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Foodborne Disease
Handbook
FOODBORNE DISEASE HANDBOOK
Editor-in-Chief
Y. H. Hui
Volume Editors
J. Richard Gorham
David Kitts
K. D. Murrell
Wai-Kit Nip
Merle D. Pierson
Syed A. Sattar
R. A. Smith
David G. Spoerke, Jr.
Peggy S. Stanfield
edited by
Y. H. Hui
Science Technology System
West Sacramento, California
Syed A. Sattar
University of Ottawa
Ottawa, Ontario, Canada
K. D. Murrell
U.S. Department of Agriculture
Beltsville, Maryland
Wai-Kit Nip
University of Hawaii at Manoa
Honolulu, Hawaii
Peggy S. Stanfield
Dietetics Resources
Twin Falls, Idaho
This book contains information obtained from authentic and highly regarded sources. Reasonable efforts have been made to publish
reliable data and information, but the author and publisher cannot assume responsibility for the validity of all materials or the
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Introduction to the Handbook
The Foodborne Disease Handbook, Second Edition, Revised and Expanded, could not be
appearing at a more auspicious time. Never before has the campaign for food safety been
pursued so intensely on so many fronts in virtually every country around the world. This
new edition reflects at least one of the many aspects of that intense and multifaceted
campaign: namely, that research on food safety has been very productive in the years
since the first edition appeared. The Handbook is now presented in four volumes instead
of the three of the 1994 edition. The four volumes are composed of 86 chapters, a 22%
increase over the 67 chapters of the first edition. Much of the information in the first
edition has been carried forward to this new edition because that information is still as
reliable and pertinent as it was in 1994. This integration of the older data with the latest
research findings gives the reader a secure scientific foundation on which to base important
decisions affecting the public's health.
We are not so naive as to think that only scientific facts influence decisions affecting
food safety. Political and economic factors and compelling national interests may carry
greater weight in the minds of decision-makers than the scientific findings offered in this
new edition. However, if persons in the higher levels of national governments and interna-
tional agencies, such as the Codex Alimentarius Commission, the World Trade Organiza-
tion, the World Health Organization, and the Food and Agriculture Organization, who
must bear the burden of decision-making need and are willing to entertain scientific find-
ings, then the information in these four volumes will serve them well indeed.
During the last decade of the previous century, we witnessed an unprecedentedly
intense and varied program of research on food safety, as we have already noted. There
are compelling forces driving these research efforts. The traditional food-associated patho-
gens, parasites, and toxins of forty years ago still continue to cause problems today, and
newer or less well-known species and strains present extraordinary challenges to human
health.
These newer threats may be serious even for the immunocompetent, but for the
immunocompromised they can be devastating. The relative numbers of the immunocom-
promised in the world population are increasing daily. We include here not just those
affected by the human immunodeficiency virus (HIV), but also the elderly; the very young;
the recipients of radiation treatments, chemotherapy, and immunosuppressive drugs; pa-
//'/'
iv Introduction to the Handbook
dents undergoing major invasive diagnostic or surgical procedures; and sufferers of debili-
tating diseases such as diabetes. To this daunting list of challenges must be added numer-
ous instances of microbial resistance to antibiotics.
Moreover, it is not yet clear how the great HACCP experiment will play out on the
worldwide stage of food safety. Altruism and profit motivation have always made strange
bedfellows in the food industry. It remains to be seen whether HACCP will succeed in
wedding these two disparate motives into a unifying force for the benefit of all con-
cerned—producers, manufacturers, retailers, and consumers. That HACCP shows great
promise is thoroughly discussed in Volume 2, with an emphasis on sanitation in a public
eating place.
All the foregoing factors lend a sense of urgency to the task of rapidly identifying
toxins, species, and strains of pathogens and parasites as etiologic agents, and of determin-
ing their roles in the epidemiology and epizootiology of disease outbreaks, which are
described in detail throughout the Foodborne Disease Handbook.
It is very fortunate for the consumer that there exists in the food industry a dedicated
cadre of scientific specialists who scrutinize all aspects of food production and bring their
expertise to bear on the potential hazards they know best. A good sampling of the kinds
of work they do is contained in these four new volumes of the Handbook. And the benefits
of their research are obvious to the scientific specialist who wants to learn even more
about food hazards, to the scientific generalist who is curious about everything and who
will be delighted to find a good source of accurate, up-to-date information, and to consum-
ers who care about what they eat.
We are confident that these four volumes will provide competent, trustworthy, and
timely information to inquiring readers, no matter what roles they may play in the global
campaign to achieve food safety.
Y. H. Hui
J. Richard Gorham
David Kitts
K. D. Murrell
Wai-Kit Nip
Merle D. Pierson
Syed A. Sattar
R. A. Smith
David G. Spoerke, Jr.
Peggy S. Stanfield
Preface
Much of the thought and action surrounding food safety deals with preventing foodborne
bacteria from causing disease—and that is as it should be. But there are other threats that
command our attention. These—the viruses and parasites—take center stage in the second
volume of the Foodborne Disease Handbook, Second Edition, Revised and Expanded.
Viruses play an important role as agents of human diseases, and indeed their relative
significance is increasing as we try to prevent and control the spread of common bacterial
pathogens. The potential for foodborne spread of viruses is also stronger now than ever
because of a combination of many current societal changes. Ongoing changes in demo-
graphics, changing lifestyles, faster and more frequent movement of peoples and goods,
and rapidly expanding global trade in produce have already had a profound impact on the
potential of viruses and other pathogens to spread through foods.
Eight chapters on foodborne viruses, contributed by internationally recognized ex-
perts in their respective fields, represent an overview of the most up-to-date information
in this area. They cover well-known viral pathogens, as well as those that are less well
understood but may acquire greater significance if left unheeded. The chapters, when
considered together, represent a valuable resource on the biology of foodborne viruses,
clinical diagnosis, and medical management as well as laboratory-based identification of
viral infections transmitted through foods, and the epidemiology, prevention, and control
of foodborne spread of viral pathogens. Wherever appropriate, the challenges and difficul-
ties of detecting viruses in foods are highlighted and research needs identified. The guide-
lines for reducing the risk of spread of hepatitis A through foods should be applicable to
many other foodborne pathogens.
It is anticipated that the information presented here will assist researchers, epidemi-
ologists, physicians, public health officials and government regulators, and those in the
food production and marketing business, to become better informed on the human health
impact of foodborne viral infections and to work collectively in making foods safer.
All chapters on parasites from the first edition have been revised and updated. The
addition of a chapter on the occurrence of parasites in seafood completes the overall sub-
ject of foodborne and waterborne diseases transmitted by parasites.
Although Americans are relatively unfamiliar with parasitic infection, three exam-
ples of areas in which diseases have been transmitted by parasites will help us to remember
v
vi Preface
this important subject: northern Taiwan (from consuming raw or undercooked beef), Asian
countries such as Thailand (undercooked pork), and Japan and Hawaii (undercooked sea-
food). Various chapters in this volume provide detailed description of these types of dis-
eases transmitted by parasites.
There is a gradual movement—sometimes voluntary, sometimes mandated—toward
implementation of HACCP principles in all aspects of the food industry, beginning with
production and harvesting and continuing through the various stages of manufacturing,
warehousing, wholesaling, retailing, and serving, until the food eventually reaches the
consumer's plate. However, for the moment, at least, it is in the area of food service that
the application of HACCP principles has reached the highest level of achievement. While
much remains to be done even in the food service sector with regard to the implementation
of HACCP, it will be seen from this second volume of the Foodborne Disease Handbook
that the mechanics of implementation have been worked out and fine-tuned, and that this
accomplishment may now serve as a model and a guide for other facets of the food in-
dustry.
The food industry in general seems to be buying into the HACCP system with an
apparent high level of commitment, and this bodes well for the consumer. But rather than
relaxing vigilance and trusting that HACCP will solve all food safety problems, the food
industry must heighten vigilance and redouble efforts to ensure that HACCP programs
are protected on all sides by a secure fortress of state-of-the-art environmental sanitation.
The editors and contributors to this volume have given researchers, microbiologists,
parasitologists, food-industry managers, food analysts, and HACCP managers a wealth
of information on how to detect and identify foodborne parasites and viral pathogens, how
to investigate the disease outbreaks they cause, and, most importantly, how to prevent
foodborne diseases by the practical application of HACCP principles.
Y. H. Hui
Syed A. Sattar
K. D. Murrell
Wai-Kit Nip
Peggy S. Stanfield
Contents
I. Poison Centers
II. Viruses
4. Rotavirus 99
Syed A. Sattar, V. Susan Springthorpe, and Jason A. Tetro
vii
viii Contents
III. Parasites
Index 497
Contributors
Ann M. Adams Seafood Products Research Center, U.S. Food and Drug Administra-
tion, Bothell, Washington
Hazel Appleton Virus Reference Division, Public Health Laboratory Service, Central
Public Health Laboratory, London, England
William C. Campbell Research Institute for Scientists Emeriti, Drew University, Madi-
son, New Jersey
Michael O. Favorov Hepatitis Branch, Division of Viral and Rickettsial Diseases, Na-
tional Center of Infectious Diseases, Centers for Disease Control and Prevention, Atlanta,
Georgia
ix
x Contributors
I. Poison Centers
3. Aeromonas hydrophila
Carlos Abeyta, Jr., Samuel A. Palumbo, and Gerard N. Stelma, Jr.
5. Brucella
Shirley M. Hailing and Edward J. Young
6. Campylobacter jejuni
Don A. Franco and Charles E. Williams
1. Clostridium botulinum
John W. Austin and Karen L. Dodds
8. Clostridium perfringens
Dorothy M. Wrigley
XI
xii Contents of Other Volumes
9. Escherichia coli
Marguerite A. Neill, Phillip I. Tarr, David N. Taylor, and Marcia Wolf
14. Shigella
Anthony T. Maurelli and Keith A. Lampel
19. Yersinia
Scott A. Minnich, Michael J. Smith, Steven D. Weagant, and Peter Feng
Index
Contents of Other Volumes xiii
I. Poison Centers
4. Alkaloids
R. A. Smith
6. Glycosides
Walter Majak and Michael H. Benn
10. Aspergillus
Zofia Kozakiewicz
12. Fusarium
Walter F. O. Marasas
13. Penicillium
John I. Pitt
xiv Contents of Other Volumes
Index
I. Poison Centers
2. Fish Toxins
Bruce W. Halstead
8. Tetrodotoxin
Joanne S. M. Yoshikawa-Ebesu, Yoshitsugi Hokama, and Tamao Noguchi
12. HACCP, Seafood, and the U.S. Food and Drug Administration
Kim R. Young, Miguel Rodrigues Kamat, and George Perry Hoskin
Index
1
The Role of Poison Centers
in the United States
I. Epidemiology 1
A. AAPCC 2
B. Poison center staff 3
C. Types of calls received 4
D. How calls are handled 5
E. What references are used 6
F. How poison centers are monitored for quality 7
G. Professional and public education programs 7
H. Related professional toxicology organizations 8
I. International AAPPC affiliations 9
J. Toxicology and poison center Web sites 10
II. U.S. Poison Information Centers 10
References 21
I. EPIDEMIOLOGY
1
2 Spoerke
A. AAPCC
1. What Are Poison Centers and the AAPCC?
The group in the United States that is most concerned on a daily basis with potential
poisonings due to household agents, industrial agents, and biologies is the American Asso-
ciation of Poison Control Centers (AAPCC). This is an affiliation of local and regional
centers that provides information concerning all aspects of poisoning and refers patients
to treatment centers. This group of affiliated centers is often supported by local govern-
ment, private funds, and industrial sources.
Poison centers were started in the late 1950s; the first were in the Chicago area.
The idea caught on quickly and at the peak of the movement there were hundreds of
centers throughout the United States. Unfortunately, there were few or no standards as to
what might be called a poison center, the type of staff, hours of operation, or information
resources. One center may have had a dedicated staff of doctors, pharmacist, and nurses
trained specifically in handling poison cases; the next center may just have a book on
toxicology in the emergency room or hospital library. In 1993, the Health and Safety Code
(Section 777.002) specified that a poison center must provide a 24-hour service for public
and health care professionals and meet requirements established by the AAPCC. This
action helped the AAPCC to standardize activities and staffs of the various centers.
The federal government does not fund poison centers, even though for every dollar
spent on poison centers there is a savings of $2 to $9 in unnecessary medical expenses
(1,2). The federal agency responsible for the Poison Prevention Packaging Act is the U.S.
Consumer Product Safety Commission (CPSC). The National Clearinghouse for Poison
Control Centers initially collected data on poisonings and provided information on com-
mercial product ingredients and biologic toxic agents. For several years the National Clear-
inghouse provided product and treatment information to the poison centers that handled
the day-to-day calls.
At first, most poison centers were funded by the hospital in which they were located.
As the centers grew in size and number of calls handled, both city and state governments
look on the responsibility of contributing funds. In recent years the local governments
have found it difficult to fund such operations and centers have had to look to private
industry for additional funding. Government funding may take several forms, either as a
line item on a state budget, as a direct grant, or as moneys distributed on a per-call basis.
Some states with fewer residents may contract with a neighboring state to provide services
to its residents. Some states are so populous that more than one center is funded by the
state. Industrial funding also varies—sometimes as a grant, sometimes as payment for
handling the company's poison or drug information-related calls, sometimes as payment
for collection of data regarding exposure to the company's product.
Every year the AAPCC reports a summary of all kinds of exposures.
2. Regional Centers
As the cost of providing this service has risen, the number of listed centers has dropped
significantly since its peak of 600-plus. Many centers have been combined into regional
organizations. These regional poison centers provide poison information, offer telephone
management and consultation, collect pertinent data, and deliver professional and public
education. Cooperation between regional poison centers and poison treatment facilities is
crucial. The regional poison information center, assisted by local hospitals, should deter-
mine the capabilities of the treatment facilities of the region. They should also have a
Poison Centers and Viral Exposure 3
working relationship with their analytical toxicology, emergency and critical care, medical
transportation, and extracorporeal elimination services. This should be true for both adults
and children.
A "region" is usually determined by state authorities in conjunction with local
health agencies and health care providers. Documentation of these state designations must
be in writing unless a state chooses (in writing) not to designate any poison center or
accepts a designation by other political or health jurisdictions. Regional poison information
centers should serve a population base of greater than 1 million people and must receive
at least 10,000 human exposure calls per year.
The number of certified regional centers in the United States is now under 50. Certi-
fication as a regional center requires the following.
1. Maintenance of a 24 hour-per-day, 365-days-per-year service.
2. Provision of service to both health care professionals and the public.
3. Availability of at least one specialist in poison information in the center at all
times.
4. Having a medical director or qualified designee on call by telephone at all
times.
5. Service should be readily accessible by telephone from all areas in the region.
6. Comprehensive poison information resources and comprehensive toxicology
information covering both general and specific aspects of acute and chronic
poisoning should be available.
7. The center is required to have a list of on-call poison center specialty consul-
tants.
8. Written operational guidelines that provide a consistent approach to evaluation,
follow-up, and management of toxic exposures should be obtained and main-
tained. These guidelines must be approved in writing by the medical director
of the program.
9. There should be a staff of certified professionals manning the phones (at least
one of the individuals on the phone has to be a pharmacist or nurse with 2000
hours and 2000 cases of supervised experience)
10. There should be a 24 hour-per-day physician (board-certified) consultation ser-
vice.
11. The regional poison center shall have an ongoing quality assurance program.
12. Other criteria, determined by the AAPCC, may be established with member-
ship approval.
13. The regional poison information center must be an institutional member in
good standing of the AAPCC. Many hospital emergency rooms still maintain
a toxicology reference such as the POISINDEXS system to handle routine
exposure cases but rely on regional centers to handle most of the calls in their
area.
medically related fields, toxicologists, and biologists. Persons responsible for answering
the phones are either certified by the AAPCC or are in the process of obtaining certifica-
tion. Passage of an extensive examination on toxicology is required for initial certification,
with periodic recertification required.
Regardless of who takes the initial call, there is a medical director and other physi-
cian back-up available. These physicians have specialized training or experience in toxi-
cology, and are able to provide in-depth consultations for health care professionals calling
a center.
1. Medical Director
A poison center medical director should be board-certified in medical toxicology or be
board-certified in internal medicine, pediatrics, family medicine, or emergency medicine.
The medical director should be able to demonstrate ongoing interest and expertise in toxi-
cology as evidenced by publications, research, and meeting attendance. The medical direc-
tor must have a medical staff appointment at a comprehensive poison treatment facility
and be involved in the management of poisoned patients.
2. Managing Director
The managing director must be registered nurse, pharmacist, physician, or hold a degree
in a health science discipline. The individual should be certified by the American Board
of Medical Toxicology (for physicians) or by the American Board of Applied Toxicology
(for nonphysicians). He or she must be able to demonstrate ongoing interest and expertise
in toxicology.
3. Specialists in Poison Information
These individuals must be registered nurses, pharmacists, or physicians, or be currently
certified by the AAPCC as specialists in poison information. Specialists in poison informa-
tion must complete a training program approved by the medical director and must be
certified by the AAPCC as specialists in poison information within two examination ad-
ministrations of their initial eligibility. Specialists not currently certified by the Association
must spend an annual average of no fewer than 16 hours per week in poison center-related
activities. Specialists currently certified by the AAPCC must spend an annual average of
no less than 8 hours per week. Other poison information providers must have sufficient
background to understand and interpret standard poison information resources and to trans-
mit that information understandably to both health professionals and the public.
4. Consultants
In addition to physicians specializing in toxicology, most centers also have lists of experts
in many other fields as well. Poison center specialty consultants should be qualified by
training or experience to provide sophisticated toxicology or patient care information in
their area(s) of expertise. In regard to viral exposures, the names and phone numbers of
persons in infectious disease at nearby hospitals might be helpful. Funding is usually a
crucial issue, so these experts should be willing to donate their expertise in identification
and handling cases within their specialty. Poison centers usually do not have specific
specialists in viral diseases. Local hospital departments are most often contacted and the
patient referred to the specialist.
on the center, its expertise, its consultants, and the appropriateness of a referral. Below
are lists of calls that generally fall into each group. Remember there is considerable varia-
tion between poison centers; if there is doubt, call the poison center and they will tell you
if your case is more appropriately referred. Poison centers do best on calls regarding acute
exposures. Complicated calls regarding exposure to several agents over a long period of
time, which produces nonspecific symptoms, are often referred to another medical special-
ist, to the toxicologist associated with the center, or to an appropriate government agency.
The poison center will often follow up on these cases to track outcome and type of service
given.
Types of Calls Usually Accepted
Drug identification
Actual acute exposure to a drug or chemical
Actual acute exposure to a biologic agent (e.g., plants, mushrooms, various ani-
mals)
Information regarding the toxic potential of an agent
Possible food poisonings
Types of Calls Often Referred
Questions regarding treatment of a medical condition (not poisoning)
Questions on common bacterial, viral, or parasitic infections
General psychiatric questions
Proper disposal of household agents such as batteries, bleach, insecticides
Use of insecticides (which insecticide to use, how to use it) unless related to a
health issue, e.g., a person allergic to pyrethrins wanting to know which prod-
uct does not contain pyrethrins)
Records of all calls/cases handled by the center should be kept in a form that is
acceptable as a medical record. The regional poison information center should submit all
its human exposure data to the Association's National Data Collection System. The re-
gional poison information center shall tabulate its experience for regional program evalua-
tion on at least an annual basis.
1. AAPCC Toxic Exposure Surveillance System
In 1983 the AAPCC formed the Toxic Exposure Surveillance System (TESS) from the
former National Data Collection System. Currently, TESS contains nearly 16.2 million
human poison exposure cases. Sixty-five poison centers, representing 181.3 million peo-
ple, participate in the data collection. The information has various uses to both governmen-
tal agencies and industry, providing data for product reformulations, repackaging, recalls,
bans, injury potential, and epidemiology.
The summation of each year's surveillance is published in the American Journal of
Emergency Medicine late each summer or fall.
Busy centers will have a single number that will ring on several lines. Calls are often
direct referrals from the 911 system. In most cases, poison center specialists are unable
to determine the virus involved, so the caller is referred to a infectious disease physician.
Poison information specialists listen to the caller, recording the history of the case
on a standardized form developed by AAPCC. Basic information such as the agent in-
volved, amount ingested, time of ingestion, symptoms, previous treatment, and current
condition are recorded, as well as patient information such as sex, age, phone number,
who is with the patient, relevant medical history, and sometimes patient address. All infor-
mation is considered a medical record and is therefore confidential.
The case is evaluated (using various references) as:
Cases are usually followed until symptoms have resolved. In cases where the patient
is referred to a health care facility, the hospital is notified, the history relayed, toxic poten-
tial discussed, and suggestions for treatment given.
AAPCC and CAPCC hold a joint scientific meeting and invite speakers and other toxicol-
ogy specialists from around the world. Some international affiliated organizations are listed
with the North American groups above.
The following poison control center telephone numbers and addresses are thought to be
accurate as of the date of publication. Poison control center telephone numbers or ad-
dresses may change. The address and phone number of the poison control center nearest
you should be checked frequently. If the number listed does not reach the poison center,
contact the nearest emergency service, such as 911 or local hospital emergency rooms.
The authors disclaims any liability resulting from or relating to any inaccuracies or changes
in the phone numbers provided below. An asterisk indicates a regional center designated
by the American Association of Poison Control Centers. This information should NOT
be used as a substitute for seeking professional medical diagnosis, treatment, and care.
ALABAMA Tuscaloosa
Alabama Poison Control System, Inc.
Birmingham 408 A Paul Bryant Drive, East
Regional Poison Control Center* Tuscaloosa, AL 35401
Children's Hospital of Alabama (800) 462-0800 (AL only)
1600 Seventh Avenue, South Birmingham, (205) 345-0600
AL 35233-1711
(800) 292-6678 (AL only)
(205) 933-4050
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[281] Place, Ninive, vol. i. p. 58.
[282] Botta, Monument de Ninive, plate 113.
[283] Ibid. plates 43 and 53.
[284] Botta, Monument, &c. plate 62.
[285] Ibid. plates 61 and 76, and vol. v. p. 124.
[286] See especially at the south end of the Nimroud Gallery,
the upper part of a male figure, numbered 17 a. The black of the
hair and beard has preserved much of its strength.
[287] “At Kouyunjik there were no traces whatever of colour.”
Nineveh, vol. ii. p. 310.
[288] Heuzey, Catalogue des Figurines en terre cuite du
Musée du Louvre, p. 18.
[289] Heuzey, Catalogue, &c. p. 19.
[290] Ibid. p. 20. Layard also found many of these blue
statuettes at Khorsabad (Discoveries, p. 357).
[291] These fragments were found by Layard in one of the
small temples at Nimroud (Discoveries, pp. 357, 358).
[292] M. Sully Prudhomme has lately embodied this idea in
his verses addressed to the Venus of the Louvre (Devant la
Vénus de Milo in the Revue politique for 6 January, 1883):—
* * * * *
Transcriber’s Notes: