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Listeriosis affects many species including domestic and wild animals as well as man. The disease has been widely overlooked, but is found with increasing frequency when adequate search methods are used. Extraordinary laboratory procedures are required to reliably recover the causative organism, which usually is Listeria monocytogenes.

Listeriosis in a sheep flock

In late winter, signs of encephalitis started appearing in a flock of 345 lambs and ewes in 3 separate areas of the same midwestern farm.¹ A full-blown epidemic was obvious in 2 to 3 days. All had a sudden onset characterized by sluggishness and incoordination; specific neurologic signs were unilateral. Drooping of an ear, torticollis, circling, nystagmus and pupillary dysfunction, conjunctival discharge, pressing the head against objects, pyrexia, and rapid incapacitation were the common features. Ultimately, 57 lambs (16.5%) were involved; most became hopelessly ill, and most were euthanatized with 24 hours of onset. Listerial encephalitis was diagnosed at necropsy. In one pasture, 34% of the flock was involved, 8% was involved in a second pasture, and 2% of a third and more widely separated area were affected. The attending veterinarian answered questions posed by a veterinary student, who was an observer.

Q: How is a diagnosis made and confirmed?

A: The clinical condition of each animal and the epidemiologic picture of the herd or flock should include characteristics compatible with listeriosis (Fig 1). Laboratory testing is essential for confirmation; this usually involves bacteriologic culturing and isolation of the organisms from CNS tissue and/or histologic examinations.

Q: Is listeriosis usually fatal?

A: Probably not. It must be realized that only the most serious cases are likely to receive attention and laboratory confirmation; CNS tissue obtained for bacteriologic culturing automatically implies a near terminal illness. In this epidemic, the overall flock mortality was 16.5%, but the case-fatality rate approached 100%. Mild, self-limiting infections probably occur, but escape detection.

Q: What treatments can be used?

A: Antimicrobial agents are used commonly, but to be effective, they must not only be inhibitory to the Listeria sp, but also must have the ability to diffuse into the CNS in effective concentrations. Penicillin ampicillin, amoxicillin, tetracyclines, or others may be effective, but to alter the course of the disease, the drug of choice must be administered shortly after the onset of clinical signs.

Q: Don't you expect to see abortions?

A: Not necessarily, although they commonly are associated with the disease. In the epidemic described, there were none, though pregnant ewes as well as newborn lambs were affected.

Q: What is the usual source of infection for ruminants?

A: Common source epidemics usually are associated with the feeding of spoiled silage. Pockets of silage that spoil and do not develop a normal acidic pH (4.0 to 4.5) allow the growth of Listeria sp, which then reach infective concentrations. Single, sporadic cases often have no identifiable source of infection. We know that the fecal-oral cycle is important and that fecal carriers are not unusual (Fig 2).

Figure 2--Possible listeria infection cycles in man and domestic animals

Q: Why was there such a difference in the attack rates between the 3 groups?

A: The difference was related directly to the proximity of each group to the incriminated silo; the silage was hauled to each. The closest group had a 34% attack rate, followed by the group with 8%, located somewhat farther away. The third group was several miles away and received little of the silage; this group may even have been unaffected by the feeding of the silage and actually represented a normal or expected level of infection. This is the dose effect, although the actual content of L monocytogenes in each portion of silage would be more precise and meaningful.

Listerial mastitis in a milking cow

One cow in a high-quality milking herd developed mastitis at the end of her third lactation.² After delivering a healthy calf, the mastitis returned and was refractory to treatment. The cow was euthanatized. Listeria monocytogenes was isolated from her milk as well as from mammary and lymphoid tissue. The owner of the cow had the following questions for the attending veterinarian.

Q: Is listerial mastitis common, and how is it diagnosed?

A: It generally is considered unusual or rare. Special laboratory procedures must be used to reliably recover listeria; however, a bacteriologic laboratory would not use these methods for milk or mammary tissue unless requested.

Q: Other than silage, what sources of infection exist?

A: It is impossible to pinpoint sources of infection without specific strain identification techniques matching Listeria spp isolated from a source with a species recovered from an infected animal. Listeria organisms are added continuously to the environment by fecal carriers and allowed to remain until the level of hygiene is improved. Thus, a cow with listerial mastitis or encephalitis could have become infected from environmental sources such as soil, surface waters, dirty floors, or other sources indirectly associated with the fecal-oral cycle.

Q: How do feeds become contaminated?

A: The organisms are soil borne and are widely distributed by fecal carriers or by the farming practice of mechanically spreading manure. Thus, crop foliage can become contaminated. Organisms easily survive the harvesting and storage process; in fact, they reproduce in storage.

Food-borne listeriosis in human beings

Listeriosis was diagnosed in 41 human beings during a 3-month period.³ Thirty-four were perinatal cases characterized by acute febrile illness in a pregnant woman, followed by spontaneous abortion (5 cases), stillbirth (4 cases), live birth of a seriously ill premature or term infant (23 cases), or live birth of a well infant (2 cases); the case-fatality rate for infants born alive was 27%. In the women, fever and other signs of illness resolved rapidly after delivery. Seven adults (6 male and 1 nonpregnant female) ranged in age from 21 to 81. Six patients had meningitis, and 1 had aspiration pneumonia and sepsis; the case-fatality rate of patients with meningitis was 33%. There was no evidence of underlying immunosuppressive illness, a common feature in human listeriosis. Investigation of food histories revealed that all the adults had consumed coleslaw. Listeria monocytogenes was recovered from residual portions. Cabbage contained in the coleslaw originated from fields known to have been fertilized with sheep manure; listeriosis had been diagnosed on the farm, but diagnostic confirmations were not mentioned. In a meeting to discuss the epidemic, one of the attending physicians and a veterinarian from the area raised the following questions of a consulting epidemiologist.

Q: Doesn't this sound like the epidemic in sheep (previously discussed), except for the food vehicle?

A: They are remarkably similar in principle; Listeria spp can reproduce at 4 C, whether in a refrigerator or in a silo.

Q: But the clinical picture was not comparable, was it?

A: Not really. In this epidemic in human beings, more fetuses and neonates were affected than adults, abortions did occur, and meningitis rather than encephalitis predominated (Fig 1).

Q: Will Listeria organisms survive cooking?

A: No, proper cooking will always kill Listeria organisms. In this case, the coleslaw was not cooked.

Q: Isn't immunosuppression considered a high-risk factor in human infections?

A: Yes, but it apparently played no role in this epidemic. As with most infectious agents, an adequate quantity of the pathogen (numbers and virulence) can override body defenses and result in infection. Immunosuppression lowers the infection threshold so that fewer pathogens (numbers and virulence) can induce the disease.

Listeriosis in immunosuppressed adult human beings

Over a 2-month summer period, 42 adults and 7 fetuses or infants were affected. Sixteen (16/49, 33%) developed listerial meningitis, 31 (63%) developed septicemia, and 2 (4%) fetuses died; all adults had preexisting illness, and 14/49 (29%) of the group died.⁴ On the basis of food consumption histories, the investigators statistically linked the epidemic to the consumption of pasteurized milk; however, bacteriologic confirmation was lacking. The milk originated from farms in a cooperative, some of which were thought, but not adequately proven, to have experienced listeriosis. Samples of raw milk yielded several serotypes of L monocytogenes, but none was of the same serotype as those isolated from sick persons. The consulting epidemiologist answered questions posed during a meeting with several physicians and veterinarians involved in the issue of listeriosis transmission via milk.

Q: Did the cows producing the milk have listerial mastitis?

A: No, although it is possible. Listeria organisms are carried in the intestinal tract and shed in the feces, along with other microorganisms of enteric origin, which contaminate the environment. The finding of Escherichia coli in milk has the same implication of fecal contamination and is used as an indicator of the level of environmental hygiene involved in the processing of the milk.

Q: Can Listeria organisms survive pasteurization?

A: It is well accepted that Listeria organisms are not killed by low-temperature methods of pasteurization (eg, 35 minutes at 61.7 C); high-temperature pasteurization (eg, 71.6 C for 15 seconds) is believed to kill them under ordinary circumstances. Considerable research is being performed to answer important and contemporary questions such as the survivability of intraleukocytic Listeria organisms in milk undergoing pasteurization.

Human listeriosis from Mexican-style cheese

In a similar situation (lacking the preexisting illness), 86 new human cases of listeriosis were identified over a 6-month period; these cases were associated with the consumption of a Mexican-style cheese produced by a single manufacturer.⁵ Listeria spp were isolated from these cheeses. Information was not given regarding the heat treatment given the milk before production or of other possible sources of Listeria organisms. The epidemiologist answered another question regarding the likelihood of acquiring listeriosis by consumption of pasteurized milk products.

Q: Is inadequate pasteurization suspected in an epidemic like this?

A: Yes, but no more so than many other factors that may be involved. The raw milk and the entire plant should be sampled thoroughly for the presence of Listeria organisms before drawing conclusions. It is likely that if organisms were found elsewhere, they could have gained entrance into the milk after pasteurization (if pasteurized at all).

Direct transmission from a cow to a man

A 64-year-old male rancher assisted in the delivery of a calf, by inserting his hands and arms into the vagina and uterus of the cow. Within 24 hours, he developed a vesicular rash on his hands and arms, which progressed into pustules. In 48 hours, he developed generalized aches, chills, and fever. The same phage type of Listeria sp was isolated from the vagina of the cow and the pustules on the rancher's arm.⁶ The rancher had several questions in discussing this episode with his veterinarian.

Q: These manipulations are common; how could this have been prevented?

A: Careful washing of the hands and arms with a germicidal soap likely would have prevented the infection. Obstetric gloves and sleeves should be worn, as they prevent direct contact and are cleaned and disinfected more easily; disposable glove sleeves are excellent.

Q: Will normal disinfectants kill Listeria organisms?

A: Yes, the organisms have no special resistance to chemicals. Listeria organisms usually are contained within body secretions and excretions; therefore, the usual rule of cleaning thoroughly before the use of chemical agents must be observed.

Q: Do Listeria organisms enter through the skin?

A: As observed in this case, Listeria sp can induce superficial lesions followed by systemic dissemination. Obstetric procedures also require that the mucous membranes of the face be close to the source of infective fluids, so that exposure also may occur via the conjunctiva and the oral or nasal mucous membranes. It is best to be suspicious that an unusual infection is present before making an examination so that exceptional care may be exercised.

Q: What is considered to be exceptional care?

A: If fluids reached the face, assume that pathogens were contained within; remember that extensive aerosols are generated in such manipulations, so it is not only the easily noticed splash that is important. The face should be washed thoroughly with a germicidal soap, and mucous membranes should be flushed with clean water. One might carry a germicidal ophthalmic ointment for just such an occasion. Infection may result if sufficient numbers of organisms are inhaled. Being vigilant for later onset of fever or unexplained illness.

Immunosuppression, stress, and listeriosis

Stress or preexisting illness sets the stage for listerial infection; this effect is widely recognized in human infections, but is important in animals as well. Extremes of weather, changes or deprivation of food or water supplies, external or internal parasites, metabolic stresses, transportation, exogenous or endogenous adrenocorticosteroids, or other endocrine-related events have been suggested or proven to alter the resistance of an animal to infection. Noise of certain frequency content and level has also been shown to increase susceptibility to infection.⁷

Listeriosis itself has been found to induce marked splenic T-cell suppression⁸; splenectomy of genetically susceptible mice increased their resistance to infection with L monocytes.⁹ Read et al¹⁰ describe a case of L monocytogenes sepsis in a human patient with a small-cell carcinoma and acquired immune deficiency syndrome, who had an additional history of other opportunistic infections. Wetli et al¹¹ describe a death in a female Haitian patient having listeriosis with lymphopenia, which suggested to the authors that the patient also had acquired immune deficiency syndrome. Listeriosis also has been found in human patients having undergone organ transplantation, whether the organisms were transplanted by surgical exchange of tissues or were preexisting and activated by the use of immunosuppressive drugs used in conjunction with transplantation.^12,13

These cases illustrate the protean nature of listeriosis, the unique role of stress and immunosuppression in precipitating the disease, the ability of the infection itself to induce immunosuppression, and the large numbers of infections that occur but have no (described) source of the agent. We can logically suspect that animal infections directly or indirectly provide a reservoir for infections that develop in the human being.

Making a diagnosis of listeriosis

The often sporadic nature of listeriosis may desensitize the veterinary or medical clinician into a lack of recognition; however, the infection should be included in differential diagnoses. The framework of recognition and confirmation is provided in Figure 1. Different species have different syndromes; the epidemiologic characteristics point out risk factors, which should increase or decrease the suspicion of listeriosis. Isolation of the organism usually is essential for confirmation. The requirements for bacterial isolation are unique, and Listeria spp may not be recovered orrecognized unless a specific request is communicated to the diagnostic laboratory. When the cold enrichment method is used in the laboratory, an increased frequency of isolation of Listeria organisms will be the result. This method requires inoculation of a portion of the clinical material (Fig 1) into a series of broth tubes and incubation at 4 C. Every 2 to 4 weeks, plates are streaked out from the broth tubes (maintaining some tubes undisturbed so they do not become contaminated for future subculture). Listeria spp may be isolated 6 to 12 months or more after initial inoculation. Kampelmacher and van Noorle Jansen¹⁴ recommended cold enrichment in tryptose phosphate broth and the use of nalidixic acid-trypiflavine serum agar as a plating medium for primary attempts at isolation or for periodic plating from cold enrichment broth. Doyle and Schoeni¹⁵ described a selective enrichment procedure for the isolation of L monocytogenes from fecal and other biological specimens.

Although the principal target organ of listeric infection is the brain or meninges, reproductive tissues, mammary glands, and the spinal cord also can be involved to the exclusion of other organs. In the previously described silage-borne epidemic in sheep, 4 lambs had chronic paralysis of one or more limbs; L monocytogenes was isolated from lesions in the spinal cord.¹⁶ A listerial spinal cord abscess also was identified in a man occupationally exposed (undefined) to farm animals; the lesion was in the cervical spinal cord.¹⁷

One must carefully evaluate the isolation of organisms from an individual with illness, as Listeria spp can be recovered from a patient regardless of presence or absence of illness. As an example, studies in the Netherlands report the recovery of Listeria spp from about 70% of fecal specimens of normal healthy office and laboratory workers¹⁸; other reports reveal lower numbers of healthy carriers (eg, 5% of the general population).³ While data derived from animals are scarce, carrier rates are assumed to be comparable.

The question of resistance of Listeria organisms

Not only do Listeria spp reproduce slowly in cold temperatures and a pH close to neutrality,¹⁹ but the natural heat caused by the fermentation process in a silo likely causes a near-optimal temperature within the silage, even in the coldest of weather. Dijkstra²⁰ found some Listeria spp to survive for up to 12 years at 5 C in brain tissue, silage, feces, and milk.

Beyond this, the literature and evidence concerning the heat tolerance of Listeria spp is conflicting. It has been widely accepted that long-term pasteurization does not kill Listeria organisms, organisms in broth cultures do not survive 30 minutes at 60 C, and correct high-temperature pasteurization guarantees the destruction of Listeria spp.²¹ Kampelmacher²² reiterated that normal short-time, high-temperature pasteurization (71 to 72 C) kills all Listeria organisms in milk. Bradshaw et al²³ developed a comparable conclusion in their studies on thermal resistance.

Little attention has been paid to the thermal death of Listeria organisms in the intervening years, until the recent occurrence of the epidemics discussed herein. Beckers et al,²⁴ working in Holland, found Listeria organisms in 7 of 63 soft cheese specimens selected from wholesale distributors. One strain of L monocytogenes isolated from cheese was found to survive in significant numbers at 80 C for 1 minute; this finding raised the question of the comparability of different means of determining the thermal death point of Listeria spp. Doyle et al²⁵ explored this possibility by artificially infecting 4 milking cows and sampling the milk of 3. They found that L monocytogenes, when contained inside leukocytes, apparently survived high-temperature pasteurization. As the conditions of the experimental inoculations were strenuous and the number of subjects limited, one may well question whether intraleukocytic Listeria may react the same under conditions more like those encountered naturally. The whole question of heat resistance and reservoirs of Listeria spp needs further examination before definitive and reproducible facts concerning the zoonotic potential of milk-borne listeriosis will be elucidated.

Figure 1--Progression of diagnostic events in listeriosis. A--Clinical findings triggering suspicion of listeriosis. B--Epidemiologic characteristics. C--Diagnostic tests.

Figure 2--Possible listeria infection cycles in man and domestic animals.

References

1. Blenden DC, Gates GA, Silberg SL. Epidemiological studies on an outbreak of listeriosis in a sheep flock, in Proceedings. 3rd Int Symp Listeriosis 1966; 233-241.

2. Gitter M, Bradley R, Blampied PH. Listeria monocytogenes infection in bovine mastitis. Vet Rec 1980; 103:390-397.

3. Schlech WF III, Lavigne PM, Bortolussi RA, et al. Epidemic listriosis--evidence for transmission by food. N Engl J Med 1983; 308:203-206.

4. Fleming DW, Cochi SL, MacDonald KL, et al. Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N Engl J Med 1985; 312:404-407.

5. Listeriosis outbreak associated with Mexican-style cheese--California. MMWR 1985; 34:357-359.

6. Cain DB, McCann VL. An unusual case of listeriosis. J Clin Microbiol 1986; 23:976-977.

7. Jensen MM, Rasmussen AF Jr. Audiogenic stress and susceptibility to infection. In: Welch BL, Welch AS, eds. Physiological effects of noise. New York: Plenum Publishing Corp, 1970; 719.

8. Chan YY, Cheers C. Mechanism of depletion of T lymphocytes from the spleen of mice infected with Listeria monocytogenes. Infect Immun 1982; 38:686-693.

9. Wood PR, Young AM, McKimm-Breschkin JL, et al. Effect of splenectomy on production of interferon and colony-stimulating factor in Listeria monocytogenes-infected mice. Infect Immun 1984; 46:860-861.

10. Read EJ, Orenstein JM, Chorba TL, et al. Listeria monocytogenes sepsis and small cell carcinoma of the rectum: an unusual presentation of the acquired immunodeficiency syndrome. Am J Clin Pathol 1985; 83:385-389.

11. Wetli CV, Roldan EO, Fojaco RM. Listeriosis as a cause of maternal death: an obstetric complication of the acquired immunodeficiency syndrome (AIDS). Am J Obstet Gynecol 1983; 147:7-9.

12. Stamm AM, Dismukes WE, Simmons BP, et al. Listeriosis in renal transplant recipients: report of an outbreak and review of 102 cases. Rev Infect Dis 1982; 3:665-682.

13. Higgins TL, Mallek JA, Slugg PH. Listeria monocytogenes endocarditis on a prosthetic heart valve. South Med J 1983; 76:675-676.

14. Kampelmacher EH, van Noorle Jansen LM. Listeriosis in humans and animals in the Netherlands (1958-1977). Zentralbl Bakteriol Parasitenkd Infektionskr Hyg Abt 1: Orig Peihe A 1980; 246:211-227.

15. Doyle MP, Schoeni JL. Selective enrichment procedure for isolation of Listeria monocytogenes from fecal and biologic specimens. Appl Environ Microbiol 1986; 51:1127-1129.

16. Gates GA, Blenden DC, Kintner LD. Listeria myelitis in sheep. J Am Vet Med Assoc 1967; 150:200-204.

17. Morrison RE, Brown J, Gooding RS. Spinal cord abscess caused by Listeria monocytogenes. Arch Neurol 1980; 37:243-244.

18. Kampelmacher EH, van Noorle Jansen LM. Further studies on the isolation of L monocytogenes in clinically healthy individuals. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg Abt 1: Orig Peihe A 1972; 221:70-77.

19. Blenden DC, Gates GA, Khan MS. Growth of Listeria monocytogenes in a corn extract silage medium. Am J Vet Res 1968; 29:2237-2242.

20. Dijkstra RG. Recent experiences on the survival times of Listeria bacteria in suspensions of brain, tissue, silage, faeces and in milk. In: Woodbine M, ed. Problems of listeriosis. Leicester, England: Leicester University Press, 1975; 71-73.

21. Seeliger HPR. Listeriosis. New York: Hafner Publishing Co, 1961; 11.

22. Kampelmacher EH. Animal products as a source of listeric infection in man, in Proceedings. 2nd Int Symp Listeric Infect 1962; 146-156.

23. Bradshaw JG, Peeler JT, Corwin JJ, et al. Thermal resistance of Listeria monocytogenes in milk. J Food Protect 1975; 48:743-745.

24. Beckers HJ, Soentoro PSS, Delfgou-von Asch EHM. The occurrence of Listeria monocytogenes in soft cheese and raw milk and its resistance to heat. Int J Food Microbiol, 1987; 4:249-256.

25. Doyle MP, Glass KA, Beery JT, et al. Survival of Listeria monocytogenes in milk during high-temperature, short-time pasteurization. Appl Environ Microbiol 1987; 53:1433-1438.

Addendum

Bunning et al¹ conclude that Listeria monocytogenes organisms, phagocytized by in vitro populations of neutrophils (predominantly), do not have increased resistance to the temperatures of pasteurization. A World Health Organization working group on food borne listeriosis concluded in 1988 that current information supports the position that pasteurization is a safe process to reduce the number of L monocytogenes in raw milk to concentrations that do not pose appreciable health risk to human beings.² Improperly performed pasteurization and contamination after pasteurization are the most likely explanations for L monocytogenes in milk.³ However, the organisms are commonly found not only in raw milk, but in vegetable products⁴ and other sources, most likely in direct proportion to the intensity of the search.

References

1. Bunning VK, Donnelly CW, Peeler JT, et al. Thermal inactivation of L monocytogenes within bovine milk phagocytes. Appl Environ Microbiol 1988; 54:364-370.

2. Foodborne listeriosis. Bull WHO 1988; 66:421-428.

3. Update-listeriosis and pasteurized milk. MMWR 1988; 37:764-766.

4. Vegetables are potential sources of Listeria. ASM News 1989; 55:591.

Addendum (1995)2

This addendum was prepared by F. T. Satalowich, DVM, MSPH and D. C. Blenden, DVM, MS

Despite its description almost 75 years ago, listeriosis is still considered an oddity and a new disease by many clinicians. Awareness of this infection must be high for it to be suspected and for the necessary laboratory studies to be done. There are now 7 species of the genus Listeria recognized. Those that are hemolytic are: L monocytogenes, L ivanovii, and L seeligeri; those that are nonhemolytic are: L innocua, L welshimeri, L grayi, and L murrayi. The first two of the hemolytic species are considered to be the pathogens, presumably related to the presence of a hemolytic enzyme listeriolysin O. These organisms are ubiquitous, providing multiple risks of exposure, but largely involve the fecal-oral cycle. Episodes of human infection have occurred in recent years, mostly related to contaminated foods.^1-3 Foods implicated were raw milk or unpasteurized dairy products, cold meats, and raw vegetables. The discovery of Listeria sp in pasteurized dairy products brought into question the effectiveness of the process.⁴ However, it has been concluded⁵ that L monocytogenes organisms, phagocytosed in vitro by populations of neutrophils, do not have increased resistance to the temperatures of pasteurization. A World Health Organization working group on food-borne listeriosis concluded in 1988 that pasteurization is a safe process to reduce the number of L monocytogenes in raw milk to numbers that do not pose appreciable health risk to consumers.⁶ Improperly performed pasteurization and contamination after pasteurization are the most likely explanations for L monocytogenes in milk.⁷ Never to be ignored is the capability of Listeria sp to reproduce at temperatures close to freezing, normally thought to be adequate for food storage. Thus, reduction by pasteurization of a population of Listeria sp to almost zero, may be reversed by replication during storage at < 4 C. The addition of flavoring materials (eg, chocolate⁴) after pasteurization provides additional possibilities.

Most listeriosis develops in people that are immunocompromised or otherwise more vulnerable, such as the elderly or pregnant, and the fetus or newborn infants.⁸ Although not as common as other secondary infections in human immunodeficiency virus (HIV)-infected people, listeriosis is seen about 300 times more frequently in them than in the general non-HIV-infected population. Surveillance for listeriosis was conducted by Centers for Disease Control in 1986.⁹ It was estimated that there were 1,700 human cases in the United States during that year for an incidence of 7.1 per 100,000. The sources for these mostly sporadic cases remain largely unknown, although food sources and oral infection seem to be most important; the infective doses and incubation periods of sporadic cases are likewise quite uncertain.

Because it seems impossible to eliminate the Listeria organism from the natural environment,¹⁰ minimizing opportunity for exposure is the only preventive alternative. The consumer should take simple precautions, such as personal and food hygiene, careful washing of vegetable foods, proper cooking of foods, and awareness of risk of extended storage of foods even near freezing temperatures.

References

1. Vegetables are potential sources of Listeria. ASM News 1989;55:591.

2. Outbreak of listeriosis in 1992. Wkly Epidemiol Record (WHO) 1993;26 March:89-92.

3. Jones D. Foodborne listeriosis. Lancet 1990;336:1171-1174.

4. Pearson LJ, Marth EH. Listeria monocytogenes-threat to a safe food supply: a review. J Dairy Sci 1990;73:912-928.

5. Bunning VK, Donnelly CW, Peeler JT, et al. Thermal inactivation of L monocytogenes within bovine milk phagocytes. Appl Environ Microbiol 1988;54:364-370.

6. Foodborne listeriosis. Bull WHO 1988;66:421-428.

7. Update-listeriosis and pasteurized milk. MMMR Morbid Mortal Wkly Rep 1988;37:764-766.

8. Schuchat A, Swaminathan B, Broome CV. Epidemiology of human listeriosis. Clin Microbiol Rev 1991;4:169-183.

9. Gellin BG, Broome CV. Listeriosis. JAMA 1989;261:1313-1320.

10. Listeriosis: the situation 2 years after the outbreak caused by "Vacherin Mont-d'Or" soft cheese. Wkly Epidemiol Record (WHO) 1991;1 Feb:28-29.