Proceedings from the Third Annual Federal/State
Conference on Food Safety
November 20-21, 1997
California Department of Health Services
Thank you, everybody, for your patience and your diligence. We'll work through
this panel fast, and get to the questions, and get to the sum up as quickly as we can.
Rather than long introductions, let me first introduce Dr. Ben Werner from our Division
of Communicable Disease Control.
California Department of Health Services
Good afternoon, everybody.
I was asked to speak about some of the health problems we've had from sprouts, and more
specifically to talk about the very large California Salmonella outbreak we had last year,
one of four major outbreaks that have been witnessed in the United States in association
with sprouts specifically, Salmonella-associated illness.
And before I begin I'd like to acknowledge contributions to some of these materials by
Dr. Larry Slutsker, who's an epidemiologist with the CDC, and also Dr. Eric Mouzan, who is
an epidemic intelligence service officer assigned by the CDC to the State of California.
This first slide shows you that since 1970 there's been an interest in reducing red
meat consumption in this country, as part of the healthy heart activities, and there's
been a replacement of those kinds of foods with fresh fruits and vegetables.
And you can see that between 1970 and 1994 there's been a 30 percent increase in per
capita consumption of vegetables and a little over 20 percent in the per capita
consumption of fruit.
The very first outbreak that I'm aware of anywhere in the world occurred in the USA in
1973 which was and that was Bacillus cereus from seed. There was a very
small outbreak in 1990, Salmonella anadum, from alfalfa in the State of Washington.
And then there are these other major outbreaks, Salmonella stanley, Newport. The
one we were involved with, a combination of Montevideo and Meleagridis in
In 1997 there was an outbreak in Missouri and Kansas, I believe. And in June of this
year there was an outbreak in Michigan and Virginia of E.coli O157:H7. Five of the
outbreaks recognized in the USA in association with sprouts have been Salmonella
The outbreaks have occurred internationally, as well. The first one was in 1988 in the
UK and elsewhere in Europe, and you could see that they've been in a lot of countries;
it's involved a lot of Salmonella types. The big one, of course, was in Japan due to E.coli
O157:H7. And it occurred again this past year, 1997. There were more than 10,000 cases of E.coli
O157:H7, especially in school children in Japan.
I want to talk about the Salmonella outbreak in California associated with sprouts, how
we got involved and exactly how we went about investigating it.
Montevideo is not that unusual Salmonella serotype. We have about 15 isolates
per month in any given month coming into the State lab. But in May of 1996 we had a big
increase in numbers to 117. And in association with that we saw some increase in Salmonella
Meleagridis. As a matter of fact, three people had dual infections, montevideo and
So our major objectives in going in on an investigation like this is to identify the
source of the outbreak and intervene if we can in order to control it.
Let me just tell you from my experience many times we go investigate an outbreak that's
already taken place, and thats good. However, we dont learn as much. This one
afforded us an opportunity to really do some good, because the problem was ongoing and
would have continued had we not identified the problem and taken some action. And as a
result of this some recommendations can be made.
We went on a fishing expedition. We like to call it a hypothesis-generating situation.
What we do is we ask open-ended questions of let's say 20 patients, and we asked literally
hundreds of questions about food exposures in the previous days before onset. And in this
case we focused on the four days before onset. And we asked about other things, as well.
And what we did was then distilled those questions down to those that made sense to ask
future cases and controls. In other words, it's hard to invoke a food source that might be
the cause of the problem of only 10 or 20 percent of the cases used it. So what we did was
we focused on those food items that were mentioned by at least 30 percent of the cases.
And we did a classic case control study. We defined our case as somebody who had
diarrhea and a positive stool culture for Salmonella montevideo in the months of
May or June. And these cases were in the northern California area, mostly centered around
Santa Clara County, but involving some six other counties.
And we looked at the most recent cases, because they would have the freshest memories.
And we arbitrarily selected 46. And we collected 46 controls. This was hard because we got
the controls by random digit dialing. We took the first five numbers of somebody's phone
number, and then tried to make a match by age, so that they would be comparable in age to
the case that we're matching with.
And just to show you how effective that was, we compared, the cases and controls by sex
and age, and you see that by sex, all across the board, there was a majority of females.
For all outbreak cases two-thirds were females. We had a slightly more among the patients
who were called. And as far as the median age they were pretty comparable, and you see
that the age range was pretty comparable. This is to show you that we had pretty good
And now as we compared the exposures of the cases with the controls, for those items
that were used by at least 30 percent of the cases, we found that on univarit analysis
only one item stood out. And this was alfalfa sprouts. Alfalfa sprouts were used by 38
percent of the cases, and only by 11 percent of the controls, which gives an odds ratio of
5. This is on the ballpark with all the other Salmonella outbreaks and other outbreaks
related to sprouts.
Sprouts is a strange vehicle in the sense that lots of times people could be eating it
and don't recognize it. You go to a deli shop, you have a sandwich in a restaurant. You
know that the roast beef is there, but you may not recognize that you also eat sprouts.
Nonetheless, some 38 percent of people could actually recall having purposely bought
sprouts or asked for it and so forth. So the true number could have been more. All I can
tell you is that in all the other outbreaks that we've looked at nationally, the frequency
of sprout use by cases has been in this ballpark of 35, 37, 38 percent.
In terms of how morbid the disease was, out of those 46 cases of Salmonella
montevideo in this case control study, you see the 39 percent did, in fact, go to an
emergency room. Some of them required intravenous hydration, and 6 percent were admitted
to a hospital. Unfortunately, a person with a bloodstream infection died. (That person
represented 2 percent of the 46 cases).
As far as the 17 cases eating sprouts, one person could actually remember eating brand
X. Eight said they simply bought their sprouts at a specific deli. And in checking with
those delis, they sold only that brand of sprouts. And then some five people bought from
supermarkets that carried sprouts alone, or sprouts in other brands.
In tracing back we found that just one sprouter business was provided seed actually
that was produced in the USA, as a matter of fact, here in California, in Imperial County.
The other sprout outbreaks in this country have primarily involved seed imported from
abroad, especially from Denmark from the Netherlands.
In the laboratory sense we could not culture Salmonella montevideo from seeds or
sprouts, but we did culture the meleagridis from sprouts taken from patients. One
woman went to the hospital. She had her onset three days after buying those sprouts, and
went to the hospital. After discharge she came home, and the sprouts were still there. We
recovered those sprouts and found meleagridis in this.
We found sprouts at retail levels in the usual clam cases, not previously opened. We
found it there. And the sprouter business had many hundreds of boxes of sprouts ready for
distribution when we visited. And we found Salmonella meleagridis in those, as
well, ready for sale.
To emphasize again the environmental studies there were at least 49 cultures of seed.
They were all negative. And in visiting the sprout producer we found lots of problems in
terms of sanitation. We found a lot of problems with flies and rodents on the premises.
So those seeds, as I mentioned, did come from California in the Imperial Valley.
Actually this mostly produced alfalfa seed for the production of hay, which went to places
in Southern California and to Mexico. But the person did supply some seed to sprouters,
and one involved the brand of sprouts we're talking about here that caused the outbreak in
northern California. He also sent seeds to southern California in the San Diego County
area. Those seeds were treated with chlorine, and as far as we know there is no problem
from those. Some of the seeds were also sent to a sprouter in Texas, and reportedly those
seeds were never used.
So the conclusions were that alfalfa sprouts, due to brand X, were implicated in an
outbreak. Montevideo was our comparison basis, we identified the association of
disease with those sprouts. And as soon as the sprouting facility agreed to a voluntary
recall, cases around the State plummeted.
We had meleagridis documented, lab-confirmed in sprouts. And they were found in
the patients, as we mentioned, in the sprouts and elsewhere. Were not really sure
how the sprouts got contaminated.
Just a few comments about sprouts in general. There's a fluctuating use of sprouts in
the country. A Foodnet population survey was done a little while back, and in the spring
months as many as 20 percent of people knew they were consuming sprouts.
There are lots of opportunity to contaminate sprouts. Where they're grown
and harvested there could be animals, rodents, reptiles and all their manure that can get
onto the product.
Then the seeds are processed at another facility, generally to get rid of gravel,
glass, metal parts and so forth. And then they're generally bagged and sent in storage and
so forth. If those are loose, woven bags, it's easy to imagine how rodents and birds and
their feces could enter the product.
In the sprouting facility you can get amplification of what pathogens are there. The
sprouting facility is basically an incubator. It's warm, it's moist, and if there are any
pathogens there at all they're going to grow.
But, on the other hand, I should tell you that routine bacteriologic surveillance was
done of seed in February 1997 of a major California producer that ships interstate, and
those seeds were reportedly soaked for two to three hours in 2000 ppm chlorine solution.
These were tested at, I believe, a private lab working for a supermarket chain.
And Salmonella oranienburg was found in those seeds. And the product was halted
before it was marketed. There were no illnesses reported. And in looking at the bags that
those seeds came in, we saw that there was clear evidence of rodent contamination with
urine on those seeds. And I believe they came from Australia.
There's several ways to decontaminate seed. You can use 2000 ppm chlorine for awhile,
30 minutes or so, and then finish it up with a 3 or 4 ppm chlorine wash.
You can use hydrogen peroxide. And here you have no hydrogen peroxide, then 1 percent,
2 percent, 4 percent and 6 percent to see what happens to Salmonella concentrations. See
fewer colony forming units of Salmonella. And it's real high if you don't have any
hydrogen peroxide. If you get down to 6 percent, there's only one Salmonella left.
Another way to decontaminate seed would be to heat it. You don't want to heat it too
much otherwise the seed will die and it won't germinate. So the idea is to get it, cook it
at about a 135 degrees for five minutes. Enough of the seed will survive. So that's
another way to do it.
For example, this particular sprouter involved in this outbreak was unknown to local
health authorities or the State food and drug branch. They had previously had a license.
However, they had moved and nobody knew where they were or was providing any oversight.
So, to reach these people could be a challenge.
What are the approaches to prevention that the consumer can use? Well, they're not
logically going to cook them. People like eating alfalfa sprouts for its texture and
taste, so they're not going to do that.
Will rinsing work? It may help reduce the Salmonella burden a little bit, but that's no
assurance. And I don't really think that I don't expect the industry or your
kitchens and restaurants are going to be washing them.
So what do you tell the consumer? I think it's in fairness consumers ought to know that
sprouts are a potentially hazardous food. That the risk is really hard to estimate.
Rinsing probably has limited benefit.
I think it would be prudent for people at the extremes of life if you're an
infant under three, four months old, or in age 60, 70s, 80 are not making stomach
acid much anymore, or at all. And you don't destroy the pathogens you occasionally
So people in the extremes of life might want to consider not eating sprouts. People who
are immunocompromised, who have AIDS, who are taking steroids or agents, chemotherapy,
radiation for various cancers would be at great risk. And a lot of perfectly healthy
people may want to pass up sprouts.
If you look at these outbreaks, as we've had in the past, they're primarily healthy,
young women who are the cases, with underlying health problems, who were sick and
sometimes hospitalized. So people have to make a decision as to whether the benefit of the
taste and texture and so forth of sprouts outweigh the potential risk.
And that's all I have. If there are any questions I can take them now or later.
California Department of Health Services
A quick comment about prevention regarding soaking of seeds in chlorine or hydrogen
peroxide. We don't feel like that's an extremely viable option for the simple reason that
even if you reduce the population of bacteria a thousandfold, reduce it from 1000
organisms to one, the sprouting process itself over a period of three to five days
requires heat, light and moisture. Those one to ten organisms can multiply rapidly over
those few days to hundreds and thousands and millions of organisms.
Better methods have to be found to insure food safety.
Just a bit of a review of our in-plant investigation. This really couldn't be
considered a plant. This was a very small operation in a corner of an old produce
warehouse. This grower is since out of business.
Sprouting, in itself, in the earlier years and today can still be a very low overhead
industry. Anyone can begin sprouting in their garage or basement with minimal investment.
Our investigation, unveiled the brand. It still took us a period of time to locate this
producer. He was using out-of-date packaging with an out-of-date address, was not
registered with us, was not licensed by the county.
It took the help of the Salinas Police Department at about 12:00 on a Saturday night to
help find this gentleman.
For those of you that have not been in a sprout production facility you'll hear a
little more about sprout production from Jay Louie. This is one method of sprout
production in fiberglass drums.
A quick synopsis is seeds are loaded into each of these four quadrants. The seeds
rotate with an internal misting system and a light source. And over a period of three to
five days, presto, you have sprouts. They are harvested in these buckets that you see.
In this facility they were then taken to a central wash tank area another area
of great concern to us. Again, notice the worker here in the background. The day of the
original investigation, looked like this one to two days after we show up, hair nets and
gloves magically appear.
We observed an air hose that connects to the bottom of this tank. There was a bubbler
for the purpose of separating the husk of the seed from the sprout to make it a more
appealing product to the consumer. The bubbler was not working for some period of time.
Therefore, the workers were manually agitating the sprouts, bare arms up to their armpits,
to clean the product.
The product was then scooped out with a net and dumped onto the tables for packaging
and storage and subsequent distribution. Again, gloves suddenly appeared. This was in a
corner of a warehouse; three sides of this facility were sheet plastic. There were
numerous rodent problems, as Ben mentioned. There were sprouts growing in dirt, sunflower
sprouts and pea sprouts in one corner of the building.
Following these outbreaks we convened a meeting of the sprout industry in California,
in Sacramento, and invited CDC, the sprout industry, State and Federal and local
regulators to help develop solutions to this.
Out of that meeting, we developed a working group composed of State and Federal
regulators and industry, which met over a period of probably six to eight months. The work
culminated with the development of once again voluntary guidelines for the sprout industry
which have been distributed to the industry.
We also are now in the process of beginning a Statewide inspection of all sprout
growers in California.
So, with that, I'll turn it over to Jay Louie, who will give an overview from the
International Sprout Growers Association
All right, thank you, Jeff. After listening to this I can see from the
consumers' point of view the future looks very dismal for sprout growers, to say the
But nevertheless, it's an industry that's composed of a lot of independent small
businesses, some dating back two generations. Our business started back in the early
1950s. We're initially primarily a mung bean sprout grower as opposed to an alfalfa sprout
grower, which the slides projected indicated.
The sprouters were previously thought of as farmers, and now we're looked upon as also
food processors, because our products are grown like you would think farmers do, but also
processed and packaged and distributed to the consumers directly. So we are both a farmer
and a food processor.
There's two major types of sprouting, both grown indoors, both in controlled
environments, grown primarily hydroponically. There are a few soil-based sprouters. And,
again, as mentioned earlier, the room temperatures are between 80 to 70 degrees
Fahrenheit, which with the sprouts as the food medium, and the water, provides an ideal
environments for bacterial growth.
The green sprouts, which are alfalfa sprouts, clover sprouts, and combination of both
are spiced up with onion and garlic. About 40 percent of all your sprout growers in the
industry focus on green sprouts.
The other 60 percent of the sprout growers consist of common mung bean sprout growers.
These you see are sold in bulk or packaged in small packages in the stores. Mung bean
sprouts are grown completely in the dark. As you can see there's no color. The alfalfa
sprouts have a green color, only because they use light as part of the process.
And also mention that there is a small faction of so-called organic growers that do use
soil as a medium, and as you can see, sometimes the soils do bring in a hazard, can
cross-contaminate some of the other products.
Now I have a description on a very gross generalization of the industry. Generally most
sprout growers are small, family-owned operations. The green sprouters are a product of
the 60s generation, popularized with the 60s trend toward eating healthier food.
The bean sprouters have been around much longer, perhaps over a century in China and
Japan. They've been in California perhaps since the mid 40s. Again, our family started in
the mid 50s. And most of the bean sprout growers that I'm aware of are of Chinese or
The sprout growers are generally secretive in the methods of production. How sprouts
are grown varies from grower to grower. Every grower has their secrets and no one taught
them how to do it. Through trial and error, they've developed their own techniques.
Visitors are often not welcome. And it would be safe to say that sprout businesses are
very small with around five to ten employees in each production.
In the 1980s, I think the secret about growing sprouts was no longer a secret. Sprout
growers in Taiwan decided it was more profitable to manufacture equipment to sell to the
sprout growers. Other growers in the United States caught on, and they, in turn, got in
the business of constructing and designing equipment for sprout growers.
With the competition among the equipment manufacturers, there was tremendous
improvement as far as the equipment was concerned. Sanitation became a very important
factor in the equipment design.
I'd like to go back, take a side track. Sanitation has always been a crucial factor in
the process of growing bean sprouts or alfalfa sprouts, basically because we are concerned
with the bacteria that affect the sprouts, themselves. That was the initial concern in the
If your sprouts were contaminated with a bacteria that are pathogenic to the sprouts,
you're going to have a very poor product, with absolutely no shelf life. And those
sprouters that remain in business are concerned with their products. They have to be very
cautious of the sanitation requirements because if the room is not sanitized, or the
growing mediums, the drums or trays that are being used, you're going to have a very poor
quality product. Your customer is going to know you're going to be out of business.
But in the 1980s the growers in New England, primarily organized, in an effort to
increase the sale of sprouts. This was the only area where they were able to get together
and do something such as this.
Other sprouters caught on to this and talked to them, and eventually that group
expanded, or started the expansion of what's now called the International Sprout Growers
Association. This organization held its first convention about 1989, along with the
produce marketing convention in San Antonio, Texas. And we have just had our eighth annual
convention in Orlando, Florida, this past June.
The ISGA, or International Sprout Growers Association, has a membership of just under
100. It is a very small organization relative to the number of sprout growers across the
United States. We have members in Canada, South America, South Pacific, from New Zealand,
Australia, Singapore. Still, it's a very small organization. We have only one paid
employee who's a part-time executive secretary.
Most of the work performed by the organization are basic volunteer work by all the
members who participate. To give you an example, I'm the member of the Board representing
the Pacific region. And the only reason I'm on the Board is because I'm the only one who
showed up at the convention. So, well, you're it.
But in California the ISGA data shows possibly that it may be 35 growers, and then
during the State health services, they did a survey of all possible growers in the State
of California, and they came up with a figure of anywhere between 70 to 80. I guess from
that figure we can safely estimate there are about 50 growers in the State of California.
Out of those 50 growers only 12 are members of the ISGA.
Because such a small percentage of growers are members in the ISGA, the lines of
communication between the industry association and the growers are very limited, almost
Again, sanitation has always been a topic for sprout growers. And the Association
established or started a committee to establish sanitation guidelines long before the
Salmonella outbreak started.
This came to the attention of the Association roughly in the summer of 1995 when there
were some documented outbreaks in Arizona and Michigan and parts of Canada. The sanitation
committee, which was already formed, now had an added task to address the Salmonella
As a result of the tremendous work by this committee over the last two years, the ISGA
has prepared for its membership the sanitation guidelines for the growing, packaging and
sale of fresh sprouts. This is similar or in line to what the WGA and International Fresh
Cut Organization has done. We have also prepared our paper in this regard. These
guidelines also included a model HACCP program, and are available to all growers for a
Now, the effect of the outbreak in 1996 was especially evident. The grower involved was
supposed to speak on the panel, and to, I guess, describe his experience with regulatory
agencies. And obviously he didn't show up because, as we later found out, he was no longer
So as members of the organization we saw firsthand the results of what could happen to
a sprout grower who had problems. And, you know, granted there are still sprout growers
out there who do have problems.
Dr. Farrar extended an invitation to the ISGA, because the ISGA was the only organized
body for sprout growers at the time. There are no local organizations, no State
organizations. Individual growers are very suspicious of each other. I don't believe a
whole lot of them are involved or even aware of the term "networking." So we
have problems trying to communicate with them.
But, anyway, from this initial invitation the members of the ISGA were made aware of
the invitation and were asked to attend, or as many across the nation could attend the
meeting in Sacramento.
From this initial invitation a small group of us continued to work with Dr. Farrar in
trying to exchange ideas, to give him a better understanding of the sprout industry. There
was a small group who were willing to volunteer their time and travel the distance to the
meetings. I think, again, it was a good two-way exchange of information. The regulators
learned a lot about the sprout industry, and the sprout growers learned a lot about
required sanitation practice.
The working group, itself, represented a broad spectrum of the sprout industry. There
were green sprouters, mung bean sprouters, large sprouters, medium and small sprouters,
organic sprouters and nonorganic sprouters. This active growing working group was
primarily from the Sacramento and San Francisco Bay Area, and myself, I represented the
central California area. There was no representation from any growers from the southern
California area. I think travel distance may have been a major factor in that regard. The
largest grower in the State did not participate.
Nevertheless the group was able to work together cohesively without compromising any
proprietary secrets, if there are any. We did use the ISGA guideline as a blueprint in
developing what we now call the Voluntary California Sprout Growing Guidelines.
After they were prepared and finalized, probably as of August 1997, these guidelines
were sent to all the sprout growers that were known at that time, along with a
questionnaire asking them about their interest in learning more about sanitation, along
with a mailer that they can obtain a more comprehensive sanitation guideline through the
The response to this mailing was less that what we had expected. Out of the
approximately 80 packages that were sent out, we received three responses concerning the
proposed free seminar. Only one of the responses came from somebody outside the working
group, itself. The ISGA received about three requests perhaps for copies of the sanitation
Based upon the growers limited response to the mailing, we can interpret this as a lack
of concern by sprout growers. On the other hand they could be very suspicious of
A majority of the sprout growers in California are not members of the ISGA. They are
perhaps uninformed of the many outbreaks of Salmonella and E.coli O157:H7 that are
linked to sprouts. Perhaps a few of the sanitation practices they already exercise are
more than adequate. After all, bean sprouts have been around for over a century with no
problems. And alfalfa sprouts, to their knowledge, have never been proven to directly
cause any food poisoning.
I'd like to consider this lack of concern as an example of Peking Duck syndrome. As you
know, Peking Duck is a specially prepared Chinese dish. It's known all over the world.
This dish has been around for centuries and enjoyed by many. Nobody has known to die from
eating Peking Duck. But in making Peking Duck, a raw uncooked duck is hung up for several
hours, or sometimes overnight, at room temperature. This process makes the skin crispy.
Under food and health standards this is illegal. I think from what I've read it's
illegal. And local and State officials several years ago attempted to put an end to this
practice. They were met with much resistance, and still they are often ignored. Chefs say
it's been done for, you know, this way for centuries and nobody has died from eating it.
Although the method for preparing Peking Duck is obviously unsafe, it has so-called
survived the test of time. And this would be perhaps the same attitude for the sprout
growers. But eventually, as far as the Peking Duck, whatever happened here is that a few
restaurant owners prevailed on one or two of their customers who happened to be a member
of the State Legislature, and through these consumers the chefs were able to obtain that
so-called Peking Duck exception to the health code.
Sprout growers have been growing sprouts for decades and believe they have done nothing
wrong. None of the customers, to their knowledge have gotten sick from eating sprouts.
They are proud of their products. And, in fact, the production processes have improved
over the last several years, compared with the practices utilized decades ago.
As a final comment I just want to just briefly say that I think the problem with
sprouters is that they are not informed, and not educated about the severity of Salmonella
and E.coli. Those of us who have participated with ISGA and through the communications in
that organization have become really aware of the severity of the situation.
A majority of the sprout growers are not members of the organization. They are not
aware, other than what they've read in the newspaper, that Salmonella outbreaks have been
statistically linked to sprouts. And to them that's a very vague concept.
A representative of the industry, we are taking a positive aggressive approach. The
industry is in jeopardy.
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