Varied clinical presentations of Vibrio vulnificus infections: a report of four unusual cases and review of the literature.

Abstract: Vibrio vulnificus is a Gram-negative, motile, curved bacillus of the family Vibrionaceae that is a rare cause of gastroenteritis, septicemia, and wound infections in humans. V. vulnificus is halophilic, flourishes in warm temperatures, and is part of the bacterial flora of the marine environment. The location of our health care setting, on the Gulf of Mexico, has given us the opportunity to observe a wide variety of clinical presentations of infections caused by this organism. In the first case, a 27-year-old man struck by lightning while windsurfing was found pulseless in the water and was resuscitated. The patient subsequently developed cardiac arrhythmias, respiratory failure, and necrotizing fasciitis; blood cultures yielded V. vulnificus. After antibiotic therapy and several fasciotomies, the patient recovered. The second case was that of a 43-year-old Asian man employed as an oyster shucker who presented with complaints of redness, tearing, and photophobia of the right eye. The diagnosis of corneal ulcer secondary to V. vulnificus was made after culture of the right eye revealed the organism. The third case involved a 46-year-old man who presented with complaints of abdominal pain, nausea, chills, and bullous lesions on the lower extremities. He developed disseminated intravascular coagulation, and cultures of the lesions on his lower extremities showed V. vulnificus. Initially, the patient denied any exposure to raw seafood or seawater, but he eventually remembered eating raw oysters 3 days before his illness. The fourth case is that of a 32-year-old, human immunodeficiency virus-positive, hepatitis C-positive woman with cirrhosis who presented with productive cough, chills, fever, and red spots on her extremities and buttocks. Blood cultures revealed V. vulnificus and the patient was treated with antibiotics and improved clinically. These four cases illustrate the wide range of clinical presentations associated with this organism.

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Vibrio vulnificus, previously described as lactose-positive Vibrio, (1) and Centers for Disease Control and Prevention (CDC) Group EF-3, (2) is a Gram-negative, motile, straight or curved bacillus associated with gastroenteritis, septicemia, and wound infections in humans. (3) A halophilic organism, V. vulnificus is found commonly in coastal waters and estuaries in tropical to subtropical climates where water temperatures range from 9[degrees] to 31[degrees]C. Isolation of V. vulnificus has been reported from marine environments in northern Europe, the United States, and Australia. (4) Biochemically, the organism is oxidase-positive, lactose-positive, lysine-positive, arginine-negative, and salicin-positive. (5) Recoverable from blood, body fluids, and tissue cultures, V. vulnificus grows well on most general isolation media, particularly when 1% NaCl is added; smooth gray colonies are the characteristic colony morphology. Growth on thiosulfate citrate bile sucrose agar produces medium-sized, opaque, yellow-green colonies. (6)

V. vulnificus may be found in high concentrations in certain aquatic animals, particularly in filter-feeding organisms such as oysters, crabs, mussels, clams, and scallops, and also in fish that inhabit coastal oyster reefs. (4) In some epidemiologic reports, V. vulnificus was recovered from up to 50% of oysters and 11% of crabs cultured during the warm summer months. Ingestion of uncooked seafood, particularly raw oysters, (7) and exposure of wounds to saltwater or marine animals are common modes of human infection. Of 422 V. vulnificus infections reported to the CDC between 1988 and 1996, 45% (n = 189) were wound infections, 43% (n = 181) were primary septicemias, 5% (n = 23) were cases of gastroenteritis, and 7% (n = 29) were from undetermined exposure. (8) Gastroenteritis associated with V. vulnificus has been defined as a diarrheal illness with vomiting and abdominal cramps in patients with no evidence of a wound infection but with V. vulnificus isolated from stool culture. In immunocompetent individuals, V. vulnificus gastroenteritis usually follows ingestion of contaminated seafood or water and is self-limited in most cases; its symptoms are rarely severe enough to require hospitalization. (4) However, V. vulnificus can readily cross the gastrointestinal mucosa and enter the bloodstream. The diagnosis of primary septicemia related to V. vulnificus requires the isolation of V. vulnificus from blood or another normally sterile site in the absence of a demonstrable wound infection. V. vulnificus septicemia usually produces fever, chills, abdominal pain, nausea, vomiting, and hypotension. Cutaneous lesions including cellulitis, ecchymoses, and bullae frequently occur on the extremities. Soft tissue wound infections associated with V. vulnificus may produce similar cutaneous lesions when acute or preexisting breaks in the skin allow entry of the organism. The associated cellulitis can progress rapidly to necrotizing fasciitis, and fasciotomies and debridements may be required for control of the infection. Wound infections may lead to secondary septicemia, with symptoms identical to primary V. vulnificus septicemia. Other rare forms of infection associated with this organism include corneal ulcers, (9) spontaneous bacterial peritonitis, (10) meningitis, (11) myositis, (12) pneumonia, (13) endometritis, (14) and osteomyelitis. (15) No evidence of person-to-person transmission of V. vulnificus has been reported.

Discussion

These four cases represent the broad spectrum of clinical presentations associated with V. vulnificus. The patient in the first case suffered extensive electrical injury after a lightning strike, but no definite "blowout" entrance or exit wounds were identified. The site of entry for the V. vulnificus organism was never determined with certainty, but entry through small incidental cutaneous injuries or ingestion of seawater are the likely possibilities. Passage of V. vulnificus infection across the gastrointestinal mucosa could have produced primary septicemia complicated by secondary cellulitis progressing to necrotizing fasciitis. Alternatively, skin injuries could have allowed entry of the organism into soft tissue, causing primary cellulitis with secondary septicemia. As in many cases of soft tissue infections with V. vulnificus, fasciotomies were required for control of the infection. Although medically necessary, these procedures are often disfiguring. This patient required extensive physical therapy to regain full mobility.

The second case represents ocular V. vulnificus infection acquired from contact with a marine animal. Although the majority of V. vulnificus infections associated with marine animals are gastroenteritises secondary to consumption of raw oysters and wound infections acquired while handling seafood, ocular contamination with the organism can produce corneal ulcers. The patient in this case acquired the organism through occupational exposure, illustrating the need for appropriate gloving and eye protection among individuals at occupational risk for acquiring V. vulnificus infections.

With a history of raw oyster consumption 3 days before clinical presentation of illness, the third case represents primary V. vulnificus septicemia related to passage of the organism across the gastrointestinal mucosa. The patient's initial symptoms of abdominal pain, nausea, and chills fit the classic pattern of septicemia, and the temporally related bullous cutaneous lesions on the lower extremities illustrate rapid progression to the cellulitis often seen with V. vulnificus septicemia. The patient's overwhelming sepsis triggered disseminated intravascular coagulation, requiring immediate aggressive transfusion medicine therapy. Mortality rates for V. vulnificus septicemia have exceeded 50% in some studies. (16)

[FIGURE 1 OMITTED]

The fourth case is an example of V. vulnificus infection in an immunocompromised patient. Although no specific source of infection could be identified, the patient's clinical presentation and symptoms indicate primary V. vulnificus septicemia. The patient gave a remote history of raw oyster consumption, but no evidence of exposure temporally related to her presentation was present. Although the patient was felt clinically to have bacterial pneumonia and her respiratory status improved while on antibiotic therapy, no infectious organisms were recovered from any of her respiratory cultures. Although a definitive cause of her pneumonia was never identified, at least one case of pneumonia related to V. vulnificus has been reported in the medical literature.

[FIGURE 2 OMITTED]

The third and fourth cases illustrate the occurrence of V. vulnificus infections in patients with chronic underlying illnesses. Individuals with immunodeficiencies, liver disease, and hematologic disorders with elevated iron levels are at increased risk for infections with V. vulnificus. (17) (18) Increased rates of infection have also been noted in individuals with chronic renal insufficiency, diabetes mellitus, and chronic gastrointestinal disease and in patients on long-term steroid therapy. (18) (19) The patient in the third case had alcohol-related liver disease, and the patient in the fourth case was HIV-positive and had hepatitis C and cirrhosis. V. vulnificus infections in immunocompromised patients are extremely difficult to treat and, in those patients who survive, tend to become chronic infections.

[FIGURE 3 OMITTED]

Because of its propensity for optimal growth at temperatures greater than 18[degrees]C, V. vulnificus reaches peak concentrations in marine waters during the summer months. (20) The incidence of infection is particularly high in the areas bordering the Gulf of Mexico. In surveillance performed in 1999 by the CDC to track noncholera Vibrio infections, V. vulnificus infections during that year were nearly twice as frequent (n = 55) in the states bordering the Gulf of Mexico (Texas, Louisiana, Mississippi, Alabama, and Florida) as in all other surveyed states combined (n = 28) including California, Connecticut, Georgia, Hawaii, Illinois, Kentucky, Massachusetts, Michigan, Minnesota, Nevada, North Carolina, Pennsylvania, Oregon, South Carolina, Virginia, Washington, and Wisconsin. Of the 55 V. vulnificus infections seen in the states bordering the Gulf of Mexico, 23 (42%) were septicemias, 21 (38%) were wound infections, 4 (7%) were gastroenteritides, and 7 were listed as others/unknowns. Eighty-nine percent of the cases were serious enough to require hospitalization, and the overall mortality rate was 40%. Although V. parahaemolyticus, a less virulent Vibrio strain that causes gastroenteritis and wound infection, was the second most common noncholera Vibrio species causing infection in the coastal states of the Gulf of Mexico, V. parahaemolyticus was the most common (n = 87) noncholera Vibrio species reported in the other surveyed states. (21)

Treatment of V. vulnificus infections depends primarily on the type of infection, but antibiotic therapy is the mainstay of treatment. V. vulnificus shows sensitivity to antibiotic therapy with tetracyclines, aminoglycosides, trimethoprim-sulfamethoxazole, third-generation cephalosporins, and chloramphenicol. (13) (22) V. vulnificus gastroenteritis may be self-limited, with relatively mild constitutional symptoms, but severe cases require hospitalization with supportive care and antibiotic therapy. Antibiotic therapy is also used in the treatment of wounds infected with V. vulnificus, but surgical procedures such as debridements and fasciotomies are often necessary to control infection. V. vulnificus septicemia, whether primary or secondary, is often difficult to treat because of related clinical sequelae such as the development of coagulopathies and necrotizing fasciitis; treatments directed to each particular clinical scenario are necessary, as are standard antibiotic therapy and general supportive care. Prompt initiation of antibiotic therapy has been shown to decrease mortality in cases of septicemia, particularly if therapy is initiated before the onset of hypotension. Unfortunately, even with current treatment methods, the mortality rate for primary V. vulnificus septicemia ranges from 60 to 75% and that for V. vulnificus would infections ranges from 20 to 30% in some studies. (23)

Preventative measures to control V. vulnificus infections are difficult to implement because of its ubiquitousness in warm coastal waters where people enjoy water-related recreational activities. Particularly troublesome is the fact that V. vulnificus concentrations peak during the warmest months of the year, when many people plan seaside vacations. Exposure to raw seafood is the most readily preventable source of infection, but in many coastal areas, raw oysters are still considered a delicacy, and changing this cultural perception is problematic from an infection-control standpoint. Currently, cooking shellfish is the only reliable method for destroying the bacterium. (4) Appropriate protective eyeware and gloves should be used when handling raw shellfish. (24)

Although general information has been compiled on the incidence of Vibrio vulnificus infections from states participating in voluntary surveillance studies, the true incidence of V. vulnificus infection in the United States is unknown. Self-limited cases of V. vulnificus gastroenteritis may never present to medical attention, and even in the cases that do present to medical attention, cultures to prove suspected infections are not always performed. Although the number of reported cases of V. vulnificus is low, with an incidence of 0.4 to 1.9 reported cases per 1 million people, (25) an average of only 40 culture-confirmed cases each year in the states bordering the Gulf of Mexico, (26) the significant mortality rate associated with these infections makes this an important public health issue; V. vulnificus is now the leading cause of food-borne mortality in Florida. (16) Currently, only five states (Alabama, California, Florida, Louisiana, and Mississippi) require that warning signs concerning infectious agents be posted where raw oysters are sold. (27) Improved legislation regarding warning signs and improved public education regarding the consumption and handling of raw shellfish appear to be the most useful measures for preventing infection. (28) Continued surveillance of V. vulnificus infections in the coastal regions will no doubt improve our understanding of the epidemiology of this relatively rare but often fatal organism.

The secret of genius is to carry the spirit of the child into old age, which means never losing your enthusiasm.

--Aldous Huxley

KEY POINTS

* The wide range of clinical presentations of Vibrio vulnificus infections is presented.

* The high mortality and morbidity rates resulting from infections associated with V.vulnificus are reviewed.

* The importance of prevention of V.vulnificus infections, particularly in susceptible individuals, is discussed.

Accepted May 15, 2003.

Copyright [c] 2004 by The Southern Medical Association 0038-4348/04/9702-0163

References

(1.) Hollis DG, Weaver RE, Baker CN, et al. Halophilic Vibrio species isolated from blood cultures. J Clin Microbiol 1976;3:425-431.

(2.) Farmer JJ III. Vibrio ("Beneckea") vulnificus, the bacterium associated with sepsis, septicaemia, and the sea. Lancet 1979;2:903 (letter).

(3.) Morris JG Jr, Black RE. Cholera and other vibrioses in the United States. N Engl J Med 1985;312:343-350.

(4.) Strom MS, Paranjpye RN. Epidemiology and pathogenesis of Vibrio vulnificus. Microbes Infect 2000;2:177-188.

(5.) Koneman EW, Allen SD, Janda WM, et al. Curved Gram-Negative Bacilli and Oxidase-Positive Fermenters: Campylobacteraceae and Vibrionaceae, in Color Atlas and Textbook of Diagnostic Microbiology, Philadelphia, Lippincott Williams & Wilkins, 1997, ed 5, pp 339-347.

(6.) Baron EJ, Finegold SM. Vibrio and Related Species, Aeromonas, Plesiomonas, Campylobacter, and Others, in Bailey and Scott's Diagnostic Microbiology. St. Louis, MO, C.V. Mosby, 1990, ed 8, pp 432-434.

(7.) Centers for Disease Control and Prevention. Vibrio vulnificus infections associated with eating raw oysters: Los Angeles, 1996. MMWR Morb Mortal Wkly Rep 1996;45(29):621-624.

(8.) Shapiro RL, Altekruse S, Hutwagner L, et al; Vibrio Working Group. The role of Gulf Coast oysters harvested in warmer months in Vibrio vulnificus infections in the United States, 1988-1996. J Infect Dis 1998;178:752-759.

(9.) DiGaetano M, Ball SF, Straus JG. Vibrio vulnificus corneal ulcer: Case reports. Arch Ophthalmol 1989;107:323-324.

(10.) Wongpaitoon V, Sathapatayavongs B, Prachaktam R, et al. Spontaneous Vibrio vulnificus peritonitis and primary sepsis in two patients with alcoholic cirrhosis. Am J Gastroenterol 1985;80:706-708.

(11.) Katz BZ. Vibrio vulnificus meningitis in a boy with thalassemia after eating raw oysters. Pediatrics 1988;82:784-786.

(12.) Kelly MT, McCormick WF. Acute bacterial myositis caused by Vibrio vulnificus. JAMA 1981;246:72-73.

(13.) Kelly MT, Avery DM. Lactose-positive Vibrio in seawater: A cause of pneumonia and septicemia in a drowning victim. J Clin Microbiol 1980; 11:278-280.

(14.) Tison DL, Kelly MT. Vibrio vulnificus endometritis. J Clin Microbiol 1984;20:185-186.

(15.) Vartian CV, Septimus EJ. Osteomyelitis caused by Vibrio vulnificus. J Infect Dis 1990;161:363 (letter).

(16.) Hlady WG, Klontz KC. The epidemiology of Vibrio infections in Florida, 1981-1993. J Infect Dis 1996;173:1176-1183.

(17.) Janda JM, Powers C, Bryant RG, et al. Current perspectives on the epidemiology and pathogenesis of clinically significant Vibrio spp. Clin Microbiol Rev 1988;1:245-267.

(18.) Blake PA, Merson MH, Weaver RE, et al. Disease caused by a marine Vibrio: Clinical characteristics and epidemiology. N Engl J Med 1979; 300:1-5.

(19.) Johnston JM, Becker SF, McFarland LM. Vibrio vulnificus: Man and the sea. JAMA 1985;253:2850-2853.

(20.) Kelly MT. Effect of temperature and salinity on Vibrio (Beneckea) vulnificus occurrence in a Gulf Coast environment, Appl Environ Microbiol 1982;44:820-824.

(21.) Centers for Disease Control and Prevention. Summary of infections reported to Vibrio Surveillance System, 1999. Available at: http://www.cdc.gov/ncidod/dbmd/diseaseinfo/files/VibCSTE99web.pdf. Accessed September 25, 2003.

(22.) Tacket CO, Brenner F, Blake PA. Clinical features and an epidemiological study of Vibrio vulnificus infections. J Infect Dis 1984;149:558-561.

(23.) Klontz KC, Lieb S, Schreiber M, et al. Syndromes of Vibrio vulnificus infections: Clinical and epidemiologic features in Florida cases, 1981-1987. Ann Intern Med 1988;109:318-323.

(24.) Whitman CM, Griffin PM. Preventing Vibrio vulnificus infection in the high-risk patient. Infect Dis Clin Pract 1993;2:275-276.

(25.) Vollberg CM, Herrera JL. Vibrio vulnificus infection: An important cause of septicemia in patients with cirrhosis. South Med J 1997;90:1040-1042.

(26.) Centers for Disease Control and Prevention. Vibrio vulnificus: Technical information. Atlanta, Centers for Disease Control and Prevention, December 2002. Available at: http://www.cdc.gov/ncidod/dbmd/diseaseinfo/vibriovulnificus_t.htm. Accessed September 25, 2003.

(27.) Martin G, Wright AM, Banakarim K. A case of fatal food-borne septicemia: Can family physicians provide prevention? J Am Board Fam Pract 2000;13:197-200.

(28.) Mouzin E, Mascola L, Tormey MP, et al. Prevention of Vibrio vulnificus infections: Assessment of regulatory educational strategies. JAMA 1997;278:576-578.

RELATED ARTICLE: Case Reports

Patient 1

A 27-year-old white male was struck by lightning while windsurfing in the waters off of Pensacola, Fla. He was found pulseless in the water and was resuscitated and intubated by emergency medical personnel and transported to a nearby hospital in Pensacola. The patient developed ventricular tachycardia, for which he was given lidocaine. Shortly after admission, swelling and redness were noted in the right upper extremity; no pulse was palpable in the right forearm. The diagnosis of compartment syndrome was made, and the patient underwent a right forearm fasciotomy. The patient was airlifted the same day to our institution in Mobile, Ala. At arrival, he was afebrile (96.9[degrees]F), his blood pressure was 123/95 mm Hg, and his Glasgow Coma Scale assessment was 3. Physical examination revealed sinus tachycardia but no demonstrable pulses in any extremity. Emergent left upper extremity and bilateral lower extremity fasciotomies were performed to relieve his compartment syndromes. The patient remained in stable condition for 2 days but then developed hypoxemia and bradycardia. Advanced cardiac life support was initiated, bilateral chest tubes were placed, and 500 ml of pleural fluid was evacuated from the left chest tube. The patient developed a high fever, and a blood culture drawn at that time revealed V. vulnificus and Enterobacter aerogenes. Antibiotic therapy consisting of cefepime, levofloxacin, and doxycycline was initiated to treat the sepsis, but the patient developed acute respiratory failure secondary to rhabdomyolysis and remained in critical condition. After 9 days of antibiotic therapy and supportive care, the patient's condition improved and he was extubated. All cultures including blood, urine, and sputum remained negative after antibiotic therapy was initiated. Subsequently, repeat bilateral upper and lower extremity fasciotomies with split-thickness skin grafts were performed, and the patient was eventually discharged in stable condition.

Patient 2

A 43-year-old Asian male who was employed as an oyster shucker at a seafood processing factory in Bayou Le Batre, Ala, presented to our institution complaining of redness, tearing, photophobia, and blurring of vision in his right eye. Approximately 1 week before his presentation, he stated that several oyster shell fragments had lodged in his eyes. He reported that this was usual for his job, and that normally he could wash the shell fragments out of his eyes at the end of each day using over-the-counter eye drops. However, irrigation of his eyes for a week had provided no relief of his presenting symptoms. On physical examination at the time of his presentation, the patient's visual acuity without correction was 20/400 in the right eye and 20/20 -2 in the left eye. Slit-lamp examination revealed a 1.5 X 1.5-mm corneal ulcer with some Descemet's membrane folds noted. The patient was admitted to the hospital and began sulfate-bacitracin zinc-neomycin sulfate drops, vancomycin drops, and ciprofloxacin drops to the right eye every hour. Also, atropine sulfate monohydrate drops were administered to the right eye three times per day, and oral acyclovir and indomethacin therapy was initiated. Tetanus toxoid was administered, and cultures of the corneal ulcer area were obtained. On the second day of hospitalization, a Gram stain from the corneal ulcer revealed Gram-negative rods, and culture results showed V. vulnificus that was sensitive to chloramphenicol, gentamicin, ampicillin, cephazolin, cefotaxime, and ofloxacin. The patient was examined each day by slit-lamp examination, and by the third hospital day postadmission, his visual acuity had improved to 20/200 in the right eye and 20/20 - 1 in the left eye. The patient remained afebrile throughout his hospital course and denied having had any globe pain. His visual acuity eventually improved to 20/70 in the right eye and 20/20 in the left eye, with decreased photophobia, tearing, and foreign body sensation. The area of corneal ulceration decreased in size, and the patient was discharged with a stable intraocular pressure of 14 OU. The patient was scheduled for follow-up in the outpatient clinic.

Patient 3

A 46-year-old white male with a history of alcoholinduced liver disease presented to our institution with complaints of abdominal pain, nausea, chills, and skin lesions on his extremities. The patient had recently moved to Mobile, Ala, from New Orleans, La. He reported a history of drinking two cases of beer per week. His symptoms had started suddenly within 24 hours of his presentation, and he reported that his skin lesions had been initially erythematous but had rapidly evolved into ecchymoses and hemorrhagic bullae. The patient was hypotensive and unable to ambulate. Physical examination on presentation revealed a protuberant abdomen with a fluid shift consistent with ascites and numerous bullous lesions on the bilateral lower extremities (Fig. 1). The bullae ranged in size from 1 to 15 cm in diameter and contained serosanguinous fluid. Initial laboratory studies revealed an elevated prothrombin time (21.5 seconds), an elevated partial thromboplastin time (40 seconds), an elevated fibrinogen level (466 mg/dL), a D-dimer level of 4.5, thrombocytopenia (85,000/m[m.sup.3]), and elevated liver-associated enzymes (aspartate aminotransferase, 135 U/L; alanine aminotransferase, 101 U/L). Disseminated intravascular coagulation secondary to sepsis was suspected, and immediate transfusion therapy with fresh frozen plasma and cryoprecipitate was initiated. Biopsies of the bullae on the lower extremities were performed, and a portion of the tissue was submitted for culture. Histologically, the biopsy specimens showed dermatitis with focal dermal necrosis, hemorrhage, and Gram-negative bacteria in the dermis (Figs. 2 and 3). Both blood cultures and the cultures of the bullous lesions on the lower extremities showed V. vulnificus. The patient was placed on a 14-day course of doxycycline and ceftazidime and underwent daily debridement of his leg lesions with dressing changes. Initially, the patient denied any recent exposure to raw seafood or seawater but eventually recalled eating raw oysters 3 days before the onset of his illness. After completing antibiotic therapy, the patient was discharged in stable condition.

Patient 4

A 32-year-old white female with a history of asthma and alcohol abuse who was human immunodeficiency virus (HIV)-positive (CD4 count, 241) and hepatitis C-positive presented to our institution with productive cough, fever, chills, nausea, vomiting, throbbing pain in the feet, and red spots on the extremities and buttocks. The patient was immediately admitted with a diagnosis of pneumonia. Admission laboratory studies revealed elevated levels of liver-associated enzymes and bilirubin. The patient was originally placed in the medical intensive care unit for observation, and over the first 24 hours of her hospitalization, her skin lesions, which were originally erythematous, evolved to bullous lesions. Blood cultures drawn at the time of admission were positive for V. vulnificus. The patient was placed on intravenous doxycycline for treatment of her pneumonia and intravenous ceftazidine for treatment of her V. vulnificus infection. The patient improved clinically and was moved from the intensive care unit to a hospital room. She continued to have mild respiratory difficulty and was placed on nebulized albuterol treatments and ipratropium bromide metered-dose inhalers. The bullous lesions on her extremities healed well, and on Day 10 of hospitalization, the patient was discharged with instructions to take a 5-day course of oral doxycycline to complete her 14-day course of antibiotic therapy for V. vulnificus septicemia. She was scheduled for follow-up at the HIV clinic at the Alabama State Board of Health.

Ozlem Ulusarac, MD, and Elliot Carter, MD

From the Department of Pathology, University of south Alabama, Mobile, AL.

Reprint requests to Elliot Carter, MD, Department of Pathology, USA Medical Center, 2451 Fillingim Street, Mobile, AL 36617. Email: [e-mail]