Campylobacter Isolates in the United States, 1982-1986*

Robert V. Tauxe, M.D., M.P.H. Nancy Hargrett-Bean, Ph.D. Charlotte M. Patton, M.S.

1. Kaye Wachsmuth, Ph.D. Enteric Diseases Branch and Statistical Services Activity Division of Bacterial Diseases Center for Infectious Diseases

INTRODUCTION

Campylobacter organisms have long been recognized as a cause of diarrhea in cattle and of septic abortion in both cattle and sheep, but they have only recently been recognized as an important cause of human illness. Both Campylobacter fetus subspecies fetus (referred to then as Vibrio fetus) and Campylobacter jejuni (related Vibrio) were isolated from blood cultures of humans in the 1950s and were thought to be rare and perhaps opportunistic pathogens (1). C. jejuni was first isolated from the diarrheal stools of humans in 1972, with use of a filtration technique developed in veterinary medicine (2,3). The development of selective Campylobacter stool culture media by Skirrow and by Blaser led to the recognition that Campylobacter was a common cause of human diarrheal illness in many countries (4,5). In a study conducted at eight U.S. hospitals in 1980 and 1981, 4.4% of patients with diarrheal illness had Campylobacter isolated from stools; by comparison, 2.3% had Salmonella and 0.9% had Shigella isolated (6).

The taxonomy of Campylobacter has been expanding rapidly. Currently, there are nine named or proposed species that may be pathogenic in humans (Table 1). All of them are curved gram-negative motile rods that are microaerophilic and oxidase- positive. The organisms do not ferment carbohydrates but can usually be distinguished from one another by a variety of biochemical tests and growth characteristics (Table 2). One species, Campylobacter pylori, differs from other Campylobacter species in several important ways and may prove to belong to a separate genus (7).

Laboratory-based national surveillance of Campylobacter infections in the United States began in 1982 with a panel of 11 states (8). Thirty-one states joined in surveillance in 1983, and since then the panel has been relatively constant. Published reports have summarized the results of surveillance for 1983-1984 and the epidemiology of common-source outbreaks of Campylobacter infections (9-11). The surveillance goals were 1) to describe the epidemiology of infections with these organisms, 2) to detect and investigate outbreaks, and 3) to generate hypotheses for further research (12). This report reviews the first 5 years of CDC's Campylobacter surveillance in the United States. METHODS

The national Campylobacter surveillance system is a passive laboratory-based surveillance system, similar to the national Salmonella and Shigella surveillance systems. Weekly reports of laboratory isolates of Campylobacter are mailed from participating state health departments to the Enteric Diseases Branch, Division of Bacterial Diseases, Center for Infectious Diseases, CDC. The data reported include species of Campylobacter; name, age, sex, and county of residence of the person from whom Campylobacter was isolated; and the clinical source of the isolate. No other clinical information is included, and deaths are not reported. Participating states vary considerably in their internal reporting requirements for Campylobacter, which is reflected in the number of Campylobacter isolations reported (8). Because the data files remain open and late reports may be added, the data included in this report may differ slightly from previously published data.

The population for nonparticipating states, as determined by the 1980 census, was subtracted from the national population for 1980 to determine the national isolation rate for each year of surveillance. Age- and sex-specific isolation rates were calculated for the 5-year span using a denominator of the total number of person-years of observation based on the age and sex distribution of the 1980 census. Incidence rates by month of age in infancy were calculated with a denominator of one-twelfth of the total number of person-years of observation for infants less than 1 year of age. RESULTS

In the 5 years of surveillance, 41,343 isolates of Campylobacter were reported to CDC, resulting in an isolation rate of 5.5 per 100,000 person-years. The annual isolation rate was highest in the first year of surveillance, decreased in the second year when a large number of states began participating, and since then has increased slightly over time (Table 3). A species was reported for 91% of isolates; C. jejuni represents 99% of the reported species (Table 4). Other reported species include C. fetus subsp fetus, Campylobacter coli, Campylobacter laridis, "Campylobacter- like organism," Campylobacter sputorum, and "Campylobacter faecalis." The last two species are not thought to be pathogenic for humans. Reported isolations of C. jejuni have shown a consistent seasonal distribution over the 5-year period (Figure 1). The seasonal distribution patterns of C. fetus subsp fetus and C. coli also show peaks in warm months, although they are less marked than those of C. jejuni.

The pattern of age- and sex-specific isolation rates of Campylobacter is unique among enteric bacteria (Figure 2). The highest isolation rate occurs in the first year of life, reaching 15 per 100,000, but a large second peak occurs in the young adult years. The isolation rate for males is higher than that for females up to age 45; over this age the isolation rates are equal. In the first year of life, the isolation rate is lowest during the first month, is highest in the second month, and levels off after that. Campylobacter is isolated more often from male than from female infants; the male-to-female ratio is 1.31:1 for isolates from infants, compared with a ratio of 1.15:1 for isolates from all ages combined.

Although overall isolation rates are two orders of magnitude less than for C. jejuni, the age-specific isolation rates of C. coli and C. fetus subsp fetus also peak in infancy and increase in young adulthood (Figure 3). C. coli appears to have a lower isolation rate among older adults, while that of C. fetus subsp fetus increases substantially among the elderly.

A clinical source was reported for 76% of the isolates (Table 5). Both C. jejuni and C. coli came predominantly from stool, whereas 54% of C. fetus subsp fetus isolates with known source were from blood. Despite this difference, the number of reported C. jejuni isolates from blood actually exceeded that of C. fetus subsp fetus because many more C. jejuni infections were reported. The proportion of isolates that came from blood did not vary by sex but did vary by age, and persons with blood isolates tended to be older (median age, 30 years) than persons with stool isolates (median age, 25 years). For C. fetus subsp fetus the median age for persons with blood isolates was 64 years; that of persons with stool isolates was 32 years. For both species the elderly were at highest relative risk for bacteremia, although this increased risk occurred in persons at a younger age for C. fetus subsp fetus than for C. jejuni (Figure 4). Common-source outbreaks

CDC receives reports of foodborne and waterborne disease outbreaks, including those caused by Campylobacter, as part of the national foodborne and waterborne disease surveillance systems. The first reported Campylobacter outbreak, in 1978, was also the largest, when a contaminated community water supply affected an estimated 3,000 persons (13). Between 1978 and 1986, 57 outbreaks of Campylobacter infections were reported, including 11 waterborne outbreaks, 45 foodborne outbreaks, and one outbreak in a tourist group for which the source was unclear (Table 6). A species was reported for 43 outbreaks: 42 outbreaks were due to C. jejuni, including one raw-milk-associated outbreak due to both C. jejuni and a thermotolerant strain of C. fetus subsp fetus (14), and one outbreak was due to a cluster of C. fetus subsp fetus infections in cancer patients (15). The median number of cases was 22 in waterborne outbreaks and 14 in foodborne outbreaks. Two fatalities were reported, one occurring during a foodborne outbreak of C. jejuni infections at a nursing home, and one occurring in a patient with metastatic melanoma. The latter patient was part of the cluster of C. fetus subsp fetus infections (15). The outbreak- associated case-fatality ratio for Campylobacter infections was two per 6,441 or three per 10,000. A vehicle was determined for 80% of the foodborne outbreaks; of these, 70% were caused by raw milk, and 8% were associated with poultry. The waterborne outbreaks were all related to drinking untreated surface water or water supplies with inadequate chlorination.

The seasonality of outbreaks of Campylobacter infections differs markedly from that of Campylobacter isolates reported through the national surveillance system (Figure 5). The distribution of foodborne and waterborne outbreaks is bimodal, with peaks in May and October. In contrast, outbreaks are rare in the summer months when the reported isolations of Campylobacter reach their peak.

The common-source outbreaks reported here were detected or reflected by local Campylobacter surveillance efforts. The national Campylobacter surveillance system has not been an instrument for the primary detection of local common-source outbreaks. National surveillance data did, however, document a striking event in November 1984, when a large temporary increase occurred in reported Campylobacter isolates (10). This increase occurred equally in all age groups and in all regions of the country, and the age and sex distributions of cases reported that month were similar to those of cases reported throughout the year. This increase in 1984 appears to have been a nationwide outbreak: no local common-source outbreaks were reported at that time, and the source of the outbreak remains unknown. DISCUSSION

The interpretation of Campylobacter surveillance data has two major limitations: 1) the collected information itself is limited and 2) the reporting systems vary from state to state. Variations in reported isolation rates among states or regions may well reflect differences in surveillance and reporting methods and should not be interpreted as true variation in the incidence of infection. Similarly, surveillance mechanisms within a given state may differ for Salmonella, Shigella, and Campylobacter, so that the isolation rates of these organisms may not be directly comparable.

Nevertheless, the Campylobacter isolation rate does not appear to be increasing rapidly. The modest increase in isolation rates between 1983 and 1986 may reflect an increase in the number of laboratories using selective culture media for Campylobacter, rather than a real increase in the frequency of infection. The reported number of isolates represents only a small fraction of the true number of isolates and a far smaller fraction of the number of infections that occurred. The population-based isolation rate of Campylobacter among members of a Seattle health maintenance organization was 71 per 100,000 per year, and in the city of Dubuque, Iowa, the rate was 28 per 100,000 per year (16, 17). These rates may be closer to the actual isolation rate for the country than the national isolation rate reported here.

The 1984 Campylobacter isolation rate of five per 100,000 is less than the analogous rate for Salmonella (16 per 100,000) and is similar to that of Shigella (5.6 per 100,000). However, several studies indicate that, when parallel cultures for all three organisms are done, Campylobacter isolations are probably more frequent than Shigella and Salmonella isolations combined. Among patients seen at hospitals, Campylobacter was isolated more frequently than Salmonella and Shigella by a ratio of 2:1 and 5:1, respectively (6). Among citizens of Dubuque the same ratios were 2.5:1 and 14:1; among college students they were 10:1 and 46:1 (17,18). Among members of the Seattle health maintenance organization, Campylobacter was isolated more frequently than Salmonella by a ratio of 2.5:1 (16). In national surveillance data the lower reporting of Campylobacter compared with other enteric bacterial isolates probably reflects infrequent use of selective media for Campylobacter along with standard enteric media, fewer referrals of isolates of Campylobacter to reference laboratories, and less-stringent reporting requirements for Campylobacter than for Salmonella or Shigella.

The seasonality of Campylobacter outbreaks and of reported Campylobacter isolates differs profoundly, suggesting that the sources of cases in outbreaks are quite different from the sources of the far more numerous sporadic cases. The reason for the bimodal seasonal distribution of outbreaks is not clear, but it may be related to the observation that the yield of cultures for Campylobacter from surface water may be temperature dependent. Reisinger reported that C. jejuni could be isolated from surface water in the spring and fall, but it could not be isolated in the summer, when water temperatures were above 25C (19).

The sources of sporadic cases of Campylobacter have been defined in several recent case-control investigations. Poultry is the predominant source; contact with pets and consumption of raw milk or surface water also play important roles. In sporadic cases occurring among members of a health maintenance organization in Seattle, at least 50% were accounted for by poultry, and 9% by foreign travel; the single outbreak in the study population was traced to raw goat's milk (16,20). Among university students in Georgia, 70% of cases were accounted for by eating chicken, often undercooked or raw, and 30% by contact with cats (21). In Dubuque, Iowa, an agricultural area, drinking raw milk was the leading identified risk factor, and 33% of the patients had consumed raw milk (17). In Colorado, the identified risk factors were drinking untreated water or raw milk, contact with cats, and eating undercooked chicken, although their independence was not assessed (22). In a second study conducted in Colorado, handling raw chicken, as opposed to eating it, emerged as a risk factor (23). Poor kitchen hygiene may well play a role; in one study, the risk of infection was inversely associated with the frequency of using soap to clean the kitchen cutting board (16).

The predominance of poultry as a source of sporadic infections could explain both the age spectrum and the seasonality of the infection. The predilection of this infection for young adults may be related to their cooking habits as they leave their childhood homes and begin cooking for themselves, the "second weaning" hypothesis. The prevalence of Campylobacter contamination of raw poultry products can be as high as 89% and appears to be seasonal with a summer peak (24,25).

The explanation for the nationwide November 1984 anomaly remains unknown. However, it appears to have been a nationwide common-source outbreak with the same age and sex distribution as is generally seen for sporadic cases. Poultry is a potential vehicle for such an outbreak.

Person-to-person transmission appears to be uncommon with C. jejuni. This rarity is somewhat surprising because volunteer trials indicate that the infectious dose of C. jejuni is 500 organisms or fewer, low enough to make person-to-person transmission seem likely (26,27). Nonetheless, neither outbreaks nor large numbers of sporadic cases have been reported in situations where person-to-person transmission of other enteric diseases are common, such as day-care centers or mental institutions. Two laboratory-acquired cases were related to handling laboratory reference strains, not to handling clinical specimens (28,29). In three published investigations of clusters of C. jejuni infections among neonates, no clear evidence of infant-to-infant transmission was reported; one appeared to be due to maternal-infant transmission at birth, and one to an unidentified common source. The route of transmission in one was not clarified (30-32). In a survey of enteric pathogens among homosexual men with intestinal symptoms, C. jejuni was found in 6.3% (33). In another survey, however, 10.5% of stool cultures from persons aged 20-29 years with diarrheal illness yielded Campylobacter (6). The lower rate of 6.3%, therefore, does not suggest that homosexual transmission of C. jejuni was occurring. Thus, despite the low infectious dose, there is little evidence that C. jejuni transmission in the United States is sustained by person-to-person transmission. This may not be the case for all species: "Campylobacter cinaedi " and "Campylobacter fennelliae," reported almost exclusively from homosexual men, may perhaps be transmitted through homosexual contact (34).

Some limited clinical inferences can be drawn from the data. The relative rarity of C. jejuni isolates from outside the intestine suggests that this organism is rarely invasive, unlike C. fetus subsp fetus. Risk factors for bacteremia remain to be determined, although a review of cases of C. fetus subsp fetus infections reported to CDC indicates that underlying gastrointestinal, hepatic, or immunosuppressive disease may predispose to bacteremia with this organism (35). The clinical significance of the C. jejuni isolates reported from the biliary tree is unknown, but raises the possibility of biliary carriage of the organism, as has been demonstrated in sheep and cattle (36). The single C. sputorum isolate came in 1984 from a blood culture of a 77-year-old man with pneumonia. The blood culture from this man also yielded Peptococcus prevotii, another oral anaerobe, which indicates that he probably had aspiration pneumonia and leaves the pathogenic role of the C. sputorum isolate in doubt. No isolates have yet been reported from cerebrospinal fluid in the United States, although Goossens recently reported an outbreak of C. jejuni meningitis in France (32).

Currently, there are several technical shortcomings in laboratory-based Campylobacter surveillance. Although serotyping systems have been developed for Campylobacter, including the heat-stable antigen systems of Penner and of Lauwers and the heat-labile antigen system of Lior, they are labor intensive and have not been adapted for widespread use by reference laboratories (37-39). Because serotyping is rarely done, laboratories have little reason to forward routine isolates to reference laboratories; this fact may lead to underreporting.

The predominance of C. jejuni among reported isolates from stool cultures may partially be an artifact, as the stool culture media currently in use may not be optimal for other Campylobacter species. Media that contain cephalothin will inhibit the growth of most strains of C. fetus subsp fetus, some strains of C. coli, Campylobacter hyointestinalis, "Campylobacter upsaliensis," and probably most strains of "C. cinaedi" and "C. fennelliae" (40-43). Unless the hippurate hydrolysis test is done, C. coli may be misidentified and reported as C. jejuni. Hippurate-negative C. jejuni occurs but probably infrequently; however, no practical tests are available to separate hippurate-negative C. jejuni from C. coli (44). Similarly, unless resistance to nalidixic acid and hippurate hydrolysis are routinely determined, C. laridis may be also misidentified and reported as C. jejuni. The frequency with which these tests are applied routinely is unknown. Some potential pathogens such as C. hyointestinalis, "C. upsaliensis," and two so-called Campylobacter-like organisms, "C. cinaedi" and "C. fennelliae," have not been reported through the surveillance system, although isolates have been forwarded to the national Campylobacter reference laboratory for confirmation.

Several questions about the epidemiology of Campylobacter are worthy of further research. The sources of the non-jejuni Campylobacter species remain to be determined. The sources of C. jejuni infections among infants have not been investigated systematically. No explanation is available as to why male infants are at higher risk than female infants, and it is difficult to think of differences in lifestyle between male and female infants that would explain this variation in isolation rates. The rarity of person-to-person transmission despite the frequency of infection in infants and the low infectious dose raises the question of whether C. jejuni in human stools is infectious. The notable lack of outbreaks in midsummer remains to be explained. If nationwide events like the November 1984 peak in isolations occur again, targeted epidemiologic investigation, including serotyping and case-control studies, will be needed to determine their source.

Considerable effort toward controlling Campylobacter infections is also required. The rarity of sustained person-to-person transmission suggests that, in the context of sporadic cases of C. jejuni infections, there is little need for public health measures such as tracing contacts, screening food handlers, or closing day-care centers. The differences between the sources of outbreaks and of sporadic cases imply that different control measures are needed for the two situations. Universal pasteurization of milk and proper treatment of all drinking water might prevent 80% of the U.S. outbreaks due to Campylobacter but would have only a limited effect on the more frequent sporadic cases. Since contaminated raw poultry is the primary source of sporadic cases, measures that reduce the level of contamination or that improve chicken-handling practices in kitchens are likely to have the greatest impact on the incidence of the illness.

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40. Lai-King N, Stiles ME, Taylor DE. Inhibition of Campylobacter coli and Campylobacter jejuni by antibiotics used in selective growth media. J Clin Microbiol 1985;22:510-14.

41. Gebhart CJ, Edmonds P, Ward GE, Kurtz HJ, Brenner DJ. PCampylobacter hyointestinalisP' sp nov: a new species of Campylobacter found in the intestines of pigs and other animals. J Clin Microbiol 1985;21:715-20.

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44. Totten PA, Patton CM, Tenover FC, et al. Prevalence and characterization of hippurate- negative Campylobacter jejuni in King County, Washington. J Clin Microbiol 1987;25:1747-52.

45. Morris GK, Patton CM. Campylobacter. In: Lennette EH, Balows A, Hausler WJ Jr, Shadomy HJ, eds. Manual of Clinical Microbiology, 4th ed. Washington, DC: American Society for Microbiology, 1985:302-8. *The authors would like to recognize the crucial contributions of the two Belgian researchers, P.J. Dekeyser, D.V.M., and J.-P. Butzler, M.D., who brought human campylobacteriosis to the attention of the world.

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