Characteristic | V. alginolyticus | V. parahaemolyticus | V. cholerae non-O1/O139 | V. vulnificus | Other species |
---|---|---|---|---|---|
Total patients | 23 (100) | 20 (100) | 10 (100) | 7 (100) | 7 (100) |
Demographics | |||||
Age, y, median (SD) | 50 (+26.7) | 53 (+22.8) | 69 (+19.7) | 66 (+11.5) | 40 (+24.8) |
Sex | |||||
M | 19 (83) | 15 (75) | 7 (70) | 7 (100) | 6 (86) |
F | 4 (17) | 5 (25) | 3 (30) | 0 | 1 (14) |
Underlying condition | |||||
Heart failure | 8 (35) | 6 (30) | 5 (50) | 4 (57) | 1 (14) |
Neoplasia | 1 (4) | 5 (25) | 4 (40) | 0 (0) | 1 (14) |
Diabetes | 2 (9) | 3 (15) | 1 (10) | 1 (14) | 1 (14) |
Kidney failure | 2 (9) | 1 (5) | 1 (10) | 0 | 3 (43) |
Immune disease | 2 (9) | 2 (10) | 1 (10) | 0 | 2 (29) |
Hemopathy | 1 (4) | 1 (5) | 1 (10) | 1 (14) | 1 (14) |
Liver disease | 1 (4) | 1 (5) | 2 (20) | 1 (14) | 0 |
Alcohol use disorder | 2 (9) | 1 (5) | 2 (20) | 2 (29) | 0 |
Preexisting wound | 3 (13) | 0 | 0 | 3 (43) | 0 |
Digestive surgery | 2 (9) | 2 (10) | 1 (10) | 0 | 1 (14) |
Time to symptom onset, d, median (SD) | 2.4 (+2.0) | 1.3 (+0.9) | 3 (+4.4) | 5.6 (+8.1) | 1 (+0.0) |
Infection type | |||||
Acute | 14 (61) | 19 (95) | 10 (100) | 7 (100) | 5 (71) |
Chronic | 9 (39) | 1 (5) | 0 | 0 | 2 (29) |
Outcome | |||||
Recovered | 21 (91) | 17 (85) | 8 (80) | 6 (86) | 7 (100) |
Died | 2 (9) | 3 (15) | 2 (20) | 1 (14) | 0 |
Table 1. Clinical characteristics of patients with Vibrio infection, by species, Bay of Biscay, France, 2001–2019*
*Values are no. (%) except as indicated.
Antibiotic | V. alginolyticus | V. parahaemolyticus | V. cholerae non-O1/O139 | V. vulnificus | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
S | I | R | S | I | R | S | I | R | S | I | R | ||||
Amoxicillin | 1 | 0 | 15 | 1 | 6 | 7 | 2 | 2 | 3 | 5 | 0 | 0 | |||
Ticarcillin | 5 | 0 | 10 | 2 | 2 | 9 | 5 | 0 | 1 | 5 | 0 | 0 | |||
First-generation cephalosporin | 10 | 4 | 0 | 13 | 1 | 0 | 4 | 1 | 0 | 4 | 1 | 0 |
Table 2. Available drug-susceptibility test results for the main antibiotics used to treat Vibrio infections, by species, Bay of Biscay, France, 2001–2019*
*Data are no. of cases. I, intermediate; R, resistant; S, susceptible.
Characteristic | No sepsis, n = 42 | Septic shock, n = 13 | p value | ||||
---|---|---|---|---|---|---|---|
No. | % (95% CI) | No. | % (95% CI) | ||||
Patient sex | |||||||
M | 35 | 83 (72–95) | 10 | 77 (54–100) | 0.685 | ||
F | 7 | 17 (5–28) | 3 | 23 (0.2–46) | |||
Underlying conditions | |||||||
Heart failure | 18 | 43 (28–58) | 6 | 46 (19–73) | Referent | ||
Neoplasia | 6 | 14 (4–25) | 4 | 31 (6–56) | 0.223 | ||
Diabetes | 7 | 17 (5–28) | 1 | 8 (0–22) | 0.664 | ||
Kidney failure | 5 | 12 (2–22) | 2 | 15 (0–35) | 0.664 | ||
Immune disease | 5 | 12 (2–22) | 2 | 15 (0–35) | 0.664 | ||
Hemopathy | 3 | 7 (0–15) | 2 | 15 (0–35) | 0.582 | ||
Liver disease | 2 | 5 (0–11) | 3 | 23 (0–46) | 0.318 | ||
Alcohol use disorder | 3 | 7 (0–15) | 4 | 31 (6–56) | 0.102 | ||
Preexisting wound | 6 | 14 (4–25) | 0 | 0 (0–0) | 0.317 | ||
Digestive surgery | 4 | 10 (1–18) | 2 | 15 (0–35) | 0.618 | ||
Species | |||||||
V. alginolyticus | 10 | 24 (11–37) | 4 | 31 (6–56) | |||
V. parahaemolyticus | 14 | 33 (19–48) | 5 | 38 (12–65) | |||
V. cholerae non-O1/O139 | 8 | 19 (7–31) | 2 | 15 (0–35) | |||
V. vulnificus | 6 | 14 (4–25) | 1 | 8 (0–22) | |||
Other Vibrio species | 4 | 10 (1–18) | 1 | 8 (0–22) | |||
Outcome | |||||||
Recovered | 40 | 95 (89–100) | 7 | 54 (27–81) | 0.001 | ||
Died | 2 | 5 (0–11) | 6 | 46 (19–73) |
Table 3. Clinical characteristics and outcome of patients with and without septic shock after acute Vibrio infection, Bay of Biscay, France, 2001–2019*
*Median patient age ( + SD) was 60 ( + 21.4) for no sepsis and 61 ( + 15.3) for septic shock.
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The cases of Vibrio infections reported in this study are the most severe cases that ended up requiring hospitalization. Non–V.cholerae and V. cholerae non-O1/O139 bacteria can cause mild diarrhea and gastroenteritis, for which patients typically are not hospitalized [7,14], and the number of vibriosis incidents per year in the region is probably higher that those reported in our study. Comparing the demographics of our population with those described in a 1996–2010 review surveillance in the United States [10], we observed a higher proportion of men (81% vs. 68%), and the age group with the highest percentage of cases was 60–69 years in our population compared with 40–49 years in the United States. This difference is probably attributable to the fact that our population mainly consists of the most severe cases of infection that occur most often in older person [15]. Vibrio infections are usually initiated from exposure to contaminated water or consumption of raw or undercooked contaminated seafood. As reported in 2008 by Dechet et al. [16], seawater-related activities as simple as walking on the beach can lead to Vibrio infections [16], which was also reported for >50% of the patients with environmental factors identified in our study. Vibrio species are responsible for 20% of bacterial illnesses related to shellfish consumption [17]. In our study, 39% of the cases were acquired after seafood handling or consumption. Vibrio bacteria caused more seafood-associated outbreaks during the warmer months [11], and all but 1 case occurred during June–September in our study population. Extreme heat waves led to unprecedented high sea surface temperatures, which appear to be responsible for the emergence of Vibrio bacteria in areas where they are usually not present [18,19]. In 2003, France experienced the hottest summer in a century, which may have led to an increase in the concentration of Vibrio on the Bay of Biscay, given that the number of reported Vibrio infections also increased this year.
We compared the results of our study to a similar investigation conducted in the US state of Florida [13]. The most common species reported in Florida over 10 years were V. vulnificus (33.1%), V. parahaemolyticus (29.4%), V. alginolyticus (15.7%), and V. cholerae non-O1/O139 (6.6%). In our study, we report a slightly different distribution: V. alginolyticus (34.3%), V. parahaemolyticus (29.9%), V. cholerae non-O1/O139 (14.9%), and V. vulnificus (10.4%). The incubation period of V. parahaemolyticus, V. vulnificus (when exposed to a wound), and V. cholerae non-O1/O139is <24 hours; for other clinical manifestations after infection with V. vulnificus, the incubation period ≈48 hours [7,14]. In our study, the time between known exposure and onset of symptoms was <48 hours in 74% of cases.
Clinical manifestations are different depending on the type of Vibrio species. V. alginolyticus has been identified as a relevant cause of superficial wound and ear infections [14]. In our study, V. alginolyticus was responsible for most cases of chronic otitis. However, contrary to what has been observed in Florida [13], this species also caused 1 death associated with wound infection. V. parahaemolyticus is the most prevalent foodborne bacterium associated with seafood consumption and typically causes acute gastroenteritis [20], but it has also been identified in wound-associated cases [13]. In our study, most V. parahaemolyticus infections caused either gastroenteritis or bacterial cellulitis, but the species was also responsible for pneumonia, phlegmonous ileitis, and otitis. V. cholerae non-O1/O139 is the causative agent of gastrointestinal and extraintestinal infections and has been reported to be the cause of one third of deaths in infected patients [21]. Of the 10 patients with V. cholerae non-O1/O139 infection reported in this study, 6 had >1 risk factor (e.g., cancer or malignant blood diseases, alcoholism, other liver diseases, and diabetes), and 1 died from the infection. V. vulnificus infections in Europe are rare and sporadic [22] but have the highest reported case-fatality rate of any foodborne pathogen [12,23]. In our study, 7 total cases were reported in 2005, 2007, 2015, 2017, and 2018, and 4 resulted in either amputation, septic shock, or death.
Because Vibrio infections can cause severe reaction or disease, treatment with a combination of a third-generation cephalosporin and a tetracycline or a fluoroquinolone alone is recommended. Higher mortality rates were observed with a β-lactam alone, compared with fluoroquinolone alone or fluoroquinolone or tetracycline plus a β-lactam [24]. In the United States, the most commonly used antibiotics for patients with Vibrio infections were quinolones (56.1%), followed by cephalosporins (24.1%), tetracyclines (23.5%), and penicillins (15.4%) [24]. Less than one third of patients with Vibrio infections received appropriate antibiotic therapy [13]. According to our study, in France, the main prescribed antibiotics for Vibrio infections were penicillins (91%), quinolones (36%), cephalosporins (30%), metronidazole (15%), and tetracycline (10%), and >50% of patients received a multidrug regimen.
The main limitations of our study are that vibriosis is not a notifiable disease in France, that not all hospitals in the Bay of Biscay participated, and that the reported cases probably underestimated the situation. Data were also not always complete on each case-patient, and details of food histories or other exposures were not always available.
In conclusion, the incidence of serious marine-related Vibrio infections has been low on the west coast of France. However, predicted rising ocean temperatures and demographic shifts (e.g., an aging population with increased risk factors) may lead to the emergence of opportunistic vibriosis in France and other coastal countries in temperate and tropical regions. Our retrospective case-series study provides a basis for identifying and treating new cases of Vibrio infections that might affect larger population sectors in the future.