sign in sign up
<<
Home , Enterocolitis

Postgraduate Medical Journal (1986) 62, 719-726 Postgrad Med J: first published as 10.1136/pgmj.62.730.719 on 1 August 1986. Downloaded from

Review Article

Campylobacter enterocolitis: general and surgical aspects

David P. Sellu Department ofSurgery, Dudley RoadHospital, Birmingham B18 7QH, UK.

Introduction Bacteria of the genus have long been serological properties ofthe two strains were distinctly known to be pathogens to animals but only recently as different. a leading cause of enterocolitis in man. The spectrum Human have been recognized since 1947 of illnesses produced by this group of organisms is (Vinzent et al., 1947), although they have been in- broad, and the patients may often present to the frequently reported until recent years. In those early surgeon. It seems timely, therefore, to review the years the organisms were isolated from blood, historical background of the organism, its biological, cerebrospinal fluid and other body fluids, and from epidemiological and other properties, and the clinical abscesses (Bokkenheuser, 1970). For, although the features ofthe infections it causes, with a discussion on patients presented mainly with gastrointestinal symp- those aspects which are of particular interest to the toms, attempts to culture the organisms from faeces copyright. surgeon. were unsuccessful because of overgrowth by coliforms. Two important coproculture methods have been Historical background used to overcome the problem of contamination of faecal specimens by coliforms. The first was reported Bacteria ofthe genus Campylobacter have been known by Cooper & Slee (1971) and by Slee (1972) in to cause abortion and diarrhoea in cattle and sheep Australia who noted that a campylobacter isolated since they were first isolated (MacFadyean & Stock- from the blood culture ofa patient with diarrhoea was man, 1909). Because of their striking morphological resistant to cephalothin. Cephalothin discs were similarity to Vibrio cholerae, they were classified as therefore applied to the surface of a blood agar plate http://pmj.bmj.com/ members of the Vibrio genus and the type species now innoculated with the patient's faeces. Following in- known as Campylobacterfetus (see below) was called cubation under microaerophilic conditions (of greatly Vibrio fetus. The term 'campylobacter', which is reduced oxygen tension), campylobacter colonies were derived from two Greek words meaning 'curved rod', noted in the zone of the cephalothin disc. The second was first proposed by Sebald & Veron in 1963 as a method was introduced by Dekeyser and colleagues generic name for these organisms on the grounds that (1972) in Brussels in 1969 and was based on the fact they differed from the classical cholera and halophilic that are small enough to pass through on October 2, 2021 by guest. Protected groups in many important respects. a filter that holds back the other organisms. Using this Elizabeth King (1957 & 1962) was the first to study method they isolated campylobacters from the stools human strains in detail. She realized that while some of of 5.1% of children with diarrhoea and 1.3% of these conformed to the classic type, others formed a children without diarrhoea. similar but distinct group which she provisionally These discoveries received little attention until 1977 called 'related vibrios'. She established the difference when Skirrow, a microbiologist at Worcester Royal between the two species of Vibrio from two character- Infirmary in England, described a method for isolating istics. First, the optimal growth temperature for campylobacters from stools that eliminated the need culture of the related vibrio is 42TC, whereas Vibrio to use the rather tedious filtration technique. In his fetus does not grow at this temperature. Second, the method (Skirrow, 1977) stools were directly in- noculated on to a selective culture medium containing Correspondence: D.P. Sellu, Ch.M., F.R.C.S. the antibiotics vancomycin, polymyxin B, and Accepted: 13 February 1986 trimethoprim, and incubated at 430C in an atmosphere C) The Fellowship of Postgraduate Medicine, 1986 720 D.P. SELLU Postgrad Med J: first published as 10.1136/pgmj.62.730.719 on 1 August 1986. Downloaded from

of 5% oxygen, 10% carbon dioxide, and 85% Epidemiology nitrogen. Skirrow examined the stools of 803 patients with diarrhoea and found that campylobacters were Birds, especially chicken and turkeys, are a common the most common enteric organisms cultured, more reservoir for C. jejuni. Wild birds also carry the common even than salmonella, , and en- organism. In nearly all the birds the excretion of the teropathic . He predicted that cam- organism is not associated with disease. It has been pylobacter would prove to be the commonest iden- demonstrated that C. jejuni can survive the commer- tifiable cause of infectious diarrhoea. Many reports cial processing procedure to which chickens and from other parts of the United Kingdom (Kendall & turkeys are subjected and this source must therefore be Tanner, 1982; Bruce et al., 1977; Dale, 1977; Pearson recognized as important in the spread of et al., 1977; Telfer Brunton & Heggie, 1977; Anon- (Simmons & Gibbs, 1979). ymous, 1978), the continent of Europe (Lindquist et Mammals are also an important source of the al., 1978; Severin, 1978; Muytjens & van Dis, 1978), organism. C. jejuni has been isolated from healthy Canada (Karmali & Fleming, 1979; Kalnins & Jack- pigs, cattle, horses and sheep, and in some of these son, 1977), United States of America (Drake et al., animals the organism may cause an illness with 1981; Blaser & Barth Reller, 1981), and Africa (De diarrhoea as a prominent symptom. Turnbull & Rose Mol & Bosmans, 1978) have confirmed this predic- (1982) have reported on the examination ofover 6,000 tion. The campylobacters are, therefore, an important raw red meat samples from retail and other outlets: C. cause of disease worldwide. jejuni was isolated from 1.6% and the workers con- cluded that contamination of meats by this organism was in general very low. Household dogs and cats are The campylobacters commonly infected, and are known to be a source of infection causing diarrhoea in man (Blaser et al., Campylobacters are small, curved, S-shaped or spiral, 1981a). Humans, both infected and symptomless motile Gram-negative rods. They are microaerophilic, carriers, may be a common source of environmental being neither truly anaerobic nor aerobic, but requir- contamination. ing an environment of reduced oxygen tension for Fresh water (Blaser et al., 1980a) and unpasteurized optimal growth. Failure to appreciate this point was in or incompletely pasteurized milk (Robinson & Jones, copyright. part responsible for the delay in recognizing this 1981) are important external sources of C. jejuni: organism as a human pathogen. They neither oxidize the organism has been cultured from fresh water in nor ferment carbohydrates. Veron & Chatelain (1973) which it has been shown to survive for up to four proposed a scheme which, with slight modification, is weeks. now widely used for classifying these organisms. Five Transmission of C. jejuni is almost certainly by the species ofthe genus Campylobacter are recognized: C. faecal-oral route by ingestion of contaminated food, fetus, C. jejuni, C. coli, C. fecalis and C. water or milk (Pearson et al., 1983). One boys' sputorum. Two ofthese, C.fetus and C. sputorum have boarding school in Sussex experienced a major subspecies which have been characterized: for the epidemic attributable to unpasteurized milk (Pearson http://pmj.bmj.com/ former they are subspecies (ss)fetus and ss veneralis, et al., 1983), and in another in Essex, 257 cases of and for the latter ss sputorum, ss bulbus and ss campylobacter were almost certainly mucosalis. Classic Vibriofetus now becomes C. fetus, due to drinking water from an unchlorinated un- and King's related vibrios C. jejuni and C. coli. As covered storage tank supplied from a borehole (Pal- these latter two species oforganism differ only slightly mer et al., 1983). Person-to-person transmission is in phenotypic characteristics (Skirrow & Benjamin, probably unimportant but it has been reported (Blaser 1980), and C.jejuni is a more common et al., pathogen, they 1981b). on October 2, 2021 by guest. Protected are often collectively referred to as C. jejuni. If the subspecies to which the organism belongs is known, the organism will be described by its genus name, Age and sex distribution followed by its species and subspecies name, for instance, C.fetus ss veneralis. At the present time only The infection has been reported in all ages from 2 C. jejuni and C. fetus ss fetus are known to cause weeks (Karmali & Fleming, 1979) to well into the 90s. disease in man. In the laboratory the organisms are Infections have also occurred in neonates who have recognized by their physical properties on light acquired the organisms from their asymptomatic microscopy, and are cultured using a selective culture mothers (Karmali & Tan, 1980). In the study by medium (usually Skirrow's medium) and incubated at Karmali & Fleming (1979) of campylobacter 42°C in a microaerophilic environment, as described in patients under the age of 15 years the highest earlier. incidence (20%) occurred in those below the age of three years. Many of the adult patients were aged CAMPYLOBACTER ENTEROCOLITIS 721 Postgrad Med J: first published as 10.1136/pgmj.62.730.719 on 1 August 1986. Downloaded from between 15 and 45, and slightly more than halfofthem (Warren & Marshall, 1983). Acute de- were men. veloping during the course of acute due to C. jejuni is well recognized (Sellu & Lynn, 1985). Predisposing factors Macroscopic and microscopic changes Initial reports of campylobacter infections observed Information on the pathological changes observed that the majority of patients affected had pre-existing during the course of this infection have come from illnesses such as alcoholism, of the liver, laparotomy, sigmoidoscopy and colonoscopy, from diabetes mellitus, atherosclerosis, rheumatic heart post-mortem examinations carried out on patients disease, lymphoma or leukaemia, had had splenec- who have succumbed from the disease, and from tomy or were on immunosuppressive therapy (Rettig, animal experiments. It is not clear whether the organ- 1979). More recent studies of both outbreaks and ism produces mucosal damage by direct invasion or by sporadic infections have established that the vast enterotoxin production (Butzler & Skirrow, 1979). majority of persons affected have been previously The pathological features depend on the severity ofthe healthy. The latter represents the true state of affairs, injury: at one extreme there may be no gross changes now that Campylobacter is widely recognized as a when the bowel is inspected from the serosal aspect human pathogen and is looked for more frequently in (Ponka et al., 1981; Lambert, J.R. et al., 1979), and at the investigation of diarrhoea. the other there may be inflammation and oedema of the full thickness of the bowel wall (Skirrow, 1977), haemorrhagic lesions (King, 1962), or even frank Pathogenesis necrosis (Evans & Dadswell, 1967), gangrene (Sellu & Lynn, 1985) and perforation (Stephenson & Cotton, Gastrointestinal involvement 1985). When the bowel is viewed from the mucosal aspect, more consistent changes are likely to be found. C. jejuni is primarily a gastrointestinal pathogen, but These include the presence ofmucus, pus and blood in affect other and The the lumen of the may organs systems. high bowel, and a haemorrhagic, copyright. prevalence of this organism in asymptomatic carriers oedematous and friable mucosa, which cannot be and in patients with only mild illness suggests that it is distinguished from (Lambert, J.R. et not as infective as other gastrointestinal pathogens al., 1979; Lambert, M.E. et al., 1979; Blaser et al., such as salmonella or shigella. 1980b). Segmental mucosal oedema, loss of vascular There is debate about the incubation period of this pattern with ulceration, linear clefts and a cobblestone infection but it is believed to be from one to 7 days appearance identical to those of Crohn's disease have (mean 4 days). Many organisms are destroyed by the also been described (Loss et al., 1980). As with acid environment of the stomach but those that reach ulcerative colitis, the has been found to be the small bowel are liable to survive and multiply; the involved in practically all patients from whose stools pH and the microaerophilic medium of the small C. jejuni has been isolated (Price et al., 1979). http://pmj.bmj.com/ bowel are more favourable. The drug cimetidine, now Histological examination of mucosal biopsy from used widely in the treatment of peptic ulcers, lowers infected patients has shown nonspecific colitis with gastric acidity, and it has been suggested that in flattening of the surface epithelium and depletion of patients on this medication a relatively small inoculum goblet cells. The crypt walls are infiltrated bypolymor- of the organism may establish infection (Blaser et al., phonuclear leucocytes, and numerous crypt abscesses 1980a; Chandra et al., 1982). Organisms are excreted are present. There is a mixed inflammatory infiltrate in into the large bowel where they are also liable to the lamina propria comprising polymorphs and on October 2, 2021 by guest. Protected multiply further. plasma cells (Willoughby et al., 1979). These changes have been interpreted as being consistent with Crohn's Sites affected in the disease or ulcerative colitis (Lambert, M.E. et al., 1979; Blaser et al., 1980b; Willoughby et al., 1979). In The sites in the gastrointestinal tract most liable to some cases the appearances have been similar to those sustain injury are the , , and colon and described for salmonella and shigella, and different rectum, but other sites may be affected. from those of typical ulcerative colitis or Crohn's Bentley et al. (1985) observed acute gingivo- disease (Price et al., 1979). stomatitis and glossitis in a child with campylobacter colitis. An organism which, by light microscopy Involvement oforgans outside the gastrointestinal tract resembles C.jejuni, has been cultured from the gastric mucosa of patients with an active form of chronic Darling et al. (1979) have described three , and may well be a cause of this condition cases of in which C. jejuni was isolated 722 D.P. SELLU Postgrad Med J: first published as 10.1136/pgmj.62.730.719 on 1 August 1986. Downloaded from

from bile. Two of the patients were operated upon gradually in some and explosively in others; in all cases during the acute phase of the illness and the third faeces become watery, offensive and often bile- electively. Cholecystitis due to this organism has been stained. Later the faeces become mixed with blood, described by other workers (Mertens & De Smet, mucus and pus, and the characteristics will then be 1979). those of inflammatory bowel disease such as acute ulcerative colitis. Diarrhoea often lasts for 3 to 4 days, Blood stream infection Bacteraemia and septicaemia and the stools gradually become solid in most cases. developing in the course of colitis by C. jejuni is now Recovery may be slow in a minority of patients in well documented. In one case (Longfield et al., 1979), whom diarrhoea may persist for several weeks. organisms were found in the blood stream during the Abdominal pain may be constant or colicky and may acute phase of the illness and also during convales- occur in any quadrant of the abdomen, but most cence. Guerrant et al. (1978) have reviewed 91 cases of frequently occurs on the right. and vomiting blood stream infections: while the organism was are common but dehydration less so. A low-grade believed to have originated from the gastrointestinal is common and rigors may occasionally occur. tract in the majority ofpatients, there was evidence to The abdomen is often mildly tender but severe tender- implicate other portals of entry such as skin, female ness, muscle guarding and rebound tenderness are genital tract and lung. sometimes present. Bowel sounds are often normal but may be increased or absent. Urinary tract Urinary tract infections with cam- pylobacter have been described (Davies & Penfold, Why campylobacter enterocolitis sometimes presents to 1979). the surgeon Skin andjoints Reactive (Kosunen et al., 1980) and Campylobacter colitis can present to the surgeon for purulent (Guerrant et al., 1978) arthritis and erythema several reasons, the most common ofwhich are: (a) It nodosum (Ellis et al., 1982) have also been reported. can mimic intra-abdominal surgical emergencies such as intestinal obstruction, appendicitis, and cholecys- Others Other infections due to include titis et the is campylobacter (Ponka al., 1981); diagnosis hampered copyright. meningitis, empyema thoracis, pustules, endocarditis by the late onset or even total absence of diarrhoea, and placental infection (Guerrant et al., 1978), septic and some of these patients have undergone unneces- thrombophlebitis in a patient with Hodgkin's disease sary operations. A patient who had spontaneous (Geffen et al., 1983) and bilateral deep venous throm- bacterial due to infection with Cam- bophlebitis (Vesely et al., 1975). Mycotic aneurysms of pylobacter jejuni has been described (McNeil et al., the abdominal aorta caused bycampylobacter(Anolik 1984); this complication was secondary to alcoholic et al., 1983; Blabey et al., 1983), or pre-existing aortic cirrhosis, a condition in which spontaneous bacterial aneurysms infected by this organism (Marty et al., peritonitis is well known to occur (Conn & Fessel, 1983) have been documented. 1971). (b) It may resemble Crohn's disease or acute ulcerative colitis. One patient who was known to have http://pmj.bmj.com/ ulcerative colitis presented with diarrhoea which was Symptoms and signs thought to be due to relapse of ulcerative colitis, but proved later to be due to campylobacter colitis Many of the features of campylobacter infections are (Chandra et al., 1982). It is important, therefore, that identical to those of other gastrointestinal infections. infection is excluded in 'relapses' of inflammatory In many other cases the clinical symptoms and signs bowel disease. (c) It can present together with a true be similar to those of intra-abdominal diseases may 'surgical' condition such as acute appendicitis (Sellu & on October 2, 2021 by guest. Protected other than those due to enterocolitis. The illness may Lynn, 1985), cholecystitis (Darling et al., 1979; Mer- be mild with few, ifany, gastrointestinal symptoms, on tens & De Smet, 1979), or mesenteric lymphadenitis the one hand, or it may present with diarrhoea and (Skirrow, 1977). (d) Campylobacter colitis may be severe abdominal pain, on the other. Diarrhoea may complicated by toxic (McKinley et al., present late in the course ofthe illness or not at all, and 1980; Kalkay et al., 1983; Stephenson & Cotton, the illness may mimic other diseases. 1985), massive lower gastrointestinal bleeding Following ingestion of the organism there is a (Michalak et al., 1980), and bowel necrosis (Evans & prodromal illness consisting of malaise, nausea, Dadswell, 1967). In one of the patients with toxic anorexia and fever lasting for a day or two. Colicky megacolon two large bowel perforations occurred and abdominal pains, muscle pains, backache and other the patient developed peritonitis (Stephenson & Cot- joint pains may be experienced. ton, 1985). Diarrhoea and abdominal pain, when present, will The latter two situations indicate that merely be- dominate the clinical picture. The diarrhoea begins cause a diagnosis of campylobacter colitis has been CAMPYLOBACTER ENTEROCOLITIS 723 Postgrad Med J: first published as 10.1136/pgmj.62.730.719 on 1 August 1986. Downloaded from

established, does not mean that a complication requir- mucosae, and of focal collections of polymorphs. ing operative treatment will not occur. There were isolated crypt abscesses and 'incipient' crypt abscesses in which, according to the authors, the majority ofpolymorphslay between the crypt cells and Diagnosis a relatively small number within the lumen; there was partial destruction or flattening of the crypt epithelial There must be a high index of suspicion of infective cells. These and other histological changes which were enterocolitis when investigating a patient with described, were different from those of typical abdominal pain, with or without diarrhoea. Rectal ulcerative colitis and Crohn's disease. However, some swabs have sometimes yielded the diagnosis when other workers (Lambert, M.E. et al., 1979; Colgan et diarrhoea has been absent (Bentley et al., 1985). al., 1980) have reported that the mucosal changes Otherwise a fresh specimen of stool must be collected cannot be distinguished from those ofCrohn's disease and sent to the laboratory immediately. or ulcerative colitis. One interesting observation is that whatever the original changes on rectal biopsy, they Microscopy of stools improve markedly in patients with infective diarrhoea during the convalescent period, whereas in those with A rapid presumptive diagnosis of campylobacter inflammatory bowel disease they persist (Dickinson et enteritis can be made during the acute phase of the al., 1979). illness by dark-field or phase-contrast microscopy performed on a fresh specimen of stool. Red cells and Barium enema neutrophils will also be present in many cases. The radiological features of campylobacter colitis Stool culture have not been described in detail, largely because the disease is self limited in many patients. In mild cases This will enable confirmation of the diagnosis. The there are minimal changes. In more severe disease the genus, species and subspecies of the organism will be changes may affect the colon as well as the ileum as will its antibiotic sensitivities. In severe J.R. et determined, (Lambert, al., 1979), and consist of ulceration copyright. infections, blood should also be sent for culture. and multiple aphthous ulcers which are similar to those caused by Crohn's disease or ulcerative colitis Serology (Kollitz et al., 1981; Bentley et al., 1985). Barium enema has been valuable in excluding obstruction and Blood should be sent for serology during the acute hence avoiding an operation in a patient with symp- phase of the illness and during convalescence 6 weeks toms and signs and plain X-ray findings suggestive of later. Specific antibodies which the patients acquire intestinal obstruction (Bentley et al., 1985). during the illness are tested for. Tube agglutination tests have detected specific agglutinins to a titre of 1:80 or more, and a four-fold or greater rise oftitre between Treatment http://pmj.bmj.com/ acute and convalescent samples has been noted (Skirrow, 1977). Conservative management Rectal biopsy Many infections with C. jejuni pursue a self-limiting course, and many patients with mild illness will The possibility of cross infection must be borne in recover completely without specific treatment (Blaser

mind when any patient with diarrhoea which may be et al., 1979). However, when symptoms are severe and on October 2, 2021 by guest. Protected due to an infective cause is being investigated by the illness protracted, or when diarrhoea is explosive sigmoidoscopy and barium enema studies. Ifadequate and bloody, it is wise to administer fluids and specific precautions are taken, sigmoidoscopy and rectal antimicrobial therapy. biopsy may yield useful information. Price and Erythromycin (as the ethylsuccinate, because of its colleagues (1979) performed sigmoidoscopy on 21 out lower risk of ) is the drug of choice, as most of 29 patients presenting to an infectious disease unit strains of C. jejuni are sensitive to it. Other with acute diarrhoea. Rectal biopsies were abnormal antimicrobial agents to which the organism will often in all but four, and in the patients with campylobacter respond include gentamicin, tetracyclines, clin- infection there was histologically a characteristic proc- damycin, and chloramphenicol. A premature return to tocolitis in each case although the rectum was macros- solid foods often precipitates a recurrence of symp- copically normal in some. The abnormalities consis- toms (Skirrow, 1977), and hence it is advisable to allow ted, in all cases, ofoedema producing separation ofthe only a fluid diet until all symptoms have subsided. crypts and a gap between their base and the muscularis Antidiarrhoeal agents such as diphenoxylate hydro- 724 D.P. SELLU Postgrad Med J: first published as 10.1136/pgmj.62.730.719 on 1 August 1986. Downloaded from chloride (Lomotil) and compounds containing kaolin operation will be avoided if pseudo-obstruction is and morphine should be avoided as they may prolong found (Bentley et al., 1985). the course of the diarrhoea. Right hemicolectomy was required in the case of a patient who developed massive gastrointestinal bleed- Operative treatment ing from multiple mucosal ulcers in the terminal ileum and at the ileo-caecal valve (Michalak et al., 1980). The large number of patients who have undergone Arteriography was very helpful in defining the other- unnecessary operations in the course of campylobac- wise grossly indefinable source of bleeding, and the ter colitis is an indication that an operation is rarely patient made good recovery from the operation. necessary in this condition (Ponka et al., 1981). In Another patient who developed and some ofthe cases in which a complication requiring an colonic perforations following campylobacter colitis operation has occurred, such a complication has been was successfully treated by subtotal colectomy and potentially life-threatening (Sellu & Lynn, 1985; ileo-rectal anastomosis (Stephenson & Cotton, 1985). Michalak et al., 1980; Stephenson & Cotton, 1985); If a patient presents with signs of intra-abdominal death from bowel necrosis has been recorded (Evans & surgical emergency, campylobacter colitis should be Dadswell, 1967). From reports of the frequency of borne in mind as a possible cause. Treatment will campylobacter infections, however, it is reasonable to depend on the clinical features and the decision to assume that few patients will need an operation during operate should be made as in other patients presenting the course ofthis illness. There are no studies as yet to with acute abdominal pain. show what the indications for surgery should be, or, when an operation is indicated, the timing ofit. Much of the advice given here is based on the few reports in Conclusions the literature and on the author's own experience of this infection. Campylobacters are a relatively common cause of Laparotomy is indicated if, despite specific enterocolitis in man. The clinician to whom the patient antimicrobial treatment, there are features to suggest a presents must have a high index of suspicion of this complication such as appendicitis or bowel necrosis. If condition, especially in those patients whose features an operation is performed, it is wise to increase the are atypical. Some of the more severe infections may copyright. number of antibiotics to include, say, gentamicin and present to the surgeon, who must balance the risk of metronidazole, in order to cover other intestinal missing a lesion for which an operation is mandatory bacteria. If acute cholecystitis is suspected, the author against that of an unnecessary operation. A believes that the patient should be treated con- knowledge of the biological behaviour of, and the servatively unless the inflammation is not subsiding or spectrum of clinical illnesses produced by, this genus there are signs ofbiliary perforation. Ifthe features are of bacteria is essential for rational therapy, and those of large it may be prudent to communication between clinicians and microbiolog- request an urgent barium enema examination, as an ists is vital for the successful outcome of the disease. http://pmj.bmj.com/

References

ANOLIK, J.R., MILDVAN, D., WINTER, J.W., PUTTLITZ, D., (1980a). Survival of Campylobacter fetus subsp. jejuni in RUBENSTEIN, S.M. & LOZMAN, H. (1983). Mycotic aortic biological milieus. Journal of Clinical Microbiology, 11, aneurysm: a complication of C.fetus septicemia. Archives 309.

ofInternal Medicine, 143, 609. BLASER, M.J., PARSONS, R.B. & WANG, W-L.L. (1980b). on October 2, 2021 by guest. Protected ANONYMOUS (1978). Campylobacter infection in Britain Acute colitis caused by Campylobacter fetus ss. jejuni. 1977. British Medical Journal, 1, 1357. , 78, 448. BENTLEY, D., LYNN, J. & LAWS, W.J. (1985). Campylobacter BLASER, M.J. & BARTH RELLER, L. (1981). Campylobacter colitis with aphthous ulceration mimicking obstruction. enteritis. New England Journal of Medicine, 305, 1444. British Medical Journal, 291, 634. BLASER, M., CRAVENS, J., POWERS, B.W. & WANG, W.L. BLABEY, R.G. JR, PARRY, M.F., BULL, S.M. & WEED, C.B. (1981a). Campylobacter enteritis associated with canine (1983). Mycotic aneurysm ofthe abdominal aorta: success- infection. Lancet, i, 979. ful management of the C. fetus aortitis. Connecticut BLASER, M.J., WALDMAN, R.J., BARRETT, T. & ERLAND- Medicine, 47, 129. SON, A.L. (1981b). Outbreaks ofcampylobacter enteritis in BLASER, M.J., BERKOWITZ, I.D., LAFORCE, F.M., RELLER, two extended families: evidence for person to person L.B. & WANG, W-L.L. (1979). Campylobacter enteritis: transmission. Journal of Pediatrics, 98, 254. clinical and epidemiological features. Annals of Internal BOKKENHEUSER, V. (1970). Vibrio fetus infection man, I. Medicine, 91, 179. Ten new cases and some epidemiologic observations. BLASER, M., HARDESTY, H.L., POWERS, B. & WANG, W-L.L. American Journal ofEpidemiology, 91, 400. CAMPYLOBACTER ENTEROCOLITIS 725 Postgrad Med J: first published as 10.1136/pgmj.62.730.719 on 1 August 1986. Downloaded from

BRUCE, D., ZOCHOWSKI, W. & FERGUSON, I.R. (1977). bridge, 88, 155. Campylobacter enteritis (letter). British Medical Journal, KING, E.O. (1957). Human infections with Vibriofetus and a 2, 1219. closely related vibrio. Journal ofInfectious Diseases, 101, BUTZLER, J.P. & SKIRROW, M.B. (1979). Campylobacter 119. enteritis. Clinics in Gastroenterology, 18, 737. KING, E.O. (1962). The laboratory recognition of Vibriofetus CHANDRA, L., BARROWMAN, J.A., KUTTY, K.P. & FARDY, and a closely related vibrio isolated from cases of human P. (1982). Campylobacter infection mimicking relapse of vibriosis. Annals ofthe New York Academy ofSciences, 98, ulcerative colitis. Canadian Medical Association Journal, 700. 126, 389. KOLLITZ, J.P.M., DAVIS, G.B. & BERK, R.N. (1981). Cam- COLGAN, T., LAMBERT, J.R., NEWMAN, A. & LUK, S.C. pylobacter colitis: a common infectious form of acute (1980). Campylobacter jejuni enterocolitis: a cinicopath- colitis. Gastrointestinal Radiology, 6, 227. ologic study. Archives of Pathology and Laboratory KOSUNEN, T.U., KAURANEN, 0. & MARTIO, J. (1980). Medicine, (Chicago), 104, 571. Reactive arthritis after Campylobacter jejuni enteritis in CONN, H.O. & FESSEL, J.M. (1971). Spontaneous bacterial patients with HLA-B27. Lancet, i, 1312. peritonitis in cirrhosis: variations on a theme. Medicine, LAMBERT, J.R., TISCHLER, M.E., KARMALI, M.A. & NEW- 50, 161. MAN, A. (1979). Campylobacter ileocolitis: an inflam- COOPER, I.A. & SLEE, K.J. (1971). Human infection by Vibrio matory bowel disease. Canadian Medical Association Jour- fetus. Medical Journal ofAustralia, 1, 1263. nal, 121, 1377. DALE, B. (1977). Campylobacter enteritis (letter). British LAMBERT, M.E., SCHOFIELD, P.F., IRONSIDE, A.G. & MAN- Medical Journal, 2, 318. DAL, B.K. (1979). Campylobacter colitis. British Medical DARLING, W.M., PEEL, R.N., SKIRROW, M.B. & MULIRA, Journal, 1, 857. A.E.J.L. (1979). Campylobacter cholecystitis. Lancet, i, LINDQUIST, B., KJELLANDER, J. & KOSUNEN, T. (1978). 1302. Campylobacter enteritis in Sweden (letter). British Medical DAVIES, J.S. &PENFOLD, J.B. (1979). Campylobacter urinary Journal, 1, 303. infection. Lancet, i, 1091. LONGFIELD, R., O'DONNELL, J., YUDT, W., LISSNER, C. & DEKEYSER, P., GOUSUIN-DETRAIN, M., BUTZLER, J.P. & BURNS, T. (1979). Acute colitis and bacteremia due to STERNON, J. (1972). Acute enteritis due to related vibrio: Campylobacter fetus. Digestive Diseases and Sciences, 24, first positive stool cultures. Journal ofInfectious Diseases, 950. 125, 390. LOSS, W.L., MAGALA, J.C. & PEREIRA, M. (1980). Cam- DE MOL, P. & E. BOSMANS, (1978). Campylobacter enteritis pylobacter colitis presenting as inflammatory bowel dis- copyright. in Central Africa. Lancet, i, 604. ease with segmental colonic ulcerations. Gastroenterology, DICKINSON, R.J., GILMOUR, H.M. & McCLELLAND, D.B.L. 79, 138. (1979). Rectal biopsy in patients presenting to an infec- MAcFADYEAN, F. & STOCKMAN, S. (1909). Report of the tious disease unit with diarrhoeal disease. Gut, 20, 141. Departmental Committee Appointed by the Board of DRAKE, A.A., GILCHRIST, M.J.R., WASHINGTON, J.A., II, Agriculture and Fisheries to Inquire into Epizootic Abor- HUIZENGA, K.A. & BAN SCOY, R.E. (1981). due tion, volume 3. His Majesty's Stationery Office: London. to Campylobacter fetus subspecies jejuni: a clinical review MARTY, A.T., WEBB, T.A., STUBBS, A.G. & PENKAVA, R.R. of 63 cases. Mayo Clinic Proceedings, 56, 414. (1983). Inflammatory abdominal aortic aneurysm infected ELLIS, M.E., POPE, J., MOKASHI, A. & BUNBAR, E. (1982). by C. fetus. Journal ofthe American Medical Association, Campylobacter colitis associated with erythema nodosum. 249, 1190. British Medical Journal, 285, 937. McKINLEY, M.J., TAYLOR, M. & SANGREE, M.H. (1980). http://pmj.bmj.com/ EVANS, R.G. & DADSWELL, J.V. (1967). Human vibriosis. Toxic megacolon with campylobacter colitis. Connecticut British Medical Journal, 3, 240. Medicine, 44, 396. GEFFEN, D.B., GILL, V.J. & CHABNER, B.A. (1983). Cam- McNEIL, N.I., BUTTOO, S. & RIDGWAY, G.L. (1984). Spon- pylobacter thrombophlebitis. Annals ofInternal Medicine, taneous bacterial peritonitis due to Campylobacterjejuni. 99, 126. Postgraduate Medical Journal, 60, 487. GUERRANT, R.L., LAHITA, R.G., WINN, W.C. & ROBERTS, MERTENS, A. & DE SMET, M. (1979). Campylobacter R.B. (1978). in man: pathogenic cholecystitis. Lancet, i, 1092.

mechanisms and review of 91 blood stream infections. MICHALAK, D.M., PERRAULT, J., GILCHRIST, M.J., on October 2, 2021 by guest. Protected American Journal ofMedicine, 65, 584. DOZOIS, R.R., CARNEY, J.A. & SHEEDY, P.F., II. (1980). KALKAY, M.N., AYANIAN, Z.S., LEHAF, E.A. & BALDI, A. Campylobacter fetus ss. jejuni: a cause of massive lower (1983). Campylobacter-induced toxic megacolon. gastrointestinal hemorrhage. Gastroenterology, 79, 742. American Journal of Gastroenterology, 78, 557. MUYTJENS, H.L. & VAN DIS, P. (1978). Campylobacterfetus KALNINS, I. & JACKSON, A.W. (1977). Isolation of Cam- subspecies jejuni als verwekker van diarree. Nederlands pylobacter fetus ss. jejuni in Canada. Canadian Diseases Tijdschrift voor Geneeskunde, 122, 504. Weekly Report, 50, 198. PALMER, S.R., GULLY, P.R., WHITE, J.M., PEARSON, A.D., KARMALI, M.A. & FLEMING, P.C. (1979). Campylobacter SUCKLING, W.G., JONES, D.M., RANES J.C.L. & PENNER, enteritis in children. Journal ofPediatrics, 94, 527. J.L. (1983). Water-borne outbreak of campylobacter gas- KARMALI, M.A. & TAN, Y.C. (1980). Neonatal campylobac- troenteritis. Lancet, i, 287. ter enteritis. Canadian Medical Association Journal, 122, PEARSON, A.D., SKIRROW, M.B., ROWE, J., DAVIES, J. & 192. JONES, D.M. (Editors). (1983). Campylobacter II: Proceed- KENDALL, E.J.C. & TANNER, E.I. (1982). Campylobacter ings ofthe Second International Workshop on Campylobac- enteritis in general practice. Journal of Hygiene, Cam- ter Infections. Public Health Laboratory Service: London. 726 D.P. SELLU Postgrad Med J: first published as 10.1136/pgmj.62.730.719 on 1 August 1986. Downloaded from

PEARSON, A.D., SUCKLING, W.G., RICARDI, I.D., KNILL, STEPHENSON, T.J. & COTTON, D.W.K. (1985). Toxic M., WARE, E. (1977). Campylobacter-associated diarrhoea megacolon complicating campylobacter colitis. British in Southampton (letter). British Medical Journal, 2, 955. Medical Journal, 291, 1242. PONKA, A., PITKANEN, T. & KOSUNEN, T.U. (1981). TELFER BRUNTON, W.A. & HEGGIE, D. (1977). Cam- Campylobacter enteritis mimicking acute abdominal pylobacter-associated diarrhoea in Edinburgh (letter). emergency. Acta Chirurgica Scandinavica, 147, 663. British Medical Journal, 2, 956. PRICE, A.B., JEWKES, J. & SANDERSON, P.J. (1979). Acute TURNBULL, P.C.B. & ROSE, P. (1982). Campylobacterjejuni diarrhoea: campylobacter colitis and the role of rectal and salmonella in raw red meats: a Public Health biopsy. Journal of Clinical Pathology, 32, 990. Laboratory Service survey. Journal of Hygiene, Cam- RETTIG, P.J. (1979). Medical progress: campylobacter infec- bridge, 88, 29. tions in human beings. Journal ofPediatrics, 94, 855. VERON, M. & CHATELAIN, R. (1973). Taxonomic study of ROBINSON, D.A. & JONES, D. (1981). Milk-borne cam- the genus Campylobacter Sebald and Veron and designa- pylobacter infection. British Medical Journal, 282, 1374. tion of the neotype strain from the type species, Cam- SEBALD, M. & VERON, M. (1963). Teneur en bases de 1'ADN pylobacter fetus (Smith and Taylor) Sebald and Veron. et classification des vibrions. Annales de l'Institut Pasteur, International Journal of Systemic Bacteriology, 23, 122. 105, 897. VESELY, D., MAcINTYRE, D.S. & RATZAN, K.R. (1975). SELLU, D.P. & LYNN, J.A. (1985). Campylobacter colitis Bilateral deep vein thrombophlebitis due to Vibrio fetus. associated with appendicitis and septicaemia. British Archives ofInternal Medicine, 135, 994. Medical Journal, 291, 1688. VINZENT, R., DUMAS, J. & PICARD, N. (1947). Septicemie SEVERIN, W.P. (1978). Campylobacter en enteritis. grave au cours de la grossesse due a un vibrion: avortment Nederlands Tzjdschrift voor Geneeskunde, 122, 499. consecutif. Bulletin de L'Academie National de Medecine SIMMONS, N.A. & GIBBS, F.J. (1979). Campylobacter spp. in (Paris), 131, 90. oven-ready poultry. Journal ofInfection, 1, 159. WARREN, J.R. & MARSHALL, B. (1983). Unidentified curved SKIRROW, M.B. (1977). Campylobacter enteritis: a "new" bacilli on gastric epithelium in active chronic gastritis. disease. British Medical Journal, 2, 9. Lancet, i, 1273. SKIRROW, M.B. & BENJAMIN, J. (1980). Differentiation of WILLOUGHBY, C.P., PIRIS, J. & TRUELOVE, S.C. (1979). enteropathogenic campylobacter. Journal ofClinicalPath- Campylobacter colitis. Journal of Clinical Pathology, 32, ology, 33, 1122. 986. SLEE, K.J. (1972). Human vibriosis an endogenous infection? Australian Journal of Medical Technology, 3, 7. copyright. http://pmj.bmj.com/ on October 2, 2021 by guest. Protected