• 1

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    • Search Google Scholar
    • Export Citation
  • 2

    Anaya DA, Dellinger EP, 2007. Necrotizing soft-tissue infection: diagnosis and management. Clin Infect Dis 44 :705–710.

  • 3

    DiNubile MJ, Lipsky BA, 2004. Complicated infections of skin and skin structures: when the infection is more than skin deep. J Antimicrob Chemother 53 (Suppl 2):ii37–ii50.

    • Search Google Scholar
    • Export Citation
  • 4

    Chen JL, Fullerton KE, Flynn NM, 2001. Necrotizing fasciitis associated with injection drug use. Clin Infect Dis 33 :6–15.

  • 5

    Miller LG, Perdreau-Remington F, Rieg G, Mehdi S, Perlroth J, Bayer AS, Tang AW, Phung TO, Spellberg B, 2005. Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N Engl J Med 352 :1445–1453.

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    • Export Citation
  • 6

    Howard RJ, Pessa ME, Brennaman BH, Ramphal R, 1985. Necrotizing soft tissue infections caused by marine vibrios. Surgery 98 :126–130.

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    Majeski J, Majeski E, 1997. Necrotizing fasciitis: improved survival with early recognition by tissue biopsy and aggressive surgical treatment. South Med J 90 :1065–1068.

    • Search Google Scholar
    • Export Citation
  • 8

    Wong CH, Chang HC, Pasupathy S, Khin LW, Tan JL, Low CO, 2003. Necrotizing fasciitis: clinical presentation, microbiology, and determinants of mortality. J Bone Joint Surg Am 85 :1454–1460.

    • Search Google Scholar
    • Export Citation
  • 9

    Elliott D, Kufera JA, Myers RA, 2000. The microbiology of necrotizing soft tissue infections. Am J Surg 179 :361–366.

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    Lille ST, Sato TT, Engrav LH, Foy H, Jurkovich GJ, 1996. Necrotizing soft tissue infections: obstacles in diagnosis. J Am Coll Surg 182 :7–11.

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    • Export Citation
  • 11

    Childers BJ, Potyondy LD, Nachreiner R, Rogers FR, Childers ER, Oberg KC, Hendricks DL, Hardesty RA, 2002. Necrotizing fasciitis: a fourteen-year retrospective study of 163 consecutive patients. Am Surg 68 :109–116.

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    • Export Citation
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    Hasham S, Matteucci P, Stanley PR, Hart NB, 2005. Necrotising fasciitis. BMJ 330 :830–833.

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    Eke N, 2000. Fournier’s gangrene: a review of 1726 cases. Br J Surg 87 :718–728.

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    • Search Google Scholar
    • Export Citation
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    Kim JH, Park JH, Lee TS, Lee HJ, Kim SJ, 2001. Distribution of pathogenic Vibrios and environmental factors affecting their occurrence in the seawater of live fish tank. J Fd Hyg Safety 16 :241–246.

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    Patz JA, 2002. A human disease indicator for the effects of recent global climate change. Proc Natl Acad Sci USA 99 :12506–12508.

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    Hiransuthikul N, Tantisiriwat W, Lertutsahakul K, Vibhagool A, Boonma P, 2005. Skin and soft-tissue infections among tsunami survivors in southern Thailand. Clin Infect Dis 41 :e93–e96.

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    Kuo YL, Shieh SJ, Chiu HY, Lee JW, 2007. Necrotizing fasciitis caused by Vibrio vulnificus: epidemiology, clinical findings, treatment and prevention. Eur J Clin Microbiol Infect Dis 26 :785–792.

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    Tsai YH, Hsu RW, Huang TJ, Hsu WH, Huang KC, Li YY, Peng KT, 2007. Necrotizing soft-tissue infections and sepsis caused by Vibrio vulnificus compared with those caused by Aeromonas species. J Bone Joint Surg Am 89 :631–636.

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    Tsai YH, Hsu RW, Huang KC, Chen CH, Cheng CC, Peng KT, Huang TJ, 2004. Systemic Vibrio Infection presenting as necrotizing fasciitis and sepsis. A series of thirteen cases. J Bone Joint Surg Am 86 :2497–2502.

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    Anaya DA, McMahon K, Nathens AB, Sullivan SR, Foy H, Bulger E, 2005. Predictors of mortality and limb loss in necrotizing soft tissue infections. Arch Surg 140 :151–157.

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Marine Bacteria as a Leading Cause of Necrotizing Fasciitis in Coastal Areas of South Korea

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  • 1 Department of Internal Medicine, Department of Laboratory Medicine, and Department of Plastic and Reconstructive Surgery, Chonnam National University Medical School, Gwangju, South Korea

Necrotizing fasciitis is a life-threatening soft-tissue infection. It is useful to know the etiology of this disease in each community and region because this information can facilitate early diagnosis and treatment. We reviewed medical records of 217 consecutive patients with necrotizing fasciitis in South Korea. Etiologic organisms were documented in 171 (78.8%) patients. Gram-negative marine bacteria were the most common organisms (68.4%). Seasonal variation in incidence occurred during warmer periods. Liver cirrhosis and alcoholism were common underlying illnesses. Gastrointestinal symptoms were more common in persons infected with gram-negative marine bacteria (56.4% versus 29.6%). Gram-negative bacteria were the predominant pathogens in multiple site involvement. Acute Physiology and Chronic Health Evaluation II scores, marine bacteria, and medical treatment without surgery affected mortality. When necrotic areas included less than three extremities, fasciotomy improved the survival rate. In coastal areas, gram-negative marine bacteria are the most common pathogens associated with necrotizing fasciitis. Fasciotomy can improve survival of patients with necrotic areas that involve less than three sites in necrotizing fasciitis.

INTRODUCTION

Necrotizing fasciitis is a relatively uncommon soft tissue infection associated with rapidly progressive necrosis of the subcutaneous tissue, fascia, and fat. It is a potentially fatal condition with reported mortality rates ranging from 6% to 76%.1 Despite the relatively low incidence of necrotizing soft tissue infections, experts project that necrotizing fasciitis occurs often enough that surgeons, family physicians, internists, and others will encounter at least one patient with this condition during their practice.2 However, unfamiliarity with this condition among clinicians delays the appropriate diagnosis and treatment. Furthermore, textbook guidelines for the aggressive and wide debridement of involved areas cause clinicians to be hesitant when deciding on surgical intervention.

Necrotizing fasciitis mainly encompasses two bacteriologic entities that include polymicrobes (type I) and group A streptococci (GAS) (type II).3 However, the microbiology and clinical characteristics of necrotizing fasciitis will depend on the region and community involved. 4,5 In coastal areas, a third type of infection caused by Vibrio spp. and other gram-negative marine bacteria is not uncommon. This type of infection is hyperacute and fatal, especially in patients with chronic liver disease.6 Therefore, it will be helpful to obtain information for each region and community to facilitate early diagnosis and treatment.

South Korea has extensive sea coasts. The purpose of our study was to evaluate the microbiologic and clinical manifestations of necrotizing fasciitis in a coastal area. In addition, we retrospectively analyzed risk factors associated with mortality caused by necrotizing fasciitis and to develop an optimal therapeutic regimen.

MATERIAL AND METHODS

We identified all cases of necrotizing fasciitis admitted to Chonnam National University Hospital during 1998–2006. This facility is a 1,000-bed hospital serving Chonnam Province and the surrounding island region (approximately 3,000 islands), which has a population exceeding 3.5 million persons. Patients who had complete medical records available for retrospective review were included. Diagnosis was confirmed by either histologic examination or clinical manifestations. Etiologic agents were defined as microorganisms isolated from bulla or blood culture obtained at admission or from tissue cultures at the time of initial fasciotomy.

For these analyses, each patient’s record was checked for information on age, sex, pre-existing illnesses, site of origin of the necrotizing infection, portal of entry, symptoms at admission, vital signs, physical and laboratory findings at the time of admission, extent of the involved area, and treatment. We simplified the extent of involvement by measuring the number of involved extremities (peripheral) and central areas (trunk, back, and groin). These values were scored from 1 (minimum) to 5 (maximum). Early surgery was defined as fasciotomy or debridement performed within 24 hours of admission. Early outcome was defined as death within 48 hours of admission. The main outcome measure used was the 30-day mortality rate. We analyzed several factors associated with death (age, liver disease, Acute Physiology and Chronic Health Evaluation II [APACHE II] score, laboratory data, gram-negative marine bacteria, mean blood pressure), and extent of involved tissues with necrotizing fasciitis.

A case was classified as a person having necrotizing fasciitis–related complications if either abscess or osteomyelitis developed, or amputation was necessary. Necrotizing fasciitis–unrelated complications were defined as underlying disease-related complications or hospital-acquired infections.

Statistical analyses.

Potential factors affecting mortality were examined by using univariate analyses. Pearson’s chi-square statistics were used to compare proportions. Fisher’s exact test for small-sample sizes and the F statistic for the comparison of means of measured variables between survivors and non-survivors were also used. Because of the large number of potentially significant variables identified by univariate analyses, further analyses using multivariate logistic regression were used. A P value of 0.05 was chosen as the criterion for initial variable entry, and P = 0.05 was set as the criterion for determining statistical significance. The variables examined included potential infectious factors affecting mortality, in addition to other demographic and therapeutic variables. Statistical analyses were performed using SPSS version 14.0 software (SPSS, Inc., Chicago, IL).

RESULTS

Epidemiology of necrotizing fasciitis.

Patients were identified from a 217 persons who were diagnosed with necrotizing fasciitis and treated at the Chonnam National University Hospital during 1998–2006. The annual rate of necrotizing fasciitis at our clinic ranged from 1.1 to 9.6 episodes/10,000 admissions (median = 6.7 episodes/10,000 admissions). Seasonal predominance was observed, with the highest rates of necrotizing fasciitis in the summer months (July–September) (71.4%). The study group comprised 164 men and 53 women, with males constituting 75.6% of the patients. The mean age of patients was 58.6 years (range = 20–89 years). The highest incidence of necrotizing fasciitis was in patients 50–59 years of age (32.3%), followed by those 40–49 years of age (31.3%).

Microbiologic and etiologic factors.

Etiologic organisms were documented in 171 patients (78.8%). The highest yields were from blood culture in 113 patients (66.1%), followed by tissue culture (73 patients, 42.7%), and bulla aspirate (48, 28.1%).

The microbiology of necrotizing fasciitis is summarized in Table 1. A single pathogen was isolated from 165 patients (96.5%). Gram-negative rods were isolated from 76% of patients, whereas gram-positive cocci were isolated from 19.9%. Of the gram-negative rods, Vibrio vulnificus was the most common pathogen (102 patients). Marine bacteria, including Vibrio spp., Aeromonas, spp., and Shewanella spp., were isolated from 117 patients (68.4%). Predominant gram-positive cocci that were causative agents of necrotizing fasciitis included Streptococcus spp. (18 patients) and Staphylococcus aureus (11). In six patients, mixed infections were isolated. The peak incidence during summer months was more evident for infections caused by marine bacteria than for other causes. Seasonal variation in necrotizing fasciitis caused by GAS was not observed.

Etiologic factors that were likely to cause necrotizing fasciitis were documented in 161 patients (74.2%). Consumption of raw or undercooked seafood (115 patients, 52.9%) was the most common etiologic factor, followed by direct exposure to seawater (15, 6.9%) and trauma unrelated to seawater (31, 14.3%). Clinical symptoms developed within a mean incubation period of 2.76 days after consumption of seafood.

Underlying medical conditions.

Chronic liver disease or alcoholism was identified in 162 (74.7%) patients. Other medical conditions included diabetes (33, 15.2%), systemic steroid use (5, 2.3%), and hematologic malignancy (3, 1.4%). A total of 37 patients (15.2%) had no underlying medical conditions.

Patients infected with marine bacteria showed higher rates of liver cirrhosis (58.1% versus 38.9%, P = 0.022) and alcoholism (62.4% versus 29.6%, P < 0.001) than patients infected with non-marine bacteria (Table 2). However, the frequency of diabetes mellitus was not significantly different in either group (15.4% versus 18.5%, P = 0.659).

Clinical manifestations.

The median ± SD time from the onset of illness to seeking medical attention was 2.0 ± 1.59 days (range = 4 hours to 10 days). Of the 217 patients, 115 (53%) were hypotensive and required treatment with inotropic agents upon admission. The median temperature at presentation was 36.2°C (range = 35.7–40.0°C). A total of 148 patients (68.2%) did not have fever or hypothermia. Gastrointestinal symptoms such as abdominal pain, vomiting, and diarrhea were more common in patients infected with gram-negative marine bacteria than in those with other causes (56.4% versus 29.6%, P = 0.002). Of the 102 patients with documented infections with V. vulnificus, 56 (54.9%) complained of gastrointestinal symptoms at admission.

Most patients showed signs of soft tissue inflammation, including pain (100%), erythema (88.9%), swelling (79.7%), petechia (47.5%), and bullae (57.1%) at the affected site. Other findings included skin necrosis and fluctuance. The mean ± SD lactate dehydrogenase (LDH) and aspartate aminotransferase (AST) levels in patients without petechia or bullae were 702 ± 472 IU/L and 157 ± 140 IU/L, respectively. Table 3 shows the affected areas of the body. The most commonly affected site was the lower extremities (120, 55.3%). One hundred one (44%) patients had lesions in multiple sites. The trunk, including the perineum, was involved in 51 patients (23.5%). Necrotizing fasciitis caused by gram-negative marine bacteria had a tendency to involve multiple sites (2.15 versus 1.28, P < 0.001).

Patient management.

Nearly all patients received antibiotics. Third-generation cephalosporin-based regimens (80%) were used most commonly. Other regimens used included fluoro-quinolone (8.3%), first-generation cephalosporin (4.6%), tet-racycline (3.7%), and β-lactam/β-lactamase inhibitors (2.8%).

A total of 124 (57.1%) patients underwent fasciotomy at a mean ± SD of 24 ± 54.1 hours after admission (range = 2–384 hours). Of these patients, 72 (58%) underwent surgery within 24 hours. In most cases, fasciotomy was performed under local anesthesia. After fasciotomy, cleansing was continued until granulation tissue grew. After vital signs stabilized, the debridement of necrotic tissue ensued. Patients underwent a mean of 4.2 debridements (range = 0–9 debridements) to control the infective process after initial fasciotomy. Amputation was performed in two patients because of progressive deterioration despite fasciotomy.

The median length of hospital stay was 13 days (range = 3 hours to 180 days). The length of stay was longer when fasciotomy was performed (42.8 days versus 10.1 days, P < 0.001).

Outcome and risk factor analysis associated with 30-day mortality rate.

Overall, the 30-day mortality rate was 45.6%. Seventy-five patients (34.6%) died within the first 48 hours of admission. Of the 30-day survivors, 25 patients had complications. Necrotizing fasciitis–related complications included osteomyelitis in three patients (V. vulnificus in 2 and Pseudomonas spp. in 1), calf muscle abscesses in two patients (V. vulnificus in 1 and GAS in 1), and amputation in two patients (V. vulnificus in 1 and Staphylococcus hominis in 1). Necrotizing fasciitis–unrelated complications included hepatic failure in two patients, hepatic encephalopathy in two patients, spontaneous bacterial peritonitis in one patient, bedsores in two patients, ventilator-associated pneumonia in nine patients, and pseudomembranous colitis in two patients.

Variables that were significantly associated with 30-day mortality rate (P = 0.05) by univariate analysis are shown in Table 4. There was a trend toward higher mortality rates among patients with liver disease than in patients without liver disease (56.2% versus 14.5%, respectively, P < 0.001). Infection with a marine bacterium, high APACHE II score, hypotension, high extent of area involved, leukopenia, azotemia, and elevated LDH and AST levels were significantly associated with increased mortality (P < 0.05). Fasciotomy was performed more frequently in the 30-day survivor group than in non-survivors (78% versus 32.3%; P < 0.001). However, early surgery (within 24 hours) was not associated with a lower 30-day mortality rate (P = 1.000). When the number of body sites involved in necrotizing fasciitis was less than three, fascitomy improved the survival rate (Table 5). Multivariate logistic regression analysis indicated that infection with a marine bacterium (odds ratio [OR] = 6.0, 95% confidence interval [CI] = 2.0–17.7, P = 0.001), high APACHE II score (OR = 3.4, 95% CI = 1.5–7.6, P = 0.003), and medical treatment without surgery (OR = 6.4, 95% CI = 2.7–14.8, P < 0.001) were independent predictors of death.

DISCUSSION

Necrotizing fasciitis is mainly a polymicrobial infection with a mixture of aerobic and anaerobic organisms.79 Only 15–30% of patients are reported as having an infection with one pathogen. 10,11 However, in our patients, most infections were mono-microbial and marine gram-negative bacteria, including Vibrio spp., Aeromonas spp., and Shewanella spp., which were the predominant organisms (68.4%).

Although the organisms isolated from patients with necrotizing fasciitis tend to reflect the distribution of normal flora, 12,13 this result reflects the distinctive features of causative organisms according to the characteristics of the community involved. South Korea is a country with extensive sea coasts where the average water temperatures in the summer are > 15°C. Vibrio spp. have been found in warm coastal waters with temperatures ranging from 9°C to 21°C. Aeromonas hydrophila is isolated from fresh water or seawater in the late summer/early autumn when temperatures are approximately 20–25°C. 14 Additionally, the Korean National Fisheries Research and Development Institute reported that V. cholera non-O1, V. parahaemolyticus, and V. vulnificus were detected in the seawater of live fish tanks. 15 In our study, the seasonal predominance of necrotizing fasciitis during the summer months supports the hypothesis that that the main organisms involved in this infection within coastal areas are marine bacteria.

Another line of evidence for involvement of marine bacteria is consumption of raw seafood and the high prevalence of chronic liver diseases such as hepatitis B and liver cirrhosis in South Korea. Although these findings could be attributed to the extraordinary nature of our community, marine bacteria such as Vibrio spp. have also been detected in other warm coastal regions, including Asia (Thailand, Taiwan, and Singapore), the Gulf of Mexico, South America, and Australia. Moreover, it is expected that additional areas will report infection by these organisms because of global warming and environmental change, global culture, and disasters such as tsunamis and hurricanes. 1618 In coastal areas, diverse marine bacteria should be considered as the major etiologic organisms causing necrotizing fasciitis after exposure to seafood and/or seawater.

Necrotizing fasciitis has been divided into two distinct groups on the basis of the causative organism. Type I infections are polymicrobial infections caused by anaerobes such as non-GAS, Bacteroides spp., and Enterobacteriaceae. Type II infections are usually caused by invasive GAS alone or with staphylococci. 19 Although the clinical manifestations of both subtypes are similar, the affected patients groups are different. Type I infections tend to occur in persons with diabetes mellitus and who have had abdominal surgery, whereas Type II infections occur in patients with no underlying co-morbidities. However, cirrhosis and corticosteroid therapy have also been identified as predisposing factors of type II infections. 20 We found 22 patients with necrotizing fasciitis caused by invasive GAS or staphylococci. Of these, nine patients had underlying liver disease, four had diabetes mellitus, and two had used steroids. Because the major pathogen involved varies on the basis of the community setting and predisposing conditions, cases cannot always be distinguished according to the traditional types of necrotizing fasciitis. Therefore, the established dichotomous classifications are not universally applicable.

It is difficult to make an early diagnosis of necrotizing fasciitis because of the unfamiliarity of most clinicians with the disease. Extreme pain disproportionate to the physical findings is the most consistent feature noted at the time of presentation. Experts refers to this characteristic as the differential point from non-necrotizing soft tissue infection. 12 In our study, all patients reported pain, and most patients had severe pain disproportionate to local findings. Other prominent complaints included gastrointestinal symptoms such as diarrhea and abdominal pain. Most of these symptoms occurred with gram-negative infection and were present before cutaneous manifestation. It is assumed that in coastal areas, the main pathogenesis of necrotizing fasciitis is gastroenteritis and ensuing septicemia after exposure to seafood. In view of our laboratory findings, upon admission, levels of muscle enzymes such as LDH, AST, creatine kinase were elevated without obvious skin changes. In coastal areas, if a patient has preceding gastrointestinal symptoms, pain disproportionate to physical findings, and increased levels of muscle enzymes after exposure to seawater or raw seafood, physicians should consider necrotizing fasciitis as a complication of primary septicemia.

In this study, fasciotomy improved the survival rate, which is consistent with previous reports. 21,22 Necrotizing fasciitis is characterized by angiothrombotic microbial invasion and liquefactive necrosis. Surgical debridement of all necrotic tissue is of paramount importance because antibiotic delivery to the involved area is ineffective because of the thrombosis of the supplying blood vessels. 21,23 However, when compared with other reports, 22,24 the rate of multiple-site involvement in this study was high, which is predominant in necrotizing fasciitis by gram-negative marine bacterium. Extensive multiple-site involvement can make it difficult to decide to perform surgery. This data confirmed that surgical debridement reduced the mortality rate in patients with involvement at one or two sites. Therefore, fasciotomy or debridement should be actively considered, especially when the affected sites involved less than three extremities.

Other studies have reported that early operative debridement remains the highest priority and decreases the mortality rate. 8,22 Although surgery within 24 hours was not associated with improved survival in our study, early fasciotomy should be performed. Necrotizing fasciitis is a most rapid, fatal, soft-tissue infection, with most patients, especially those infected with V. vulnificus, having a fulminating course and dying within 48 hours after admission. In this study, 75% of 30-day non-survivors died within 48 hours of admission.

The textbook guidelines outlining aggressive and wide debridement of all involved areas in necrotizing fasciitis cause clinicians to hesitate when deciding on surgical intervention. In fact, it was not possible for wide debridement to be performed on all involved sites during the initial surgery. At our institution, emergency fasciotomy was performed under local anesthesia at the patients’ bedside because of his or her poor general condition. If the lesion progressed, repeated fasciotomy was performed. Regular review of the patients’ condition (performed every few hours) was extremely helpful in determining if additional fasciotomy was necessary. Emergency fasciotomy under local anesthesia and timely repeated surgery resulted in amputation in only two patients in our case series. This procedure is superior to those reported in other studies, which recommended extensive debridement or immediate limb amputation in necrotizing fasciitis and showed an amputation rate ranging from 27.6% to 46.2%. 24,25 Furthermore, when confined to single-site involvement, the mortality rate of 30.1% was lower than those of other reports (range = 31.5–38%). This finding emphasizes that careful attention and timely repeated debridement on the basis of the patient’s general condition is better than a one-time extensive debridement or immediate limb amputation for limb salvage.

Various studies have attempted to identify the risk factors associated with mortality in patients with necrotizing fasciitis. Previously published independent predictors of mortality include age, female sex, medical condition, hypotension, creatinine levels, high leukocyte counts, delayed surgical treatment, organ failure upon hospital admission, Clostridium spp. infection, and GAS infection. 1,11,26,27 In our study, in addition to high APACHE II scores and medical treatment without surgery, necrotizing fasciitis caused by marine bacteria had a 6.0-fold higher risk of mortality than necrotizing fasciitis in patients not infected with marine bacteria. This higher mortality rate associated with marine bacteria can be explained by underlying medical conditions such as chronic liver disease, organism virulence, and primary septicemia after ingestion of raw seafood.

Although our study was a retrospective review and thus has limitations, to our knowledge, it is the largest review of consecutive patients with necrotizing fasciitis in a coastal area. In conclusion, in coastal areas, gram-negative marine bacteria are the most common pathogen causing necrotizing fasciitis. Knowledge regarding clinical and laboratory characteristics of necrotizing fasciitis may assist in early diagnosis. In conjunction with antibiotics, timely surgery, including fasciotomy, can improve the survival of patients with necrotic areas that involve less than three sites of necrotizing fasciitis.

Table 1

Organisms identified in patients with necrotizing fasciitis, South Korea

Table 1
Table 2

Underlying medical condition and necrotizing fasciitis–causing organisms, South Korea

Table 2
Table 3

Areas involved in patients with necrotizing fasciitis, South Korea

Table 3
Table 4

Univariate analysis of risk factors associated with 30-day mortality in patients with necrotizing fasciitis, South Korea*

Table 4
Table 5

Effects of surgery on mortality according to extent of involvement, South Korea

Table 5

*

Address correspondence to Sook-In Jung, Department of Infectious Diseases, Chonnam National University Hospital, 8 Hak-dong, Dong-gu, Gwangju 501–757, South Korea. E-mail: sijung@chonnam.ac.kr

Authors’ addresses: Kyung-Hwa Park, Sook-In Jung, and Young-Sun Jung, Department of Infectious Diseases, Chonnam National University Hospital, Infectious Diseases, 8 Hak-dong, Dong-gu, Gwangju 501–757, South Korea, E-mail: medkid@dreamwiz.com. Jong-Hee Shin, Department of Laboratory Medicine, Chonnam National University Hospital, 8 Hak-dong, Dong-gu, Gwangju 501–757, South Korea, E-mail: shinjh@chonnam.ac.kr. Jae-Ha Hwang, Department of Plastic and Reconstructive Surgery, Chonnam National University Hospital, 8 Hak-dong, Dong-gu, Gwangju 501–757, South Korea, E-mail: actto2001@yahoo.com.

REFERENCES

  • 1

    McHenry CR, Piotrowski JJ, Petrinic D, Malangoni MA, 1995. Determinants of mortality for necrotizing soft-tissue infections. Ann Surg 221 :558–563.

    • Search Google Scholar
    • Export Citation
  • 2

    Anaya DA, Dellinger EP, 2007. Necrotizing soft-tissue infection: diagnosis and management. Clin Infect Dis 44 :705–710.

  • 3

    DiNubile MJ, Lipsky BA, 2004. Complicated infections of skin and skin structures: when the infection is more than skin deep. J Antimicrob Chemother 53 (Suppl 2):ii37–ii50.

    • Search Google Scholar
    • Export Citation
  • 4

    Chen JL, Fullerton KE, Flynn NM, 2001. Necrotizing fasciitis associated with injection drug use. Clin Infect Dis 33 :6–15.

  • 5

    Miller LG, Perdreau-Remington F, Rieg G, Mehdi S, Perlroth J, Bayer AS, Tang AW, Phung TO, Spellberg B, 2005. Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N Engl J Med 352 :1445–1453.

    • Search Google Scholar
    • Export Citation
  • 6

    Howard RJ, Pessa ME, Brennaman BH, Ramphal R, 1985. Necrotizing soft tissue infections caused by marine vibrios. Surgery 98 :126–130.

  • 7

    Majeski J, Majeski E, 1997. Necrotizing fasciitis: improved survival with early recognition by tissue biopsy and aggressive surgical treatment. South Med J 90 :1065–1068.

    • Search Google Scholar
    • Export Citation
  • 8

    Wong CH, Chang HC, Pasupathy S, Khin LW, Tan JL, Low CO, 2003. Necrotizing fasciitis: clinical presentation, microbiology, and determinants of mortality. J Bone Joint Surg Am 85 :1454–1460.

    • Search Google Scholar
    • Export Citation
  • 9

    Elliott D, Kufera JA, Myers RA, 2000. The microbiology of necrotizing soft tissue infections. Am J Surg 179 :361–366.

  • 10

    Lille ST, Sato TT, Engrav LH, Foy H, Jurkovich GJ, 1996. Necrotizing soft tissue infections: obstacles in diagnosis. J Am Coll Surg 182 :7–11.

    • Search Google Scholar
    • Export Citation
  • 11

    Childers BJ, Potyondy LD, Nachreiner R, Rogers FR, Childers ER, Oberg KC, Hendricks DL, Hardesty RA, 2002. Necrotizing fasciitis: a fourteen-year retrospective study of 163 consecutive patients. Am Surg 68 :109–116.

    • Search Google Scholar
    • Export Citation
  • 12

    Hasham S, Matteucci P, Stanley PR, Hart NB, 2005. Necrotising fasciitis. BMJ 330 :830–833.

  • 13

    Eke N, 2000. Fournier’s gangrene: a review of 1726 cases. Br J Surg 87 :718–728.

  • 14

    Maalej S, Mahjoubi A, Elazri C, Dukan S, 2003. Simultaneous effects of environmental factors on motile Aeromonas dynamics in an urban effluent and in the natural seawater. Water Res 37 :2865–2874.

    • Search Google Scholar
    • Export Citation
  • 15

    Kim JH, Park JH, Lee TS, Lee HJ, Kim SJ, 2001. Distribution of pathogenic Vibrios and environmental factors affecting their occurrence in the seawater of live fish tank. J Fd Hyg Safety 16 :241–246.

    • Search Google Scholar
    • Export Citation
  • 16

    Patz JA, 2002. A human disease indicator for the effects of recent global climate change. Proc Natl Acad Sci USA 99 :12506–12508.

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