Not All Inflammation in the Right Lower Quadrant Is Appendicitis: A Case Report of Escherichia Coli O157:H7 With a Review of the Literature

Although significant work has been presented on this subject in pediatric, infectious disease, and epidemiologic literature, there is a noteworthy lack of information on Escherichia coli O157:H7 in any surgical journals. As this disease can present with signs and symptoms often ascribed to the acute abdomen, it is imperative that the general surgeon, pediatric surgeon, and colorectal surgeon are all familiar with this infection and its clinical ramifications. A case report followed by a review of the literature is presented.

Case Report

A 19-year-old white woman presented to the emergency room with a 3-day history of crampy abdominal pain. The pain was initially throughout the lower abdomen but had increased in severity and localized to the right lower quadrant during the past 24 hours. She also admitted to at least four or five loose bloody stools per day. The patient denied nausea, vomiting, fever, chills, chest pain, back pain, weight loss, or jaundice. She had no current respiratory or urinary symptoms. She denied any previous similar episodes of abdominal pain or bloody diarrhea.

On further questioning, the patient stated that she had completed a 1-week course of Septra DS and ciprofloxacin 6 days prior as therapy for a urinary tract infection. She also admitted to eating a rare steak for dinner the night before the onset of her discomfort. Her dinner companions had also eaten meat but were not symptomatic. She confirmed one primary residence and denied any recent travel or any prior history of inflammatory bowel disease, irritable bowel syndrome, or colonic disease.

The past medical history was significant for septic arthritis of the left hip approximately 10 years prior. The patient denied any surgical history. The patient stated she used oral contraceptives to regulate her menses; she denied allergies to any medications, use of tobacco, alcohol, or illicit drugs, or any family history of inflammatory bowel disease, autoimmune disease, or polypoid syndromes.

In the emergency room, the patient’s vital signs were temperature 98.3F, pulse 114, blood pressure 114/62, and respiratory rate 16. Physical examination revealed a well-developed, well-nourished woman in mild distress. Her skin had normal turgor, her oropharynx appeared normal, and her cardiopulmonary examination was remarkable only for sinus tachycardia. Auscultation of the abdomen revealed active bowel sounds, and palpation was significant for a soft, non- distended abdomen with mild tenderness of the right lower quadrant without guarding or rebound. Rectal examination was significant for grossly bloody stool, but no tenderness, masses, fissures, or fistulas. The sphincter tone was normal at rest and squeeze.

The patient’s laboratory results included white blood count (WBC) 8.8K without evidence of a left shift, hemoglobin (Hgb) 14K, platelets (Plt) 165K, chloride (Cl) 103, carbon dioxide (CO2) 26, blood urea nitrogen (BUN) 8, creatinine (Cr) 0.9. Liver function tests, amylase, lipase, and urinalysis were within normal limits. Abdominal films displayed a nonspecific bowel gas pattern. CT scan of the abdomen and pelvis were interpreted as marked circumferential thickening of the cecum and terminal ileum with stranding of the pericecal and ileal fat consistent with appendicitis, as well as a small amount of free fluid within the pelvis and several enlarged lymph nodes within the root of the mesentery. There was no evidence of abscess or free peritoneal air. Surgery consultation was requested to rule-out appendicitis.

As the patient’s symptomatology and presentation was more consistent with an infectious colitis or inflammatory colitis, the diagnosis was questioned. Further review of the CT scan showed inflammation involving the entire ascending colon, rather than simply the cecum and terminal ileum (Fig. 1). The patient was admitted to the hospital with a diagnosis of infectious colitis; initial treatment included bowel rest and resuscitation with intravenous fluids. Stool was sent for culture including Clostridium difficile, shigella, Salmonella, Escherichia coli O157:H7, ova, and parasites.

During the next 2 days, the patient experienced less abdominal pain and fewer episodes of bloody diarrhea; however, she was not completely resolved of her symptoms. The physical examination was significant for low-grade fever and right-sided abdominal tenderness (although improved). At this time, her laboratory results revealed leukocytosis (14.7K) with left-shifted differentiation (82% segmented), mild thrombocytopenia (120K), and large amounts of protein and ketones in her urine. Her stool cultures (repeated each day) remained negative for all bacterial, fungal, and parasitic pathogens. Intravenous metronidazole was initiated at this time for a presumed invasive infectious colitis.

FIG. 1. CT scan of abdomen and pelvis demonstrating marked circumferential thickening of the cecum and ascending colon with stranding of the pericolonic fat suggestive of inflammatory changes.

FIG. 2. Endoscopic appearance of E. coli O157:H7 colitis. The mucosa is friable and ulcerated with large areas of confluent subepithelial hemorrhage and necrosis.

Colonoscopy was performed to examine the colonic mucosa and obtain tissue samples for pathological review. There were ulcerations and areas of confluent mucosal necrosis with subepithelial hemorrhages in the cecum, ascending colon, and proximal transverse colon (Fig. 2). The remainder of the distal colon and rectum appeared normal. Additional stool cultures were sent from aspiration samples during the colonoscopy.

A biopsy of the ascending colon showed extensive mucosal ulceration with marked acute inflammation. Microthrombi were noted in vessels of the lamina propria associated with small regenerative glands (Fig. 3). There was goblet cell depletion in the glands with acute cryptitis and crypt abscess formation. A biopsy of the left colon showed normal mucosa.

With a working diagnosis of E. coli O157:H7 colitis, the patient was continued on intravenous fluid support and bowel rest. The intravenous metronidazole was discontinued. During the next 36 hours, the patient was without fever or abdominal complaints and was having normal bowel movements. She initiated oral intake and advanced to a regular diet without incident. Although her white blood count returned to normal (8.0K), her thrombocytopenia worsened (27K). Additionally, she developed signs of renal insufficiency including fluid sequestration, anasarca, oliguria, and elevation of BUN (25) and creatinine (1.6), despite large volumes of intravenous fluid support. Neurologic manifestations developed at this time, including hallucinations and generalized confusion. A single stool culture from the day of admission was now reported as positive for E. coli O157:H7. All other stool and blood cultures remained negative.

FIG. 3. Pathologic examination revealed mucosal ulceration with small regenerative glands and microthrombi in the capillaries.

The patient’s course suggested E. coli O157:H7 colitis- associated hemolytic-uremic syndrome (HUS). She was transferred to the intensive care unit for worsening renal insufficiency, pulmonary edema, severe thrombocytopenia, anemia, and the onset of seizures. At this time, laboratory data revealed Hgb 8.2, Pl 33, Cr 2.1, PT 15.4, D-dimer 9.9, and LDH 4120. Her urinalysis showed severe proteinuria and hematuria.

Plasmapheresis therapy was initiated. The patient underwent a total of 12 plasma exchanges, remained in the ICU for 6 days and in the hospital for a total of 17 days. At the time of discharge from the hospital, she had improved renal function, normalizing blood tests, and an unremarkable neurologic examination. At her 2-month follow-up visit, she had a normal physical examination, and normal blood tests, including Hgb 13, Plt 183, Cr 0.8, and LDH 100.

Discussion

Originally described in 1983,1 E. coli O157:H7 is now recognized as a common cause of bloody and nonbloody diarrhea and is responsible for most cases of hemolytic-uremic syndrome in children in North America. In the United States alone, E. coli O157:H7 is believed to cause more than 20,000 infections and approximately 250 deaths each year.2 Although individuals of all ages may be infected, the highest rates occur in children younger than 5 years of age.3 Outbreaks have been reported more frequently during the past decade, as awareness increases among medical and public health professionals. Sporadic cases and outbreaks are more frequent in the northern states and during the warmer months, but it is not well understood why these trends exist.

Ingestion of undercooked bovine meat such as hamburger patties has been responsible for many of the large outbreaks of E. coli O157:H7 colitis, but other modes of transmission have been reported as well. Infection from pork, chicken, steak, unpasteurized milk, yogurt, vegetables from manured gardens, apple cider, and municipal drinking water has occurred. Sporadic cases have also been attributed to swimming in contaminated lakes (fecal-oral route). Lastly, personto-person modes of transmission have also been documented in child-care centers, nursing h\omes, and between family members in the home.3-6 Typically, incubation period is 3 to 4 days but may be as short as 1 day or as long as 21 days.7

The mechanism by which E. coli O157:H7 causes gastrointestinal and systemic symptoms is not completely understood. Bacterial factors such as those required for adhesion to enterocyte apical membranes may be responsible for the diarrheal response. The bacterium adheres to the endothelial cells of the gut mucosa and produces verotoxin (shiga-like toxin) that probably acts locally and systemically. There is evidence that the verotoxin locates on the endothelium of the intestinal vasculature, which may help explain the breakdown of the blood tissue barrier.8 Loss of intestinal integrity allows exposure of systemic circulation to inflammatory agents such as bacterial lipopolysaccharide (LPS), verotoxin(s), and various cytokines. The multiorgan failure sometimes seen in patients with HUS may be secondary to the damaging effects on each organ’s vascular endothelium by these and other inflammatory mediators.3 Patients who develop bloody diarrhea and signs of invasive infection, rather than simply watery diarrhea, are more prone to hemolytic-uremic syndrome and other organ injury.9

The range of clinical presentation is broad, often making diagnosis difficult. Patients may be asymptomatic or present with nonbloody diarrhea, bloody diarrhea, the hemolytic-uremic syndrome, thrombocytopenia purpura, seizure, coma, or death.7 Typically, patients experience crampy abdominal pain and diarrhea, which becomes bloody after 48 hours, and some may have nausea, vomiting, and low-grade fever. The colitis will be characterized by diarrhea in 100 per cent, bloody stool in 90 to 95 per cent, abdominal pain in 91 to 95 per cent, nausea and/or vomiting in 40 to 54 per cent, and fever in 27 to 45 per cent.4, 10 As many as 8 per cent may present with rectal prolapse.7 Obtaining a thorough history in regard to recent eating habits and travel is extremely important in these patients. Differential diagnosis should include other infactious causes of diarrhea, inflammatory bowel disease, ischemic colitis, intussusception (in children), and causes of the acute abdomen.

Routine blood tests may reveal leukocytosis, bandemia, dehydration, or proteinuria. Abdominal radiographs can demonstrate ileus and in more severe cases thumbprinting patterns in the colon. Stool cultures for E. coli O157:H7 must be specifically requested, as MacConkey-sorbitol agar plates and agglutination with 0157 antiserum is required for routine diagnosis.6 A single stool culture when performed early in the disease can be expected to be approximately 43 to 72 per cent sensitive.6, 7 Several factors may limit detection of E. coli O157:H7 in stool culture including unsuspecting treating physicians, failure to request or properly process specific stool cultures, short detection periods of the organism in the stool, and frequent use of antibiotics before obtaining cultures. After HUS develops, it is difficult to detect the organism in stool samples.3

Further information may be gained from endoscopy, which often shows edematous, hyperemic mucosa and superficial ulcerations and provides opportunity for biopsy. Classically, the mucosal abnormalities progress in severity from rectum to cecum.3 Although often dramatic, as in this case report, the pathologic findings are nonspecific. Histological examination reveals infectious or ischemic patterns of colonic injury, usually in a patchy distribution and occasionally with fibrin microthrombi. The differential diagnosis in biopsies often includes pseudomembranous colitis, ischemia, and fulminant inflammatory bowel disease in addition to hemorrhagic colitis associated with E. coli O157:H7. However, pathology and culture reports do not return for days, often after the gastrointestinal manifestations have improved.

On average, the gastrointestinal prodrome lasts 1 week and resolves without permanent sequelae. Hemolytic-uremic syndrome can be expected to develop at this time in 7 to 25 per cent of patients4- 6 and is characterized by microangiopathic hemolytic anemia, thrombocytopenia, acute renal dysfunction, and central nervous system manifestations. HUS is a multi-system disease, and although the microangiopathy that characterizes the disease primarily affects the kidneys, any organ system may be involved.

Studies to elucidate risk factors for the development of HUS in patients infected with E. coli O157:H7 have been somewhat informative. Most authors agree that fever, leukocytosis, and use of antimotility agents all predict higher rates of subsequent HUS. Others have suggested elevated C-reactive protein (CRP), severity of colitis, use of antibiotic therapy, and age (infants and elderly) as additional predictors of HUS. Ikeda et al.9 proposed a “predictor index scoring system,” giving scores of 0 or 1 for different values of CRP, WBC, and temperature. Those with scores of 2 or higher were significantly more likely to develop HUS (32.6% vs 1.8%).

Those patients who develop HUS are at risk for both acute and long-term sequelae. Neurologic complications including seizure, coma, and hemiparesis may develop in 30 per cent of these patients.3 During their acute illness, 64 to 76 per cent of patients will require transfusion of packed red blood cells, and 10 to 53 per cent will require platelet transfusions.2, 7 Platelet transfusions should be avoided if possible because of the theoretical risk of augmenting the thrombotic process with fresh platelets. More than half will require either acute dialysis or plasmapheresis. Dialysis therapy or hemofiltration should be instituted early in oliguric patients with HUS as it has been shown to improve mortality.3

Mortality rates up to 5 per cent can be expected in patients who develop HUS and its associated morbidities. An additional 5 per cent may suffer chronic renal failure and/or permanent neurologic injury. Lopez et al.11 reported that 21 per cent of patients had persistent proteinuria at 1 year and 35 per cent had significantly decreased creatinine clearance at their last follow-up (up to 10 years). These authors also found that patients who originally presented with more severe colitis had higher incidences of extraintestinal morbidity and worse long-term outcomes. They concluded that the spectrum of gastrointestinal manifestations relates to the subsequent microvascular process and its consequences.

During the first week of the illness (gastrointestinal prodrome), management entails fluid resuscitation, bowel rest, and early culturing of stool. It is important to monitor patients for signs of noncolonic organ dysfunction. Hypertension, edema, or oliguria may alert the physician to impending renal insufficiency, and pallor, malaise, or tachycardia might suggest anemia. Tests such as peripheral-blood smears, blood counts, electrolyte profiles, and urinalysis should be ordered. Specifically, evidence of leukocytosis, anemia, thrombocytopenia, and azotemia are worrisome. Fragmented erythrocytes, schistocytes, and burr cells seen on blood smear help establish the diagnosis of HUS.3, 12

No specific therapy has been proved effective in the treatment of E. coli O157:H7 colitis. The question of antibiotic use in this disease has generated much controversy and research effort. Retrospective evidence suggests the use of antibiotics (trimethoprimsulfamethoxazole) may increase the risk of developing HUS.13 However, bias is inherent in such retrospective data as the more ill patients were probably treated with antibiotics more frequently. Proulx et al.10 conducted a randomized, controlled trial of antibiotic therapy for E. coli O157:H7 enteritis and demonstrated no improvement in the clinical course; did not convert patients to negative cultures sooner; and did not statistically change the incidence of HUS. Most recently, Wong et al.14 conducted a prospective cohort study of 71 children with E. coli O157:H7 infections. Upon multivariate analysis, antibiotic treatment was found to increase the risk of HUS. Antimotility agents are contraindicated in patients with bloody diarrhea and have been shown to increase the incidence of HUS and neurologic sequelae in these patients.2, 15

Management of HUS includes meticulous attention to fluid balance and electrolyte replacement. Overhydration must be avoided in the face of oliguria. Hyponatremia, hyperkalemia, hyperphosphatemia, and metabolic acidosis should be managed medically; however, should medical treatment fail, dialysis or hemofiltration is indicated.16 Quite often, transfusion of blood products and plasmapheresis is required. Convulsions are treated with intravenous administration of diazepam or phenytoin. Less standardized therapies include intravenous immunoglobulin, verotoxin inhibitors, and thrombolytics.

The highest success in managing E. coli O157:H7 infection can be achieved through public health initiatives. Education regarding proper preparation and cooking of meats, health policies regarding food processing and handling, and rapid detection and containment of outbreaks can prevent and control future infection. When seeing the patient in consultation, as always, obtaining a thorough history and physical at the time of presentation is of paramount importance. Early suspicion of E. coli O157:H7 infection should lead to more rapid diagnosis, improved hospital courses, and decreased long-term morbidity and mortality.

REFERENCES

1. Riley LW, Remis RS, Helgerson SD, et al. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 1983;308:681-5.

2. Boyce TG, Swerdlow DL, Griffin PM. Escherichia coli 0157:H7 and the hemolytic-uremic syndrome. N Engl J Med 1995; 333:364-8.

3. Pickering LK, Obrig TG, Stapleton FB. Hemolytic-uremic syndrome and enterohemorrhagic Escherichia coli. Pediatr Infect Dis J 1994;13:459-76.

4. Slutsker L, Ries AA, Maloney K, et al\. Nationwide case control study of Escherichia coli O157:H7 infection in the United States. J Infect Dis 1998;177:962-6.

5. Bell BP, Goldoft M, Griffin PM, et al. A multistate outbreak of Escherichia coli O157:H7 associated bloody diarrhea and hemolytic uremic syndrome from hamburgers: the Washington experience. JAMA 1994;272:1349-53.

6. Belongia EA, Osterholm MT, Soler JT, et al. Transmission of Escherichia coli O0157:H7 infection in Minnesota child day care facilities. JAMA 1993;269:883-8.

7. Brandt JR, Fouser LS, Watkins SL, et al. Esherichia coli O57:H7-associated hemolytic-uremic syndrome after ingestion of contaminated hamburgers. J Pediatr 1994;125:519-26.

8. Richardson SE, Karmali MA, Becker LE, Smith CR. The histopathology of the hemolytic uremic syndrome associated with verocytotoxin-producing E. coli infections. Hum Pathol 1988;19: 1102- 8.

9. Ikeda K, Ida O, Kimoto K, et al. Predictors for the development of haemolytic uraemic syndrome with Escherichia coli O157:H7 infections with focus on the day of illness. Epidemiol Infect 2000;124:343-9.

10. Proulx F, Turgeon JP, Delage G, et al. Randomized, controlled trial of antibiotic therapy for Escherichia coli O157:H7 enteritis. J Pediatr 1992;121:299-303.

11. Lopez EL, Devoto S, Fayad A, et al. Association between severity of gastrointestinal prodrome and long-term prognosis in classic hemolytic-uremic syndrome. J Pediatr 1992;120:210-5.

12. Igarashi T, Inatomi J, Wake A, et al. Failure of pre- diarrheal antibiotics to prevent hemolytic uremic syndrome in serologically proven Escherichia coli O057:H7 gastrointestinal infection. J Pediatr 1999;135:768-9.

13. Tarr PI, Neil MA, Christie DL, Anderson DE. Escherichia coli O157:H7 hemorrhagic colitis (letter). N Engl J Med 1988; 318:1697.

14. Wong CS, Jelacic S, Habeeb RL, et al. The risk of hemolytic- uremic syndrome after antibiotic treatment of Escherichia coli O157:H7 infections. N Engl J Med 2000;342:1930-5.

15. Cimolai N, Morrison BJ, Carter JE. Risk factors for the central nervous system manifestations of gastroenteritis-associated hemolytic-uremic syndrome. Pediatr 1992;90:616-21.

16. Kaplan BS, Meyers KE, Schulman SL. The pathogenesis and treatment of hemolytic uremic syndrome. J Am Soc Nephrol 1998;9:1126- 33.

SETH A. ROSEN, M.D.,* STEVEN D. WEXNER, M.D.,* SHERRY WOODHOUSE, M.D.,[dagger] PATRICK COLQUHOUN, M.D.,* ERIC G. WEISS, M.D.,* JUAN J. NOGUERAS, M.D.,* JONATHAN EFRON, M.D.,* ANTHONY VERNAVA, III, M.D.*

From the Departments of * Colorectal Surgery and [dagger] Pathology, Cleveland Clinic Florida, Weston and Naples, Florida

Address correspondence and reprint requests to Dr. A. Vernava, Cleveland Clinic Florida, 2950 Cleveland Clinic Blvd., Weston, FL 33331.

Copyright The Southeastern Surgical Congress Jun 2005