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ORIGINAL ARTICLE

Two Clusters of Ciguatera Fish Poisoning in Paris, France, Related to Tropical Fish Imported From the French Caribbean by Travelers Loïc Epelboin, MD,∗† Alice Pérignon, MD,∗ Virginie Hossen, MSc,‡ Renaud Vincent, MD,§ Sophie Krys, PhD,‡ and Eric Caumes, MD, PhD∗† ∗ Infectious

and Tropical Diseases Department, Assistance Publique-Hôpitaux de Paris, Groupe Hospitalier Pitié-Salpêtrière, Paris, France; † Faculté de Médecine, Université Pierre et Marie Curie, Paris, France; ‡ French Agency for Food, Environmental and Occupational Health (ANSES), Food Safety Laboratory of Maisons-Alfort, National Reference Laboratory for the Control of Marine Biotoxins, Maisons-Alfort, France; § Centre Antipoison et de Toxicovigilance de Paris, Assistance Publique-Hôpitaux de Paris, Hôpital Fernand Widal, Paris, France DOI: 10.1111/jtm.12161

Guest Editor: Robert Steffen

Background. Ciguatera fish poisoning (CFP) is a food-borne illness due to the consumption of reef fish containing pathogenic toxins. CFP is endemic to tropical areas and may be described in travelers in non-endemic areas. Methods. We describe two clusters of autochthonous cases of CFP in Paris, France. They were related to two fish caught in Guadeloupe (French West Indies) and consumed in Paris after being air-transported in a cooler. In both cases, fish flesh was analyzed and the presence of ciguatoxins by mouse bioassay (MBA) was confirmed. Results. The first cluster involved eight individuals among whom five presented gastrointestinal symptoms and four presented neurological symptoms after consuming barracuda flesh (Sphyraena barracuda). The second cluster involved a couple who consumed a grey snapper (Lutjanus griseus). Most of them consulted at different emergency departments in the region of Paris. Conclusions. CFP may be seen in non-traveler patients outside endemic countries resulting from imported species of fish. Thus, CFP may be undiagnosed as physicians are not aware of this tropical disease outside endemic countries. The detection of ciguatoxins by MBA in the French National Reference Laboratory is useful in the confirmation of the diagnosis.

C

iguatera fish poisoning (CFP) is a food-borne illness caused by the consumption of reef fish containing ciguatoxins.1,2 Ciguatera may lead not only to gastrointestinal and neurological symptoms but also to cutaneous, cardiovascular, and respiratory disturbances of variable severity.3 CFP is a significant public health issue in endemic areas that extend between 35∘ N and 35∘ S, approximately.4 CFP is probably mostly undiagnosed even if its worldwide incidence is estimated to be around 50,000 cases annually. CFP is the most

common poisoning linked to the consumption of finfish. Most of the cases are reported from countries within and surrounding the Pacific and Indian Oceans and the Caribbean.4 Although most ciguatera cases are seen in endemic tropical areas, there is an increasing potential for cases to be encountered in temperate regions, as recently described.5 In this study, we aim to describe two clusters of collective common-source CFP in Paris due to consumption of two fish imported from Guadeloupe (French West Indies).

This paper has been presented at the 9th International Conference on Moluscan Shellfish Safety, Sydney, Australia, 17–21 March 2013.

Methods

Corresponding Author: Loïc Epelboin, MD, Service de Maladies Infectieuses et Tropicales, Centre Hospitalier PitiéSalpêtrière, 47-83 bd de l’Hôpital, F-75013 Paris, France. E-mail: [email protected]

Data Collection and Analysis In February 2011, two successive cases of CFP were referred to our hospital. In both cases, patients presented with gastrointestinal and neurological symptoms after a collective consumption of tropical fish brought back from Guadeloupe in a cooler and then placed in a © 2014 International Society of Travel Medicine, 1195-1982 Journal of Travel Medicine 2014; Volume 21 (Issue 6): 397–402

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freeezer on arrival. We interviewed patients regarding the people with whom they had eaten the fish. Information about symptoms and treatment were obtained by contacting every person at risk over the telephone and/or accessing medical records when the patients had consulted another hospital. We thus retrospectively reviewed the cases of 10 persons involved in two collective CFP clusters and who presented at different emergency departments of the Ile-de-France region in and around Paris (Table 1). Mouse Bioassay for the Detection of Toxicity Level of Fish Samples As fish remains were available for both clusters and were kept frozen, they were sent to the National Reference Laboratory for performing ciguatoxin analysis. For cluster 1 (outbreak due to barracuda), the mouse bioassay (MBA) was performed 15 days after fish consumption, and for cluster 2 (outbreak related to snapper), the MBA could only be done after sample receipt, ie, 2 months later. However, even though the fish flesh was partially spoiled and remnants of fish samples were frozen, as ciguatoxins are highly chemically stable, the MBA was still applicable. A 50-g sample of raw fish flesh homogenate was extracted twice with methanol (2× 100 mL), defatted with hexane (170 mL), and extracted twice with diethyl ether (2× 340 mL). The combined Table 1

diethyl ether fractions were concentrated to dryness using a rotary evaporator (Büchi R-134, Fisher Bioblock Scientific, Illkirch, France). The residue was dissolved in 80% methanol (2 mL) and defatted again with hexane (2 mL). The solvents used were of analytical grade (purchased from Fisher Scientific). The aqueous methanolic extract was finally dried under a gentle stream of nitrogen gas at 40∘ C (Reacti-Vap; Pierce Biotechnology, distributed by Interchim, Montluçon, France) and then tested for toxicity by the MBA according to Vernoux 1994 with modifications as described by Krys and colleagues.6,7 The MBA protocol was specifically designed for the detection of the toxicity level due to ciguatoxins where the two main end points are mortality and weight loss of more than 5% of at least one mouse tested. Controls to consolidate the results of the test were as follows: a negative control corresponding to a fish sample previously tested negative by MBA (no symptoms in the animals tested) and a positive control corresponding to a fish sample previously involved in a typical ciguateric outbreak. Two male Swiss albino mice of 18–22 g (Charles River Laboratory, L’Arbresle, France) were used for testing each fish sample. Mice were allowed free access to food and tap water throughout the experimental period. Dried extract was dissolved in 2 mL of 1% Tween 60. The solution was injected to mice

Characteristics of the 10 individuals involved in the two clusters of ciguatera fish poisoning (CFP)

Gender

Age (years old)

Fish species

Quantity of flesh consumed*

Cluster 1 B1

M

37

Sb

2+

Diarrhea, vomiting, abdominal pain

B2

F

43

Sb

2+

Diarrhea, vomiting

B3

M

33

Sb

3+

B4 B5 B6 B7 B8

F M M M M

32 12 7 8 ∼40

Sb Sb Sb Sb Sb

1+ 4+ 0+ 0+ 0

Diarrhea, vomiting, abdominal pain Stomach pain Diarrhea, vomiting None None None

Cluster 2 S1

M

56

Lg

4+

Abdominal pain

S2

F

∼50

Lg

2+

Abdominal pain

Patient

Digestive signs

*Quantity of consumed fish flesh from 0 (no fish consumed) to 4+, a high quantity of flesh. Sb = Sphyraena barracuda; Lg = Lutjanus griseus.

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Neurological signs

Chills, flushing, asthenia, paresthesia of extremities, hot and cold inversion, hypotension, bradycardia, sleep disorders (day 4) Chills, sweating, paresthesia of lips and limbs extremities, myalgia, muscle weakness, dizziness, generalized itching, hot and cold inversion Headache, paresthesia, sensation of breathing cold air, myalgia None Headache, myalgia None None None

Paresthesia, weakness, cold inversion hot, sensation of burning hands in water, generalized itching, widespread pain (in the bones) Same symptoms as S1 but milder symptoms

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intraperitoneally (0.04 mL/g of mouse body weight). The signs of intoxication, the time to death, or the weight loss within a period of 24 hours were recorded. Typical ciguateric signs include reduced activity, hypersalivation, lachrymation, ataxia, dyspnea, diarrhea, piloerection, and penile cyanosis. Gasping and hypoxic convulsions usually precede death. The observation of mortality in mice and/or loss of weight after 24 hours are the criteria by which the toxicity of extracts is determined. The death of one or two mice means that the fish is not edible and the test result is indicated as positive. Weight loss of more than 5% for at least one mouse means that the fish is at the safety limit and the result is also positive. If the mice gain or lose less than 5% of their weight, then the fish sample is considered as edible and the result is qualified as negative. Ethical Statement Patients’ medical records were retrospectively reviewed, and all data collected were identified in standardized forms according to the procedures of the Commission Nationale de l’Informatique et des Libertés (the French Information Protection Commission). Results Cluster 1 The first cluster involved eight individuals. Four persons (one child of 12 years old and three adults from 32 to 43 years old) consulted in different emergency departments of the Parisian area for gastrointestinal symptoms 3–24 hours after sharing the same dinner with four other individuals (Table 1). All but one had consumed various quantities of fried barracuda head flesh (Sphyraena barracuda) cooked in tomato sauce on the same day. The fish had been bought by one of them in Anse Bertrand, Guadeloupe (French West Indies), and brought back by an airliner in a cooler. The other guests did not travel. Among the eight guests, five presented with digestive symptoms, such as watery diarrhea, vomiting, and abdominal pain. The symptoms appeared 2–12 hours after the meal, and their intensity apparently depended on the amount of flesh consumed. In the following hours and days (1–4 days), four patients complained of neurological symptoms such as myalgias (three persons), hot and cold inversion (three), paresthesia of the fingers and toes (three), headache (two), chills (two), flushing (one), sweating (one), asthenia (one), and dizziness (one). Cardiovascular signs such as bradycardia (two) and hypotension (one) were also found once in the hospital. Serum biochemistry in three of them showed moderate renal dysfunction in one patient, whereas one other patient had elevated aspartate aminotransferase (ASAT) level at 55 IU/L (N < 42 IU/L) and creatine phosphokinase level at 409 IU/L (N < 220 IU/L) (Table 2). Among the three other guests, none was symptomatic, two were children and had barely tasted the fish, and one person did not eat fish flesh at all.

Table 2 Biological characteristics of the four individuals with ciguatera fish poisoning (CFP) Patient

WBC

PMN

Urea

Creatinine

ASAT

ALAT

CPK

B1 B2 B3 S1

17,600 8,800 9,900 3,600

5,994 5,870 8,680 900

nd 3.4 8.9 nd

93 56 124 91.1

37 18 44 22

55 15 37 16

409 70 nd nd

WBC = white blood cells (N < 10 × 109 /L); urea (N < 7 mmol/L); PMN = polymorphonuclear neutrophil (N < 8 × 109 /L); creatinine (N < 90 μmol/L); ALAT = alanine aminotransferase (N < 42 IU/L); ASAT = aspartate aminotransferase (N < IU/L); CPK = creatine phosphokinase (N < IU/L); nd = no data.

In the different emergency departments where they consulted, the diagnosis of a food poisoning outbreak was made, but the diagnosis of ciguatera was not systematically raised until consulting our department with neurological symptoms that appeared after 1–4 days. CFP was suspected. Despite the recommendations to treat patients within the first 24 hours of onset of neurological symptoms,8,9 mannitol was administered for two of them, on days 2 (B2) and 4 (B1), respectively. All patients fully recovered within 2 days to more than 2 months, with the exception of one treated patient (B2) who presented with persistent irritability as well as digestive intolerance to fish and other seafood for more than 12 months. The MBA performed on the barracuda fish remains was tested as positive; both mice died within 75 and 80 minutes, respectively, although the second mouse received only 50% of the dose recommended in the protocol. This suggested a high content of ciguatoxins in the barracuda flesh. Cluster 2 The patient was a 55-year-old man from Guadeloupe, with no significant past medical history. He bought a 6-kg grey snapper (Lutjanus griseus) from a fisherman during his stay in Guadeloupe and brought it back to Paris in a cooler by airliner. The day after his return, the patient and his 50-year-old wife (who had not traveled) consumed the fish. The man ate this fish meal everyday for 1 week, including the head, while his wife ate only one meal the first day, then stopped eating it because of the appearance of indigestion symptoms (Table 1). Both complained of diffuse pain in the bones several hours after the first meal, especially at night, associated with muscle weakness, burning sensation when he put his hands in cold water, and abdominal pain. As the patient had acute symptoms that were lasting for more than 4 weeks, he consulted our department. His wife who had only shorter and milder symptoms did not consult. CFP diagnosis was raised because of the nature of the symptoms (especially paresthesia and dysesthesia) and the fact that the symptoms appeared after consumption of tropical fish in both the consumers. No mannitol was provided because of the long duration. The symptoms improved slowly and lasted for more than 2 months in the patient. One year later, he still J Travel Med 2014; 21: 397–402

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complained of mild itching when he came in contact with water. The MBA performed on the grey snapper fish remains was found positive; none of the mice died within 24 hours, but both the mice lost more than 5% of their body weight in 24 hours (18 and 20%, respectively), suggesting that it was less contaminated than the barracuda responsible for the infection in the first cluster. Discussion These two clusters of CFP seen in Paris, France, illustrate that this tropical disease can be seen in non-traveling patients living outside endemic countries through the import of fish that contain the ciguatoxins. CFP is the most frequent form of human poisoning due to the consumption of reef fish contaminated with ciguatoxins.1,2 These toxins are produced by benthic dinoflagellates of the genus Gambierdiscus, growing predominantly in association with macroalgae in coral reefs in tropical and subtropical climates. The toxin is ingested by herbivorous fish and metabolized to a more toxic form at each successive trophic level, accumulating up the food chain to the carnivorous fish. These are in turn consumed by humans, which are at the end of the transmission chain and experience the full effects of biomagnification.10 Hundreds of fish species have been identified as carriers of CFP. In the West Indies, four fish families have been especially identified with high trophic levels of toxicity: Carangidae, Lutjanidae, Serranidae, and Sphyraenidae.11 Percentages of toxic fishes to humans reached 55% for Caranx latus and 33% for Caranx bartholomaei and Caranx lugubris.11 CFP is a major public health problem in the Pacific and Caribbean tropical areas where the pathology is known to most of the physicians and where prevention is regularly performed to inform the population and particularly the fishermen about the risk of consumption of carnivorous reef fish.1 Data from both the Pacific and Caribbean areas collated in two recent publications document that high incidence rates (eg, over 100 incidences per 10,000 population per year) occur in both the Pacific and Caribbean areas, albeit with high variability.12,13 In Guadeloupe, a French island in the Caribbean, CFP is well known,14 and selling of the fish responsible for ciguatera has been forbidden since 1946.15 CFP incidence varies from 0.27 to 55 cases per 10,000 inhabitants per year in this region.12,15 Species considered for transmitting CFP after consumption by humans are listed in the local regulations (Prefectorial order no 1249, 2002), which has been available since 2002 and enables the local public health service to appropriately manage this problem.16 Among the species responsible for both the cases described in this study, the great barracuda S. barracuda is indicated as a species for which harvest and sale are entirely prohibited. However, the grey snapper L. griseus is not included in this list although a study evaluating the levels of ciguatera toxicity of fish caught around Saint J Travel Med 2014; 21: 397–402

Epelboin et al.

Barthélemy Island in French West Indies showed that it contained ciguatoxins.17 In the Caribbean, the rules are very nation dependent, eg, barracuda is sold quite widely in Barbados without significant problem. However, geographic distribution of CFP can change quite quickly and occur on reefs that have been previously clear of toxin, and the highly heterogenic repartition of the cases in the Caribbean region, with some countries such as St. Lucia and St. Vincent and the Grenadines reporting no instances from 1980 to 2006, and others reporting very high incidences, depending on the study methodology, with over 400 cases per 10,000 inhabitants annually, such as in US Virgin Islands.12,18 At least it should be recommended that travelers to the Caribbean specifically should not eat barracuda or moray eel and be careful with other fish known to cause infection frequently, such as grouper and snapper (http://www.cdc.gov/nceh/ciguatera/default.htm). In this study, the diagnosis of CFP was supported by the MBA detection of ciguatoxins in both the consumed fish, which is rarely reported. The MBA is still the most widely used method since it provides a global response in terms of toxicity without requiring any standards that are not yet available. Thus, the MBA is a convenient tool to screen fish samples for their edibility. The toxicity end points for MBA are the mortality and weight loss of more than 5% in at least one tested mouse. Regarding the samples analyzed in this work, no additional specific symptoms such as penile cyanosis or diarrhea were observed. However, mouse lethality in one case and loss of weight of more than 5% in the other case were observed, which evidenced the toxicity level in relation to the presence of ciguatoxins. Other analytical methods based on the identification and quantification of CTXs such as liquid chromatography coupled to mass spectrometry are promising but not still available as validated methods, especially for official controls. The main drawbacks for their development are related to the wide chemical diversity of CTX analogs. Indeed, their chemical structures vary depending on the geographical areas from which the samples come; they also depend on the species of fish contaminated and on the species of the toxin-producing dinoflagellates. Also, appropriate standards for acute quantification are lacking as CTX-certified materials are not available in the market. Most of the cases previously described in Metropolitan France in non-traveling patients were diagnosed according to compatible clinical pictures and epidemiological context.19 – 21 From 1995 to 1999, 23 collective CFP outbreaks involving 98 cases were reported to the French Institute for Public Health Surveillance.19 Most ciguatera outbreaks occurred in the overseas French territories (Caribbean, La Réunion Island, Indian Ocean) after familial local consumption of reef fish such as grouper, barracuda, and jack. CFP can be largely prevented by educating people living or traveling in endemic areas. They have to be aware of the risk and discard consumption of fish considered to be at risk (mainly large carnivorous fish such

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Ciguatera in Paris Related to Fish Imported From the Caribbean

as snapper or barracuda, as in the case of our patients). Moreover, it should be recommended to avoid consuming viscera, head, or roe, known to be concentrated in toxins. In the first case, symptoms were particularly severe after eating the head. Thus, the collective CFP outbreaks reported here show that the diagnosis of ciguatera toxicity must be considered, and an appropriate travel and dining history be obtained, when facing clusters of patients who exhibit digestive and atypical neurologic signs and symptoms. Because of its rarity in temperate-zone countries, this disease is not well known among local emergency physicians as evidenced in our first cluster. The atypical neurological symptoms make the diagnosis difficult, especially when the relation to the consumption of fish was not demonstrated in one case. Indeed, one of our patients consulted for digestive symptoms in another emergency department in Paris where the subsequent diagnosis of a food-borne intoxication outbreak was made. However, CFP diagnosis is difficult to determine before the onset of neurological symptoms as shown in our two clusters. Until recently, this disease was considered to be strictly restricted to the tropical latitudes, but since 2005, fish caught in waters of the Canary and Madeira Island groups in Europe were also reported to be responsible for clusters of CFP.5,22 Nevertheless, in temperate areas, the disease can also occur in persons traveling to tropical regions when returning to their country of origin.19,20 Moreover, some imported species may be contaminated by ciguatoxins, as demonstrated by several cases reported in patients eating such tropical fish imported in Europe23 and in North America.24 – 26 Lastly the change in dietary habits (ie, increased consumption of fish and exotic foods) and the wider geographic distribution of food products will increase the risk of CFP in patients without a history of travel in endemic areas because of consumption of fish imported from tropical or subtropical areas. Physicians should be informed about this particular form of food poisoning and the clinical signs and symptoms of CFP to consider the diagnosis even in the absence of a relevant travel history. In France, ciguatera, as every food-borne illness defined by the occurrence of at least two similar cases symptomatology, usually gastrointestinal troubles, and for which the same food source was evidenced, must be reported to the French Institute for Public Health Surveillance, which then alerts the Veterinary Services of the Ministry of Agriculture. The investigation is being conducted as soon as possible in order to identify the culprit fish and source of the outbreak so that appropriate control measures for preventing the appearance of new cases can be immediately initiated. Conclusions With the increase in travel and international exchanges, CFP cases may become more commonly seen in non-endemic areas. Therefore, physicians especially

from the emergency departments of non-endemic countries should be informed about this disease, in order to make early diagnosis and offer appropriate management to patients. Acknowledgments The authors thank Prof. Bruno Riou, Emergency Department, AP-HP, Groupe Hospitalier PitiéSalpêtrière Hospital, Paris, France; Dr Geoffroy Safrano, Emergency Department, Hôpital Le RaincyMontfermeil Hospital, Montfermeil, France; and Dr Georges Chanis, Emergency Department, Hôpital de Longjumeau, Longjumeau, France, for providing us with data concerning patients consulting in their respective emergency departments. Declaration of Interests The authors state that they have no conflicts of interest to declare. References 1. Friedman MA, Fleming LE, Fernandez M, et al. Ciguatera fish poisoning: treatment, prevention and management. Mar Drugs 2008; 6:456–479. 2. Swift AE, Swift TR. Ciguatera. J Toxicol Clin Toxicol 1993; 31:1–29. 3. Bagnis R, Kuberski T, Laugier S. Clinical observations on 3,009 cases of ciguatera (fish poisoning) in the South Pacific. Am J Trop Med Hyg 1979; 28:1067–1073. 4. Achaibar KC, Moore S, Bain PG. Ciguatera poisoning. Pract Neurol 2007; 7:316–322. 5. Nunez D, Matute P, Garcia A, et al. Outbreak of ciguatera food poisoning by consumption of amberjack (Seriola spp.) in the Canary Islands, May 2012. Euro Surveill 2012; 17(23). 6. Vernoux JP. The mouse ciguatoxin bioassay: directions for use to control fish for consumption. Mem Queensl Mus 1994; 34:625–629. 7. Krys S, Marcaillou-Le Baut C, Fessard V, Vernoux JP. Analytical methods based on the mode of action. In: Quae, ed. Toxines d’algues dans l’alimentation (Coordination: Jean-Marc Frémy & Patrick Lassus). Brest, France: Ifremer, 2001:449–480. 8. Palafox NA. Review of the clinical use of intravenous mannitol with ciguatera fish poisoning from 1988 to 1992. Bull Soc Pathol Exot 1992; 85:423–424. 9. Palafox NA, Jain LG, Pinano AZ, et al. Successful treatment of ciguatera fish poisoning with intravenous mannitol. JAMA 1988; 259:2740–2742. 10. Derne B, Fearnley E, Goater S, et al. Ciguatera fish poisoning and environmental change: a case for strengthening health surveillance in the Pacific? Pac Health Dialog 2010; 16:99–108. 11. Pottier I, Vernoux JP. Evaluation de la ciguatoxicité de poissons des Antilles par les bioessais souris et poussin. Bull Soc Pathol Exot 2003; 96:24–28. 12. Tester PA, Feldman RL, Nau AW, et al. Ciguatera fish poisoning and sea surface temperatures in the Caribbean Sea and the West Indies. Toxicon 2010; 56:698–710. J Travel Med 2014; 21: 397–402

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