summaries

Vibrio illness in Florida, 1998–2007

K. E. WEIS1,2*, R. M. HAMMOND2, R. HUTCHINSON2

AND C. G. M. BLACKMORE2

1 Council of State and Territorial Epidemiologists Applied Epidemiology Fellowship, Atlanta, GA, USA 2 Bureau of Environmental Public Health Medicine, Division of Environmental Health, Florida Department of Health, Tallahassee, FL, USA

(Accepted 18 May 2010; first published online 14 June 2010)

SUMMARY

This study characterized the current epidemiology of vibrio infections in Florida and examined

cases reported from 1998 to 2007. Logistic regression was used to determine risk of death. There

were 834 vibrio infections in 825 individuals (average annual incidence rate 4.8/1 000 000).

Common Vibrio species reported were Vibrio vulnificus (33%), V. parahaemolyticus (29%), and

V. alginolyticus (16%). Most exposures were attributed to wounds (42%), and the most common

clinical syndromes were wound infections (45%) and gastroenteritis (42%). Almost half of

individuals reported an underlying health condition. Risk of death was associated with any

underlying condition and increased with the number of conditions (P<0.0001). In Florida, incidence of vibriosis associated with raw oyster consumption has decreased while incidence

associated with wound infections has increased. Most prevention efforts to date have focused on

oyster consumption. New educational messages focusing on the risk of vibriosis from wound

infections should target high-risk populations.

Key words: Epidemiology, infectious disease, Vibrio vulnificus.

INTRODUCTION

Vibrio are Gram-negative, rod-shaped bacteria com-

monly found in warm coastal waters worldwide

[1, 2]. The Centers for Disease Control and Preven-

tion (CDC) estimates that Vibrio spp. cause over 8000

infections annually [3], and the incidence of vibriosis

has increased for all species since 1996 [4, 5], due in

part to better surveillance and reporting. In the USA,

most cases of vibriosis are reported from Gulf Coast

states, where vibrios are commonly found in their

natural habitat [6–8]. Infections are acquired by

consuming contaminated food or water or exposing

wounds and abrasions to marine environments [1, 2].

Cases typically occur in the warm summer months.

The more common species in the USA include

Vibrio vulnificus and V. parahaemolyticus. V. vulnifi-

cus is often associated with raw oyster consumption,

wound infections, and primary septicaemia [2].

V. parahaemolyticus is typically associated with gas-

troenteritis. Other common species include V. chol-

erae non-O1 (gastroenteritis) and V. alginolyticus

(wound infections) [1].

Vibriosis has the highest case-fatality rate (CFR)

of any enteric disease, mainly attributable to V. vul-

nificus, making this a very important public health

* Author for correspondence: K. E. Weis, Ph.D., MPH, Division of Environmental Health, Florida Department of Health, 4052 Bald Cypress Way, Bin A08, Tallahassee, FL 32399-1712, USA. (Email: [email protected])

Epidemiol. Infect. (2011), 139, 591–598. f Cambridge University Press 2010 doi:10.1017/S0950268810001354

concern despite the low incidence reported annually.

Based on FoodNet data from 2007, the incidence

of vibriosis was 0.2 cases/100 000 individuals, and

the CFR was 3.6% [9]. Incidence rates for other

common foodborne bacterial enteric diseases in the

USA are higher, although CFRs are much lower.

Based on these same data, rates for the most common

foodborne diseases are (incidence per 100000, case

fatality): Salmonella (14.9, 0.4%), Campylobacter

(12.8, 0.1%), Shigella (6.2, 0.1%), and Escherichia

coli O157:H7 (1.2, 0.2%) [9]. The highest overall

CFR for common foodborne enteric diseases (Sal-

monella, 0.4%) is almost 90% less than the overall

CFR for vibriosis (3.6%). Historically, Florida’s

incidence rate for vibriosis (0.4/100 000) is double

and the CFR (10.0%) is almost triple the national

rate [10].

Because of the high CFRs associated with V. vul-

nificus from consumption of raw oysters, there has

been a focus in the Gulf Coast states to increase

awareness in high-risk individuals, i.e. those with

underlying health conditions. As required by Florida

law since 1993, all food establishments selling raw

oysters must have a visible warning posted to make

the consumer aware of health risks associated with

their consumption. The Florida Department of

Health (FDOH) also regularly distributes educational

materials and presents data and risk reduction mess-

ages at venues statewide to a variety of audiences,

from health professionals to consumers. The goal

of these efforts is to increase awareness in high-risk

population groups and healthcare providers in order

to reduce incidence and case fatality. The vast

majority of the current messaging is related to the

risk of infection with V. vulnificus associated with

raw oyster consumption.

Vibriosis has been a notifiable disease in Florida

since 1981, in the Gulf Coast states since 1988, and

nationally since 2007. However, most states have been

voluntarily reporting since 1997. The epidemiology

of vibrio infections in Florida has been described

previously [10, 11]. From 1981 to 1993, the annual

incidence of vibriosis was 4.3/1 000 000 individuals.

The most common species reported during this period

were V. parahaemolyticus, V. vulnificus, and V. chol-

erae non-O1, respectively, with gastroenteritis being

the most commonly reported clinical syndrome, with

raw oyster consumption in the week prior to illness

reported in 45% of cases [10]. To determine whether

trends in vibriosis have changed with time, we

sought to describe the current epidemiology of vibrio

infections in Florida using data collected from 1998

to 2007.

METHODS

We examined cases of vibriosis reported to FDOH

with onset dates from 1998 to 2007. Data were col-

lected using the ‘Cholera and Other Vibrio Illness

Surveillance Report’ (CDC Form 52.79). The average

annual incidence rate for cases of vibriosis was cal-

culated using yearly population data from Florida

Charts [12] based on data from the Florida

Legislature, Office of Economic and Demographic

Research.

Descriptive analyses were performed for all re-

ported cases and examined by species. Medians

(ranges) were reported for non-normally distributed

continuous variables and frequencies (percentages)

for categorical variables. Kruskal–Wallis tests were

used to compare median values. Crude odds ratios

(ORs) and 95% confidence intervals (CIs) were re-

ported for bivariate analyses.

Logistic regression was used to assess the associ-

ation between various demographic and disease

characteristics and death from vibriosis. Predictor

variables that were considered in our analyses in-

cluded age, race/ethnicity, gender, clinical syndrome,

exposure, and presence and numbers of underlying

health conditions. The clinical syndrome field in-

cluded the following categories: septicaemia, the

presence of bacteria in the blood which can be

characterized by fever and chills to hypotension and

shock; wound infection, either from injuries sustained

in aquatic environments or from pre-existing wounds

and characterized by fever, cellulitis, and pain around

the site of infection; and gastroenteritis, an inflam-

mation of the stomach and intestines characterized

by diarrhoea and vomiting. Adjusted ORs and 95%

CIs were reported. Data were analysed using SAS

version 9.1 (SAS Institute, USA).

RESULTS

All species

There were 834 cases of vibriosis in 825 individuals

reported to FDOH from 1998 to 2007 (median 82.5/

year). The average annual incidence rate was 4.8

cases/1000 000 individuals. Infections were most

common in males (71.8%), whites (84.5%), and non-

Hispanics (84.9%). The median age of reported cases

592 K. E. Weis and others

was 50.0 years (range 0–96 years), with the majority

(74.9%) between the ages of 30 and 79 years. Seven

individuals were simultaneously infected with mul-

tiple species.

The most common species were V. vulnificus,

V. parahaemolyticus, and V. alginolyticus (Table 1).

The frequency of isolated species varied by year of

diagnosis (Fig. 1), with most cases occurring during

months when the water temperature and weather are

warmer (Fig. 2). Seasonality did not vary by species;

however, age at diagnosis was different (P<0.0001). The median age at diagnosis for cases of V. vulnificus

was 58 years, compared to 36 years in cases of V. al-

ginolyticus and 42 years for V. parahaemolyticus.

Wound-related symptoms were reported for 373

(44.7%) cases, followed by 350 (42.0%) with gastro-

enteritis, 45 (5.4%) with septicaemia, and 66 (7.9%)

with other reported symptoms (Fig. 3). There were

220 (26.4%) cases attributed to raw oyster consump-

tion, 313 (37.5%) to wound infections, 96 (11.5%) to

other seafood exposures, and 205 (24.6%) had no

reported exposure (Fig. 4).

Presence of any underlying health condition was

reported for 400 (48.5%) cases. Of these, 228 (57.0%)

had multiple conditions reported. Heart disease, al-

coholism, and liver disease were the most common

(Table 2).

There were 82 deaths reported, yielding a CFR of

9.9%. Age at onset, gender, presence of any underly-

ing health condition and total number of conditions,

mode of exposure, and clinical syndrome were sig-

nificantly associated with death. The odds of death

from vibriosis increased by 2.3% for every 1 year in-

crease in age (P=0.0001). Median age at diagnosis was higher (P=0.0001) for cases resulting in death

Table 1. Number of reported cases of vibriosis by

species, Florida, 1998–2007

Vibrio species No.* %

V. vulnificus 276 33.1

V. parahaemolyticus 245 29.4 V. alginolyticus 131 15.7 V. cholerae non-O1 55 6.6

V. fluvialis 46 5.5 V. hollisae 30 3.6 V. damsela 14 1.7

V. mimicus 13 1.6 Other vibrios 5 0.6 Species not identified 19 2.3

Total 834 100

* Seven individuals were infected with multiple Vibrio

species.

140 120 100 80 60 40 20 0

N um

be r

of c

as es

1998 1999 2000 2001 2002 2003 2004 2005 2006 2007

V. vulnificus V. parahaemolyticus V. alginolyticus Other vibrios

Fig. 1. Cases of vibriosis by species and year of diagnosis, Florida, 1998–2007.

160 140 120 100 80 60 40 20

0

N um

be r

of c

as es

Jan. Feb. Mar. Apr. May June July Aug. Sep. Oct. Nov. Dec.

V. vulnificus V. parahaemolyticus V. alginolyticus Other vibrios

Month of onset

Fig. 2. Seasonality of vibriosis by species, Florida, 1998–2007.

400

350

300

250

200

150

100

50

0

N um

be r

of c

as es

Wound Gastroenteritis Septicaemia Other

V. vulnificus V. parahaemolyticus V. alginolyticus Other vibrios

Fig. 3. Clinical syndromes of vibriosis by species, Florida, 1998–2007.

350

300

250

200

150

100

50

0 Wound Oyster Other seafood* Unknown

N um

be r

of c

as es

V. vulnificus V. parahaemolyticus V. alginolyticus Other vibrios

Fig. 4. Exposures associated with cases of vibriosis by species, Florida, 1988–2007. * Other seafood includes clams, mussels, shrimp, crab, fish, etc.

Vibriosis in Florida, 1998–2007 593

than those that did not. Being male was associated

with death (crude OR 2.92, 95% CI 1.48–5.78). Most

deaths (95.1%) had one or more underlying health

conditions reported. The odds of death in cases with

one or more underlying health conditions were 25.5

(95% CI 9.2–70.4) times that of cases with no under-

lying condition. The odds increased with the total

number of underlying health conditions (P<0.0001). Odds of death also differed by exposure and clinical

symptoms, with oyster consumption, gastroenteritis,

and septicaemia being significantly associated with

death (Table 3).

In multivariable analyses, the best predictive model

for death from vibriosis included total number of

underlying health conditions and exposure, based on

model fit statistics. The odds of death increased with

increasing number of underlying conditions: one (OR

9.8, 95% CI 2.7–35.6), two (OR 18.7, 95% CI

5.3–66.3), and three or more conditions (OR 50.7,

95% CI 14.5–177.1). The odds of death were greater

for exposure through oyster consumption (OR 6.7,

95% CI 3.2–14.0) compared to wound infection.

V. vulnificus

From 1998 to 2007, there were 276 cases of V. vul-

nificus reported (average annual incidence 1.6/

1 000 000). There were 141 (50.7%) cases presenting

with wound-related symptoms, 79 (28.6%) cases pres-

enting with gastroenteritis, 40 (14.5%) with septi-

caemia, and 16 (5.8%) with unknown syndrome

reported (Fig. 3). The most common cause was

wound infection (125 cases, 45.3%). Ninety-one

(33.0%) cases were associated with oyster consump-

tion, 12 (4.3%) with other seafood consumption, and

48 (17.4%) had unknown cause (Fig. 4). At least one

underlying health condition was reported for 75.0%

of cases, with most (70.0%) reporting multiple con-

ditions.

There were 76 deaths among V. vulnificus infections

(CFR 27.5%), with 33 deaths in those presenting with

septicaemia (CFR 82.5%), and 73 in those with

underlying health conditions (CFR 96.1%). Most

(56%) deaths were associated with raw oyster con-

sumption, and 14% were associated with wound in-

fections. The odds of death in cases of V. vulnificus

with one or more underlying conditions were 11.8

(95% CI 3.6–38.8) times the odds of death in those

with none.

V. parahaemolyticus

There were 245 cases of V. parahaemolyticus reported

(average annual incidence 1.4/1 000 000). The most

common presenting clinical syndromes were gastro-

enteritis (137 cases, 55.9%) and wound infection

(96 cases, 39.2%) (Fig. 3). Most (50.2%) cases were

associated with consumption of seafood: 73 (29.8%)

with oysters and 50 (20.4%) with other seafood (e.g.

crabs, shrimp). There were 86 (35.1%) cases associ-

ated with wound infections (Fig. 4). Eighty-four

(32.6%) cases had an underlying health condition

reported. There was one death in cases of V. para-

haemolyticus infection.

From 1998 to 2007, there were 28 documented

outbreaks of V. parahaemolyticus that included 301

individuals [average 11 cases (range 2–115)]. Of the

outbreaks, 35.7% were laboratory confirmed. Most

(82.1%) were associated with seafood consumption

at a restaurant. Crustacean shellfish were the most

commonly implicated source (50.0%), followed by

molluscan shellfish (28.6%), with specific vehicles in-

cluding shrimp (28.6%), crabs (25.0%), and oysters

(21.4%). The most frequent contamination factors

were cross-contamination from raw ingredients of

animal origin, bare-handed contact, and inadequate

cleaning. Almost all of the reported proliferation

factors were related to time-temperature abuse, in-

cluding inadequate cold-holding and slow cooling.

Table 2. Underlying conditions in cases of vibriosis,

Florida, 1998–2007

Characteristics of underlying

conditions No. %

Total cases 825 100.0 Number of underlying conditions per case

0 425 51.5 1 172 20.9 2 122 14.8

3 75 9.1 o4 31 3.8

Type of underlying condition Heart disease 141 17.1

Alcoholism 132 16.0 Liver disease 131 15.9 Diabetes 105 12.7 Malignancy 62 7.5

Renal disease 49 5.9 Immunodeficiency 45 5.5 Haematological disease 42 5.1

Gastric surgery 35 4.2 Peptic ulcer 34 4.1

594 K. E. Weis and others

V. alginolyticus

There were 131 cases of V. alginolyticus reported

(average annual incidence 0.7/1 000 000). Most cases

presented with wound infections (97 cases, 74.1%) or

other symptoms (27 cases, 20.6%) (Fig. 3), and most

were associated with exposure from wounds (74 cases,

56.5%) (Fig. 4). All cases in individuals aged 0–19

years presented with wound or other symptoms.

Forty-one (31.3%) cases had at least one underlying

health condition. There were no outbreaks and no

deaths associated with V. alginolyticus during this

10-year period.

DISCUSSION

This analysis updates a previous summary of reported

vibrio infections in Florida [10]. The clinical and epi-

demiological features of vibriosis have changed since

the 1996 report. Most notably, we have seen a change

in common species and risk factors and an increase in

incidence and CFRs. The most commonly reported

species changed from V. parahaemolyticus (1981–

1993) to V. vulnificus (1998–2007). Cases of vibriosis

attributed to raw oyster consumption have decreased

from 45% to 26% over the same time-frame. Wound

infections were the most common clinical syndrome in

the current analysis compared to gastroenteritis as

reported by Hlady et al. [10]. Incidence of vibriosis

has increased in Florida from 4.3/1 000 000 in-

dividuals (1981–1993) to 4.8/1 000 000 (1998–2007).

CFRs also increased for vibriosis presenting with

gastroenteritis (2–9%) and septicaemia (47–76%).

Due to changes in the way risk factor and background

population data were recorded over the years, we

were unable to assess the relative risks in certain

high-risk groups, such as people with AIDS and raw

oyster-consuming adults, as done previously [10].

V. vulnificus was the most common species in

Florida, unlike other areas of the country where

V. parahaemolyticus was the most common [13].

V. vulnificus is associated with more serious illness

[1, 4, 7], and is the leading cause of death related to

seafood consumption [6, 7]. V. parahaemolyticus is re-

cognized as the leading cause of gastroenteritis associ-

ated with seafood consumption in the USA [14–16],

and is often associated with foodborne outbreaks

[1, 14, 17]. The median number of cases reported an-

nually in Florida has increased from 16 (1981–1993)

[10] to 20 cases (1998–2007). An increase in incidence

of V. parahaemolyticus has also been noted through-

out the USA and in other countries [1, 14]. Rising

Table 3. Predictors of death in cases of vibriosis, Florida, 1998–2007

Non-fatal Fatal Crude associations

No. % No. % OR 95% CI

Presence of any underlying condition* 322 43.3 78 95.1 25.5 (9.2–70.4) Number of underlying conditions 0 421 56.7 4 4.9 1.0 (reference)

1 155 20.9 17 20.7 11.5 (3.8–34.8) 2 101 13.6 21 25.6 21.9 (7.3–65.2) o3 66 8.9 40 48.8 63.8 (22.1–184.1)

Exposure# Wound infection 300 53.4 11 14.1 1.0 (reference)

Oyster consumption 174 31.0 44 56.4 6.9 (3.5–13.7) Other seafood consumption 88 15.7 5 6.1 1.6 (0.5–4.6)

Clinical syndromes Wound infection 355 47.8 14 17.1 1.0 (reference)

Gastroenteritis 316 42.5 30 36.6 2.4 (1.3–4.6) Septicaemia 11 1.5 34 41.5 78.4 (33.0–186.1) Other 61 8.2 4 4.9 1.7 (0.5–5.2)

Gender

Female 218 29.3 10 12.2 1.0 (reference) Male 522 70.3 70 85.4 2.9 (1.5–5.8)

OR, Odds ratio; CI, confidence interval. * Compared to no underlying condition.

# Excludes cases with unknown exposure (n=203).

Vibriosis in Florida, 1998–2007 595

water temperatures [1, 17] and the emergence of

new strains of V. parahaemolyticus throughout the

world, specifically the O3:K6 strain and its serovari-

ants [18] have been suggested as possible causes.

Finally, V. alginolyticus is commonly associated with

ear infections and illness in younger individuals [8],

with similar associations found in Florida.

Wound infections and seafood consumption were

an equal source of exposure to Vibrio spp. in Florida,

whereas seafood consumption is most often associated

with vibriosis throughout the USA [13]. A possible

cause for increased wound-related exposures is that

Florida has over 2000 miles of shoreline [19]. This

access may lead to increased participation in water

activities, possibly yielding a higher number of wound

exposures. Further, Florida has higher average ambi-

ent air and water temperatures year-round than many

parts of the country, which may increase the likeli-

hood of such exposures because of the longer season

for water activities and higher vibrio bacterial counts.

In accord with other studies, incidence and mor-

tality rates associated with vibriosis in Florida were

higher in summer months [4, 17] and in males [1, 8],

consistent with historical Florida trends [10]. Male

gender was significantly associated with death in

crude analysis; however, gender was not a significant

predictor or confounder in adjusted analyses.

Another important feature of vibriosis is that the

greatest risk of illness and death is in those with

underlying health conditions. We also found a strong

association between underlying health conditions and

death from V. vulnificus. Individuals with alcoholism

and liver or heart disease have increased risk of in-

fection, as well as increased risk of death.

Increases in incidence and CFRs seen in Florida

may be partially attributable to increased awareness

of vibriosis in healthcare providers and increased

surveillance. In addition, we have experienced several

large outbreaks of V. parahaemolyticus in Florida

during this period. However, increases in incidence

have also been found in FoodNet states [4]. Even after

excluding cases of V. parahaemolyticus that occurred

during known outbreaks, incidence in this species in

the FoodNet states has also increased [4].

It is alarming that there are higher incidence and

fatality rates in Florida despite increased educational

campaigns aimed at high-risk groups. Other Gulf

Coast states have seen similar increases in incidence

over time, as well. Louisiana had an average annual

incidence rate in 2000–2001 of 5.9 cases/1 000000

compared to 6.7 in 2006–2007, while Mississippi

increased from 2.3 to 2.9/1 000 000 and Texas in-

creased from 1.4 to 2.3/1 000 000 during those same

years [20].

Florida law requires a warning notice in all food

service establishments and retail markets serving or

selling raw oysters. The FDOH interacts with state-

wide medical organizations and health support

groups to present prevention messages to the health-

care community, and distributes educational pam-

phlets and materials at health fairs. Further, there

are several ongoing national educational campaigns

sponsored by the Interstate Shellfish Sanitation

Conference (ISSC) [21] and the Gulf & South Atlantic

Fisheries Foundation [22] that aim to raise awareness

in people with underlying health conditions regarding

their risk of V. vulnificus infection associated with raw

oyster consumption [23]. Given the increasing inci-

dence seen nationwide, the ISSC is currently also

working on regulatory policies related to molluscan

shellfish in order to prevent vibriosis.

Florida education efforts seem to have been suc-

cessful, with an almost 50% reduction in total number

of cases associated with raw oyster consumption

compared to that reported previously [10]. Despite this

success, these campaigns are mainly funded to focus

on one high-risk group, raw oyster consumers, and

exclude those with wound infections. Florida has seen

an increase in the number of cases associated with

wound infections. While there is a continued need to

warn consumers about the risk from consuming raw

oysters, future prevention efforts should focus on

those at highest risk for wound infections such as those

with diabetes. Outreach efforts should target specialist

groups for wounds such as wound care treatment

centres, endocrinologists, and other providers that

treat diabetic patients, as well as local diabetes support

groups. These new educational campaigns should

include risk messaging related to wounds sustained

during water-related recreational activities or ex-

posure to aquatic environments. Outreach pro-

grammes should focus on V. vulnificus-related wound

infections. Although it is possible to get wound infec-

tions from other vibrios, V. vulnificus is particularly

virulent, and messaging should focus on the recog-

nition, treatment, and prevention of these infections.

Little research has focused specifically on wound-

related cases of vibriosis which are more numerous

than oyster-related V. vulnificus infections; therefore,

another direction would be to examine the extent

of wound infections and treatment of these cases,

including wound debridement and amputation.

596 K. E. Weis and others

Research is also needed to address the potential im-

pact that the environment has on increasing incidence

of vibriosis, particularly the role that environmental

conditions in oyster harvesting areas have on the

bacterial count of harvested oysters.

There are a few limitations that should be noted.

We chose to examine the 10 most recent years with

complete vibrio data available. The previous study

included data up to 1993 [10]. However, we did not

include the years 1994–1997 in our analysis due to

concerns regarding data quality for those years. As

with all foodborne illnesses, cases of vibriosis are un-

derreported, and reporting is probably biased towards

more severe cases. Cases of non-cholera vibriosis were

not nationally notifiable until 2007 but have been re-

ported in Florida since 1981. This may account for

some of the differences between the epidemiology of

vibriosis in Florida and elsewhere in the USA. Data

were also not always complete on each individual. In

Florida, case investigation and reporting is typically

performed at the county-level, and there may be

inconsistencies in the way data were collected.

Moreover, patients or their families were not always

able to recall details of food histories or other ex-

posures. Almost 25% of reported cases had no known

exposure, a huge gap in epidemiological data. Finally,

we were unable to assess some factors related to vib-

riosis (e.g. hospitalization, treatment) since these

variables were not included in our database.

The changing patterns of vibriosis noted in this and

other studies may be related to increased awareness

and surveillance, as well as higher water temperatures

and other environmental factors. However, the in-

creased incidence in vibrio infections highlights the

need for continued and improved education and risk

reduction for at-risk populations, with a new focus on

wound-related infections. Because certain Vibrio spp.

are associated with significant morbidity and mor-

tality, especially in those with underlying health con-

ditions, a continuing focus on increasing awareness

and understanding of vibriosis in healthcare pro-

viders, high-risk populations with specific underlying

health conditions, seafood consumers, and those with

occupational or recreational exposures to seawater is

needed.

ACKNOWLEDGEMENTS

The Council of State and Territorial Epidemiologists

provided financial support for K. Weis during her

Applied Epidemiology Fellowship.

DECLARATION OF INTEREST

None.

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598 K. E. Weis and others

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