Symposium on Infectious Diseases — February 2017
Tex Med. 2017;113(2):39-41.
By Linda Gaul, PhD, and John Hellerstedt, MD
Protecting the public from communicable infectious disease outbreaks is one of the most important, and most challenging, functions of public health. Foodborne outbreaks are not uncommon, and they can be especially difficult. This true story of the epidemiologic investigation into a typhoid fever outbreak illustrates the critical importance of timely reporting by front-line clinicians, extensive interprofessional teamwork, and statewide coordination.
The First Call
This is a story of first-rate scientific detective work. It demonstrates the benefits that can flow from combining advanced science with tenacious dedication and hard work.
The first call came to the lead foodborne illness epidemiologist at the Austin headquarters of the Texas Department of Health (TDH, now the Texas Department of State Health Services) one morning in late August 2003. The caller was an epidemiologist at the City of Houston Department of Health and Human Services. "I'm investigating a case of typhoid fever, and I've been talking with the epidemiologist in the Montgomery County Department of Health and Human Services [MCHHS], who is also investigating a case of typhoid fever. We're wondering which of the Centers for Disease Control and Prevention [CDC] forms we should use to report these cases."
The call piqued the interest of the TDH epidemiologist because of the unusual occurrence of two cases of typhoid fever occurring in the same area of the state during the same time period. Typhoid fever, caused by Salmonella enterica serotype Typhi bacteria, is rare and not endemic within the United States. About three dozen cases are reported annually in Texas, and nearly all are linked to travel outside the United States. However, the two new case-patients had not traveled outside the country during their incubation periods, which average 33 days but can be as long as three months. The more stunning news: The organisms from the two case-patients had the same molecular fingerprint. That meant the cases were most likely caused by a contaminated food. Now, it would be up to the epidemiologists to determine what that food was.
The molecular fingerprint used in this case was PFGE, or pulsed-field gel electrophoresis, a method of bacterial molecular subtyping. The treating physicians had ordered tests to determine the cause of the illness. Once the culprit has been isolated and grown in the lab, a series of tests, including PFGE and molecular subtyping, can be performed. The subtyping results are uploaded to the PulseNet laboratory network, an electronic database maintained by CDC.
Once in PulseNet, public health epidemiologists around the country can compare the organisms recovered in their jurisdictions with those from other areas. The epidemiologists are notified when their isolates match (or very closely resemble) PFGE patterns found in other cases. This matching function allows outbreaks to be identified that previously would have gone undetected because the cases were few in number or located far apart. For this outbreak, there were no similar isolates outside of Texas.
During the first round of information gathering, the two Houston-area adult male case-patients were interviewed at length, but no common food or other exposure was identified. Both reported eating most meals in their own residences. These two cases were not the end.
A few days later, the TDH epidemiologist was notified of a third case, also in Harris County but within the jurisdiction of the Harris County Department of Public Health and Environmental Services. The specimen from this adult female grew out S. Typhi with the same PFGE pattern as the first two cases. This individual had also not traveled outside the United States before her illness onset. Further in-depth interviews did not reveal a likely common source for the three illnesses.
The TDH epidemiologist knew there had to be a common exposure because the PFGE patterns were not only highly similar but also rare. She hypothesized that the food vehicle was an unusual food item — probably a food that is normally eaten without being cooked. She suggested the epidemiologists reinterview the case-patients using a more extensive 14-page questionnaire. The questionnaire gathered names of places where the individuals had eaten and food items of specific concern, such as condiments (e.g., banana peppers), as well as raw animal protein items, including raw oysters. (Raw, protein-containing foods of animal origin — oysters, raw milk, and steak tartare — are considered delicacies by some.)
The female case-patient had especially good recall for the foods she ate and the names of the establishments where she dined during the several months before her illness. She was thorough. She checked her credit card receipts and confirmed dates for the meals eaten away from home. She reported consuming raw oysters on two occasions at the same establishment in her area. Neither of the two male case-patients reported they had consumed raw oysters or eaten at the same food establishment. Neither man reported eating raw oysters during the several months before illness onset. When the results were analyzed, no common food items were reported eaten by all three case-patients during their potential incubation period for typhoid fever.
The TDH epidemiologist was not deterred: "What we need now is another case." She believed the common food item consumed was raw oysters, even though the two male case-patients couldn't recall if or when they may have eaten them during the incubation period. At this point, there was nothing to do except wait and see if other cases would be reported.
As (bad) luck would have it, about a week later, another PFGE-matching case of S. Typhi was reported. This newest case-patient, also an adult male, lived in the San Antonio area. When interviewed using the long questionnaire, he reported having traveled to Galveston several weeks before his illness and eating raw oysters there once. But, again, all four outbreak case-patients reported no common food item. Once again, the TDH epidemiologist said, "What we need now is another case." She had a strong suspicion that raw oysters were the culprit food item, but there simply weren't enough cases reporting them to proceed with investigations of that potential source.
The pace of the outbreak picked up. Two additional cases with the same PFGE patterns as the first four cases were reported two days later. Both adult male case-patients lived in Austin and had not traveled outside Travis County during the several months before their illness. The six outbreak case-patients had developed illness during a three-week period between mid-July and early August; four were hospitalized for their illnesses.
There was clearly a food item in commercial distribution that was contaminated with S. Typhi, but its identification was eluding investigators. With a small number of cases, and considering the long potential incubation period and the difficulty most people have remembering what they have eaten even within the past few days, this lack of conclusive proof was not surprising. It was, however, frustrating. The public health investigators were anxious to get the causal food item out of circulation and prevent more serious illnesses.
The Austin/Travis County Health and Human Services Department (ATCHHSD) epidemiologist attempted to interview the two new case-patients. She interviewed one, using the 14-page questionnaire modified to include several Austin-area eating establishments. The case-patient reported consuming raw oysters at a restaurant in Austin before his illness onset, though he couldn't remember the date. The epidemiologist was not able to contact the other case-patient. She called him multiple times and even went to his home, leaving a business card and a questionnaire for him to complete. He did not respond. Finally, after several weeks, the case-patient called and was interviewed. He had been hospitalized for his serious illness, and without health insurance he was working long hours to pay for his large medical bills and to make up for lost pay. He did not report eating any raw oysters. Still, no common food item was being reported by all six outbreak cases.
The interim health authority for ATCHHSD was concerned and frustrated when he learned the two Austin cases were part of the outbreak and it had not yet been solved. He suggested that he, the ATCHHSD, TDH epidemiologists, and the two Austin case-patients meet and see if the two men might recall something that could lead to the identification of a common food establishment and common food item. Because the case-patients agreed to discuss their illnesses with each other, confidentiality laws would not be violated. During a dinner meeting, conversation about the two men's illnesses flowed easily. In fact, they determined they had both eaten at the same restaurant before their illness onsets. And the restaurant served raw oysters.
The case-patient who had previously reported he likely ate raw oysters now recalled this had occurred on either a Monday or Tuesday evening in mid-July and possibly again a week later. When he heard the name of the restaurant, the second case-patient remembered he had also eaten at that establishment at about the same time. He said it would have been on a Monday evening, as he went to watch preseason Monday night football. He also recalled that although he didn't usually eat raw oysters, he did once because he wanted to catch the attention of a cute-looking waitress. As the two men compared dates on their calendars, they realized they both ate at the restaurant on the same Monday in July.
Meanwhile, the first two case-patients identified in the outbreak had contacted their local health departments and reported they remembered eating raw oysters more than once. The two men did not eat the oysters at any of the same restaurants.
When the TDH epidemiologist first suspected raw oysters were the typhoid fever vehicle in the outbreak, she contacted the head of the department's Seafood Safety section, which is responsible for inspecting and investigating the harvesting, packing, and shipping establishments that provide raw oysters to restaurants and stores. These are vital functions, as raw oyster consumption is associated with severe and often fatal infections, particularly among immunocompromised people. The usual culprit bacterium is Vibrio vulnificus, which normally inhabits the warm coastal waters of the Gulf of Mexico. Immunocompromised people who consume raw oysters or who have a break in their skin while wading in the Gulf can develop V. vulnificus septicemia within a few days. These infections are often fatal. In Texas, about a dozen cases each year are reported that are linked to raw oyster consumption, and about half of these case-patients die.
When a case of V. vulnificus infection or similarly serious seafood-related illness is reported, the Seafood Safety section investigates the establishment. Raw oysters, because of their risk for being the source of potentially serious food-borne illness, must, by law, bear tags indicating exactly when, where, and by whom they were harvested. These tags must be retained by the eating establishment for at least 90 days. This tag requirement makes it possible to trace raw oysters consumed by an ill person back to the oysters' source. Most contaminated food items cannot be traced so readily.
The Seafood Safety director worked with the regional and local health departments with jurisdiction where the case-patients lived. The health department staff members contacted the restaurants where the case-patients had reported eating and obtained copies of the oyster tags potentially relevant for the patients' illnesses. (Because oysters can be sold for up to two weeks after harvest, and a restaurant might obtain raw oysters from several different sources, it isn't always clear which oysters might have caused a patient's illness.) The Seafood Safety director compiled the information into a spreadsheet and sent it to the department's epidemiologist. The table showed the answer they had all been looking for: All six case-patients had consumed raw oysters on at least one occasion that were harvested from the same area of the Gulf of Mexico, by the same raw oyster dealer, by the same boat and the same crew. The implicated oysters were harvested over a 12-day period. The mystery had been solved using advanced scientific detective skills and dogged perseverance.
It remained to be determined if any of the implicated oysters were still in commerce. By the time the mystery had been solved, at least two months had passed since the oysters had been harvested. The TDH Seafood Safety director worked with the oyster dealer to determine where oysters harvested from the specific area of the Gulf during the period of harvest for the outbreak case-patients had been shipped. All of these establishments were contacted, and none had any product remaining from that time period. It turned out that a different nearby dealer had purchased some oysters from the implicated dealer because he couldn't harvest enough oysters to meet his customers' demand.
This second dealer sold only raw oysters he treated using an approved post-harvest treatment process demonstrated to reduce V. vulnificus bacteria to below-detectable levels. The process involved flash freezing and holding below freezing for a period of time. What this dealer didn't know was that bacteria are not readily killed by freezing temperatures. In fact, all strains of Salmonella are quite hardy. The Seafood Safety director collected 30 samples of the implicated oysters, which had been comingled with other oysters, but none were found to contain S. Typhi. All workers still employed with the dealer provided clinical specimens for testing, but none grew S. Typhi. The director also required that the dealer destroy all remaining implicated product he possessed.
The source of the oyster contamination that caused the outbreak could not be identified. It could have occurred at the harvest site, which was near the Houston ship channel where many ships pass and one might have (illegally) discharged S. Typhi-contaminated sewage. Or a worker on the harvesting boat might have dumped urine or sewage over the side of the boat. It most likely occurred while the oysters were still in the bay waters, as during and after harvest the oysters' shells would remain closed until pried open for consumption. The best news was that no additional cases had been detected.
This is an especially dramatic example of the protection that the high-tech, highly trained, and dedicated members of the public health community provide to Texans every day.
We hope that the physician and health care professional community will take special note of the fact that, in each case, this serious and potentially fatal communicable infectious disease only came to the attention of the public health response team because of the knowledge, skill, and diligence of the professionals involved. The treating physicians had to have an index of clinical suspicion sufficient to order testing, and the laboratories had to have the skill to identify the culprit and take the steps required to report their finding. Only then could public health take action to identify and remedy the source.
The teamwork of professional acumen, laboratory expertise, and public health investigation is the basis for all of our efforts to protect the public. Remember: The public is all of us.
Linda Gaul, PhD, is the state epidemiologist. She was a faculty member in biological sciences at The University of Texas at Austin for 11 years.
John Hellerstedt, MD, is commissioner of the Texas Department of State Health Services. Before that he served as chief medical officer of the Seton Family of Hospitals.