemination of pandemic strains fromendemic areas of V. parahaemolyticus has been attributed to thedischarge of ballast water from cargo ships. Ballast water dis-charges are recognized as a major vehicle for worldwide biologicalinvasions of marine species (Niimi, 2004). Nutrients present in bal-last water may support the propagation of pathogenic Vibrio spp.(Ruiz et al., 2000). Ballast discharge from cargo ships was associ-ated with the arrival of epidemic V. cholerae O1 in the US from La-

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tin American ports in 1991 (DePaola et al., 1992; McCarthy &Khambaty, 1994). It was suggested that the dissemination of path-ogenic V. parahaemolyticus through ballast water discharge wasresponsible for outbreaks in Texas in the US (Daniels et al.,2000a) and A Coruña in Spain (Martinez-Urtaza et al., 2008). Ineach of these episodes, infections arose in areas close to activeinternational ports and were related to pandemic strains. Strainsbelonging to the pandemic clonal complex were not detected ineither area prior to the outbreaks and were not detected in clinicalcases or in the environment after these outbreaks (DePaola et al.,2000; Rodriguez-Castro et al., 2010). Certainly, one of the greatmysteries of the V. parahaemolyticus pandemic is why the pan-demic clonal complex became endemic in Asia and Latin Americabut not in Europe or North America.

Seasonal V. parahaemolyticus cases are concentrated over thewarmest months of the year in temperate regions (Daniels et al.,2000b), where the rise in seawater temperature over the summerpromotes a higher abundance of V. parahaemolyticus. Due to thedose-dependence of V. parahaemolyticus infections, higher levelsof V. parahaemolyticus increase the risk of illness. Infections canpersist year-round in geographical areas with a tropical climate(Joseph et al., 1982). The dependence of V. parahaemolyticus popu-lations on rising temperatures suggests that illnesses caused bythis organism may be especially influenced by climate change.Even a slight warming of the environment will affect the growthrates of V. parahaemolyticus and reduce the restrictions that coldwinters have on their life cycle (Harvell et al., 2002). An average1.5 �C increase in water temperature will significantly extend theseasonal period and geographical range of higher abundance andgreater risk (Harvell et al., 2002). Warming environments will alsoalter the physiological activity of estuarine fauna that are con-sumed as seafood and this could also affect their ability to serveas vehicles of vibrio diseases.

Anomalies in seawater temperature may also explain the sud-den emergence of V. parahaemolyticus outbreaks in new areas.Unusually warm coastal seawater temperatures were detectedconcurrently with the epidemic onset of many large outbreaks,such as those occurring in Chile in 1997 and 2004 (Gonzalez-Esca-lona et al., 2005), Peru in 1997 (Martinez-Urtaza et al., 2008), USPacific Northwest in 1997 (CDC, 1998), Spain in 1999 (Baker-Aus-tin, Stockley, Rangdale, & Martinez-Urtaza, 2010), and Alaska in2004 (McLaughlin et al., 2005). In some cases ballast water dis-charges in conjunction with high temperatures may account forthe arrival of V. parahaemolyticus and the subsequent emergenceof infections (McLaughlin et al., 2005).

1.2. Vibrio vulnificus

V. vulnificus occupies an ecological niche similar to V. parahae-molyticus but does not tolerate low temperatures or high salinity,and is more suited for brackish water environments (FAO/WHO.,2005; Nishibuchi & DePaola, 2005). It presents a much differentdisease syndrome than V. parahaemolyticus, capable of causing se-vere systemic illnesses including primary septicemia after con-sumption of raw seafood, or secondary septicemia from woundexposure to seawater and seafood (Strom & Paranjpye, 2000). V.vulnificus may cause gastroenteritis, but these cases are relativelymild and infrequently reported. Nearly all primary septicemiacases occur in individuals with underlying chronic illnesses includ-ing liver disease, diabetes, or disorders that compromise the im-mune system (Nishibuchi & DePaola, 2005). Most of the researchon human illnesses has been conducted in the US, where this bac-terium was first recognized in the 1970’s. Nearly all cases in the USare associated with consumption of raw oysters harvested fromcoastal areas along the Gulf of Mexico during warm weathermonths (Nishibuchi & DePaola, 2005).

V. vulnificus minimal growth temperature in oysters is �13 �Cand the optimal growth temperature is �37 �C (FAO/WHO, 2005;Kaspar & Tamplin, 1993). FAO and WHO conducted a risk assess-ment of V. vulnificus in raw oysters from the Gulf of Mexico (VVRA)that was released in 2005 (FAO/WHO, 2005). V. vulnificus levels inoysters at harvest were influenced primarily by water tempera-ture; levels at consumption and risk of illness were further influ-enced by ambient air temperature between harvest and initialrefrigeration. Nearly all oyster-associated V. vulnificus illnesses inthe US occur when water temperatures are >20 �C (Nishibuchi &DePaola, 2005) and until the late 1990’s, the V. vulnificus illness riskseason was considered to span the months of May through Octo-ber. V. vulnificus is much less abundant in oysters from high salinity(>30 ppt) waters, regardless of temperature, and few illnesses aretraced to oysters harvested from areas with high salinity (Motes& DePaola, 1996; Motes et al., 1998).

While the virulence of V. vulnificus has been studied extensively,there is no one virulence marker that is definitively associated withhuman illness as tdh is with V. parahaemolyticus. The ability to ac-quire iron, produce capsule, hemolysins and a variety of enzymesplay important roles in the pathogenicity of V. vulnificus but thesetraits are present in most environmental and clinical strains(Nishibuchi & DePaola, 2005; Strom & Paranjpye, 2000). However,evidence is accumulating that certain genetic markers such as se-quence polymorphisms of the 16S rRNA gene, another gene of un-known function but referred to as the virulence correlated gene(vcg) and pilF (associated with pilus-type IV assembly) are muchmore prevalent in clinical isolates than those found in environmen-tal strains (Nilsson, Paranjpye, DePaola, & Strom, 2003; Roig, Sanj-uan, Llorens, & Amaro, 2010; Rosche, Yano, & Oliver, 2005). Areal-time PCR assay was developed to differentiate 16S rRNA se-quence variants and further confirmed that the B sequence typewas primarily responsible for foodborne primary septicemia ill-nesses (Vickery, Nilsson, Strom, Nordstrom, & DePaola, 2007). Thisstudy also reported that both A and B sequence types were similarlyprevalent in wound infection isolates from Denmark but woundinfection isolates associated with handling of tilapia in Israel con-tained a combination of A and B sequences in all strains. The limitedwork on the seasonal prevalence of V. vulnificus strains with genetictraits (type B rRNA sequence type in Galveston Bay, Texas) associ-ated with human illness suggest that a more virulent populationis associated with warmer waters (Lin & Schwarz, 2003).

The epidemiology of V. vulnificus is covered in detail in the FAOand WHO VVRA (FAO/WHO, 2005) and elsewhere (Nishibuchi &DePaola, 2005; Strom & Paranjpye, 2000). Primary septicemia isthe most significant disease caused by this pathogen and resultsfrom intestinal colonization followed by systemic infection (Shap-iro et al., 1998). V. vulnificus is responsible for nearly all seafood-associated deaths in the US and has a case fatality rate of >50%,which is the highest of any foodborne pathogen. Similar fatalityrates were reported in Asia (Chuang, Yuan, Liu, Lan, & Huang,1992; Park, Shon, & Joh, 1991). Healthy individuals rarely developprimary septicemia and are generally considered to be at low riskfor this syndrome (Shapiro et al., 1998). Individuals with chronicunderlying illnesses such as liver or blood diseases and immunedisorders are most at risk. CDC estimates approximately 100 food-borne primary septicemia cases in the US annually with the major-ity of cases attributed to consumption of raw oysters harvestedfrom the Gulf of Mexico (Mead et al., 1999). A typical meal of 12raw Gulf Coast oysters during warm months contains >107 cultur-able V. vulnificus cells (FAO/WHO, 2005). Even with this high expo-sure level, primary septicemia is estimated to occur only once inevery 20,000 meals of raw oysters consumed by high risk consum-ers (FAO/WHO, 2005). Foodborne illnesses consist of sporadic casesand a foodborne V. vulnificus outbreak has never been reported(Shapiro et al., 1998). Infections tend to be most common in males

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over 40 years old (Nishibuchi & DePaola, 2005). V. vulnificus cancause mild gastroenteritis but such illnesses account for <5% of re-ported cases (Nishibuchi & DePaola, 2005).

V. vulnificus infections are rarely reported in Europe where casesare almost exclusively restricted to wound infections. Typically,these cases occurred in years with anomalously high water tem-peratures and were usually in Northern Europe (Andersen, 1991;Frank, Littman, Alpers, & Hallauer, 2006; Høi, Larsen, Dalsgaard,& Dalsgaard, 1998; Melhus, Holmdahl, & Tjernberg, 1995). Therewas a single outbreak associated with V. vulnificus in Israel duringthe late 1990’s among fish market workers (Bisharat & Raz, 1996;Bisharat et al., 2005). These workers developed severe soft tissueinfections and bacteremia from wounds resulting from handlinglive tilapia and no foodborne transmission was reported. Unlikeother instances of human infections that are caused by heteroge-neous strains of V. vulnificus, the strains from the Israel outbreakwere quite homogeneous and were designated as biotype 3. Whilethe origins of this outbreak were not determined, a significant cor-relation between warm temperatures and emergence of infectionswas reported (Paz, Bisharat, Paz, Kidar, & Cohen, 2007). The sum-mers of 1996–1998, when the outbreaks peaked, were the hottestperiods recorded in Israel in over 40 years.

2. Evidence linking climate change and foodborne illnessescaused by V. parahaemolyticus and V. vulnificus

Vibrio infections in the US, which are largely attributable to V.parahaemolyticus and V. vulnificus, have increased in recent years.CDC data indicate that vibrio infections have increased since 2000,while the relative rates of infections from other major foodbornepathogens have decreased (Fig. 1) (CDC, 2009). Increasing numbersof infections and outbreaks due to V. parahaemolyticus were also evi-dent in other countries, such as Chile and Spain. Below, we explorethe extent to which climate change may contribute to these trends.

Increased access to historical epidemiological records and rapidaccess to environmental information from remote sensing systemson a global scale have provided new opportunities for retrospectiveanalysis of large V. parahaemolyticus outbreaks from an oceanicperspective. Many of the larger V. parahaemolyticus outbreaks wereconcurrent with temperature anomalies which transported warmwaters from areas located hundreds or thousands of kilometersaway from the outbreak region. The presence of warm waters oftropical or subtropical origin were observed during the onset of ill-

Fig. 1. Relative trend in reported number of vibrio infections occurring annually inthe US since 2000, compared with that of other foodborne pathogens (CDC FoodNetdata, MMNR 58:333–337, 2008).

nesses in Peru and Chile in 1997 (Martinez-Urtaza et al., 2008), inthe Northwest of Spain in 1999 (Baker-Austin et al., 2010), and inAlaska in 2004 (as described herein). Satellite remote sensing dataconfirm warm seawater moving into proximal coastal regions con-current with reported outbreaks. These events were not associatedwith local changes in the coastal environments, but rather with theinvasion of foreign waters of higher temperature and, in somecases, of lower salinity, than those prevailing under normal sea-sonal conditions in these regions. Other oceanographic changesalso occurred including a sharp reduction in upwelling in the areaand collapse of the native zooplankton populations which were re-placed by allochthonous zooplankton (Baker-Austin et al., 2010;Martinez-Urtaza et al., 2008). Changes in ocean circulation pat-terns could influence the epidemic dynamics of V. parahaemolyticusby providing a mechanism for the long-distance propagation ofpathogenic populations on zooplankton (Martinez-Urtaza et al.,2008). Zooplankton represents an important food source for vib-rios, allowing for an enhanced survival of these bacteria in the mar-ine environment (Amako, Shimodori, Imoto, Miake, & Umeda,1987; Dawson, Humphrey, & Marshall, 1981; Dumontet et al.,1996; Huq et al., 1983). The presence of non-native zooplanktonin concurrence with the onset of V. parahaemolyticus outbreaks(Martinez-Urtaza et al., 2008) suggests a possible role of planktonin the dispersal of pathogenic Vibrio mediated by currents andmovement of water masses.

Due to biological and ecological characteristics, plankton isprobably one of the most sensitive of biological groups to minorchanges in the environment (Chavez et al., 1999; Edwards & Rich-ardson, 2004). The biological association of zooplankton with Vib-rio spp. makes zooplankton ecology essential in understanding theeffects of climate change on vibrio populations. Rapid shifts in thebiogeographical distribution of zooplankton species were observedin various regions of the world in recent years (IPCC, 2007). Forexample, warm-water plankton distribution has moved polewardby 10� in the North Atlantic over the last four decades with theequivalent retreat of cold-water plankton species (Beaugrand &Reid, 2003). The warm-water zooplankton, Temora stylifera, wasabsent along the Northern Spanish coast in 1978 but was recordedas moving poleward since the mid 1990s (International Council forthe Exploration of the Sea, ICES Climate change: changing oceans(Richardson, 2008; http://www.ices.dk/iceswork/bulletin/ICE-S%20CLIM.pdf). Warm-water zooplankton occupying higher lati-tudes in response to global climate fluctuations may transportvibrio populations that subsequently colonize new regions and ex-tend their distribution range. This scenario implies a constant andslow displacement of native zooplankton with a more permanentestablishment of the vibrio population in contrast with transientinvasions of planktonic vibrios that would more likely disappearwith recession of these waters (Martinez-Urtaza et al., 2008). How-ever, invasive organisms may become endemic if ecological condi-tions are favorable for their establishment in new areas, as mayhave occurred with the arrival of pandemic O3:K6 populations inSouthern Chile (García et al., 2009; Fuenzalida et al., 2006). Thefundamentals behind the capacity of pathogenic vibrio populationsto survive in new geographical areas and to become endemic arecritical to understanding the epidemic potential of vibrio illnessesand in designing measures to control and prevent these diseases.

3. V. parahaemolyticus and oceanic anomalies: geographicexpansion of outbreaks in Peru and Alaska

3.1. Peru

In 1991, the seventh cholera pandemic emerged along the coastof Peru with dramatic consequences for a number of Latin Ameri-

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can countries (Tauxe, Mintz, & Quick, 1995). A new epidemic asso-ciated with V. parahaemolyticus emerged in Peru in 1997, wheninfections caused by the pandemic clone appeared along the entirecoast of the country (Martinez-Urtaza et al., 2008). Infections wererecorded in northern areas of the country in July and spread morethan 1500 km in 4 months, reaching the southern Peruvian borderin November, just before the onset of V. parahaemolyticus illnessesin the northern Chilean city of Antofagasta (Gonzalez-Escalonaet al., 2005).

Similar to the cholera epidemic, the routes of dissemination andorigins of the V. parahaemolyticus infections in Peru were unknown,and no consistent explanation could be provided for the arrival ofAsian endemic strains to the Pacific coast of South America. A ret-rospective investigation of the oceanographic conditions duringthe appearance of cholera and V. parahaemolyticus illnesses in Perurevealed that the emergence of cases was concurrent with the ar-rival of two episodes of El Niño to Peru (Martinez-Urtaza et al.,2008). El Niño is a complex phenomenon of oscillation of theocean–atmosphere system in the equatorial Pacific Ocean, which

Fig. 2. Progression of V. parahaemolyticus cases in Peru in concert with the arrival and socases recorded by the Peruvian National Institute of Health of Peru throughout 1997 and(B), and dates of the first cases of V. parahaemolyticus infections showing the southwardNiño waters was measured by deviation of the sea height from a climatologic annualwww.jason.oceanobs.com/).

severely impacts the weather around the globe. This phenomenonis also characterized by the zonal movement of warm and less sal-ine water from the western Pacific to the coasts of South America(Picaut, Ioualalen, Menkes, Delcroix, & McPhaden, 1996). This dis-rupts the ecological conditions of coastal areas and impacts biolog-ical systems.

Integration of oceanic data from satellite imagery with epidemi-ological and laboratory data provide an innovative perspective ofthe origins of the Asian strains in South America (Fig. 2). Infectionscaused by the pandemic clone emerged along the coasts of Peru in1997 and moved poleward in concert with the El Niño expansion(Martinez-Urtaza et al., 2008). This pattern of dissemination wassimilar to that observed during the onset of a cholera epidemicin 1991 (Seas et al., 2000). Results suggest that El Niño eventsmay be a mechanism for the dissemination of Asian vibrio strainsin South America, opening the possibility of a long-distance dis-persal of vibrio pathogens through marine currents. The arrival offoreign zooplankton, and the collapse of the native zooplanktonpopulations, concurred with these outbreaks (Chavez et al., 1999;

uthward advance of the El Niño waters during the 1997–1998 epidemic. Number of1998 (A), position of the warm El Niño water in May, October and December of 1997

progression along the coast of Peru during 1997 (C). The movement of the 1997 Elmean. We use the gridded sea height anomaly fields computed by AVISO (http://

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Gonzalez, Pages, Sobarzo, & Escribano, 2002; IMARPE, 1998; Ulloaet al., 2001). The arrival of invasive copepods associated with ElNiño was suggested as a potential source of pathogenic vibriosand origin of the vibrio epidemics in Peru (Martinez-Urtaza et al.,2008).

3.2. Alaska

A large outbreak of V. parahaemolyticus (62 reported illnesses)associated with the consumption of oysters was reported in Alaskain 2004 (McLaughlin & Martinek, 2004). Cases of gastroenteritis oc-curred during most of July and were primarily associated with V.parahaemolyticus strains of serotype O6:K18. This was the first doc-

Fig. 3. V. parahaemolyticus cases in Alaska during the 2004 outbreak in relation to the aTemperature (SST) illustrate the poleward displacement of warm waters along the Pacificthe anomaly observed in 2004 when warm waters crossed the boundary of 40� latitudethe emergence of V. parahaemolyticus infections. Daily maps of SST in 2003 and 2004 werand sponsored by the NASA Earth Science MEaSUREs DISCOVER Project.

umented outbreak of V. parahaemolyticus in Alaska, extending therange of dispersion of V. parahaemolyticus infections over 1000 km.

Cases of infection were concurrent with the arrival of extraordi-narily warm (>15 �C) seawater in oyster harvesting areas of PrinceWilliam Sound (McLaughlin et al., 2005). A single case was re-ported the following year during similarly warm conditions. Nocases have been reported since 2005 due to the return of coolersummers typical of Alaska (personal communication, Sara Longan,Alaska Dept. Environmental Conservation, 2009). However,changes in harvest practices such as lowering oyster cages belowthe thermocline to waters <10 �C may also account for the lack ofrecent illnesses.

A retrospective study of oceanographic conditions before the on-set of infections in the Prince William Sound area was conducted

rrival and incursion of warm waters into Alaska coastal areas. Maps of Sea Surfacecoast of North America in 2003 and 2004, characteristic of the summer months, and

into the Prince William Sound area. This anomaly arrived in Alaska simultaneous toe obtained from the AMSRE-E OI SST product produced by Remote Sensing Systems

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with the aid of remote sensing data and provided insights into thepossible routes of V. parahaemolyticus dissemination in Alaska.Warm waters flowing poleward along the Pacific coast arrived alongthe Alaska coast a few days prior to the first reported cases of infec-tion (Fig. 3). The northward displacement of warm waters along thePacific coast is characteristically observed during the summer in thisarea, but rarely extends beyond latitude 40�N. However, during theoceanic anomaly of 2004, warm water reached the Prince WilliamSound and persisted throughout the V. parahaemolyticus outbreakand beyond. Satellite imagery identified the Pacific coast of the con-tinental US as the most probable origin of the warm waters. Strainsrecovered from the Alaska outbreak were genetically indistinguish-able from V. parahaemolyticus stains isolated in previous outbreaksand oysters harvested in the Puget Sound and nearby areas. Theavailability of additional information on primary production andzooplankton abundance and composition would permit a more com-prehensive ecological interpretation of the oceanic circumstancesassociated with this outbreak.

Another unexpected finding from the Alaska V. parahaemolyti-cus outbreak was the high attack rate associated with the relativelylow numbers of pathogenic V. parahaemolyticus likely ingested(McLaughlin et al., 2005). An attack rate of approximately 30% onthree consecutive cruises was reported for cruise ship passengersconsuming one to six oysters. On a fourth cruise, after the outbreakwas recognized and raw oysters were not being served to passen-gers, samples from the same farm were tested for V. parahaemolyt-icus. The V. parahaemolyticus levels in duplicate samples were 2.1and 3.5 MPN/g. The ten isolates examined tested positive for thetdh gene; five isolates matched the serotype (O6:K18) and pulsetype of the outbreak strain. It is uncertain whether similar levelsoccurred in the oysters that were linked to illnesses from the threeprevious cruises but environmental conditions were similar andthe farmer indicated similar handling procedures. The observationof 100% frequency of pathogenic V. parahaemolyticus (tdh+) was ex-tremely unusual as only �3% of V. parahaemolyticus isolates fromUS Pacific Coast oysters normally contain tdh. Additionally, similarlevels of total and pathogenic V. parahaemolyticus were reported in29 oyster samples collected from the implicated farm and otherlocations in the Prince William Sound after harvesting from the en-tire Sound was closed. While the frequency of pathogenic V. para-haemolyticus was high, the ingested dose was relatively low due tothe low V. parahaemolyticus densities and numbers of oystersconsumed.

To put these observations in perspective, the probable dose–re-sponse based on the Alaska outbreak data was compared to thedose–response determined in human feeding studies and thedose–response inferred to correspond to exposure via the oyster

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Fig. 4. Estimated dose–response for V. parahaemolyticus in raw oysters based on2004 Alaska outbreak.

food matrix, as used in the FDA-VPRA (Anonymous, 2005). Theestimated dose–response relationships are shown in Fig. 4. In theoutbreak, the dose corresponding to the 30% attack rate in Alaskawas between 103 and 104 pathogenic V. parahaemolyticus cells,which is significantly lower than that (107–108 cells) estimatedin the FDA-VPRA. It is not known whether this apparent 4-log dif-ference in virulence for the Alaska outbreak strain is due to differ-ences in virulence genes or gene expression related toenvironmental factors encountered in Prince William Sound.

Strains indistinguishable from the Alaska outbreak strain werefound in the Puget Sound, WA, but were associated with only afew sporadic cases of V. parahaemolyticus infections. Assuming thatthe outbreak strain was transported from the Puget Sound areawith the large mass of warmer water, the cells could have inter-acted with various flora and fauna over a 1000 km journey, whichcould have affected gene expression or transfer and impacted vir-ulence. Interestingly, Prince William Sound has the highest densityof sea otters in the world, and V. parahaemolyticus was isolated inmoribund and dead in sea otters, both wild and captive during thissame period. Sea otters feed heavily on bivalve mollusks in PrinceWilliam Sound and their intestinal tracts provide a warm andnutrient rich environment for V. parahaemolyticus proliferation.Unpublished data from a 2005 ecological study in Prince WilliamSound indicated that rectal swabs from three of seven sea otterswere positive for pathogenic V. parahaemolyticus. Possibly, V. para-haemolyticus excreted by sea otters may have adapted to mamma-lian gastrointestinal conditions becoming more virulent in othermammals, including humans. This phenomenon has been notedfor V. cholerae after rabbit gastrointestinal tract passage (Dutta,Panse, & Jhala, 1963). There are likely many other possibilities forchanges in virulence associated with climate change.

4. Vibrio vulnificus: seasonal expansion in Gulf of Mexico

Recent CDC data (Fig. 1) indicates an increase in vibrio infec-tions since 2000, which are among the warmest years on recordin the USA. These observations suggest that climate change inthe US may expand the V. vulnificus illness risk season. In particu-lar, the frequency and severity of extremes in temperature and pre-cipitation are increasing in the southeastern US due to climateanomalies and increasing ocean temperatures in the western Paci-fic (Lau, Leetmaa, & Nath, 2008; Ning, Turner, Doyle, & Abdollahi,2003; Twilley et al., 2001). These changes predominantly occurduring the cold season with effects that vary according to thewarm and cold phases of El Niño Southern Oscillation (ENSO)activity. During the warm (El Niño) phase of the ENSO cycle, theGulf Coast typically experiences colder than normal temperaturesand above-average precipitation. Conditions are reversed duringthe cold (La Niña) phase of ENSO, with higher than normal temper-atures and below-average precipitation. The intensity of the effectsof the warm and cold phases of ENSO, relative to nominal or base-line conditions, is strongest in the winter, although timing andduration of the warm- and cold-phase events are variable (Higgins,Leetmaa, & Kousky, 2002).

Fluctuations in regional climate due to ENSO appear to correlatewith changes in vibrio densities in oysters. From June, 1998,through July, 1999, FDA conducted a nationwide market surveyof live oysters intended for raw consumption (Cook et al., 2002).The levels of V. parahaemolyticus and V. vulnificus were approxi-mately one log higher in oysters harvested from coastal areas ofthe Gulf of Mexico during the autumn of 1998 than the nominalmean levels predicted by subsequent risk assessments for V. para-haemolyticus and V. vulnificus (Anonymous, 2005; FAO/WHO,2005). The nominal levels were based on aggregate (average) waterand air temperature data from 1987 through 1997. A retrospective

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7002-89917991-98917991-9891 1998-2007

NovemberApril

Fig. 6. Incidence of oyster-associated V. vulnificus cases per metric ton of oystermeats harvested and the frequency of occasions when maximum daily watertemperatures exceeded 20 �C during the periods April and November, 1989–1997and 1998–2007 (personal communication, Marc Glatzer, FDA; personal communi-cation, National Marine Fisheries Service, Fisheries Statistics Division, Silver Spring,MD; National Buoy Data Center, Stennis Space Center, MS).

J. Martinez-Urtaza et al. / Food Research International 43 (2010) 1780–1790 1787

examination of temperature data indicated that the coastal seawa-ter temperatures were �3–4 �C warmer in the autumn of 1998than the corresponding mean temperatures used in the risk assess-ments. The warmer temperatures in the autumn of 1998 were dueto a strong la Niña that persisted through the winter. Based on thisobservation, 1998 levels were predicted using the V. vulnificus riskassessment model and the autumn temperatures observed thatyear (FAO/WHO, 2005). The predicted levels were shifted upwardfrom the nominal levels and were in close agreement with thoseobserved in the market study (Fig. 5). Additionally, a review of dataon oyster-related V. vulnificus illnesses maintained by FDA and CDCindicated 11 cases in November, 1998. This was the most ever re-corded for any month of the year to that point, and has been ex-ceeded only once since then (personal communication, MarcGlatzer, FDA). One reason for the high levels of V. parahaemolyticusand V. vulnificus observed in the autumn of 1998 was that thetime–temperature requirements for November harvest were lessstringent than for the summer months (14 vs. 10 h from harvestto refrigeration). November is also one of the months with highestoyster consumption, which increases exposure (FAO/WHO, 2005).

V. vulnificus levels in oysters at the point of consumption, andthe corresponding consumer risk, are strongly influenced by cli-mate, especially water and air temperatures. While the most com-pelling and best documented example is the 1998 la Niña climateanomaly in the Gulf of Mexico (Bell et al., 1999; FAO/WHO, 2005),recent data indicate a seasonal expansion into April and November.The lack of evidence of geographical expansion, as observed with V.parahaemolyticus, may be due to the low production of oysters dur-ing the summer months along the mid-Atlantic coast of the US.There are active oyster restoration programs in the mid-Atlanticstates. If these programs are successful and summer productionof raw oysters increases, the role of climate change and climateanomalies may become a more visible public health issue for con-sumers of oysters from these areas.

We re-examined monthly illness data, oyster landings, andclimate data for two periods (1989–1997 and 1998–2007) to de-velop a clearer understanding of how climate may have extendedthe V. vulnificus risk season since 1997. In Fig. 6 we present resultsfor April and November comparing the percentage of days withharvest water temperature >20 �C and the number of V. vulnificuscases per metric ton of oyster meat harvested. The number of daysin April with a water temperature >20 �C increased by an averageof 5 days in the period after 1997; reported V. vulnificus illnessesincreased more than threefold. In November the increase in thenumber of days with a water temperature >20 �C after 1998 was

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Fig. 5. Seasonal levels of V. vulnificus in US Gulf Coast oysters determined during1998–1999 market survey in comparison to model-predicted levels based onaverage temperatures (1987–1997). Anomalously high temperatures occurred inthe autumn of 1998 and winter of 1999 (FAO, Microbiological Risk AssessmentSeries No. 8, Rome, Italy, 2005).

even greater than the increase in April, but with less than a two-fold increase in V. vulnificus illnesses. Since 1997, the number ofreported cases of V. vulnificus in April and November have beensimilar to those in the traditional V. vulnificus risk season of Maythrough October. The extent to which expansion of the vibrio riskseason has contributed to an increase in foodborne illnesses asso-ciated with Vibrio spp. in the US will require further study.

5. Mitigating elevated risk during climate anomalies

While the magnitude and consequences of climate change areuncertain over the long-term, it is certain that climate anomalieswill continue to occur. To mitigate the public health impact ofgreater vibrio abundance and risk during these episodes, adjust-ments in industry practices and regulatory policy should be con-sidered, especially for seafood that is consumed raw, such asbivalve mollusks. Options may include more stringent post-harvesttime–temperature controls in response to expansion of seasonal orgeographical ranges. In the 2004 Alaska V. parahaemolyticus out-break, levels at harvest were sufficient for a high attack rate irre-spective of post-harvest controls. In 2005, the oyster industry inPrince William Sound adopted new practices to lower oyster rear-ing cages 15–30 m to colder waters (<10 �C) below the thermo-cline. A 2005 investigation indicated that V. parahaemolyticuslevels were approximately one log lower in oysters held one monthbelow the thermocline than in oysters in the warmer surfacewaters (unpublished FDA data). Although water temperaturesand V. parahaemolyticus levels in oysters in Prince William Soundduring the summer of 2005 were similar to those in 2004, only asingle V. parahaemolyticus case was reported in 2005 (vs. 62 in2004) (personal communication, Sara Longan, Alaska Departmentof Environmental Conservation).

In the US, post-harvest processing of raw oysters is used to re-duce the risk of V. parahaemolyticus and V. vulnificus illnesses. Post-harvest processes include mild heat, high hydrostatic pressure, andfreezing, which greatly reduce the levels of these pathogens whilegenerally retaining raw sensory characteristics. Irradiation was re-cently approved as a post-harvest process and, while levels of vib-rios are greatly reduced, the oysters remain alive for up to a weekafter treatment (personal communication, Victor Garrido, Univer-sity Florida, 2009). Another mitigation approach is to relay oystersto off-shore sites of high salinity waters. One study demonstratedthat V. vulnificus levels could be reduced to <3 MPN/g within14–17 days in waters with salinity >32 ppt (Motes & DePaola,

1788 J. Martinez-Urtaza et al. / Food Research International 43 (2010) 1780–1790

1996). More stringent controls could also include seasonal closuresor requirements to cook or process.

Further development of risk models for V. parahaemolyticus andV. vulnificus may also help elucidate the risks resulting from cli-mate change and temperature anomalies. Current models arebased almost entirely on water temperature, which explain onlyabout half of the inter-annual variation in levels of these pathogens(Anonymous, 2005; FAO/WHO, 2005). These risk models are beingintegrated with satellite imagery of sea surface temperature toprovide near real-time risk assessment for V. parahaemolyticus lev-els (Phillips, DePaola, Bowers, Ladner, & Grimes, 2007). A web siteis under development to use this approach to estimate levels of V.parahaemolyticus and V. vulnificus at harvest and consumption aswell as risk under various post-harvest management practices(personal communication, Jay Grimes, University of Southern Mis-sissippi). Other parameters such as salinity, turbidity, and chloro-phyll are impacted by climate events and have been associatedwith vibrio levels (Zimmerman et al., 2007). These parameterscan also be monitored remotely by satellite imagery. Refining riskmodels to include effects of additional parameters will facilitatemore accurate predictions which, when coupled with satelliteimagery data, could provide a useful tool to guide regulators andindustry for timely implementation of controls proportional tothe ever-changing risk due to climate variations.

6. Conclusions

This review demonstrates the potential utility of time lapse sa-tellite imagery for forecasting movement of warm water massesand the associated vibrio risk. Vibrios are among the most diverseand adaptable bacteria in nature. These traits coupled with theirshort generation times allow them to respond rapidly to changingconditions and multiply to levels hazardous to human health. Ourresults demonstrate that such change can occur over relativelyshort periods of time in areas and during seasons rarely or neverassociated with vibrio illnesses. While this review focused on tem-perature anomalies, many experts also expect precipitation ex-tremes to become more widespread and frequent as climatechanges. The major Vibrio spp. exhibit different optimal salinityranges and the risk is likely to shift upstream during droughtsand offshore during periods of high precipitation. Similarly, sea-food production areas that have traditionally been associated withillnesses from one Vibrio spp. may suddenly experience illnessesand even outbreaks due to different Vibrio spp. It is critical thatpublic health systems develop the capacity to recognize the signalsof approaching hazards and respond with appropriate control mea-sures in time to mitigate risk. Public health would benefit from thedevelopment of a system that integrates ocean observing data,environmental monitoring of vibrio levels and epidemiologicaldata as they are collected instead of relying on retrospective stud-ies after outbreaks have occurred. The output of such a systemcould also be valuable in improving the accuracy of risk assess-ment models, especially in linking exposure to illnesses. The wide-spread application of these technologies into an integrated systemhas great potential to improve seafood safety even under theworst-case scenarios of climate change.

References

Alam, M. J., Miyoshi, S., & Shinoda, S. (2003). Studies on pathogenic Vibrioparahaemolyticus during a warm weather season in the Seto Inland Sea, Japan.Environmental Microbiology, 5(8), 706–710.

Amako, K., Shimodori, S., Imoto, T., Miake, S., & Umeda, A. (1987). Effects of chitinand its soluble derivatives on survival of Vibrio cholerae O1 at low temperature.Applied Environmental and Microbiology, 53(3), 603–605.

Andersen, H. K. (1991). Vibrio vulnificus. Ugeskr Laeger, 153, 2361–2362.Anonymous (1999). Vibrio parahaemolyticus, Japan 1996–1998. Infectious Agents

Surveillance Report (IASR), 20(7), 1–2.

Anonymous (2005). Quantitative risk assessment on the public health impact ofpathogenic Vibrio parahaemolyticus in raw oysters. Washington, DC: US Food andDrug Administration.

Ansaruzzaman, M., Lucas, M., Deen, J. L., Bhuiyan, N. A., Wang, X. Y., Safa, A., et al.(2005). Pandemic serovars (O3:K6 and O4:K68) of Vibrio parahaemolyticusassociated with diarrhea in Mozambique: Spread of the pandemic into theAfrican continent. Journal Clinical Microbiology, 43(6), 2559–2562.

Baker-Austin, C., Stockley, L., Rangdale, R., & Martinez-Urtaza, J. (2010).Environmental occurrence and clinical impact of Vibrio vulnificus and Vibrioparahaemolyticus: A European perspective. Environmental Microbiology Reports,2(1), 7–18.

Barker, W. H. Jr., (1974). Vibrio parahaemolyticus outbreak in the United States:1969–1972. In T. Fujino, G. Sakaguchi, R. Sakazaki, & Y. Takeda (Eds.),International symposium on Vibrio parahaemolyticus (pp. 47–52). Tokyo, Japan:Saikon Publishing Co., Ltd..

Barker, W. H., Weaver, R. E., Morris, C. K., & Martin, W. T. (1975). Epidemiology ofVibrio parahaemolyticus infection in humans. In D. Schlcssinger (Ed.),Microbiology – 1974 (pp. p. 257). Washington, DC: American Society forMicrobiology.

Bell, G. D., Halpert, M. S., Ropelewski, C. F., Kousky, V. E., Douglas, A. V., Schnell, R. C.,et al. (1999). Climate assessment for 1998. Bulletin of the AmericanMeteorological Society, 80(5), S1–S48.

Beaugrand, G., & Reid, P. C. (2003). Long-term changes in phytoplankton,zooplankton and salmon related to climate. Global Change Biology, 9, 801–817.

Bisharat, N., Cohen, D. I., Harding, R. M., Falush, D., Crook, D. W., Peto, T., et al.(2005). Hybrid Vibrio vulnificus. Emerging Infectious Diseases, 11(1), 30–35.

Bisharat, N., & Raz, R. (1996). Vibrio infection in Israel due to changes in fishmarketing. Lancet, 348, 1585–1586.

Centers for Disease Control and Prevention (CDC) (1998). Outbreak of Vibrioparahaemolyticus infections associated with eating raw oysters–PacificNorthwest, 1997. Morbidity and Mortality Weekly Reports, 47(22), 457–462.

Center for Disease Control and Prevention (CDC) (2009). Preliminary FoodNet dataon the incidence of infection with pathogens transmitted commonly throughfood – 10 states, 2008. Morbidity and Mortality Weekly Reports, 58(22), 333–337.

Chavez, F. P., Strutton, P. G., Friederich, C. E., Feely, R. A., Feldman, G. C., Foley, D. C.,et al. (1999). Biological and chemical response of the equatorial Pacific Ocean tothe 1997–98 El Nino. Science, 286, 2126–2131.

Chowdhury, N. R., Chakraborty, S., Ramamurthy, T., Nishibuchi, M., Yamasaki, S.,Takeda, Y., et al. (2000a). Molecular evidence of clonal Vibrio parahaemolyticuspandemic strains. Emerging Infectious Diseases, 6, 631–636.

Chowdhury, N. R., Chakraborty, S., Eampokalap, B., Chaicumpa, W., Chongsa-Nguan,M., Moolasart, P., et al. (2000b). Clonal dissemination of Vibrio parahaemolyticusdisplaying similar DNA fingerprint but belonging to two different serovars(O3:K6 and O4:K68) in Thailand and India. Epidemiology Infectious, 125, 17–25.

Chuang, Y. C., Yuan, C. Y., Liu, C. Y., Lan, C. K., & Huang, A. H. (1992). Vibrio vulnificusinfection in Taiwan: Report of 28 cases and review of clinical manifestationsand treatment. Clinical Infectious Diseases, 15, 271–276.

Cook, D. W., O’Leary, P., Hunsucker, J. C., Sloan, E. M., Bowers, J. C., Blodgett, R. J.,et al. (2002). Vibrio vulnificus and Vibrio parahaemolyticus in U.S. retail shelloyster: A national survey from June 1998 to July 1999. Journal of Food Protection,65, 79–87.

Dadisman, T. A., Nelson, R., Molenda, J. R., & Carber, H. J. (1972). Vibrioparahaemolyticus gastroenteritis in Maryland. I. Clinical and epidemiologicaspects. American Journal of Epidemiology, 96(6), 414–426.

Daniels, N. A., Ray, B., Easton, A., Marano, N., Kahn, E., McShan, A. L., et al. (2000a).Emergence of a new Vibrio parahaemolyticus serotype in raw oysters: Aprevention quandary. JAMA, 284(12), 1541–1545.

Daniels, N. A., MacKinnon, L., Bishop, R., Altekruse, S., Ray, B., Hammond, R. M., et al.(2000b). Vibrio parahaemolyticus infections in the United States, 1973–1998.Journal Infectious Diseases, 181(5), 1661–1666.

Dawson, M. P., Humphrey, B. A., & Marshall, K. C. (1981). Adhesion: A tactic in thesurvival strategy of a marine Vibrio during starvation. Current Microbiology, 6,195–199.

DePaola, A., Capers, G. M., Motes, M. L., Olsvik, O., Fields, P. I., Wells, J., et al. (1992).Isolation of Latin American epidemic strain of Vibrio cholerae O1 from US GulfCoast. Lancet, 339, 624.

DePaola, A., Kaysner, C. A., Bowers, J. C., & Cook, D. W. (2000). Environmentalinvestigations of Vibrio parahaemolyticus in oysters following outbreaks inWashington, Texas, and New York (1997, 1998). Applied and EnvironmentalMicrobiology, 66, 4649–4654.

Dumontet, S., Krovacek, K., Baloda, S. B., Grottoli, R., Pasquale, V., & Vanucci, S.(1996). Ecological relationship between Aeromonas and Vibrio spp. andplanktonic copepods in the coastal marine environment in southern Italy.Comparative Immunology, Microbiology & Infectious Diseases, 19(3), 245–254.

Dutta, N. K., Panse, M. V., & Jhala, H. I. (1963). Choleragenic property of certainstrains of El Tor, nonagglutinable, and water vibrios confirmed experimentally.British Medical Journal, 1, 1200–1203.

Edwards, M., & Richardson, A. J. (2004). Impact of climate change on marine pelagicphenology and trophic mismatch. Nature, 430, 881–884.

FAO/WHO. (2005). Risk assessment of Vibrio vulnificus in raw oysters: Interpretativesummary and technical report. Microbiological Risk Assessment Series No. 8.Rome, Italy: FAO.

FAO/WHO (in press). Risk assessment of Vibrio parahaemolyticus in seafood:Interpretative summary and technical report. Microbiological Risk AssessmentSeries 16. Rome, Italy: FAO.

J. Martinez-Urtaza et al. / Food Research International 43 (2010) 1780–1790 1789

Fishbein, M., Wentz, B., Landry, W. L., & MacEachern, B. (1974). Vibrioparahaemolyticus isolates in the U.S.: 1969–1972. In T. Fujino, G. Sakaguchi,R. Sakazaki, & Y. Takeda (Eds.), International symposium on Vibrioparahaemolyticus (pp. 53–58). Tokyo, Japan: Saikon Publishing Co., Ltd..

Frank, C., Littman, M., Alpers, K., & Hallauer, J. (2006). Vibrio vulnificus woundinfections after contact with the Baltic Sea, Germany. European CommunicableDisease Bulletin, 11(8).

Fuenzalida, L., Hernández, C., Toro, J., Rioseco, M. L., Romero, J., & Espejo, R. T. (2006).Vibrio parahaemolyticus in shellfish and clinical samples during two largeepidemics of diarrhoea in southern Chile. Environmental Microbiology, 8,675–683.

Fujino, T. (1974). Discovery of Vibrio parahaemolyticus. In T. Fujino, G. Sakaguchi, R.Sakazaki, & Y. Takeda (Eds.), International symposium on Vibrio parahaemolyticus(pp. 1–5). Tokyo, Japan: Saikon Publishing Co., Ltd..

Fujino, T., Okuno, D., Nakada, A., Aoyama, A., Fukay, K., Mukay, T., et al. (1953). Onthe bacteriological examination of shirasu food poisoning. Medical Journal ofOsaka University, 4, 299–304.

García, K., Torres, R., Uribe, P., Hernández, C., Rioseco, M. L., Romero, J., et al. (2009).Dynamics of clinical and environmental Vibrio parahaemolyticus strains duringseafood-related summer diarrhea outbreaks in southern Chile. Applied andEnvironmental Microbiology, 75(23), 7482–7487.

Gonzalez-Escalona, N., Cachicas, V., Acevedo, C., Rioseco, M. L., Vergara, J. A., Cabello,F., et al. (2005). Vibrio parahaemolyticus diarrhea, Chile, 1998 and 2004.Emerging Infectious Diseases, 11(1), 129–131.

Gonzalez-Escalona, N., Martinez-Urtaza, J., Romero, J., Espejo, R. T., Jaykus, L. A., &DePaola, A. (2008). Determination of molecular phylogenetics of Vibrioparahaemolyticus strains by multilocus sequence typing. Journal ofBacteriology, 190(8), 2831–2840.

Gonzalez, H. E., Pages, F., Sobarzo, M., & Escribano, R. (2002). Effects of the 1997–98El Niño on the oceanographic conditions and zooplankton community structurein the coastal upwelling system off northern Chile. Investigaciones Marinas, 30,112–114.

Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S., et al.(2002). Climate warming and disease risks for terrestrial and marine biota.Science, 296, 2158–2162.

Higgins, R. W., Leetmaa, A., & Kousky, V. E. (2002). Relationships between climatevariability and winter temperature extremes in the United States. Journal ofClimate, 15, 1555–1572.

Høi, L., Larsen, J. L., Dalsgaard, I., & Dalsgaard, A. (1998). Occurrence of Vibriovulnificus biotypes in Danish marine environments. Applied Environmental andMicrobiology, 64, 7–13.

Hugh, R., & Sakauki, R. (1975). Minutes of the meeting of the subcommittee on thetaxonomy of Vibrios. International Journal of Systematic Bacteriology, 25, 389.

Huq, A., Small, E. B., West, P. A., Huq, M. I., Rahman, R., & Colwell, R. R. (1983).Ecological relationships between Vibrio cholerae and planktonic crustaceancopepods. Applied Environmental and Microbiology, 45(1), 275–283.

Instituto del Mar de Peru (IMARPE) (1998). Informe 130. Crucero de evaluaciónhidroacustica de recursos pelágicos BIC Humboldt 9709-10 entre Matarani yPaita. Callao, Peru.

IPCC (2007). In M. L. Parry, O. F. Canziani, J. P. Palutikof, P. J. van der Linden, & C. E.Hanson (Eds.), Climate change 2007: Impacts, adaptation and vulnerability.Contribution of working group II to the fourth assessment report of theintergovernmental panel on climate change (pp. 976). Cambridge, UK:Cambridge University Press.

Johnson, C. N., Flowers, A. R., Young, V. C., Gonzalez-Escalona, N., DePaola, A., Noriea,N. F., et al. (2008). Genetic relatedness among tdh+ and trh+ Vibrioparahaemolyticus cultured from Gulf of Mexico oysters (Crassostrea virginica)and surrounding water and sediment. Microbiology Ecology, 57, 437–443.

Joseph, S. W., Colwell, R. R., & Kaper, J. B. (1982). Vibrio parahaemolyticus and relatedhalophilic Vibrios. Critical Reviews in Microbiology, 10, 77–124.

Kaneko, T., & Colwell, R. R. (1975). Ecology of Vibrio parahaemolyticus in ChesapeakeBay. Applied and Environmental Microbiology, 30, 251–257.

Kaneko, T., & Colwell, R. R. (1978). The annual cycle of Vibrio parahaemolyticus inChesapeake Bay. Microbial Ecology, 4, 135–155.

Kaspar, C. W., & Tamplin, M. L. (1993). Effects of temperature and salinity on thesurvival of Vibrio vulnificus in seawater and shellfish. Applied and EnvironmentalMicrobiology, 59, 2425–2429.

Lau, N. C., Leetmaa, A., & Nath, M. J. (2008). Interactions between the responses ofNorth American climate to El Nino–La Nina and to the secular warming trend inthe Indian–Western Pacific oceans. Journal of Climate, 21, 476–494.

Lin, M., & Schwarz, J. R. (2003). Seasonal shifts in population structure of Vibriovulnificus in an estuarine environment as revealed by partial 16S ribosomal RNAsequencing. FEMS Microbiological Ecology, 45, 23–27.

Lipp, E. K., Huq, A., & Colwell, R. R. (2002). Effects of global climate on infectiousdisease: The cholera model. Clinical Microbiology Reviews, 15, 757–770.

Martinez-Urtaza, J. M., Simental, L., Velasco, D., DePaola, A., Ishibashi, M.,Nakaguchi, Y., et al. (2005). Pandemic Vibrio parahaemolyticus O3:K6, Europe.Emerging Infectious Diseases, 8, 1319–1320.

Martinez-Urtaza, J., Huapaya, B., Gavilan, R. G., Blanco-Abad, V., Ansede-Bermejo, J.,Cadarso-Suarez, C., et al. (2008). Emergence of Asiatic Vibrio diseases in SouthAmerica in phase with El Niño. Epidemiology, 19, 829–837.

Martinez-Urtaza, J., Lozano-Leon, A., DePaola, A., Ishibashi, M., Shimada, K.,Nishibuchi, M., et al. (2004). Characterization of pathogenic Vibrioparahaemolyticus isolates from clinical source in Spain and comparison withAsian and North American pandemic isolates. Journal Clinical Microbiology, 42,4672–4678.

Matsuda, F., Ishimura, S., Wagatsuma, Y., Higashi, T., Hayashi, T., Faruque, A. S. G.,et al. (2008). Prediction of epidemic cholera due to Vibrio cholerae O1 in childrenyounger than 10 years using climate data in Bangladesh. Epidemiology andInfection, 136, 73–79.

Matsumoto, C., Okuda, J., Ishibashi, M., Iwanaga, M., Garg, P., Rammamurthy, T.,et al. (2000). Pandemic spread of an O3:K6 clone of Vibrio parahaemolyticusand emergence of related strains evidenced by arbitrarily primed PCR and toxRSsequence analyses. Journal Clinical Microbiology, 38, 578–585.

McCarthy, S. A., & Khambaty, F. M. (1994). International dissemination of epidemicVibrio cholerae by cargo ship ballast and other nonpotable waters. AppliedEnvironmental and Microbiology, 60, 2597–2601.

McLaughlin, J. B., DePaola, A., Bopp, C. A., Martinek, K. A., Napolilli, N. P., Allison, C.,et al. (2005). Outbreak of Vibrio parahaemolyticus gastroenteritis associatedwith Alaskan oysters. New England Journal of Medicine, 353, 1463–1470.

McLaughlin, J., & Martinek, K. (2004). Outbreak of Vibrio parahaemolyticusgastroenteritis associated with consumption of Alaskan Oysters – part II.State of Alaska Epidemiology Bulletin. <http://www.epi.alaska.gov/bulletins/docs/b2004_24.pdf>.

Mead, P. S., Slutsker, L., Dietz, V., McGaig, L. F., Bresee, J. S., Shapiro, C., et al. (1999).Food-related illness and death in the United States. Emerging Infectious Diseases,5, 607–625.

Melhus, A., Holmdahl, T., & Tjernberg, I. (1995). First documented case ofbacteremia with Vibrio vulnificus in Sweden. Scandinavian Journal of InfectiousDiseases, 27, 81–82.

Miles, D. W., Ross, T., Olley, J., & McMeekin, T. A. (1997). Development andevaluation of a predictive model for the effect of temperature and water activityon the growth rate of Vibrio parahaemolyticus. International Journal of FoodMicrobiology, 38, 133–142.

Motes, M. L., & DePaola, A. (1996). Offshore suspension relaying to reduce levels ofVibrio vulnificus in oysters (Crassostrea virginica). Applied and EnvironmentalMicrobiology, 62, 3875–3877.

Motes, M. L., DePaola, A., Cook, D. W., Veazey, J. E., Hunsucker, J. C., Garthright, W. E.,et al. (1998). Influence of water temperature and salinity on Vibrio vulnificus innorthern Gulf and Atlantic Coast oysters (Crassostrea virginica). AppliedEnvironmental and Microbiology, 64, 1459–1465.

Nair, G. B., Ramamurthy, T., Bhattacharya, S. K., Dutta, B., Takeda, Y., & Sack, D. A.(2007). Global dissemination of Vibrio parahaemolyticus serotype O3:K6 and itsserovariants. Clinical Microbiology Reviews, 20(1), 39–48.

Niimi, A. J. (2004). Role of container vessels in the introduction of exotic species.Marine Pollution Bulletin, 49, 778–782.

Nilsson, W. B., Paranjpye, R. N., DePaola, A., & Strom, M. S. (2003). Sequencepolymorphism of the 16S rRNA gene of Vibrio vulnificus is a possible indicator ofstrain virulence. Journal Clinical Microbiology, 41, 442–446.

Ning, Z. H., Turner, R. E., Doyle, T., & Abdollahi, K. K. (2003). Integrated assessment ofthe climate change impacts on the Gulf Coast Region (pp. 79–82). Gulf CoastClimate Change Assessment Council (GCRCC) and Louisiana State University(LSU) Graphic Services.

Nishibuchi, M., & DePaola, A. (2005). In M. B. A. K. S. J. L. Fratamico (Ed.), Foodbornepathogens: Microbiology and molecular biology (pp. 251–271). Norfolk, UK:Caister Academic Press.

NOAA National Buoy Data Center. Stennis Space Center, MS. <http://www.nbdc.noaa.gov>.

NOAA National Marine Fisheries Service, Fisheries Statistics Division, Silver Spring,MD. <http://www.st.nmfs.noaa.gov/st1/commercial/index.html>.

Okuda, J., Ishibashi, M., Hayakawa, E., Nishino, T., Takeda, Y., Mukhopadhyay, A. K.,et al. (1997). Emergence of a unique O3:K6 clone of Vibrio parahaemolyticus inCalcutta, India, and isolation of strains from the same clonal group fromSoutheast Asian travelers arriving in Japan. Journal Clinical Microbiology, 35,3150–3155.

Ottaviani, D., Leoni, F., Rocchegiani, E., Santarelli, S., Canonico, C., Masini, L., et al.(2008). First clinical report of pandemic Vibrio parahaemolyticus O3:K6 infectionin Italy. Journal Clinical Microbiology, 46(6), 2144–2145.

Quilici, M. L., Robert-Pillot, A., Picart, J., & Fournier, J. M. (2005). Pandemic Vibrioparahaemolyticus O3:K6 spread, France. Emerging Infectious Diseases, 11,1148–1149.

Park, S. D., Shon, H. S., & Joh, N. J. (1991). Vibrio vulnificus septicemia in Korea:Clinical and epidemiologic findings in seventy patients. Journal of AmericanAcademy of Dermatology, 24, 397–403.

Paz, S., Bisharat, N., Paz, E., Kidar, O., & Cohen, D. (2007). Climate change and theemergence of Vibrio vulnificus disease in Israel. Environmental Research, 103,390–396.

Phillips, A. M. B., DePaola, A., Bowers, J. C., Ladner, S., & Grimes, D. J. (2007). Anevaluation of the use of remotely sensed parameters for prediction of theincidence and risk associated with Vibrio parahaemolyticus in Gulf Coast oysters(Crassostrea virginica). Journal of Food Protection, 70, 879–884.

Picaut, J., Ioualalen, M., Menkes, C., Delcroix, T., & McPhaden, M. J. (1996).Mechanism of the zonal displacements of the Pacific warm pool: Implicationsfor ENSO. Science, 274, 1486–1489.

Richardson, A. J. (2008). In hot water: Zooplankton and climate change. ICES Journalof Marine Science, 65, 279–295.

Rosche, T. M., Yano, Y., & Oliver, J. D. (2005). A rapid and simple PCR analysisindicates there are two subgroups of Vibrio vulnificus which correlate withclinical or environmental isolation. Microbiology and Immunology, 49, 381–389.

Rodo, X., Pascual, M., Fuchs, G., & Faruque, A. S. (2002). ENSO and cholera: Anonstationary link related to climate change? Proceedings of the NationalAcademy of Sciences USA, 99, 12901–12906.

1790 J. Martinez-Urtaza et al. / Food Research International 43 (2010) 1780–1790

Rodriguez-Castro, A., Ansede-Bermejo, J., Blanco-Abad, V., Varela-Pet, J., Garcia-Martinez, O., & Martinez-Urtaza, J. (2010). Prevalence and genetic diversity ofpathogenic populations of Vibrio parahaemolyticus in coastal waters of Galicia,Spain. Environmental Microbiology Reports, 2(1), 58–66.

Roig, F. J., Sanjuan, E., Llorens, A., & Amaro, C. (2010). PilF Polymorphism-based PCRto Distinguish Vibrio vulnificus strains potentially dangerous to public health.Applied and Environmental Microbiology, 76, 1328–1333.

Ruiz, G. M., Rawlings, T. K., Dobbs, F. C., Drake, L. A., Mullady, T., Huq, A., et al.(2000). Global spread of microorganisms by ships. Nature, 408, 49–50.

Shapiro, R. L., Altekruse, S., Hutwagner, S., Bishop, R., Hammond, R., Wilson, S., et al.(1998). The role of Gulf Coast oysters harvested in warmer months in Vibriovulnificus infections in the United States, 1988–1996. Journal Infectious Diseases,178, 752–759.

Seas, C., Miranda, J., Gil, A. I., Leon-Barua, R., Patz, J., Huq, A., et al. (2000). Newinsights on the emergence of cholera in Latin America during 1991: ThePeruvian experience. American Journal of Tropical Medicine and Hygiene, 62(4),513–517.

Strom, M. S., & Paranjpye, R. N. (2000). Epidemiology and pathogenesis of Vibriovulnificus. Microbes and Infection, 2, 177–188.

Tauxe, R. V., Mintz, E. D., & Quick, R. E. (1995). Epidemic cholera in the new world:Translating field epidemiology into new prevention strategies. EmergingInfectious Diseases, 1(4), 141–146.

Twilley, R., Barron, E. J., Gholtz, H. L., Harwell, M. A., Miller, R. L., Reed, D. J., et al.(2001). Confronting climate change in the Gulf Coast region. Union ofConcerned Scientists.

Ulloa, O., Escribano, N., Hormazabal, S., Quinones, R. A., Gonzalez, R. R., & Ramos, M.(2001). Evolution and biological effects of the 1997–98 El Nino in the upwellingecosystem off northern Chile. Geophysical Research Letter, 28, 1591–1594.

Vickery, M. C. L., Nilsson, W. B., Strom, M. S., Nordstrom, J. L., & DePaola, A. (2007). Areal-time PCR assay for the rapid determination of 16S rRNA genotype in Vibriovulnificus. Journal of Microbiological Methods, 68, 376–384.

Wong, H. C., Liu, S. H., Wang, T. K., Lee, C. L., Chiou, C. S., Liu, D. P., et al. (2000).Characteristics of Vibrio parahaemolyticus O3:K6 from Asia. AppliedEnvironmental and Microbiology, 66(9), 3981–3986.

Yu, P., Puhr, N., Bopp, C., Gerner-Smidt, P., & Painter, J. (2006). Vibrioparahaemolyticus hemolysins associated with decreased hospitalization fromshellfish-borne illness. In International Conference on Emerging InfectousDiseases.

Zimmerman, A. M., DePaola, A., Bowers, J. C., Krantz, J. A., Nordstrom, J. L., Johnson,C. N., et al. (2007). Variability of total and pathogenic Vibrio parahaemolyticusdensities in coastal Gulf of Mexico water and oysters (Crassostrea virginica).Applied and Environmental Microbiology, 73, 7589–7596.