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Toxins
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Ciguatoxins 2022–2023
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Ciguatoxins 2022–2023

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Marine and Freshwater Toxins".

Deadline for manuscript submissions: closed (20 September 2023) | Viewed by 19066

Special Issue Editors

Dr. Panagiota Katikou

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Guest Editor
Hellenic Agricultural Organization—DIMITRA, Veterinary Research Institute of Thessaloniki, Department of Hy-giene and Technology of Food of Animal Origin and Toxicology, 57001 Thermi, Greece
Interests: marine biotoxins; phycotoxins; harmful algal blooms; toxic pufferfish; emerging marine toxins; tetrodotoxins; ciguatoxins; lipophilic toxins; toxic episodes management; phycotoxins regulatory monitoring; marine toxins analysis; mouse bioassay; liquid chromatography mass spectrometry
Special Issues, Collections and Topics in MDPI journals
Dr. Marie-Yasmine Dechraoui Bottein

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Guest Editor
Université Côte d’Azur, CNRS, UMR 7035 ECOSEAS, Nice, France
Interests: food safety; food security; sustainable development; harmful algal blooms; contaminants; risk management; capacity building; marine biotoxins
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Ciguatoxins (CTXs), which are responsible for Ciguatera fish poisoning (CFP), are liposoluble toxins produced by microalgae of the genera Gambierdiscus and Fukuyoa. With an estimated number of cases exceeding 50,000 per year worldwide, some fatal, CFP is the most common non-bacterial illness associated with seafood. Until recently, CFP intoxications were perceived as endemic to (sub)tropical regions of the Pacific and Indian Ocean and the Caribbean Sea, but they are nowadays responsible for intoxications in other places around the world. In particular, in Europe, intoxications occur due to both consumption of imported ciguatoxin-contaminated seafood from endemic areas, and consumption of ciguatoxin-contaminated seafood from certain areas of Macaronesia, such as Azores, the Madeira Islands (Portugal), and the Canary Islands (Spain).

The presence of CTXs in fish can be detected via screening methods, such as mouse bioassays, in vitro cell tests, and receptor binding assays, and confirmed using mass-spectrometry-based analyses. However, the shortage of commercially available reference materials clearly indicates a challenge for marine toxins research. The increased presence of CTXs, combined with their occurrence in new latitudes and the contribution of climate change, is raising global concern. In this context, further investigations regarding CTX presence and origin in aquatic environments, the development of more sophisticated analysis methods, additional data on human intoxication incidents and the toxicological potency of CTX analogues, as well as potential mitigation/regulatory management measures are considered to be extremely important.

This Special Issue aims to focus on new information and scientific evidence mainly with regard to: (i) CTX occurrence in aquatic environments, with an emphasis on edible aquatic organisms; (ii) analysis methods for the determination of CTXs; (iii) advances regarding CTX-producing organisms; (iv) environmental factors involved in the presence of CTXs; and (v) the assessment of public health risks related to the presence of CTXs, as well as risk management and mitigation strategies. Studies addressing any other questions of relevance or reviews related to CTXs are also considered to be of interest and welcome for submission.

Dr. Panagiota Katikou
Dr. Marie-Yasmine Dechraoui Bottein
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a double-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Toxins is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • ciguatera fish poisoning (CFP)
  • ciguatoxins
  • climate change
  • Gambierdiscus spp.
  • Fukuyoa spp.
  • analytical methods
  • risk management
  • analogues
  • toxicology
  • occurrence and epidemiology

Related Special Issues

Published Papers (8 papers)

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Research

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20 pages, 1295 KiB  
Article
Model of the Origin of a Ciguatoxic Grouper (Plectropomus leopardus)
by Michael J. Holmes and Richard J. Lewis
Toxins 2023, 15(3), 230; https://doi.org/10.3390/toxins15030230 - 21 Mar 2023
Cited by 5 | Viewed by 1623
Abstract
Published data were used to model the transfer of ciguatoxins (CTX) across three trophic levels of a marine food chain on the Great Barrier Reef (GBR), Australia, to produce a mildly toxic common coral trout (Plectropomus leopardus), one of the most [...] Read more.
Published data were used to model the transfer of ciguatoxins (CTX) across three trophic levels of a marine food chain on the Great Barrier Reef (GBR), Australia, to produce a mildly toxic common coral trout (Plectropomus leopardus), one of the most targeted food fishes on the GBR. Our model generated a 1.6 kg grouper with a flesh concentration of 0.1 µg/kg of Pacific-ciguatoxin-1 (P-CTX-1 = CTX1B) from 1.1 to 4.3 µg of P-CTX-1 equivalents (eq.) entering the food chain from 0.7 to 2.7 million benthic dinoflagellates (Gambierdiscus sp.) producing 1.6 pg/cell of the P-CTX-1 precursor, P-CTX-4B (CTX4B). We simulated the food chain transfer of ciguatoxins via surgeonfishes by modelling Ctenochaetus striatus feeding on turf algae. A C. striatus feeding on ≥1000 Gambierdiscus/cm2 of turf algae accumulates sufficient toxin in <2 days that when preyed on, produces a 1.6 kg common coral trout with a flesh concentration of 0.1 µg/kg P-CTX-1. Our model shows that even transient blooms of highly ciguatoxic Gambierdiscus can generate ciguateric fishes. In contrast, sparse cell densities of ≤10 Gambierdiscus/cm2 are unlikely to pose a significant risk, at least in areas where the P-CTX-1 family of ciguatoxins predominate. The ciguatera risk from intermediate Gambierdiscus densities (~100 cells/cm2) is more difficult to assess, as it requires feeding times for surgeonfish (~4–14 days) that overlap with turnover rates of turf algae that are grazed by herbivorous fishes, at least in regions such as the GBR, where stocks of herbivorous fishes are not impacted by fishing. We use our model to explore how the duration of ciguatoxic Gambierdiscus blooms, the type of ciguatoxins they produce, and fish feeding behaviours can produce differences in relative toxicities between trophic levels. Our simple model indicates thresholds for the design of risk and mitigation strategies for ciguatera and the variables that can be manipulated to explore alternate scenarios for the accumulation and transfer of P-CTX-1 analogues through marine food chains and, potentially, for other ciguatoxins in other regions, as more data become available. Full article
(This article belongs to the Special Issue Ciguatoxins 2022–2023)
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23 pages, 3199 KiB  
Article
Local and Traditional Ecological Knowledge of Fish Poisoning in Fiji
by Jimaima Veisikiaki Lako, Sereima Naisilisili, Veikila C. Vuki, Nanise Kuridrani and Dominic Agyei
Toxins 2023, 15(3), 223; https://doi.org/10.3390/toxins15030223 - 16 Mar 2023
Viewed by 3654
Abstract
Fish poisoning (FP) affects human health, trade and livelihood in Fiji, where management has depended mainly on traditional ecological knowledge (TEK). This paper investigated and documented this TEK through a 2-day stakeholder workshop, group consultation, in-depth interviews, field observations, and analyses of survey [...] Read more.
Fish poisoning (FP) affects human health, trade and livelihood in Fiji, where management has depended mainly on traditional ecological knowledge (TEK). This paper investigated and documented this TEK through a 2-day stakeholder workshop, group consultation, in-depth interviews, field observations, and analyses of survey data from the Ministry of Fisheries, Fiji. Six TEK topics were identified and classified as preventative and treatment options. The preventive approach involves identifying toxic reef fishes, the spawning season of edible seaworms, hotspot areas of toxic fishes, folk tests, and locating and removing toxic organs. For example, 34 reef fish species were identified as toxic. The FP season was associated with the spawning of balolo (edible seaworm) and the warmer months of October to April (cyclone seasons). Two well-known toxic hotspots associated with an abundance of bulewa (soft coral) were identified. Folk tests and locating and removing toxic fish organs are also practised for moray eels and pufferfish. At the same time, various locally available herbal plants are used to treat FP as the second line of defence. The TEK collated in this work can help local authorities better identify the sources of toxicity, and applying TEK preventive measures could stem the tide of fish poisoning in Fiji. Full article
(This article belongs to the Special Issue Ciguatoxins 2022–2023)
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8 pages, 1252 KiB  
Article
Bimodal Cell Size and Fusing Cells Observed in a Clonal Culture of the Ciguatoxin-Producing Benthic Dinoflagellate Gambierdiscus (WC1/1)
by Michael J. Holmes and Richard J. Lewis
Toxins 2022, 14(11), 767; https://doi.org/10.3390/toxins14110767 - 07 Nov 2022
Cited by 1 | Viewed by 1153
Abstract
Cells in a clonal culture of the WC1/1 strain of Gambierdiscus that produced ciguatoxin and maitotoxin-3 were observed to spontaneously fuse during the light phase of culture growth. Cells in the process of fusion were indistinguishable from other cells under the light microscope, [...] Read more.
Cells in a clonal culture of the WC1/1 strain of Gambierdiscus that produced ciguatoxin and maitotoxin-3 were observed to spontaneously fuse during the light phase of culture growth. Cells in the process of fusion were indistinguishable from other cells under the light microscope, except that at least one (often both) of the fusing cells displayed an extendible, finger-like protrusion (presumed peduncle) arising from near the sulcul region. Fusion started with one of the cells turning 90° to place the planes of the girdles approximately at right angles to each other, and movement of the transverse flagella ceased in both cells, or in the cell seen in girdle (lateral) view. The cell in girdle view appeared to fuse into the theca of the other cell. The cell that had turned 90° often rounded up and become egg shaped (obovoid) during early fusion. Fusion can be quick (<10 min) or can take more than an hour. We saw no evidence of the theca being shed during fusion. Measurement of the dorsoventral and transdiameters revealed a wide range for cell sizes that were distributed as a bimodal population in the clonal culture. This bimodal cell population structure was maintained in clonal cultures reisolated from a small or large cell from the original WC1/1 culture. Cellular production of ciguatoxins by the WC1/1 clone increased during the first two years in culture with a corresponding decrease in production of maitotoxin-3, but this inverse relationship was not maintained over the following ~1.5 years. Full article
(This article belongs to the Special Issue Ciguatoxins 2022–2023)
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11 pages, 602 KiB  
Article
Clinical Characteristics of Ciguatera Poisoning in Martinique, French West Indies—A Case Series
by Dabor Résière, Jonathan Florentin, Hossein Mehdaoui, Zakaria Mahi, Papa Gueye, Didier Hommel, Jean Pujo, Flaubert NKontcho, Patrick Portecop, Rémi Nevière, Hatem Kallel and Bruno Mégarbane
Toxins 2022, 14(8), 535; https://doi.org/10.3390/toxins14080535 - 03 Aug 2022
Cited by 2 | Viewed by 1977
Abstract
Ciguatera poisoning (CP) is one of the most common causes worldwide of marine poisoning associated with fish consumption from tropical areas. Its incidence is underreported. CP cases seem to increase with grouped cases reported during summer. Exposure to ciguatoxins, toxins responsible for CP [...] Read more.
Ciguatera poisoning (CP) is one of the most common causes worldwide of marine poisoning associated with fish consumption from tropical areas. Its incidence is underreported. CP cases seem to increase with grouped cases reported during summer. Exposure to ciguatoxins, toxins responsible for CP with sodium-channel agonistic, voltage-gated potassium channel blocking, cholinergic, and adrenergic activities, may result in a large spectrum of manifestations. We aimed to describe the clinical characteristics, management, and outcome of CP in Martinique, French West Indies. We conducted an observational retrospective single-center study during six years (October 2012 to September 2018) including all CP patients managed by the prehospital medical services, admitted to the university hospital emergency department, or declared to the regional health agency. A total of 149 CP patients (81 females/63 males; median age, 46 years (interquartile range, 34–61)) were included. Acute features consisted in general (91%; mainly, myalgia pruritus, and asthenia), gastrointestinal (90%; mainly diarrhea, abdominal pain, and nausea), neurological (72%; mainly, paresthesia, dysgeusia, and impairment of hot/cold feeling), and cardiovascular manifestations (22%; bradycardia, hypotension, and heart conduction disorders). Management was supportive. No patient died but symptoms persisted in 40% of the 77 patients with follow-up at day 15. CP was mainly attributed to the ingestion of trevallies (59%), snappers (13%), and king mackerels (8%) with collective contaminations (71%). Unusual fish (tuna, salmon, and spider conchs) were suspected in rare cases. Ingestion of trevallies was associated with significantly higher persistent symptoms (odds ratio, 3.00; 95% confidence interval, (1.20–8.00); p = 0.03). CP incidence was 0.67 cases per 10,000 patient-years in Martinique over the study period. To conclude, CP represents an increasing public health issue in Martinique, as is the case in other Caribbean islands. Patients present usual but possibly life-threatening features. Outcome is excellent despite frequently prolonged manifestations. Full article
(This article belongs to the Special Issue Ciguatoxins 2022–2023)
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11 pages, 685 KiB  
Article
Origin of Ciguateric Fish: Quantitative Modelling of the Flow of Ciguatoxin through a Marine Food Chain
by Michael J. Holmes and Richard J. Lewis
Toxins 2022, 14(8), 534; https://doi.org/10.3390/toxins14080534 - 03 Aug 2022
Cited by 6 | Viewed by 1754
Abstract
To begin to understand the impact of food chain dynamics on ciguatera risk, we used published data to model the transfer of ciguatoxins across four trophic levels of a marine food chain in Platypus Bay, Australia. The data to support this first attempt [...] Read more.
To begin to understand the impact of food chain dynamics on ciguatera risk, we used published data to model the transfer of ciguatoxins across four trophic levels of a marine food chain in Platypus Bay, Australia. The data to support this first attempt to conceptualize the scale of each trophic transfer step was limited, resulting in broad estimates. The hypothetical scenario we explored generated a low-toxicity 10 kg Spanish mackerel (Scomberomorus commerson) with a flesh concentration of 0.1 µg/kg of Pacific-ciguatoxin-1 (P-CTX-1, also known as CTX1B) from 19.5–78.1 µg of P-CTX-1 equivalents (eq.) that enter the marine food chain from a population of 12–49 million benthic dinoflagellates (Gambierdiscus sp.) producing 1.6 × 10−12 g/cell of the P-CTX-1 precursor, P-CTX-4B. This number of Gambierdiscus could be epiphytic on 22–88 kg of the benthic macroalgae (Cladophora) that carpets the bottom of much of Platypus Bay, with the toxin transferred to an estimated 40,000–160,000 alpheid shrimps in the second trophic level. This large number of shrimps appears unrealistic, but toxic shrimps would likely be consumed by a school of small, blotched javelin fish (Pomadasys maculatus) at the third trophic level, reducing the number of shrimps consumed by each fish. The Spanish mackerel would accumulate a flesh concentration of 0.1 µg/kg P-CTX-1 eq. by preying upon the school of blotched javelin and consuming 3.6–14.4 µg of P-CTX-1 eq. However, published data indicate this burden of toxin could be accumulated by a 10 kg Spanish mackerel from as few as one to three blotched javelin fish, suggesting that much greater amounts of toxin than modelled here must at certain times be produced and transferred through Platypus Bay food chains. This modelling highlights the need for better quantitative estimates of ciguatoxin production, biotransformation, and depuration through marine food chains to improve our understanding and management of ciguatera risk. Full article
(This article belongs to the Special Issue Ciguatoxins 2022–2023)
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16 pages, 1906 KiB  
Article
Reductive Amination for LC–MS Signal Enhancement and Confirmation of the Presence of Caribbean Ciguatoxin-1 in Fish
by Fedor Kryuchkov, Alison Robertson, Elizabeth M. Mudge, Christopher O. Miles, Soetkien Van Gothem and Silvio Uhlig
Toxins 2022, 14(6), 399; https://doi.org/10.3390/toxins14060399 - 09 Jun 2022
Cited by 3 | Viewed by 2329
Abstract
Ciguatera poisoning is a global health concern caused by the consumption of seafood containing ciguatoxins (CTXs). Detection of CTXs poses significant analytical challenges due to their low abundance even in highly toxic fish, the diverse and in-part unclarified structures of many CTX congeners, [...] Read more.
Ciguatera poisoning is a global health concern caused by the consumption of seafood containing ciguatoxins (CTXs). Detection of CTXs poses significant analytical challenges due to their low abundance even in highly toxic fish, the diverse and in-part unclarified structures of many CTX congeners, and the lack of reference standards. Selective detection of CTXs requires methods such as liquid chromatography coupled to tandem mass spectrometry (LC–MS/MS) or high-resolution MS (LC–HRMS). While HRMS data can provide greatly improved resolution, it is typically less sensitive than targeted LC–MS/MS and does not reliably comply with the FDA guidance level of 0.1 µg/kg CTXs in fish tissue that was established for Caribbean CTX-1 (C-CTX-1). In this study, we provide a new chemical derivatization approach employing a fast and simple one-pot derivatization with Girard’s reagent T (GRT) that tags the C-56-ketone intermediate of the two equilibrating C-56 epimers of C-CTX-1 with a quaternary ammonium moiety. This derivatization improved the LC–MS/MS and LC–HRMS responses to C-CTX-1 by approximately 40- and 17-fold on average, respectively. These improvements in sensitivity to the GRT-derivative of C-CTX-1 are attributable to: the improved ionization efficiency caused by insertion of a quaternary ammonium ion; the absence of adduct-ions and water-loss peaks for the GRT derivative in the mass spectrometer, and; the prevention of on-column epimerization (at C-56 of C-CTX-1) by GRT derivatization, leading to much better chromatographic peak shapes. This C-CTX-1–GRT derivatization strategy mitigates many of the shortcomings of current LC–MS analyses for C-CTX-1 by improving instrument sensitivity, while at the same time adding selectivity due to the reactivity of GRT with ketones and aldehydes. Full article
(This article belongs to the Special Issue Ciguatoxins 2022–2023)
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17 pages, 1103 KiB  
Article
Ciguatoxin Detection in Flesh and Liver of Relevant Fish Species from the Canary Islands
by María José Ramos-Sosa, Natalia García-Álvarez, Andres Sanchez-Henao, Freddy Silva Sergent, Daniel Padilla, Pablo Estévez, María José Caballero, José Luís Martín-Barrasa, Ana Gago-Martínez, Jorge Diogène and Fernando Real
Toxins 2022, 14(1), 46; https://doi.org/10.3390/toxins14010046 - 09 Jan 2022
Cited by 11 | Viewed by 3592
Abstract
The Canary Islands are a ciguatoxin (CTX) hotspot with an established official monitoring for the detection of CTX in fish flesh from the authorised points of first sale. Fish caught by recreational fishermen are not officially tested and the consumption of toxic viscera [...] Read more.
The Canary Islands are a ciguatoxin (CTX) hotspot with an established official monitoring for the detection of CTX in fish flesh from the authorised points of first sale. Fish caught by recreational fishermen are not officially tested and the consumption of toxic viscera or flesh could lead to ciguatera poisoning (CP). The objectives of this study were to determine the presence of CTX-like toxicity in relevant species from this archipelago, compare CTX levels in liver and flesh and examine possible factors involved in their toxicity. Sixty amberjack (Seriola spp.), 27 dusky grouper (Epinephelus marginatus), 11 black moray eels (Muraena helena) and 11 common two-banded seabream (Diplodus vulgaris) were analysed by cell-based assay (CBA) and Caribbean ciguatoxin-1 (C-CTX1) was detected by liquid chromatography mass spectrometry (LC-MS/MS) in all these species. Most of the liver displayed higher CTX levels than flesh and even individuals without detectable CTX in flesh exhibited hepatic toxicity. Black moray eels stand out for the large difference between CTX concentration in both tissues. None of the specimens with non-toxic liver showed toxicity in flesh. This is the first evidence of the presence of C-CTX1 in the common two-banded seabream and the first report of toxicity comparison between liver and muscle from relevant fish species captured in the Canary Islands. Full article
(This article belongs to the Special Issue Ciguatoxins 2022–2023)
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Review

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15 pages, 1771 KiB  
Review
A 15-Year Retrospective Review of Ciguatera in the Madeira Islands (North-East Atlantic, Portugal)
by Pedro Reis Costa, Catarina Churro, Susana Margarida Rodrigues, Bárbara Frazão, Miguel Barbosa, Lia Godinho, Lucía Soliño, Viriato Timóteo and Neide Gouveia
Toxins 2023, 15(11), 630; https://doi.org/10.3390/toxins15110630 - 27 Oct 2023
Cited by 1 | Viewed by 1579
Abstract
The first ciguatera fish poisoning (CFP) in Portugal dates from 2008 when 11 people reported CFP symptoms after consuming a 30 kg amberjack caught around the Selvagens Islands (Madeira Archipelago). Since then, 49 human poisonings have been reported. The emergence of a new [...] Read more.
The first ciguatera fish poisoning (CFP) in Portugal dates from 2008 when 11 people reported CFP symptoms after consuming a 30 kg amberjack caught around the Selvagens Islands (Madeira Archipelago). Since then, 49 human poisonings have been reported. The emergence of a new threat challenged scientists and regulators, as methods for toxic microalgae analyses and ciguatoxin (CTX) detection were not implemented. To minimise the risk of ciguatera, the Madeira Archipelago authorities interdicted fisheries in Selvagens Islands and banned the capture of amberjacks weighing more than 10 kg in the entire region of Madeira Archipelago. The accurate identification and quantification of the benthic toxin-producing algae species spreading to new areas require efforts in terms of both microscopy and molecular techniques. Two ciguatera-causing dinoflagellates, Gambierdiscus excentricus and Gambierdiscus australes, were identified in the Madeira Island and Selvagens sub-archipelago, respectively. Regarding the CTX analysis (N2a cell-based assay and LC-MS) in fish, the results indicate that the Selvagens Islands are a ciguatera risk area and that fish vectoring CTX are not limited to top predator species. Nevertheless, advances and improvements in screening methods for the fast detection of toxicity in seafood along with certified reference material and sensitive and selective targeted analytical methods for the determination of CTX content are still pending. This study aims to revise the occurrence of ciguatera cases in the Madeira Archipelago since its first detection in 2008, to discuss the risk management strategy that was implemented, and to provide a summary of the available data on the bioaccumulation of CTX in marine fish throughout the marine food web, taking into consideration their ecological significance, ecosystem dynamics, and fisheries relevance. Full article
(This article belongs to the Special Issue Ciguatoxins 2022–2023)
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