[Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997]

Special Issue

Maximizing the Usefulness of Food Microbiology Research

Terry A. Roberts
Food Safety Consultant; Chairman, International Commission on
Microbiological Specifications for Foods
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      Funding for food microbiology research often follows disease
      outbreaks: botulism from vacuum-packed white-fish chubs,
      listeriosis from soft cheeses, or illness due to Salmonella
      Enteritidis or Escherichia coli. As a consequence of research,
      detection, identification, and subtyping methods improve, and
      more is learned about pathogenicity and virulence. Research
      also explores the organisms' capacity to multiply or survive in
      food and to be killed by established or novel processes.
      However, rarely is there a critical overview of progress or
      trustworthy statements of generally agreed-on facts. That
      information is not maintained in a form that can readily be
      used by regulatory departments and the food industry to ensure
      a safe food supply. A centralized system is urgently needed
      that is accessible electronically and carries information in a
      standardized format on the essential properties of the
      organisms, including pathogenicity, methods of detection,
      enumeration and identification, alternative prevention and
      control methods, and growth and survival characteristics.

Most countries aim to regulate food and the food industry to ensure a safe
and wholesome supply. Although the technology of food processing is based
on tradition (drying, freezing, fermentation), research has resulted in a
wide range of processes to meet the ever-changing requirements of
consumers. Canning of low-acid foods set an enviable example of
microbiologic safety. Today, consumers demand less heavily processed foods
that contain a minimum of chemical preservatives, have a long shelf life,
and are "fresh" yet microbiologically safe. Competitive food retailing
requires such products to be no more expensive than existing products. In
the United Kingdom, there has been a swing toward convenience foods and
foods with ethnic flavors, sometimes with a premium price. Commercial
success is evident, but relatively few of those foods have been evaluated
experimentally for microbiologic safety. Emphasis is on risk assessment, on
Hazard Analysis and Critical Control Points (HACCP) and process control,
all of which rely heavily on existing knowledge. That knowledge, and the
raw data from which it is derived, could be better organized and easier to
use.

The International Commission on Microbiological Specifications for Foods
(ICMSF)

The history of microbiologic aspects of food control is reflected in the
publications of ICMSF. ICMSF was established in 1962 as foodborne disease
greatly increased microbiologic testing of foods. Increased testing, in
turn, created widespread practical and regulatory problems in the
international food trade. At that time, analytical methods were not
standardized, sampling plans were of doubtful statistical validity, and the
interpretation of results applied different concepts of biologic
significance and acceptance criteria that confused and frustrated industry
and regulatory agencies alike.

ICMSF was founded to assemble, correlate, and evaluate evidence about the
microbiologic safety and quality of foods; to consider whether
microbiologic criteria would improve and ensure the microbiologic safety of
particular foods; to propose, where appropriate, such criteria; and to
recommend methods of sampling and examination.

The primary purpose of the commission remains to give guidance on
appraising and controlling the microbiologic safety of foods, with due
attention to microbiologic quality. Meeting the commission's objectives
would facilitate international trade; the work of national control
agencies, the food industry, and international agencies concerned with the
humanitarian aspects of food distribution; and the health of consumers.

An advisory body, the ICMSF provides basic information through extensive
study and experience and makes recommendations, without prejudice, based on
that information. Results of the studies are published as books or papers.

At its meetings, the ICMSF functions as a working group. Its membership
consists of 18 food microbiologists from 11 countries whose interests
include research, public health, official food control, education, product
and process development, and quality control. Members are from government
laboratories in public health, agriculture, and food technology;
universities; and the food industry. ICMSF also seeks assistance from
consultants specializing in particular areas of microbiology. Four
subcommissions (Balkan and Danubian, Latin American, Middle East and North
African, and Southeast Asian) promote activities similar to those of ICMSF
among food microbiologists on a regional scale and facilitate worldwide
communication.

ICMSF raises its own funds and pays for its activities and meetings. The
commission obtained support from government agencies, the World Health
Organization, International Union of Microbiological Sciences and
International Union of of Biological Sciences, and the food industry (more
than 80 food companies and agencies in 13 countries).

During its first 25 years, ICMSF devoted the major portion of its effort to
methodology research, improved standardization of methods, and 17 refereed
publications (1). One important finding was that in analyzing salmonellae,
samples could be composited, making it practical to collect and analyze the
large number of samples recommended in some stringent sampling plans. With
the evolution of alternative methods, rapid test kits, and the
everexpanding list of biologic agents involved in foodborne illness, the
commission reluctantly discontinued its program of comparison and
evaluation of methods.

The long-term objective of enhancing the microbiologic safety of foods in
international commerce was addressed initially in books recommending
uniform analytical methods (2), sound sampling plans and criteria (3), and
the microbial ecology of foods (4,5), which familiarized the analyst and
food technologist with processes used in the food industry and foods
submitted to the laboratory. Knowledge of the microbiology of major foods
and the factors affecting their microbial content helps interpret
analytical results.

At an early stage, the commission concluded that no food sampling plan
could ensure the absence of a pathogen. Testing foods at ports of entry, or
end-product testing elsewhere in the food chain, cannot guarantee food
safety. This led the commission to investigate the potential value of HACCP
for enhancing food safety. A joint ICMSF/World Health Organization meeting
in 1980 led to a report on the use of HACCP for controlling microbiologic
hazards in food, particularly in developing countries (6-8).

The commission published the principles of HACCP and procedures for
developing HACCP plans (9); the publication discussed the relative
importance of controlling the production and harvesting, preparing, and
handling of foods. Recommendations are given for the application of HACCP
at each step in the food chainfrom production and harvest to consumption.

The commission recognized that a major weakness in the development of HACCP
plans is hazard analysis; knowing about the many biologic agents
responsible for foodborne illness has become difficult. The commission's
latest book (1) proposes to facilitate the development and assessment of
HACCP plans, improve the safety of foods, and facilitate risk assessment. A
thorough concise review of reports on growth and death responses of
foodborne pathogens, it is intended as a relatively quick reference manual
to assist in making decisions. The commission is revising Microbial Ecology
of Foods: (Vol. 2) Food Commodities with publication planned as
Microorganisms in Foods 6 in late 1997.

ICMSF submitted its recommendations for sampling foods and acceptance
criteria for Listeria monocytogenes to the Secretariat of Codex
Alimentarius in 1993. To stimulate discussion, the recommendations were
initially provided to the Codex; they were subsequently published (10) and
revised after further discussion (11). At the request of the Secretariat of
Codex, the commission developed recommendations for the revision of
Principles for the Establishment and Application of Microbiological
Criteria for Foods, which appears in the Procedural Manual of Codex.

Members of ICMSF believe that the original objectives of the commission
still apply. The formation of the European Union, the many other worldwide
political changes, the growth of developing countries seeking export
markets, and the increased worldwide interest in international trade, as
evidenced by the passage of the General Agreement on Tariffs and Trade and
the North American Free Trade Agreement, all point to the continuing need
for unprejudiced guidance and advice. Import and export policies must be as
uniform as possible and based on scientific facts. The commission will
strive to meet this goal through a combination of educational materials,
promotion of HACCP, and recommendations, where appropriate, of sampling
plans and microbiologic criteria. In addition, commission members will
continue to transfer information on food safety through symposia, meetings,
committee activities, and in their daily work. The future success of ICMSF
will continue to depend on extensive support from consultants and those who
provide the financial support essential to the commission's activities.

Research and Its Current Uses

Research Procedures and Funding

In most countries, funding for research has become more competitive, and
has even decreased in recent years. The following observations are based on
experience in the United Kingdom and the European Union.

The researcher first identifies the sources of funds and writes a proposal.
If funds are granted, the research proceeds. The output may include
confidential reports to the sponsor, refereed scientific publications, and,
increasingly, a patent or a licensed process or technique. Because funding
has so many different sources, writing proposals takes a substantial
proportion of the researchers' time. In many cases, the best researchers
also write the most persuasive proposals, but is this an efficient use of
the researchers' time?

In the United Kingdom, research generally falls into two categories:
research funded by the parent body and research supported by a contract.
The Institute of Food Research falls under the Biotechnology & Biological
Sciences Research Council (BBSRC), formerly the Agriculture and Food
Research Council. A proportion of the institute's funds comes directly from
the BBSRC, although these funds are declining and facing increased
competition among BBSRC institutes.

In addition, funds may be obtained from the central government: the
Ministry of Agriculture, Fisheries, and Food (MAFF) and the Department of
Health, both of which have research programs focusing on food microbiology.
In addition, Scotland and Northern Ireland have separate research budgets,
which traditionally have been spent in those countries. Funds from these
sources sometimes support projects for 3 years, but more recently for
shorter periods.

The European Union supports research across very wide areas, of which only
a small part is food technology and food microbiology, e.g., Food-Linked
Agro-Industrial Research, now ended, and European Cooperation in Scientific
and Technical Research. European Union programs run for 4 or 5 years, but
funding is usually less than 100% (often 50% and dependent on financial
support from the institute or on parallel funding from one of the above
sources).

In the United Kingdom, research funds from the food industry are usually
restricted either to very short trouble-shooting projects or to
confidential investigations. MAFF encourages industrial support of research
in LINK programs, with the government contributing up to 50% of the total
funding, provided that the research contains elements of novelty and a
consortium of companies, sometimes only three or four.

Not only is the researcher faced with attracting funds from a variety of
sources, but the requirements of those funding sources differ greatly.
Research on genetic or physiologic reasons for phenomena, such as the
unusual acid tolerance of Vero cytotoxin-producing Escherichia coli
strains, might meet BBSRC's stringent requirements of scientific quality.
MAFF publishes a Requirements Document each year, identifying areas and
topics that fit into its policy to maintain a safe and wholesome food
supply. Some of the research is basic science, e.g., developing novel
methods of detecting or identifying microbes; some is more mundane, e.g.,
improving the effectiveness of sanitizing surfaces in food processes. MAFF
also supports a limited program of surveillance for particular foodborne
pathogens. These funds are available for research institutes, universities,
and other laboratories, and proposals are judged by both MAFF staff and
independent assessors from outside. Research is organized into programs on
hygienic food processing, separation and detection of pathogens and their
toxins, physicochemical principles underlying microbial growth, growth
conditions for pathogens, ending in 1997-98, and new programs on assessing
microbiologic hazards and risks and managing microbiologic hazards and
risks of salmonellae and campylobacters in poultry. The Department of
Health also supports food safety researchpartly as surveillance and partly
as programs targeted at a specific organism, e.g., E. coli O157:H7. The
Department of Health also responds to topics identified by the Advisory
Committee on Microbiological Safety of Foods.

University departments in England are subjected to a different form of
scrutiny to determine the amount of research funding they receive from the
central government, judged by the Higher Education Funding Council for
England. The quality of publications is judged against the number of
researchers, and the funding is directed toward research excellence. Newly
established departments find it difficult to compete.

Research Output

Output from research has been regarded as the report to the contractor,
sometimes confidential and sometimes public. More recently, funding
agencies have encouraged exploitation of research through patents or
licensing agreements. To the researcher, expertise must be recognized
through refereed publications. Although in addition to detailed papers,
overviews and sometimes summaries for the industry are provided, there is
generally less consideration for the research user. In recent years, many
reviews have become mere compilations of completed research. Moreover, most
computerized databases terminate in about 1970, thus ignoring a wealth of
earlier information. HACCP and risk assessment would be greatly facilitated
if data on microbial responses (growth, survival, death) were collated in a
more standardized form. Details should include the food commodity (e.g.,
meat, fish, vegetables, or fruit), the subgroup (e.g., for meat, beef,
pork, or lamb), and the process applied (e.g., cooked, cured, smoked, or
fermented). Details of the packaging should include the pack atmosphere
(%CO2, %O2, %ballast gas). In the longer term, it might become important to
know the exact identity of the organism including serotype, phage type,
strain, and, in time, virulence factors and even sequences for 16S rRNA and
for toxin genes. Other items that should be tabulated include inoculum
concentration; prior history of the inoculum, especially if that history
might alter the response; incubation temperature(s); measure of water (%
brine, aw); pH; other factors (e.g., nitrite, sorbate); microbiologic
method(s); response (growth rate, D value, time to toxin); and estimate of

the reliability of the measures of the responses.

Many readers assume that these details are included in most, if not all,
publications. However, our experience in compiling published data for
comparisons with models of growth, thermal death, or survival (nonthermal
death) illustrates that much desirable information is lacking (12-15).
Attempts to define the boundary between growth and no growth are not new
(16-19). Despite different methods and strains of microbes, compilations of
reported data often show a trend (Figure).
 
[Figure Not Available in ASCII]

 Figure. Specific growth rate of Listeria monocytogenes predicted by
 different models and independent observers (provided by J. Baranyi,
 Institute of Food Research, Reading Laboratory). Estimates of specific
 growth rate from published papers are shown vertically. The response
 surfaces were generated from predictive models and are not a surface
 fitted to the values.

Research Users

Despite an overall neglect of the research user's needs, some useful
listings are available (20) as are helpful overviews and discussions
(21-26). There remains, however, an opportunity for the researcher to make
a product more attractive to the research user, e.g., the food industry
(both national and international), regulatory bodies, and informed
consumers.

Additional Research Needs

Required research includes developing a database of reliable information on
microbial responses to food processing conditions. The database needs to be
easy to access and use. In addition, because understanding of growth
responses and thermal death is greater than our understanding of survival,
i.e., little or no loss of viability over many months, we need to have a
better understanding of the factors determining that survival and of the
underlying microbial physiology. In recent years, we have been faced with
such new microbiologic challenges as Salmonella Enteritidis Phage Type 4,
multidrug-resistant S. Typhimurium Definitive Type 104, verocytotoxigenic
E. coli, Shiga like toxin-producing E. coli, and increasingly
vancomycin-resistant Enterococcus faecium, and we lack the capacity to
anticipate emergence of new pathogens. Finally, new technologies make it
possible to study genetic stability and variation in populations, perhaps
identifying why particular strains are, or become, more virulent and more
pathogenic.

Control of Food Safety

Food safety has traditionally been controlled by inspection and compliance
with ordinances or codes of practice. Much faith has been placed in
sampling plans and associated microbiologic criteria. However, this
approach is retrospective, depending on the microbiologic examination of
product that has often been dispatched or consumed. The number of samples
that can be examined statistically is too small to detect low levels of
"defectives." HACCP was a substantial step forward, with the concept that
safety could be designed into a food process. However, HACCP demands
substantial knowledge about the characteristics of the food, the process,
and the microbes of concern. The knowledge required to implement HACCP
effectively is not organized into systems that are easy to use.

Address for correspondence: Terry A. Roberts, Ph.D., 59 Edenham Crescent,
Reading RG1 6HU, United Kingdom; fax: 44-118-956-6998.

References

  1. International Commission on Microbiological Specifications for Food.
     Microorganisms in foods. 5. Characteristics of microbial pathogens.
     London: Blackie Academic & Professional;1996. p. 511-3.
  2. International Commission on Microbiological Specifications for Food.
     Microorganisms in foods. 1. Their significance and methods of
     enumeration. 2nd ed. Toronto: Univ. of Toronto Press;1978.
  3. International Commission on Microbiological Specifications for Food.
     Microorganisms in foods. 2. Sampling for microbiological analysis:
     principles and specific applications. 2nd ed. Toronto: Univ. of
     Toronto Press;1986.
  4. International Commission on Microbiological Specifications for Food.
     Microbial ecology of foods. Vol. 1. Factors affecting life and death
     of microorganisms. New York: Academic Press;1980.
  5. International Commission on Microbiological Specifications for Food.
     Microbial ecology of foods. Vol. 2. Food commodities. New York:
     Academic Press;1980.
  6. International Commission on Microbiological Specifications for Food.
     Report of the WHO/ICMSF meeting in hazard analysis: critical control
     point system in food hygiene. Geneva: World Health Organization;1982.
     VHP/82.37.
  7. International Commission on Microbiological Specifications for Food.
     Prevention and control of foodborne salmonellosis through application
     of the hazard analysis critical control point system. Report of an
     International Commission on Microbiological Specifications for Foods
     (ICMSF) ad hoc committee. Geneva: World Health Organization;1986.
     WHO/CDS/VPH/86.65.
  8. Simonsen B, Bryan FL, Christian JHB, Roberts TA, Tompkin RB, Silliker
     JH. Report from the International Commission on Microbiological
     Specifications of Foods (ICMSF). Prevention and control of food-borne
     salmonellosis through application of hazard analysis critical control
     point (HACCP). Int J Food Microbiol 1987;4:227-47.
  9. International Commission on Microbiological Specifications for Food.
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Emerging Infectious Diseases
National Center for Infectious Diseases
Centers for Disease Control and Prevention
Atlanta, GA

URL: ftp://ftp.cdc.gov/pub/EID/vol3no4/ascii/roberts.txt