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Campylobacter jejuni Infections: Updateon Emerging Issues and Trends Ban Mishu Allos
Departments of Preventive Medicine and Medicine, Division of Infectious Diseases, Vanderbilt University School of Medicine, Nashville, Tennessee Infection with Campylobacter jejuni is one of the most common causes of gastroenteritis worldwide; it occurs more frequently
than do infections caused by Salmonella species, Shigella species, or Escherichia coli O157:H7. In developed countries, the
incidence of Campylobacter jejuni infections peaks during infancy and again during early adulthood. Most infections are
acquired by the consumption and handling of poultry. A typical case is characterized by diarrhea, fever, and abdominal
cramps. Obtaining cultures of the organism from stool samples remains the best way to diagnose this infection. An alarming
recent trend is the rapid emergence of antimicrobial agent-resistant Campylobacter strains all over the world. Use of antibiotics
in animals used for food has accelerated this trend. It is fortunate that complications of C. jejuni infections are rare, and
most patients do not require antibiotics. Guillain-Barre' syndrome is now recognized as a post-infectious complication of C.
jejuni infection, but its incidence is !1 per 1000 infections. Careful food preparation and cooking practices may prevent
some Campylobacter infections.
Campylobacter jejuni infection is one of the most commonly 1957 [4], and their impact in terms of sheer numbers of human identified bacterial causes of acute gastroenteritis worldwide. In infections emerged only in the past 20 years. The first recog- developing countries, Campylobacter species are an important nized Campylobacter infections were reported in the early part cause of childhood morbidity caused by diarrheal illness. They of the 20th century and occurred in farm animals. The infec- are among the most common causes of diarrhea in travelers tions were attributed to Vibrio fetus (now known to be Cam- from developed nations. Remarkably, in many studies in the pylobacter fetus) and were realized by veterinarians to be a cause United States and other industrialized countries, Campylobacter of septic abortions in sheep and cattle. In 1947, V. fetus was infections were found to cause diarrheal disease 12-7 times as reported to be the cause of septic abortion in a woman, and frequently as infections with Salmonella species, Shigella species, during the next 3 decades, the organism was believed to be a or Escherichia coli O157:H7 [1, 2]. Although 14 species of Cam- rare, opportunistic, invasive pathogen that occurred principally pylobacter have been identified, in the United States 199% of reported infections with Campylobacter are with C. jejuni [3].
In 1973, the new genus Campylobacter was proposed [5].
Therefore, this paper will be limited to a discussion of C. jejuni. Finally, the development and increasingly widespread use ofselective media for isolation of Campylobacter from stool sam-ples in the 1970s led to the recognition in the early 1980s of the importance of these infections as a cause of human gas- Despite their widespread occurrence, Campylobacter species trointestinal illness. By the mid-to-late 1980s, it had been de- were not understood as a cause of diarrhea in humans until termined that Campylobacter species are one of the most com-mon bacterial causes of diarrhea worldwide.
Received 4 August 2000; revised 4 December 2000; electronically published 28 March Reprints or correspondence: Dr. Ban Mishu Allos, A3310 Medical Center North, Division MICROBIOLOGY
of Infectious Diseases, Vanderbilt University School of Medicine, Nashville, TN 37232(Ban.Mishu.Allos@mcmail.vanderbilt.edu).
Campylobacter species are gram-negative bacilli that have a Clinical Infectious Diseases
2001; 32:1201-6
curved or spiral shape (hence their initial classification as vib- 2001 by the Infectious Diseases Society of America. All rights reserved.
rios). Recently, the complete genome sequence of C. jejuni was • CID 2001:32 (15 April) • 1201
characterized. Of note was the finding of hypervariable regions not yet a standard practice. Species-specific assays, such as PCR- that might be important in the survival of the organism [6].
enzyme-linked immunosorbent assays to detect Campylobacter Campylobacter species are motile by means of unipolar or bi- antigens in stool samples, have been developed and also may polar flagellae. The organisms grow quite slowly; 72-96 h are become useful in the diagnosis of Campylobacter infections required for primary isolation from stool samples, and isolation from blood can take even longer. They grow best at 42ЊC.
Because most Campylobacter species are resistant to cephalothin(an agent to which most other stool flora are susceptible), the COMPLICATIONS OF CAMPYLOBACTER
usual method for isolation from stool samples is use of a me- INFECTIONS
dium that contains cephalothin. Because some Campylobacterspecies, especially non-jejuni Campylobacter species, are sus- Local complications of Campylobacter infections occur as a re- ceptible to cephalothin, the filter method and antibiotic-free sult of direct spread from the gastrointestinal tract and can media should be used if initial results of cultures are negative include cholecystitis, pancreatitis, peritonitis, and massive gas- and the suspicion of Campylobacter infection is high. This trointestinal hemorrhage. Extraintestinal manifestations of method involves first filtering the stool onto an antibiotic-free Campylobacter infection are quite rare and may include men- medium through 0.45-0.65-mm filters; the filters will block the ingitis, endocarditis, septic arthritis, osteomyelitis, and neonatal passage of most stool flora but will permit the passage of smaller sepsis. Bacteremia is detected in !1% of patients with Cam- bacteria such as Campylobacter species [7].
pylobacter enteritis and is most likely to occur in patients whoare immunocompromised or among the very young or veryold [12]. Transient bacteremia in immunocompetent hosts with CLINICAL CHARACTERISTICS
C. jejuni enteritis may be more common but not detected be- OF CAMPYLOBACTER GASTROENTERITIS
cause most strains are rapidly cleared by the killing action ofnormal human serum and because blood cultures are not rou- Most typically, infection with C. jejuni results in an acute, self- tinely performed for patients with acute gastrointestinal illness.
limited gastrointestinal illness characterized by diarrhea, fever, Serious systemic illness caused by Campylobacter infection and abdominal cramps. Clinically, Campylobacter infection is rarely occurs but can lead to sepsis and death. The case-fatality indistinguishable from acute gastrointestinal infections pro- rate for Campylobacter infection is 0.05 per 1000 infections.
duced by other bacterial pathogens, such as Salmonella, Shigella, The most important postinfectious complication of C. jejuni and Yersinia species. In most patients, the diarrhea is either infection is the Guillain-Barre' syndrome (GBS). GBS is an acute loose and watery or grossly bloody; 8-10 bowel movements demyelinating disease of the peripheral nervous system that per day occur at the peak of illness [2]. In some patients, the affects 1-2 persons per 100,000 population in the United States diarrhea is minimal and abdominal cramps and pain are the each year. Although C. jejuni infections are a common trigger predominant features; this can lead to a mistaken diagnosis of of GBS (probably preceding 30% of GBS cases), the risk of acute abdomen and unnecessary laparotomy. Fever is reported developing GBS after C. jejuni infection is actually quite small by 190% of patients and can be low-grade or 140ЊC and persist (!1 case of GBS per 1000 C. jejuni infections) [13]. The risk for up to 1 week. By that time, the illness has usually resolved, of developing GBS is increased after infection with certain Cam- even in the absence of specific antibiotic treatment. Occasion- pylobacter serotypes. In the United States, Penner type O:19 is ally, however, patients can develop a longer, relapsing diarrheal most commonly associated with GBS [14]; in South Africa, illness that lasts several weeks [8]. Although Campylobacter is Penner type O:41 is the serotype most frequently associated rarely identified in the stools of healthy persons, depending upon the population studied, as many as 50% of persons who GBS that occurs after C. jejuni infection is usually a more are infected during outbreaks are asymptomatic [9].
severe disease, associated with extensive axonal injury, a greater Fecal leukocytes and RBCs are detected in the stools of 75% likelihood of the need for mechanical ventilation, and increased of infected persons [10]. The peripheral WBC count may be risk of irreversible neurological damage. In contrast, the severity mildly elevated. Other laboratory studies, including liver func- of C. jejuni infection is not associated with an increased risk tion, electrolytes, and hematocrit levels, are normal. Because of the development of GBS. Indeed, many GBS-associated C. diffuse colonic inflammation may be seen on sigmoidoscopic jejuni infections are asymptomatic [15]. Because the neurolog- examination, Campylobacter enteritis may be confused with ical symptoms of GBS that follow C. jejuni infection typically early inflammatory bowel disease. Diagnosis of Campylobacter occur 1-3 weeks after the onset of diarrheal illness, humoral enteritis is confirmed by obtaining cultures of the organism immunopathogenic mechanisms are likely involved. Molecular from stool samples. Some laboratories have begun performing mimicry between peripheral nerve glycolipids or myelin pro- PCR analysis on stool samples for Campylobacter, but this is teins and structures on the lipopolysaccharides of some Cam- 1202 • CID 2001:32 (15 April) • FOOD SAFETY
Rates of selected enteric bacterial infections
pylobacter strains likely plays a role in the pathogenesis of Cam- detected by the Foodborne Active Surveillance Network
of the Centers for Disease Control and Prevention (United
Persons with the HLA-B27 histocompatibility antigen are States, 1996-1999).
prone to the development of reactive arthritis several weeksafter infection with Campylobacter [17]. Other postinfectious complications of infection include uveitis, hemolytic anemia, hemolytic uremic syndrome, carditis, and encephalopathy.
EPIDEMIOLOGY
Incidence.
In the United States, Campylobacter infections became reportable illnesses in many states in the early 1980s; Active surveillance was done in Maryland, Oregon, se- however, from the outset, the reporting systems routinely un- lected counties in California, Connecticut, and Georgia. Table is mod- derestimated the impact of these infections. In the early years of Campylobacter surveillance, many hospital microbiology lab-oratories did not seek Campylobacter when they performedstool cultures for other enteric pathogens. Later studies con- early 1980s, the infections have demonstrated a marked sea- firmed that when diarrheal stool samples were cultured for sonal distribution, with a surge that begins in May and peaks Campylobacter every time they cultured for Salmonella or Shi- gella, Campylobacter was identified 2-7 times more frequently Sources and transmission of infection.
than was Salmonella or Shigella. Even currently, estimates have important route of Campylobacter infections in the United shown that only 1 in 38 cases of detected Campylobacter in- States and other industrialized nations remains the consump- tion and handling of chicken. In studies in many parts of the Accurate estimates of the true incidence of Campylobacter United States, Europe, and Australia, 50%-70% of all Cam- infections in the United States and other industrialized nations pylobacter infections have been attributed to consumption of depend upon many data sources. In 1996, the Emerging In- chicken [20-22]. Perhaps this should not be surprising in light fections Program Foodborne Diseases Active Surveillance Net- of the frequency with which poultry products are consumed work (Foodnet) of the Centers for Disease Control and Pre- and the nearly universal contamination of chicken carcasses vention (CDC) began the collection of data on 9 foodborne with Campylobacter [23]. Indeed, it has been estimated that illnesses in selected United States cities. In the first year, Cam- just 1 drop of chicken juice may contain 500 infectious or- pylobacter was detected more frequently than was any other ganisms [24]. Even with strict attention to good handwashing pathogen-more frequently than Salmonella and Shigella com- and cleaning of cutting boards, it is easy to see how simple bined. However, from 1996 through 1999, the incidence of errors in the handling of food might result in cross-contami- Campylobacter infection decreased 26%, although the organism nation in the kitchen and, therefore, human illness. Because remained the most commonly identified enteric pathogen [19] heat kills viable Campylobacter species, thorough cooking of (table 1).The decreased rates were attributed to disease pre- chicken should be emphasized as an important food-safety vention efforts that had been implemented in food service es- tablishments, meat and poultry processing plants, and egg pro- Other foods and activities also have been implicated as duction farms [19]. Currently, the CDC estimates that 2.4 sources of Campylobacter infection. Although outbreaks of in- million cases of Campylobacter infection occur in the United fection account for a small fraction of Campylobacter infections States each year, involving almost 1% of the entire population in humans (most infections are sporadic), consumption of un- pasteurized milk is the most frequently reported cause of out- Demographic data.
The age and sex distributions of Cam- breaks of infection [3]. Other sources of sporadic infection pylobacter infections are unique among bacterial enteric path- include sausages or red meat (especially in Scandinavian coun- ogens. In industrialized nations, 2 age-peaks occur: the first is tries), contaminated water, contact with pets (especially birds at !1 year of age, and a second surge occurs during young and cats), and international travel [25-27].
adulthood, at 15-44 years of age. Furthermore, there is a pre- Because the infectious dose of Campylobacter is quite high ponderance of males among infected persons, which begins in comparison with that of Shigella or Giardia (800-106 ingested during early childhood and persists until old age [3]. The rea- organisms are needed to produce illness in 10%-50% of per- sons for these age and sex distributions remain unknown. Since sons) [28], person-to-person transmission is unusual. Out- the beginning of national reporting on Campylobacter in the breaks of Campylobacter infection in day care centers or mental FOOD SAFETY • CID 2001:32 (15 April) • 1203
institutions are almost unheard of. Although the reported in- cultures. Fluoroquinolones were especially apt to be used for cidence of Campylobacter infection among homosexual men is the treatment of traveler's diarrhea.
almost 40 times greater than in the general population [29], However, in the past few years, a rapidly increasing pro- recent analysis shows the rate is not higher than among het- portion of Campylobacter strains all over the world have been found to be fluoroquinolone-resistant (table 2). Primary resis- Campylobacter in developing countries.
tance to quinolone therapy in humans was first noted in the ogy of Campylobacter infections is quite different in developing early 1990s in Asia and in European countries such as Sweden, countries than in the industrialized world. In tropical devel- The Netherlands, Finland, and Spain. Not surprisingly, this oping countries, Campylobacter infections are hyperendemic coincided with initiation of the administration of the fluoro- among young children, especially those aged !2 years. Asymp- quinolone, enrofloxacin, to food animals in those countries tomatic infections occur commonly in both children and adults, [31]. A similar increase in rates of resistance to fluoroquino- whereas, in developed countries, asymptomatic Campylobacter lones in Campylobacter isolates from humans was observed in infections are unusual. In addition, in developing countries, out- the United Kingdom after the approval of the use of fluoro- breaks of infection are uncommon and the illness lacks the quinolones in veterinary animals there as well [32].
marked seasonal nature observed in industrialized nations. Nev- In the United States, the licensure of sarafloxacin in 1995 ertheless, in both developed and developing countries, Campy- and enrofloxacin in 1996 for use in poultry flocks contributed lobacter remains one of the most common bacterial causes of to an increase in the number of domestically acquired fluor- oquinolone-resistant Campylobacter infections in Minnesota[33]. In that state, fluoroquinolone resistance among Campy-lobacter isolates from humans increased from 1.3% in 1992 to TREATMENT AND RESISTANCE
10.2% in 1998. The impact of the use of fluoroquinolones infood animals upon human health was the subject of a recent Maintenance of hydration and electrolyte balance, not anti- World Health Organization meeting [34]. In addition to more biotic treatment, is the cornerstone of treatment for Campy- prudent use of these agents in people, international controls lobacter enteritis. Indeed, most patients with Campylobacter in- on the use of antibiotics in food animals may become necessary fection have a self-limited illness and do not require antibiotics to curtail the development of additional resistance among food- at all. Nevertheless, there are specific clinical circumstances in which antibiotics should be used. These include high fevers, Erythromycin has once again come to be considered the bloody stools, prolonged illness (symptoms that last 11 week), optimal drug for treatment of Campylobacter infections. Despite pregnancy, infection with HIV, and other immunocompromised decades of use, the rate of resistance of Campylobacter to eryth- romycin remains quite low. Other advantages of erythromycin The decision to use antibiotics should be made judiciously.
include its low cost, safety, ease of administration, and narrow In the United States, the most common cause of bloody di- spectrum of activity. Unlike the fluoroquinolones and tetra- arrhea is not Campylobacter but E. coli O157:H7 infection [1].
cyclines, erythromycin may be administered safely to children Recent studies suggest that administration of antibiotics to chil- and pregnant women and is less likely than many agents to dren with E. coli O157:H7 infection actually increases the risk exert an inhibitory effect on other fecal flora. Erythromycin of the hemolytic uremic syndrome (HUS) [30], a recognized stearate is acid-resistant, stable, and incompletely absorbed.
sequela of this infection. Therefore, young children with bloody Therefore, in addition to its systemic effects, it may be capable diarrhea (and others who might be at risk of infection with E. of exerting a contact effect throughout the bowel [35]. The coli O157:H7 and HUS) should not be treated with antibioticsunless it is absolutely necessary or until this infection is ruled Percentage of Campylobacter isolates (from humans)
with primary resistance to fluoroquinolones.
Until a few years ago, if antimicrobial therapy was indicated for Campylobacter infection, fluoroquinolones were considered the drugs of choice. This approach was the simplest for phy- sicians and patients alike because the symptoms of Campylo- bacter enteritis (fever, abdominal cramps, and diarrhea) are clinically indistinguishable from those of bacterial gastroenter- itis caused by other organisms, such as Salmonella or Shigella species. Because these other pathogens were also generally sus- ceptible to fluoroquinolones, empirical treatment with these drugs could be used without waiting for the results of stool 1204 • CID 2001:32 (15 April) • FOOD SAFETY
recommended dosage for adults is 500 mg administered orally sumption of unpasteurized milk; this should be emphasized to 2 times per day for 5 days. For children, the recommended pregnant women, the elderly, immunocompromised persons, dosage is 40 mg per kg per day in 2 divided doses for 5 days.
or other persons in whom C. jejuni infection may have serious The newer macrolides, azithromycin and clarithromycin, are consequences. Persons who travel to developing countries and also effective against C. jejuni infections, but they are more campers should be cautioned against drinking untreated water.
expensive than erythromycin and provide no clinical advantage.
Routine use of antibiotic prophylaxis to prevent Campylobacter Campylobacter species also are generally susceptible to amino- glycosides, chloramphenicol, clindamycin, nitrofurans, and im-ipenem. High rates of resistance make tetracycline, amoxicillin, References
ampicillin, metronidazole, and cephalosporins poor choices forthe treatment of infections with C. jejuni. All Campylobacter 1. Slutsker LA, Ries AA, Greene KD, Wells JG, Hutwagner L, Griffin PM.
species are inherently resistant to vancomycin, rifampin, and Escherichia coli O157:H7 diarrhea in the United States: clinical and
epidemiological features. Ann Intern Med 1997; 126:505-13.
2. Blaser MJ, Wells JG, Feldman RA, Pollard RA, Allen JR, the Collab- orative Diarrheal Disease Study Group. Campylobacter enteritis in the
United States: a multicenter study. Ann Intern Med 1983; 98:360-5.
PREVENTION
3. Friedman CR, Neimann J, Wegener HC, Tauxe RV. Epidemiology of Campylobacter jejuni infections in the United States and other indus-trialized nations. In: Nachamkin I, Blaser MJ, eds. Campylobacter. 2d Because most Campylobacter infections are acquired by con- ed. Washington, DC: ASM Press, 2000:121-38.
suming or handling poultry, the ideal way to control the num- 4. King EO. Human infections with Vibrio fetus and a closely related ber of human infections would be to limit contamination of Vibrio. J Infect Dis 1957; 101:119-28.
5. Vernon M, Chatlain R. Taxonomic study of the genus Campylobacter poultry flocks. However, the near-universal contamination of (Sebald and Veron) and designation of the neotype strain for the type poultry with Campylobacter and the heavy bacterial burden in species, Campylobacter fetus (Smith and Taylor) Sebald and Veron. Int these flocks [24] make elimination of Campylobacter in chickens J Syst Bacteriol 1973; 23:122-34.
6. Parkhill J, Wren BW, Mungall K, et al. The genome sequence of the impractical, if not impossible. Current mass processing and foodborne pathogen Campylobacter jejuni reveals hypervariable se- distribution of chicken may amplify the bacterial load; perhaps quences. Nature 2000; 403; 66-8.
future investigations will lead to the creation of a system that 7. Nachamkin I. Campylobacter and Arcobacter. In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH, eds. Manual of clinical mi- will produce chickens that are only lightly colonized with Cam- crobiology. Washington, DC: American Society for Microbiology, 1995:
pylobacter. New strategies will likely include limiting animals' consumption of antibiotics, disinfection of their food and wa- 8. Kapperud G, Lassen J, Ostroff SM, Aasen S. Clinical features of sporadic ter, treatment of their manure, and isolation of the contagiously Campylobacter infections in Norway. Scand J Infect Dis 1992; 24:741-9.
9. Calva JJ, Ruiz-Palacioz GM, Lopez-Vidal AB, Ramos A, Bojalil R. Co- ill. Perhaps the irradiation of foods of animal origin will one hort study of intestinal infection with Campylobacter in Mexican chil- day become sufficiently acceptable to the public to make this dren. Lancet 1988; 1:503-6.
a feasible method of control of the bacterial contamination of 10. Blaser MJ, Berkowitz ID, LaForce FM, Cravens J, Reller LB, Wang W- LL. Campylobacter enteritis: clinical and epidemiologic features. Ann Intern Med 1979; 91:179-85.
Observing careful food-preparation habits in the kitchen is 11. Lawson AJ, Logan AM, O'Neill GL, Desai M, Stanley J. Large-scale also important in the prevention of infections. Chicken should survey of Campylobacter species in human gastroenteritis by PCR and
PCR-enzyme-linked immunosorbent assay. J Clin Microbiol 1999; 37:
be adequately cooked-not charred on the outside and left pink near the bone. Use of a meat thermometer may help to ensure 12. Skirrow MB, Jones DM, Sutcliffe E, Benjamin J. Campylobacter bac- that temperatures adequate to kill Campylobacter species or- teraemia in England and Wales, 1981-1991. Epidemiol Infect 1993;
ganisms are achieved. Cutting boards and utensils used in han- 13. Allos BM. Association between Campylobacter jejuni infection and dling uncooked poultry or other meats should be washed with Guillain-Barre' syndrome. J Infect Dis 1997; (Suppl 2):S125-8.
hot soapy water before being used for preparation of salads or 14. Allos BM, Lippy FE, Carlsen AR, Blaser MJ. Serotype, serum resistance and 125I-C3 binding among C. jejuni strains from patients with Guillain-Barre' syndrome or with uncomplicated enteritis. Emerg Infect Dis Although person-to-person transmission of C. jejuni infec- 1998; 4:263-8.
tion is unusual, persons with any acute diarrheal illness should 15. Kuroki S, Saida T, Nukina M, et al. Campylobacter jejuni strains from avoid preparation and handling of food until their illness re- patients with Guillain-Barre' syndrome belong mostly to Penner ser-
ogroup 19 and contain B-N-acetylglucosamine. Ann Neurol 1993; 33:
solves. Of course, as part of good general hygiene, all persons should wash their hands after using the bathroom, especially 16. Yuki N, Taki T, Inagaki F, et al. A bacterium lipopolysaccharide that if they have diarrhea. Similarly, all people, but especially those elicits Guillain-Barre' syndrome has a GM1 ganglioside-like structure.
who handle pets or other animals, should wash their hands J Exp Med 1993; 178:1771-5.
17. Rautelin H, Koota K, von Essen R, Jahkola M, Sitonen A, Kosunen before eating. Prevention of many outbreaks of C. jejuni in- TU. Waterborne Campylobacter jejuni epidemic in a Finnish hospital fection could be accomplished with avoidance of the con- for rheumatic diseases. Scand J Infect Dis 1990; 22:321-6.
FOOD SAFETY • CID 2001:32 (15 April) • 1205
18. Mead PS, Slutsker L, Dietz V, et al. Food-related illness and death in 30. Wang CS, Jalacic S, Habeeb RL, Watkins SL, Tarr PI. The risk of the United States. Emerg Infect Dis 1999; 5:607-25.
hemolytic-uremic syndrome after antibiotic treatment of Escherichia 19. Centers for Disease Control and Prevention. Preliminary FoodNet data coli O157:H7. N Engl J Med 2000; 342:1930-6.
on the incidence of foodborne illness: selected sites, United States, 31. Endtz HP, Ruijs GJ, van Klingeren B, Jansen WH, van der Reyden T, 1999. MMWR Morb Mortal Wkly Rep 2000; 49:201-5.
Mouton RP. Quinolone resistance in Campylobacter isolated from man 20. Harris NV, Weiss NS, Nolan CM. The role of poultry and meats in and poultry following the introduction of fluoroquinolones in veter- the etiology of Campylobacter jejuni/coli enteritis. Am J Public Health inary medicine. J Antimicrob Chemother 1991; 27:199-208.
1986; 76:407-10.
32. Sam WIC, Lyons MM, Waghorn DJ. Increasing rates of ciprofloxacin 21. Deming M, Tauxe RV, Blake PA, et al. Campylobacter enteritis at a resistant Campylobacter. J Clin Pathol 1999; 52:709-10.
university: transmission from eating chicken and from cats. Am J Ep- 33. Smith KE, Besser JM, Hedberg CW, et al. Quinolone-resistant Cam- idemiol 1987; 126:526-34.
pylobacter jejuni infections in Minnesota, 1992-1998. N Engl J Med 22. Adak GK, Cowden JM, Nicholas S, Evans HS. The Public Health Lab- 1999; 340:1525-32.
oratory Service national case-control study of primary indigenous spo- 34. Use of quinolones in food animals and potential impact on human radic cases of Campylobacter infection. Epidemiol Infect 1995; 115:15-22.
health. Report and proceedings of a WHO meeting, Geneva, Switzer- 23. Food Safety and Inspection Service. Nationwide broiler chicken mi- land, June 2-June 5, 1998. Geneva: World Health Organization, 1998.
crobiologic baseline data collection program, 1994-1995. Washington, 35. Skirrow MB, Blaser MJ. Campylobacter jejuni. In: Blaser MJ, Smith PD, DC: US Department of Agriculture, 1996.
Ravdin JI, Greenberg HB, Guerrant RL, eds. Infections of the gastro- 24. Hood AM, Pearson AD, Shahamat M. The extent of surface contam- intestinal tract. New York: Raven Press, 1995:825-48.
ination of retailed chicken with Campylobacter jejuni serogroups. Ep- 36. Sjogren E, Lindblom G-B, Kaijser B. Norfloxacin resistance in Cam- idemiol Infect 1988:100:17-25.
pylobacter jejuni and Campylobacter coli isolates from Swedish patients.
25. Kapperud G, Skjerve E, Bean NH, Ostroff SM, Lassen J. Risk factors J Antimicrob Chemother 1997; 40:257-61.
for sporadic Campylobacter infections: results of a case-control study 37. Prasad KN, Mathur SK, Dhole TN, Ayyagari A. Antimicrobial suscep- in southeastern Norway. J Clin Microbiol 1992; 30:3117-21.
tibility and plasmid analysis of Campylobacter jejuni isolated from diar- 26. Nielsen EM, Engberg J, Madsen M, Wegener HC. Foodborne risk fac- rhoeal patients and healthy chickens in northern India. J Diarrhoeal tors associated with sporadic campylobacteriosis in Denmark. Dansk Dis Res 1994; 12:270-3.
Veterinaertidsskrift 1998; 81:702-5.
38. Hoge CW, Gambel JM, Srijan A, et al. Trends in antibiotic resistance 27. Schorr D, Schmid H, Rieder HL, Baumgartner A, Vorkauf H, Bumens among diarrheal pathogens isolated in Thailand over 15 years. Clin A. Risk factors for Campylobacter enteritis in Switzerland. Zentralbl Infect Dis 1998; 26:341-5.
Hyg Umweltmed 1994; 196:327-37.
39. Saenz Y, Zarazaga M, Lantero M, Gastanares MJ, Baquero F, Torres C.
28. Black RE, Levine MM, Clements ML, Hughes TP, Blaser MJ. Experi- Antibiotic resistance in Campylobacter strains isolated from animals, mental Campylobacter jejuni infections in humans. J Infect Dis 1988;
foods, and humans in Spain in 1997-1998. Antimicrob Agents Chem- other 2000; 44:267-71.
29. Sovillo FJ, Lieb LE, Waterman SH. Incidence of campylobacteriosis 40. Talsma E, Goettsch WG, Nieste HL, Schrijnemakers PM, Sprenger MJ.
among patients with AIDS in Los Angeles County. J Acquir Immune Resistance in Campylobacter species: increased resistance to fluoro- Defic Syndr 1991; 4:598-602.
quinolones and seasonal variation. Clin Infect Dis 1999; 29:845-8.
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