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Food Contamination PART 1 FOODBORNE and MICROBIAL TOXINS COPYRIGHTED MATERIAL PART 1 FOODBORNE and MICROBIAL TOXINS I Chemical Contamination and Additives 5 15 Clostridium botulinum by Cyrus Rangan, MD, FAAP (Botulism) 103 1 Food Contamination 5 16 Clostridium perfringens 114 2 Food Additives and Sensitivities 22 17 Escherichia coli 120 18 Listeria monocytogenes 133 II Staples and Spices 34 19 Salmonella 141 3 Akee Fruit and Jamaican Vomiting Sickness 20 Shigella Species (Blighia sapida Köenig) 34 (Shiga Enterotoxins) 150 4 Cinnamon 21 Staphylococcus aureus 156 (Cinnamomum Species) 39 22 Streptococcus Species 162 5 Cyanogenic Foods (Cassava, Fruit Kernels, and 23 Vibrio Species 167 Cycad Seeds) 44 24 Yersinia enterocolitica 174 6 Cycad Seeds and Chronic Neurologic Disease B Other Microbes 181 (Cycas Species) 54 25 Cyanobacteria 181 7 Djenkol Bean 26 Protozoa and Intestinal Parasites 191 [Archidendron jiringa (Jack) I. C. Nielsen] 59 27 Gastrointestinal Viruses 202 8 Grass Pea and Neurolathyrism IV Seafood 212 (Lathyrus sativus L.) 62 28 Amnesic Shellfi sh Poisoning and 9 Nutmeg Domoic Acid 212 (Myristica fragrans Houtt.) 67 29 Azaspiracid Shellfi sh Poisoning 10 Pepper and Capsaicin and Azaspiracid Toxins 218 (Capsicum and Piper Species) 71 30 Diarrhetic Shellfi sh Poisoning and 11 Potatoes, Tomatoes, and Solanine Toxicity Okadaic Acid 222 (Solanum tuberosum L., Solanum lycopersicum L.) 77 31 Neurotoxic Shellfi sh Poisoning and Brevetoxins 227 12 Rhubarb and Oxalosis (Rheum Species) 84 32 Paralytic Shellfi sh Poisoning and Saxitoxins 231 III Microbes 89 33 Ciguatera Fish Poisoning and Ciguatoxins 238 A Bacteria 89 34 Puffer Fish Poisoning and Tetrodotoxin 247 by Cyrus Rangan, MD, FAAP 35 Red Whelk and Tetramine 253 13 Bacillus cereus 89 36 Scombroid Fish, Scombrotoxin, and 14 Campylobacter jejuni 96 Histamine 256 I Chemical Contamination and Additives Chapter 1 FOOD CONTAMINATION Cyrus Rangan , MD , FAAP Records of outbreaks of human illness caused by toxic ing. 5 Prominent outbreaks of illnesses associated with contaminants in foods appeared at least several centu- chemical contamination of cooking oils include tri - ries BC, when mad honey poisoning was associated with ortho - cresyl phosphate - induced neuropathy (Morocco, an illness among troops under the command of the 1959), 6 yusho ( “ rice oil disease, ” Japan, 1968), yu - cheng Greek historian and mercenary, Xenophon. 1 One of the ( “ oil disease, ” Taiwan, 1979), toxic oil syndrome (Spain, fi rst recorded foodborne outbreaks of ergotism occurred 1981), and epidemic dropsy (India, 1998). Some con- in Limoges, France during the Capetian Dynasty in 994 taminants are unavoidable in food manufacturing. In AD. 2 The ingestion of rye bread contaminated with the United States, the Food and Drug Administration ergot alkaloids during this epidemic caused the deaths (FDA) imposes “ Current Good Manufacturing Prac- of approximately 20,000 – 50,000 victims. Numerous epi- tices ” (CGMP) on food manufacturers. These manda- sodes of ergotism have occurred throughout history. tory codes enable the FDA to cite food products as unfi t Although ergotism is a possible explanation for the if an unavoidable contaminant poses a risk of harm by bizarre behavior that occurred before and during the violating a standard or action level for that unavoidable Salem Witch Trials of 1692, there is no defi nite evidence contaminant (e.g., afl atoxin). Food products are consid- that ergotism was a contributing factor. 3 In the 1950s, ered adulterated when concentrations of avoidable mining operations in the Toyama region of Japan contaminants (e.g., pesticides) exceed established stan- released cadmium into the Jinzu River. The use of this dards, sometimes prompting food recalls after sale and water for drinking and for irrigation of nearby rice fi elds distribution. resulted in a disease called itai - itai (translation: “ ouch - Metal contaminants such as lead, mercury, arsenic, ouch ” ), manifest by osteoporosis and renal dysfunction and cadmium come from factory emissions, mining primarily in middle - aged women. 4 In the same decade, operations, and metal - containing industrial products numerous neonates born near Minamata Bay, Japan, used in food production. Methyl mercury found in com- developed birth defects and neurological abnormalities mercially sold seafood is deemed an unavoidable con- after pregnant women were exposed to seafood con- taminant because contamination preexists in the raw taminated by methyl mercury released into the bay material; therefore, the contamination does not result from a local factory. A methyl mercury - based fungicide from food processing or distribution. Fish and shellfi sh caused an outbreak of mercury poisoning in Iraq in 1971 acquire methyl mercury primarily from microorganisms after grain seeds treated with the fungicide were inad- that methylate environmental inorganic mercury com- vertently used for food manufacturing instead of plant- pounds released primarily from industrial sources. Medical Toxicology of Natural Substances, by Donald G. Barceloux, MD Copyright © 2008 John Wiley & Sons, Inc. 5 PART 1 FOODBORNE and MICROBIAL TOXINS 400) containing PCBs into the rice oil. This contaminant YUSHO and contained PCB compounds, primarily tetra - chlorinated biphenyls. In 1969, the Study Group initially concluded YU - CHENG that PCBs caused yusho. 9 However, a lack of similar symptoms (besides chloracne) in PCB workers who had signifi cantly higher tissue burdens (mean blood PCB H I S T O R Y level: 45 ppb) contradicted this conclusion. Furthermore, the dermatological lesions could not be reproduced in animals following the oral administration of PCB com- The fi rst known case of yusho (rice oil disease) involved pounds or by Kanechlor 400, and the severity of the a 3 - year - old girl in northern Kyushu, Japan, who had an clinical features of yusho did not correlate to serum acute onset of an acneiform rash (chloracne) in June, concentrations of PCB compounds. Therefore, other 1968. Her family members, followed by other familial compounds (e.g., polychlorinated dibenzofurans) in the clusters, presented to a single clinic with complaints of adulterated rice oil probably contributed to the devel- acneiform rash, hyperpigmentation, and eye discharge opment of yusho. 10,11 over the next 2 months. By January 1969, 325 cases were reported. After a small minority of patients initially Yu - cheng identifi ed rice oil as the causative agent of yusho, Kyushu University convened the Study Group for Yusho to As with the yusho incident, the suspected causative investigate yusho; about 2,000 affl icted patients were agents of yu - cheng were PCDFs rather than PCBs. 12 subsequently identifi ed. The clinical features of yusho Contamination of the cooking oil occurred when PCBs included fatigue, headache, cough, abdominal pain, used for the indirect heating of rice - bran oil leaked peripheral numbness, hepatomegaly, irregular menstrual into the cooking oil. Repeated heating of the partially cycles, nail deformities, and hypersecretion of sebaceous degraded PCBs produced PCDFs, as well as polychlori- glands. A fi eld survey of canned rice oil associated the nated terphenyl and polychlorinated quaterphenyl disease with the use of “ K Rice Oil ” produced or shipped compounds. 13 by the K Company on February 5 – 6, 1968. 7 The yu - cheng epidemic involved over 2,000 individuals in Food Processing Taiwan in 1979, when an accidental leakage of thermal exchange fl uid resulted in the contamination of rice - High temperatures ( > 200 ° C) in dielectric thermal bran oil with polychlorinated biphenyls (PCBs), diben- exchange fl uid during the deodorization step of oil refi n- zofurans (PCDFs), and quaterphenyls (PCQs). 8 The ing contributed to the development of yusho and yu - clinical features of yu - cheng and yusho were similar. cheng by degrading PCBs in the contaminated rice oil to PCDFs, PCDDs (polychlorinated dibenzo dioxins), EXPOSURE and PCQs (polychlorinated quaterphenyls). 14 Source DOSE RESPONSE Polychlorinated biphenyls (PCBs) and polychlorinated Exposure to toxic contaminants in the rice oil from the dibenzofurans (PCDFs) are thermal heat exchanger yusho and yu - cheng epidemics was assessed by record- compounds used in food processing machinery. Leakage ing the lot numbers of purchased oil containers and of these compounds into rice oils during manufacturing comparison of the volume of oil purchased to the volume led to the yusho and yu - cheng outbreaks. of oil remaining in the containers retrieved from affected households. Consumption of the contaminated rice oil by household members was estimated by proportional Yusho distribution to each family member. Positive relation- Epidemiological studies revealed that 95.7% ( p < 0.01) ships were observed between estimated individual oil of surveyed patients recalled consumption of rice oil consumption and incidences of yusho and yu - cheng. 15,16 from K Company in Western Japan. 7 A case - control The mean concentrations of PCBs, polychlorinated qua- study revealed rice oil as the only associated etiologic terphenyls (PCQs), and PCDFs in fi ve samples of con- factor, and a cohort study demonstrated a 64% risk of taminated cooking oil from the yu - cheng outbreak were yusho in K rice oil consumers compared with no risk for 62 ppm, 20 ppm, and 0.14 ppm, respectively. 17 The conge- nonexposed individuals. 7 Food engineers confi rmed the ners of these compounds were similar in the cooking leakage of dielectric thermal exchange fl uid (Kanechlor oils from these two
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