article: Ciguatera is a type of fish poisoning that occurs throughout the tropics, particularly in vulnerable island communities such as the developing Pacific Island Countries and Territories (PICTs). After consuming ciguatoxin-contaminated fish, people report a range of acute neurologic, gastrointestinal, and cardiac symptoms, with some experiencing chronic neurologic symptoms lasting weeks to months. Unfortunately, the true extent of illness and its impact on human communities and ecosystem health are still poorly understood. A questionnaire was emailed to the Health and Fisheries Authorities of the PICTs to quantify the extent of ciguatera. The data were analyzed using t-test, incidence rate ratios, ranked correlation, and regression analysis. There were 39,677 reported cases from 17 PICTs, with a mean annual incidence of 194 cases per 100,000 people across the region from 1998–2008 compared to the reported annual incidence of 104/100,000 from 1973–1983. There has been a 60% increase in the annual incidence of ciguatera between the two time periods based on PICTs that reported for both time periods. Taking into account under-reporting, in the last 35 years an estimated 500,000 Pacific islanders might have suffered from ciguatera. This level of incidence exceeds prior ciguatera estimates locally and globally, and raises the status of ciguatera to an acute and chronic illness with major public health significance. To address this significant public health problem, which is expected to increase in parallel with environmental change, well-funded multidisciplinary research teams are needed to translate research advances into practical management solutions.
  The developing Pacific Island Countries and Territories (PICTs) are under increasing threat from both acute and chronic diseases ranging from HIV/AIDS to obesity. In addition, people residing in PICTs are highly vulnerable to environmental impacts from the sea level rise and extreme weather events associated with global warming. Ciguatera is a prevalent tropical and subtropical disease that has been an under-appreciated cause of acute and chronic disease in island communities and might be increasing in incidence due to increasing vulnerabilities (i. e. poverty, global warming, eutrophication) in these populations [1]–[3]. Ciguatera is caused by the consumption of coral reef fish contaminated by ciguatoxin and related toxins from dinoflagellates (microalgae) and cyanobacteria [1], [2]. The ciguatoxin bioaccumulates up the food web, either directly from incidental uptake by herbivorous fish or indirectly by carnivorous fish [1]. After the consumption of coral reef fish contaminated with ciguatoxin, people experience potentially severe acute neurologic, gastrointestinal and cardiac symptoms as well as, in some cases, chronic neurologic symptoms lasting weeks to months [1], [2]. Ciguatera occurs globally, in coastal tropical waters, and is particularly prevalent across the PICTs. Cases of ciguatera have also been reported in temperate regions of the world due to travel and coral reef fish export. Ciguatera poisoning is often under-diagnosed and under-reported, with only 2 to 10% of cases reported to health authorities (Friedman et al 2008). Estimates of the incidence of ciguatera in Oceania have ranged from 0. 5/10,000/year in Hawaii to 5,850/10,000/year in French Polynesia [2]. Fish is the staple protein source in many PICT communities, with many islands in the region suffering ongoing outbreaks of ciguatera leading to potentially significant impacts on large portions of the population of small island communities when toxic fish are consumed [3]. Dinoflagellates of the genera Gambierdiscus, that grow epiphytically on macro- and turf-algae on coral reefs, produce the ciguatoxins predominantly responsible for the disease known as ciguatera. Coral reef damage, or when algal growth is not controlled by herbivorous fish, provide increased potential habitat for Gambierdiscus growth that might increase the risk of ciguatera [4]. Despite extensive research, we know little about the ecology and the environmental factors that cause the blooms of the ciguatera caustive organisms, nor do we understand the role (if any) of other dinoflagellate genera including Ostreopsis (palytoxin producers) and Prorocentrum (okadaic acid and dinophysistoxins producers) or marine cyanobacteria [5]. Presently, ciguatoxin can only be detected in fish and Gambierdiscus in specialized labs, and diagnosis in humans is based almost exclusively on symptoms associated with the recent consumption of a potential ciguateric fish; factors that hamper its effective management and highlight important research needs [1], [2]. A number of factors have been associated with ciguatera cases and the presence of ciguatoxic dinoflagellates. Military activities causing coral reef damage in the Pacific, including from World War II, and nuclear test explosion programs, have been linked with outbreaks and changing incidence of ciguatera in some locations [6]. The prevalence of ciguatera in the South Pacific increases dramatically where average sea surface temperatures are at least 28 to 29°C [7]. Elevated sea surface temperatures associated with global warming are believed to already be exacerbating the extent and the range of ciguatera [8], . Reportedly, ciguatera occurrences are most prevalent in the warmest regions of the Caribbean, and all indigenous ciguatera cases have occurred where annual average temperatures are >25°C [4]. Nutrient enrichment and warming sea surface temperatures have been shown to stimulate Gambierdiscus growth which results in higher cell densities [10]. Also, benthic dinoflagellate species, including those of the genera Gambierdiscus, might have extended biogeographical ranges, induced by human activity. For example, benthic dinoflagellates are likely to be able to colonize previously unoccupied locations through transport in ship ballast [11]. Certain species of Gambierdiscus has now been found to be highly ciguatoxic compared to the other species [12], and blooms of these species are likely to contribute most to ciguatera risk. Given changes in global climate patterns, increased degradation of coastal marine environments through coastal development and land run-off, and increased exploitation of coastal marine resources, the incidence of ciguatera cases is predicted to continue to increase in the future [4], [13]. Therefore, we hypothesized that ciguatera incidence is an increasing human health and ecological concern across the PICTs. To test this hypothesis, we report on changes in ciguatera incidence across the Pacific, and the social consequences of changing ciguatera incidence by comparing two 11 year periods of data: 1973–1983 vs 1998–2008.
  To obtain the ciguatera records for the period of 1998 to 2008, we first contacted the Secretariat of the Pacific Community (SPC), Division of Fisheries, Aquaculture and Marine Ecosystems (FAME) to obtain the list of institutions responsible for maintaining ciguatera records within PICTs. We considered these repositories were comaparable to the data collection repositories used in the Lewis et al. study [14]. The questionnaire (Supporting Information S1) was sent by email to the institutions in October 2009. Updates on the returning of the questionnaires were sent to PICTs on four occasions over the period, and questionnaires were returned from the PICTs up until April 2010. The questionnaire was developed by the co-authors in collaboration with the PICTs. The questionnaire included questions and definitions from prior ciguatera studies to provide consistency of data gathering and allow comparison across studies. The 3 key sections of the questionnaire collected information on: 1) Temporal incidence of ciguatera; 2) Environmental disturbance, to examine if coral reef condition and occurrence of coral bleaching and cyclones might influence ciguatera incidence (these data were considered purely speculative on the part of the respondent); and 3) Social consequences of ciguatera including changing diet and associated medical conditions, proactive and reactive management of ciguatera, and the desire for external assistance in response to ciguatera.
  The reported cases for the recent 11 year period showed high levels of inter-year variability within and between PICTs. In Fiji, Kiribati and French Polynesia, more cases occurred at the start of the period. Annual reported cases peaked around the middle of the period at Cook Islands, Marshall Islands, Tokelau, Mariana' s, and Hawaii. Reported cases in Vanuatu peaked towards the later part of the 11 year period and since 2005, Fiji experienced an increase in the number of ciguatera cases. Finally, Palau, Hawaii, Guam, Samoa, Wallis and Futuna, and Nauru all had relatively consistent incidence rates of under 5/100,000 (Table 1). Additional data relating to ciguatera incidence within PICT archipelagos are presented in Table 2. Within the 35 year period (1973–2008), including the study by Lewis [14] and this study, there was a clear overall increase in CPF incidence; however, the results show inter-PICT incidence variability between the two time periods (Figure 1). Cook Islands, Vanuatu, Fiji, Tokelau, Marshall Islands, Niue, Tonga, and Palau all have increased ciguatera incidence (Table 3). Others have shown a decrease in ciguatera incidence in comparison to the other PICTs (such as Tuvalu and New Caledonia). From 1973–1983, only four nations demonstrated a ciguatera incidence over 300/100,000; now seven nations have an incidence over this value. Fiji now outranks French Polynesia as the nation with the highest number of ciguatera cases. Previously only four nations had over 2,000 ciguatera cases; recently six nations reported ciguatera cases over this value. Fiji, French Polynesia, Vanuatu, Kiribati, Cook Islands, and Tokelau all demonstrated an increase in the number of ciguatera cases; New Caledonia, Tuvalu and Guam showed a decrease in the number of cases. Statistical analysis of temporal change in ciguatera incidence showed varied results. There was no statistically significant difference between 1973–1983 mean incidence and 1998–2008 mean incidence across PICTs (p = 0. 949), comparing all PICTs (except the State of Hawaii which was not presented by Lewis [14]) using paired t-test (Table 4). However, there was a highly significant difference in mean incidence, between the two time periods when comparing mean incidence across years (p = 0. 002), using independent-sample t-test. Linear regression analysis of annual mean incidence from 1973 to 2008 was also statistically significant (p = 0. 005) despite high inter-year variability. The rate ratio (1998–2008 mean annual incidence/1973–1983 mean annual incidence) was 1. 60; therefore, there was a 60% increase in the mean annual incidence from the earlier period to the more recent period. Hawaii, North Marianas, Marshall Islands, and Palau were omitted for the independent sample t-test, regression analysis and the rate ratio due to data limitations (Table 1). Of the 18 PICTs in this study, 11 reported on all (i. e. coral bleaching, cyclone incidence and perceived reef condition), whilst New Caledonia reported only on coral bleaching (Table 5). All three environmental disturbance types were positively related to ciguatera incidence. However, there was no statistically significant correlation between mean annual ciguatera incidence and occurrence of bleaching (p = 0. 20), cyclone incidence (p = 0. 17) or perceived coral reef condition (p = 0. 57). Responses to questions relating to the social consequences of ciguatera demonstrated that the incidence of ciguatera might be having a negative impact on PICT communities. Seven PICTs reported changes in diet as a result of ciguatera, whilst six PICTs reported that there was no change in diet as a result of ciguatera. Also, seven PICTs reported secondary medical problems (such as diabetes due to dietary changes) as a result of ciguatera. Five PICTs reported both a change in diet and secondary medical problems as a result of ciguatera. Seven PICTs reported taking reactive management measures (such as closure of fishing areas) to manage ciguatera outbreaks, whilst four PICTs reported taking no reactionary measures. Four PICTs reported that preventative management (such as catchment management) was occurring, whilst four PICTs reported that there was no preventative management. Eight PICTs reported that additional support would improve the management of ciguatera, whilst four reported that it would not. There was a positive and marginally significant relationship between changing diet and per capita incidence of ciguatera (p = 0. 06), and secondary medical problems and per capita incidence of ciguatera (p = 0. 08) (Table 6). Neither reactive nor proactive management was correlated with per capita incidence of ciguatera. However, perceived improvement in management as a result of increased support was positively correlated with per capita incidence of ciguatera (p = 0. 013). There was no significant difference (p≤0. 05) in per capita incidence of ciguatera between nations that did and did not respond to questions on the social consequences of ciguatera.
  It is possible that the unusual collaboration of the majority of the PICTs in this project might have contributed to the observed increased reporting of ciguatera (as well as other unidentified infrastructure changes), and thus a possible reporting bias for the more recent 1998–2008 data when compared with the 1973–83. However, these data represent a decade of reporting during a period of competing public health interests and lack of surveillance resources for ciguatera in the PICTs. As with all ciguatera studies where the case definition does not include active confirmation of ciguatoxin in the fish consumed, there is the possibility of the misclassification of reported cases; however, this situation has not changed from the 1970s [2]. It is also beyond the scope of this study to speculate on the causes of the high spatial and temporal variability of ciguatera [4]. This study, instead, aimed to demonstrate that ciguatera is still of major and possibly growing concern in the region. Addressing ciguatera will require significant investment in research and continuing education campaigns. If the suspected disturbances (including coral bleaching, cyclones, shipwrecks, and port facilities) are major causes of ciguatera outbreaks, then it is likely that the general temporal pattern of increased outbreaks will continue in the region, and be a far more expensive concern in the future, if our understanding of, and response to, ciguatera is not extensively improved. Despite over 50 years of ciguatera research in the Pacific, no comprehensive region-wide action has occurred to better manage ciguatera. Based on this study, an estimated 500,000 persons might have contracted ciguatera in the last 35 years, corresponding to a lifetime prevalence of 25%. It is remarkable that ciguatera has largely been ignored by the PICT national governments, with only two nations having an ongoing monitoring program and only one nation having a small unit devoted to researching ciguatera (Toxic Micro-algae Unit of the Institut Louis Malarde, French Polynesia). Given the rapidly changing physical environment (including global warming, extreme weather, and coral reef degradation) as well as the dependence of local populations upon fish for their physical and cultural survival, research into improved disease treatment and toxin detection, and a better understanding of the environmental factors contributing to ciguatera, are required to help reduce the likely growing adverse impacts of ciguatera.
summary: Ciguatera fish poisoning occurs throughout the tropics. After consuming contaminated coral reef fish, people report a range of acute neurologic, gastrointestinal, and cardiac symptoms, with some experiencing chronic neurologic symptoms lasting weeks to months. Ciguatera is largely caused by toxins from benthic microalgae of the genera Gambierdiscus that are bioaccumulated in reef fish through the marine food chain. Unfortunately, the true extent of illness and its impact on human communities and ecosystems are still not well understood. Using data gathered from Health and Fisheries Authorities of the Pacific Island Countries and Territories we identified a 60% increase in the annual incidence of ciguatera from 1988–2008 to 1973–1983 and estimate over 500,000 Pacific islanders might have suffered from ciguatera in their lifetime. The incidence of ciguatera is expected to continue to rise in conjunction with continued reef degradation and global warming, with greatest impact likely to be experienced in the developing PICTs and potentially the archipelagoes of southeast Asia. Despite this threat, little funding is available for research that might lead to better management of the problem either locally, regionally or globally.
keywords: public health and epidemiology
  epidemiology
  environmental epidemiology
  biology
  population biology
title: Ciguatera Fish Poisoning in the Pacific Islands (1998 to 2008)