CDC - Anthrax of the Gastrointestinal = Tract

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Vol.=20 8, No. 7
July = 2002


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Perspectives

Anthrax of the=20 Gastrointestinal Tract

Thira Sirisanthana* and Arthur E. Brown=86
*Chiang = Mai=20 University, Chiang Mai, Thailand; and =86Armed Forces Research = Institute of=20 Medical Sciences, Bangkok, Thailand

When = swallowed,=20 anthrax spores may cause lesions from the oral cavity to the = cecum.=20 Gastrointestinal anthrax is greatly underreported in rural=20 disease-endemic areas of the world. The apparent paucity of this = form of=20 anthrax reflects the lack of facilities able to make the = diagnosis in=20 these areas. The spectrum of disease, ranging from subclinical = infection=20 to death, has not been fully recognized. In some community-based = studies, cases of gastrointestinal anthrax outnumbered those of=20 cutaneous anthrax. The oropharyngeal variant, in particular, is=20 unfamiliar to most physicians. The clinical features of = oropharyngeal=20 anthrax include fever and toxemia, inflammatory lesion(s) in the = oral=20 cavity or oropharynx, enlargement of cervical lymph nodes = associated=20 with edema of the soft tissue of the cervical area, and a high=20 case-fatality rate. Awareness of gastrointestinal anthrax in a=20 differential diagnosis remains important in anthrax-endemic = areas but=20 now also in settings of possible = bioterrorism.

The epidemiology of human anthrax has been described as = agricultural=20 and industrial (1). In = the=20 agricultural setting, infections occur from exposure to = Bacillus=20 anthracis spores on the skin or the mucosal surfaces of the=20 gastrointestinal (GI) tract. Primary infections of the respiratory = tract=20 are rare in agricultural settings. Generally, reports state that = the=20 cutaneous form of anthrax is much more common than the GI form (2,3). = We=20 propose that the apparently overwhelming predominance of the = cutaneous=20 form of anthrax is rather a reflection of the difficulty of = diagnosis of=20 the GI form.

GI anthrax may be diagnosed on the basis of epidemiology or=20 microbiologic, pathologic, or serologic testing. Serologic = diagnosis is=20 available only in a few research laboratories; pathologic = evaluation=20 requires surgery or necropsy in an appropriate hospital; = microbiologic=20 testing requires at least microscopy and preferably bacterial = culture=20 capacity; and epidemiology requires a level of suspicion and an = ability to=20 properly perform outbreak investigations. Herbivores, which = provide most=20 of the human exposure risk for anthrax, become infected in rural = parts of=20 the world where spores in the soil perpetuate endemicity. Mild = cases of=20 gastroenteritis attract little attention, and people with severe=20 infections, leading to death within 2=963 days, may never reach a = medical=20 facility.

Areas endemic for anthrax exist in all continents containing = tropical=20 and subtemperate regions. In the English published reports, deaths = from GI=20 anthrax have been reported in Thailand (4=966), = India=20 (7,8),=20 Iran (9=9611),=20 Gambia (12), = and=20 Uganda (13).=20 Anthrax-contaminated beef from a locally infected cow was eaten in = Minnesota in 2000. Cooking the meat may have prevented human cases = (14).=20 Despite this wide distribution of endemicity, no large series of=20 pathologically described cases exists. Based on limited reports of = GI=20 anthrax, the disease spectrum ranges from the asymptomatic to the = fatal,=20 by shock or sepsis. When swallowed, anthrax spores may cause = lesions from=20 the oral cavity to the cecum. Ulcerative lesions, usually multiple = and=20 superficial, may occur in the stomach, sometimes in association = with=20 similar lesions of the esophagus and jejunum (4,5,15). = These=20 ulcerative lesions may bleed; hemorrhaging in severe cases may be = massive=20 and fatal (4,5).

Reported cases indicate that lesions farther down the GI tract, = in the=20 mid-jejunum, terminal ilium, or cecum, tend to develop around a = single=20 site or a few sites of ulceration and edema, more analogous to = cutaneous=20 lesions. These lesions may lead to hemorrhage (6,16),&nb= sp;=20 obstruction (10,17,18),= =20 perforation (17,18),= or=20 any combination of these. Ascites may complicate GI anthrax (6,7,9,11,18,19).=20 In some patients, the fluid shift from the vascular compartment = leads to=20 shock and death (6,7,9).<= /P>

The pathologic examination of anthrax lesions with entry via = the GI=20 tract shows that the mucosa is always involved, as are regional = lymph=20 nodes, which are enlarged and hemorrhagic (15). = The=20 GI tract may also be involved after disseminated infection in = pulmonary=20 and sometimes cutaneous cases (20=9622). = In=20 this situation, the localization is in the submucosa as a result = of its=20 blood flow, and the mucosa and regional lymph nodes become = involved only=20 secondarily.

These reports are biased toward the hospitalized patients with = severe=20 cases. Thorough epidemiologic reports are scarce. One informative=20 description of an outbreak investigation and response comes from = Uganda=20 (13).=20 Gastroenteritis developed and death occurred in 155 persons who = feasted on=20 an infected zebu (Asian ox); 2 days after exposure, the incident = was=20 reported to authorities who flew in a multiministry team the next = day.=20 Gastroenteritis developed in most (92%) of those exposed within = 15=9672=20 hours. All nine deaths were in children and occurred in the first = 2 days;=20 all 12 asymptomatic cases were in adults. Authorities referred 134 = symptomatic people to the hospital for rehydration and treatment = with=20 antibiotics; all recovered. Thus, for most people exposed, the = syndrome=20 was gastroenteritis; a differential diagnosis would not normally = have=20 included anthrax. The age differences suggest that in this setting = previous exposure may have occurred, leaving some adults with = partial=20 immunity.

Another community anthrax outbreak of note was investigated by = officers=20 from the Field Epidemiology Training Program of the Thai Ministry = of=20 Public Health (23). = From=20 January through June 1982, an outbreak of human anthrax was = recognized in=20 two districts in Udon Thani Province in northeastern Thailand = after an=20 outbreak in cattle that killed 36 water buffalos (Bubalus = bubalus)=20 and 7 cows and bulls. Of the 102 patients, 28 had cutaneous = anthrax and 74=20 gastrointestinal anthrax. The only symptom in 67 of these 74 = patients with=20 gastrointestinal anthrax was acute diarrhea (i.e., = gastroenteritis). The=20 other seven patients had additional symptoms of nausea, vomiting,=20 abdominal distention, and severe abdominal pain. Three patients = died; the=20 case-fatality rate was 4%. Thus, in these two community-based = studies, the=20 number of patients with GI anthrax far outnumbered those with the=20 cutaneous form of the disease.

	Figure = 1

	Click to view enlarged = image Figure 1. A = 29-year-old=20 man, 1 day after the onset of symptoms of oropharyngeal = anthrax.=20 Marked and painful swelling of the right side of the neck = was=20 present.

	Figure=20 2

	Click to view enlarged = image Figure 2. A = 27-year-old=20 man, 5 days after the onset of symptoms of oropharyngeal = anthrax....=20

	Figure 3=20

	Click to view enlarged = image Figure 3. The = same patient=20 as in Figure 2. This picture is 9 days after the onset of = symptoms=20 of oropharyngeal anthrax....

In addition to lack of epidemiologic, microbiologic, = pathologic, and=20 serologic expertise and facilities in the rural settings where = anthrax=20 outbreaks take place, the oropharyngeal form is underreported = because few=20 physicians are aware of the disease. Only six publications in the = MEDLINE=20 database report anthrax lesions in the mouth or oropharynx (24=9629= ).=20 Davies described a major epidemic of anthrax involving >9,000 = patients=20 in Zimbabwe from 1978 to 1980 (24). = He=20 cited four cases in which lesions were on the tonsil and the = tongue but=20 provided no details. We reported an outbreak of human anthrax = after=20 anthrax was found in water buffaloes in March=96April 1982 in = Chiang Mai,=20 northern Thailand (25). A = total of 52 cases of cutaneous anthrax and 24 cases of = oropharyngeal=20 anthrax were recognized in humans. All patients with oropharyngeal = anthrax=20 had recently eaten water buffalo meat. The mean incubation period = was 42=20 hours (range 2=96144 hours). All but one patient were admitted to = the=20 hospital. All patients sought medical attention because of painful = neck=20 swelling, and all but one complained of fever. The other common = symptoms=20 were sore throat, dysphagia, and hoarseness. The neck swelling was = usually=20 marked and was caused by enlargement of cervical lymph nodes and = soft=20 tissue edema (Figure= =20 1). Mouth lesions were located on the tonsils, posterior = pharyngeal=20 wall, or the hard palate. In severe cases, the tonsillar lesions = extended=20 to involve the anterior and posterior pillars of fauces, as well = as the=20 soft palate and uvula. Early lesions were edematous and congested. = By the=20 end of the first week, central necrosis and ulceration had = produced a=20 whitish patch (Figure= =20 2). In the second week, this patch developed into a = pseudomembrane=20 covering the ulcer (Figure= =20 3). Diagnosis could be made by culture taken from the lesion = in the=20 mouth. A Gram stained smear from the lesion showed numerous=20 polymorphonuclear leukocytes and gram-positive bacilli. Studies of = serum=20 antibody to anthrax antigens confirmed the diagnosis (27).=20 Despite hospital admission and antibiotic treatment, 3 of the 24 = patients=20 died, for a case-fatality rate of 12.4%. In 1986, Doganay and = colleagues=20 reported six patients from Turkey with essentially the same = clinical=20 syndrome (28). = The=20 case-fatality rate in that study was 50%. The most recent case = report,=20 also from Turkey, was in 1993 (29).

When cattle die of anthrax, the bacteremia is massive, and=20 manifestations of the infection are visible to the butcher. In = some=20 settings, people may eat meat they know to be contaminated, as was = the=20 situation in a poor village of Harijans (=93untouchables=94) in = India (8). = More=20 common may be the situation in which meat is sold to those unaware = of the=20 animal disease as was the case in the Chiang Mai outbreak (25). = Only=20 those who eat dishes that are raw or undercooked are exposed to = infectious=20 material. Disease is likely related to a dose of viable spores and = the=20 immune state of host. In contrast to the extreme susceptibility of = cattle=20 to this infection and its bacteremia, studies in chimpanzees = suggest that=20 primates are relatively resistant (30).

While the biowarfare and bioterrorist development of anthrax = has=20 focused on inhalation, ingestion has been considered as well. The = Japanese=20 experiments in China during the 1930s and 1940s included attempts = to=20 poison children with chocolate impregnated with anthrax (31). = More=20 recently, the apartheid government of South Africa had developed=20 biological weapons, including another attempt at = anthrax-containing=20 chocolate (32). = Given=20 the large community outbreak of salmonellosis caused by an = intentional=20 contamination of restaurant salad bars the in United States by the = Rajneeshees (33),=20 awareness of the potential for GI anthrax due to bioterrorism is=20 important.

In conclusion, GI anthrax is probably greatly underreported in = rural=20 disease-endemic areas of the world. The spectrum of disease, = ranging from=20 no symptoms to death, has not been fully appreciated. Awareness of = anthrax=20 in a differential diagnosis remains important in disease-endemic = areas and=20 also in settings of possible bioterrorism.

Dr. Sirisanthana is professor of medicine and director of the = Research=20 Insitute for Health Sciences, Chiang Mai University, Thailand. He = received=20 his medical degree from Mahidol University in Bangkok and then = trained in=20 internal medicine in infectious disease at Indiana University, the = University of Chicago and the Medical College of Wisconsin from = 1975 to=20 1979.

LTC Brown is chief, Department of Retrovirology, at the Armed = Forces=20 Research Institute for Medical Sciences in Bangkok. He is a fellow = of the=20 Infectious Disease Society of American with training in tropical = public=20 health. Dr. Brown=92s research in tropical infectious diseases has = been=20 based largely in Thailand for the past 20 years.

References

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Davies JCA. A major epidemic of anthrax in Zimbabwe. = Cent Afr J=20 Med 1982;28:291=968.=20
Sirisanthana T, Navachareon N, Tharavichitkul P, = Sirisanthana V,=20 Brown AE. Outbreak of oral-pharyngeal anthrax: an unusual=20 manifestation of human infection with Bacillus = anthracis. Am=20 J Trop Med Hyg 1984;33:144=9650.=20
Navacharoen N, Sirisanthana T, Navacharoen W, Ruckphaopunt = K. Oropharyngeal anthrax. J Laryngol Otol = 1985;99:1293=965.=20
Sirisanthana T, Nelson KE, Ezzell JW, Abshire TG. Serologic studies of patients with cutaneous and = oral-oropharyngeal anthrax from northern Thailand. Am J Trop = Med Hyg=20 1988;39:575=9681.=20
Doganay M, Almac A, Hanagasi R. Primary throat anthrax. A report of six = cases. Scand J=20 Infect Dis 1986;18:415=969.=20
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Daley S. In support of apartheid: poison whisky and = sterilization.=20 New York Times, June 11, 1998, section A, page 3.=20
Torok TJ, Tauxe RV, Wise RP, Livengood JR, Sokolow R, = Mauvais S, et=20 al. A large community outbreak of salmonellosis = caused by=20 intentional contamination of restaurant salad bars. JAMA=20 1997;278:389=9695.

Comments to the=20 Authors

Address = for=20 correspondence: Arthur E. Brown, AFRIMS, APO AP 96546; = fax:=20 66-02-644-4824; e-mail: brownae@thai.amedd.army.mil

Comments to the EID=20 Editors

Please use this form to submit comments to = the EID=20 Editors.=20

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		This page = posted May 8, 2002 This=20 page last reviewed July=20 8, 2002 =

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