Clinical features in enteritis due to vibrio parahemolyticus

Clinical Features in Enteritis Due to Vibrio Parahemolyticus

JAMES

L. BOLEN,

SHIELA

A. ZAMISKAT

WILLIAM

M.D.’

B. GREENOUGH

Baltimore,

Clinical features of a case of enteritis due to Vibrio parahemolyticus are presented. Superficial ulcerations of colonic mucosa were observed directly by sigmoidoscopy. Previously such damage had not been documented but inferred from the presence of red cells and leukocytes in the stools. The literature pertinent to V. parahemolyticus and its recent presence in the United States is reviewed.

Ill, M.D.

Maryland

Although

the marine

or halophilic

bacterium,

Vibrio

parahemolyti-

cus, is responsible for many cases of bacterial food poisoning in Japan [ 11, it was not until 1970 that infection due to this organism was reported in the United States. The first major outbreak of food poisoning attributed to this organism occurred in Maryland in 1971 [2]. There has been little information about the clinical features of this disease as it occurs in this country to date. We describe a case of enteritis due to V. parahemolyticus which was observed at The Johns Hopkins Hospital. These observations include direct sigmoidoscopic visualization of superficial ulcerations of colonic mucosa which have previously been inferred from the presence of red cells and leukocytes in the stools, but not directly observed. CASE REPORT This 32 year old black woman (P.W.) was admitted to The Johns Hopkins Hospital at 9 AM on July 6, 1972, and diarrhea

which began

with the acute onset of abdominal

abruptly

2 hours earlier.

been well and denied having any gastrointestinal history for the past several From

the Department

Infectious

Diseases,

Laboratory

Medicine,

of Medicine, and

the

Division of

Department

The Johns

Hopkins

mately

of

tute of Allergy and Infectious National

Institutes

land 20014.

of Health,

Requests

Diseases

of the

Bethesda,

Mary-

“different.” patient

for reprints should be ad-

The American

Journal

previously

that day. Several

cooked,

had been ob-

of her children also con-

No other participant

in the meal subsequently 12 hours after

from sleep with severe,

tenesmus.

Over the next half hour, she experienced

movements

and vomited

crampy

clear

umbilical-abdominal

stomach

she noted feverishness,

became

this meal

on three

dizziness and several

she

pain and

six watery,

contents

ill. The

when

yellow occa-

more wa-

tery bowel movements. Upon arriving in the emergency room 2 hours after the onset of symptoms, three bright bloody diarrhea1 stools were passed. On admission she appeared moderately dehydrated, and somewhat toxic but well oriented, with a pulse rate of 100 beats/min, blood pressure of 120185 mm Hg and rectal temperature of 10 1 OF. Examination of the abdomen revealed decreased bowel sounds. mild diffuse tender-

Maryland 21030.

1974

The crabs,

felt well until approximately

sions. Thereafter.

l

October

earlier

awakened bowel

es, The Johns Hopkins University School of Medicine and Hospital, Baltimore, Maryland 21205. Manuscript accepted January 9, 1974. Present address: 4109 Sutherland, Palo Alto, California 94304. t Present address: 1F Springhead Court,

636

Her dietary that approxi-

sumed crabs with the patient, although no one shared the crab that tasted

dressed to Dr. William B. Greenough Ill, Department of Medicine, Division of Infectious Diseas-

Cockeysville,

“different.”

tained from a relative

versity School of Medicine and Hospital, Baltimore, Maryland 21205. This work was supported by .Grant No. AI-0009 from the National Insti-

except

12 hours before the onset of her illness she had eaten crabs, one

of which tasted

Uni-

symptoms.

days was unremarkable,

pain

She had previously

of

Medicine Volume 57

VIBRIO PARAHEMOLYTICA

ness without rebound, and no organomegaly. Moderate perirectal irritation was present. The hematocrit value was 39 per cent, the white blood cell count was 19,100/mm3 and exhibited a marked shift to the left. Plasma electrolytes were within normal limits. Three blood cultures were sterile. The stool was watery and tinged with blood. The fecal leukocyte count was 10,600/mm3. No ova or parasites were seen on several examinations of fresh stools. Gram stain of the stool showed normal flora. Sigmoidoscopy to 20 cm shortly after admission revealed slightly hyperemic mucosa that was not friable. Six to eight shallow 1 cm* ulcers, which exhibited punctate bleeding, were noted throughout the rectosigmoid. The patient noted no further abdominal pain or nausea after admission, and her sense of well-being improved with intravenous fluids (4 liters of 0.5N saline solution over 18 hours). No antibiotics were given. During her first 24 hours of hospitalization, she had only four soft, nonbloody bowel movements. Her temperature and white blood cell count returned to normal by the 3rd hospital day. She was discharged after 5 days’ hospitalization. Three stool cultures taken at the time of admission grew organisms identifed as Vibrio parahemolyticus. Because of prior reports of V. parahemolyticus in the Chesapeake Bay area [2,14,16], the Bacteriology Laboratory of The Johns Hopkins Hospital from June to September of 1972 routinely plated all stool cultures onto TCBS (Thiosulfate Citrate Bile Salts Sucrose) agar, as well as onto the more standard media. V. parahemolyticus forms colonies with blue to greenish centers on TCBS agar, and cultures with these characteristics can be tentatively identifed as V. parahemolyticus. Such colonies were grown from this patient’s stool; nutrient requirement and biochemical reactions positively identified the organism as V. palrahemolyticus. This conclusion was confirmed by the Maryland State Bacteriology Laboratory. COMMENTS V. parahemolyticae are halophilic, gram-negative rods which exhibit considerable pleomorphism in culture [3]. By various biochemical and nutrient requirement tests, they can be divided into two subgroups, only one of which is probably enteropathogenic [ 3,4]. Pathogenicity in animals has been demonstrated in mice and with the ligated rabbit gut [3]. Human enteropathogenicity has been established on epidemiologic grounds [3-51 and by human feeding experiments ]5,6], and may be correlated with the ability to produce hemolysis on a special blood agar

151. The filrst recorded occurrence of gastroenteritis due to V. parahemolyticus was an epidemic in Osaka, Japan, in 1950 and was reported in 1953 with a striking mortality of about 8 per cent [8]. Un-

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ENTERITIS-EIOCEN

ET AL.

fortunately, the halophilic properties of the bacterium isolated in the outbreak were not recognized, and the bacterium was incorrectly named Pasteurella parahemolytica. Takikawa [6,7] is credited with first recognizing the halophilic character of the bacterium during an epidemic of acute gastroenteritis in Yokahama National Hospital in 1955, but he called it Pseudomonas enteritis. It was not until 1963 that the organism was correctly established as belonging to the genus Vibrio and was named Vibrio parahemolyticus numerous Japanese studies [ 31. Subsequently, [ 1,3,4] have documented the frequency of gastroenteritis due to V. parahemolyticus, although mortality has been extremely low or nonexistent in epidemic outbreaks, isolated cases in volunteer subjects [ 46]. The high incidence of the disease in Japan is probably related to the prominent place of fish and shellfish, frequently eaten raw, in the Japanese diet. The bacterium has now been isolated from fish or shellfish from Germany [9]. the Netherlands 1IO], Canada [ 111, Australia [ 121, India 1131 and in several areas of the United States /14- 16,191. In Japan the organism is isolated in high frequency from marine environs during the summer months, and the major clinical outbreaks show the samle seasonal pattern 131. Definite clinical disease outside Japan has been reported only recently. Thirteen cases of acute diarrhea from which a Vibrio genus with biochemical characteristics identical to V. parahemolyticus were seen in Calcutta in 1968 113 ]. No other pathogenic organisms could be isolated from the stools of these patients. Clinically, the illnesses varied from mild gastroenteritis to a full blown dysenteric syndrome with bloody diarrhea, abdomina:l pain, vomiting, pyrexia and dehydration. Although there are reports of acute gastroenteritis associated with the ingestion of shellfish in the United States prior to 1971, no etiologic agent was obtained, but cultuire methods were not studied. The first association of V. parahemolyticus with human disease in the United States was an unusual case of leg gangrene and shock in which V. parahemolyticus was cultured [ 181. The patient was a “clammer” in a New England Bay; V. parahemolyticus was subsequently isolated from these waters. The first documented case of gastroenteritis within the United States was reported in 197 1 [ :2] Approximately 320 of 550 persons attending a picnic, and subsequently approximately 20 of 30 persons attending a nearby picnic, in Eastern Marylancl became ill with acute gastroenteritis in August 1971. Cultures of stools from four patients, two from each picnic, were positive for V. parahemolyticus. A comlmon source supplier of crabs for both picnics was found, and V.

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parahemolyticus was cultured from two such crabs. Cu!tures for enteric pathogens were negative. A second outbreak, occurring in August 1972 in Louisiana, has subsequently been reported [ 191. An estimated 600 of 1,200 persons attending a “shrimp boil” became ill with acute gastroenteritis. Stool specimens from 10 symptomatic persons, specimens of the boiled shrimp and samples of fresh shrimp from Louisiana coastal waters were positive for V. parahemolyticus. Clinically, the disease bears many similarities to acute gastroenteritis due to Salmonella or Shigella, and possibly there have been many outbreaks of gastroenteritis in the United States due to V. parahemolyticus in which the cause was undetermined. Takikawa [6] has probably best studied the clinical manifestations of epidemic cases in Japan and of experiments in human volunteers. The incubation period seems dependent on the numbers of organisms ingested. but in the epidemic (Japanese) form it ranges from 9 to 25 hours with a mean of 17 hours. Diarrhea (96 per cent) and abdominal pain (95 per cent) are nearly universal and the earliest symptoms, but nausea (66 per cent), fever (64 per cent), headache (53 per cent) and vomiting (43 per cent) are commonly seen. The diarrhea is sudden and often quite profuse, with up to 15 stools in the first 24 hours of the clinical illness not being uncommon. Shock due to fluid loss is, however, the exception. Blood and mucus within these stools is common. Interestingly, a striking leukocytosis of 20,000 cells/mm3 or more is not uncommon. This was noted in our patient. Most patients recover in 2 to 3 days from the onset of the acute illness. Fatigue may persist for several additional days. Except for the original description of the illness [7], mortality has been negligible, although a very toxic illness has been described in volunteers who ingested a numerically larger bacterial inoculum [6]. Although some patients have been treated with antibiotics [5,6] this is not usual. No studies on the effect or efficacy of antibiotics on the clinical disease have been reported. In vitro, culture sensitivities have shown the organism to be sensitive to ampicillin, cephalosporin and gentamicin [ 181, and to streptomycin, tetracycline and chloramphenicol [3]. The median incubation period of the first outbreak in the United States [2] was 15 hours (range from 8 to 22 hours), and the median duration of illness was 2 days (range from 1 to 5 days). Diarrhea (98 per cent), abdominal cramps (78 per cent), nausea (76 per cent), vomiting (74 per cent), fever (26 per cent) and headache (25 per cent) were prominent symptoms. No laboratory data were included for these patients. There were no deaths. In the second outbreak [ 191, the mean incubation period was 23 hours

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(range from 5 to 92 hours). and the illness was reported to last from a few hours to more than a week. Similar symptoms were noted. Again, laboratory data were not recorded. The presence of fecal

leukocytes

in acute

diar-

rhea1 illness apparently depends primarily on a break in the integrity of the intestinal mucosa [ 191. Thus, fecal leukocytosis is seen in enteritis due to Shigella, Salmonella and invasive Escherichia coli, and distinguishes the diarrhea in these entities from that due to an enterotoxin such as is produced by Vibrio cholerae. A documented fecal leukocytosis was seen in this patient which suggested that V. parahemolyticus actually invaded the bowel mucosa to produce symptoms. This fact is corroborated by the sigmoidoscopic findings. Small superficial ulcerations were observed. No previous description of sigmoidoscopic findings in such patients has been published. Such superficial ulcerations of the bowel are occasionally seen in acute Salmonellosis and more commonly with Shigellosis [20]. Essentially nothing is known of the pathology of V. parahemolyticus enteritis. Fujino 181, in the first reported epidemic, included autopsy findings in 8 of 20 fatal cases and noted “catarrh of the stomach” and “slight erosion of the jejunum and ileum,” but he did not give a description of the colon. Our case, in terms of the clinical picture, seems comparable to those described in the Japanese literature. Acute gastroenteritis due to V. parahemolyticus may already have been a common entity in the United States, the failure to recognize it thus far being secondary to the absence of clinical description in American literature and the failure to isolate the bacteria by usual methods of culturing for enteric pathogens. Certainly, isolation of the bacterium from many U.S. coastal areas and from shellfish harvested from such regions suggest that the potential for infection is present. In addition, the potential for imported cases is manifest from the recent report of an outbreak of severe disease in passengers on a charter flight from Thailand [22]. In patients presenting with an acute diarrhea1 illness, with an appropriate dietary history, and particularly with peripheral and fecal leukocytosis, appropriate culture technics for isolation of V. parahemolyticus should be used. Treatment should be directed at the prompt replacement of fluid losses when indicated by clinical evidence of dehydration or shock. ACKNOWLEDGMENT

We are indebted to Mr. James Dick and members of The Johns Hopkins Hospital Bacteriology Laboratory for their work in isolating and identifying the Vibrio parahemolyticus.

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REFERENCES Zen-Yoli l-f: Vibrio Parahemolyticus Symposium of June 12, 1968; U.S. Department of Agriculture, Consumer and Marketing Service, Beltsville, Maryland.

3.

4.

6

8. 9.

10

11

Dadisman TA, Nelson R, Molenda JR, Garber HJ: Vibrio parahaemolyticus gastroenteritis in Maryland. I. Clinical and epidemiologic aspects. Am J Epidemioi 96: 414, 1972. Sakazaki R, lwanami S. Fukumi H: Studies on the enterofacultatively halophilic bacteria, Vibrio pathogenic, parahemolyticus, I. Japan J Med Sci Biol 16: 161, 1963. Zen-Yoji l-l, Sakai S. Terayama T, et al.: Epidemiology, enteropathogenicity and classification of Vibrio parahemolyticus J Infect Dis 115: 436, 1965. Sakazaki R. Tamura K, Kato T, et al.: Studies on the enteropathogenic facultatively halophilic bacteria. Vibrio parahemolytrcus, ill. Japan J Med Sci Biol 21: 325, 1968. Takikawa I: Studies on pathogenic halophilic bacteria. Yokoh.ama Med Bull 9: 313, 1958. Takikawa I, Fujisana T: An outbreak of food poisoning caused by a marine bacterium. Shokuhin Eiseikenkyu 3: 15, 1956 Fujino T: On fhe bacteriological examination of Shirasu food poisoning. Med J Osaka Univ 4: 299, 1953 Nakanishi H, Leistner L, Hechelmann H. et al.: Weitere Untersuchugen uber das Vorkommen von Vibrio parahaemolyticus und Vibrio alginolyticus. Arch Cebensmittelhyg 19: 49, 1968 Kampelmacher EH, Mossel DAA, van Noorle Jansen LM. et al.: A survey on the occurrence of Vibrio parahemolyticus in fish and shellfish marketed in the Netherlands. J Hyg (Camb) 68: 189, 1970. Thomson WK. Trenholm DA: The isolation of Vibrio parahe-

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molyticus and related halophilic bacteria from Canadian Atlantic shellfish. Can J Microbial 17: 545, 197 1. 12

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Battey YM, Wallace RB, Allan BC. et al: Gastroenteritis in Australia caused by a marine vibrio. Med J Aust 1. 430, 1970. Chatterjee BD, Neogy KN, Gorbach Sl: Study of Vibrio parahemolyticus from cases of diarrhea in Calcutta Indian J Med Res 58: 234, 1970. Krantz GE, Colwell RR, Lovelace E: Vibrio oarahemolvticus from the Blue Crab Callinectes Sapidus in the Chesaoeake Bav. Science 164: 1286, 1969. Baioss J, Liston J: Occurrence of Vibrio parahemolyticus and related hemolytic vibrios in marine environments in Washington State. Appl Microbial 20: 179. ‘1970. Fishbein M, Mehlman IJ, Pitcher J: Isolation of Vibrio parahemolyticus from the processed meat of Chesapeake Bay Blue Crabs. Appl Microbial 20: 176, 1970. Ratzan KR, Brojan JA, Krackow J: An outbreak of gastroenteritis associated with the ingestion of raw clams. J Infect Dis 120: 265, 1969. Roland FP: Leg gangrene and endotoxin s,hock due to Vibrio parahemolyticus: an infection acquired in New England Coastal Waters. N Engl J Med 282: 1306, 1970. Morbidity and Mortality Weekly Report: Vibrio Parahemolyticuss--Louisiana,vol 21, 1972, p 341 Harris TC, DuPont HL, Hornick RB: Fecal leukocytes in diarrhea illness. Ann Intern Med 76: 697. 1973. Horn RC: The Alimentary Tract, Pathology, 5th ed (Anderson WAD, ed), St. Louis, C.V Mosby Co. 1966, p 858. Peffers ASR, Bailey J. Barrow GI. et al.: Vibrio parahemolyticus gastroenteritis and international air travel Lancet 1: 143. 1973.

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