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Successfully Treated Upper-Extremity Necrotizing Fasciitis Caused by Photobacterium damselae

Open AccessPublished:November 01, 2022DOI:https://doi.org/10.1016/j.jhsg.2022.10.004
      Necrotizing fasciitis is a soft-tissue infection associated with significant morbidity and mortality. The bacteria most associated with necrotizing fasciitis include Streptococcus pyogenes (group A), Clostridium species, Streptococcus species, and Staphylococcus species. Photobacterium damselae (P. damselae), formerly known as Vibrio damselae, is a halophilic, gram-negative bacillus known to infect marine organisms in warm coastal waters. Necrotizing fasciitis associated with P. damselae has been reported to have higher rates of serious complications and mortality because of an atypical presentation and a rapidly progressive course. This report presents a case of successfully treated P. damselae necrotizing fasciitis of the upper extremity and the nuances of management that led to a favorable outcome in which the patient was discharged for home without complications.

      Key words

      Necrotizing fasciitis (NF) is a soft-tissue infection associated with significant morbidity and mortality. It is a bacterial infection of the skin, subcutaneous tissue, and muscle and typically occurs after an initial break in the skin related to trauma or surgery. Necrotizing fasciitis is characterized by rapidly expanding tissue necrosis.
      • Flevas D.A.
      • Syngouna S.
      • Fandridis E.
      • Tsiodras S.
      • Mavrogenis A.F.
      Infections of the hand: an overview.
      The clinical features suggestive of NF include palpable crepitus, skin ecchymosis or bullae, severe pain out of proportion to examination, and rapid progression of the disease process.
      • Flevas D.A.
      • Syngouna S.
      • Fandridis E.
      • Tsiodras S.
      • Mavrogenis A.F.
      Infections of the hand: an overview.
      ,
      • McDonald L.S.
      • Bavaro M.F.
      • Hofmeister E.P.
      • Kroonen L.T.
      Hand infections.
      Early recognition and diagnosis are imperative because NF is a surgical emergency. The initial management includes resuscitation, intravenous antibiotics, and aggressive surgical debridement. Repeat debridements are often required for infection control.
      • Flevas D.A.
      • Syngouna S.
      • Fandridis E.
      • Tsiodras S.
      • Mavrogenis A.F.
      Infections of the hand: an overview.
      ,
      • McDonald L.S.
      • Bavaro M.F.
      • Hofmeister E.P.
      • Kroonen L.T.
      Hand infections.
      A definitive diagnosis is determined at the time of debridement using histologic confirmation.
      • Flevas D.A.
      • Syngouna S.
      • Fandridis E.
      • Tsiodras S.
      • Mavrogenis A.F.
      Infections of the hand: an overview.
      ,
      • McDonald L.S.
      • Bavaro M.F.
      • Hofmeister E.P.
      • Kroonen L.T.
      Hand infections.
      The survival rate for upper-extremity NF can exceed 90% with strict adherence to principles of debridement and broad-spectrum antibiotic coverage.
      • Flevas D.A.
      • Syngouna S.
      • Fandridis E.
      • Tsiodras S.
      • Mavrogenis A.F.
      Infections of the hand: an overview.
      • McDonald L.S.
      • Bavaro M.F.
      • Hofmeister E.P.
      • Kroonen L.T.
      Hand infections.
      • Schecter W.
      • Meyer A.
      • Schecter G.
      • Giuliano A.
      • Newmeyer W.
      • Kilgore E.
      Necrotizing fasciitis of the upper extremity.
      The most common bacterial isolates include Streptococcus pyogenes (group A), Clostridium species, Streptococcus species, and Staphylococcus species.
      • Flevas D.A.
      • Syngouna S.
      • Fandridis E.
      • Tsiodras S.
      • Mavrogenis A.F.
      Infections of the hand: an overview.
      ,
      • Schecter W.
      • Meyer A.
      • Schecter G.
      • Giuliano A.
      • Newmeyer W.
      • Kilgore E.
      Necrotizing fasciitis of the upper extremity.
      Photobacterium damselae (P. damselae), formerly known as Vibrio damselae, a halophilic, gram-negative bacillus known to infect marine organisms in warm coastal waters, can rarely cause a severe form of NF, with less than 15 reported cases in the literature.
      • Martin D.P.
      • Barron O.A.
      • Wu C.H.
      Photobacterium damsela necrotizing fasciitis of the arm.
      In this report, we present a case of upper-extremity NF caused by P. damselae infection that was successfully treated with interval surgical debridement and broad-spectrum antibiotics and discuss the nuances of diagnosis and management.

      Case Report

      Statement of consent

      Written informed consent was obtained from the patient for publication of this case report and the accompanying images.
      A 75-year-old woman with significant left forearm pain, rapidly spreading edema, and associated hypotension was transferred to our emergency department from an outside hospital. The patient had a history of hypothyroidism status after resection. She had no other significant medical history.
      The patient reported scraping herself on barnacles after a fall from a dock in Florida 2 days before admission, with the onset of the symptoms approximately 24 hours before transferring to our hospital. At the time of admission, the patient reported rapidly progressing edema and pain extending distally into the hand and proximally into the elbow over the last few hours. On examination, the patient had severe tenderness to palpation over the dorsal and volar aspects of the forearm, exhibited severe pain with passive range of motion of the fingers, and had significant edema and bullous lesions extending outside the range marked at the previous hospital (Fig. 1).
      Figure thumbnail gr1
      Figure 1Dorsal and volar aspects of the forearm exhibiting significant edema with multiple small scrapes and bullous lesions at the time of presentation.
      On initial evaluation, the patient was normotensive and had received vancomycin, clindamycin, levofloxacin, and piperacillin or tazobactam. Her laboratory tests revealed mild leukocytosis, with a white blood cell count of 12.17 × 103/μL (reference range, 4.00 × 103/μL–11.00 × 103/μL), an elevated absolute neutrophil count of 11.74 × 103/μL (reference range, 1.8 × 103/μL–8.00 × 103/μL), an elevated C-reactive protein level of 5.0 mg/dL (reference range, <0.5 mg/dL), and a normal erythrocyte sedimentation rate of 7 mm/h (reference range, 0–30 mm/h). The LRINEC (Laboratory Risk Indicator Score for Necrotizing Soft Tissue Infection) score at the time of admission was 4 (hemoglobin, 12.1; sodium, 134; glucose, 196).
      The patient was emergently taken to the operating room for complete fasciectomies of the volar, dorsal, and mobile wad compartments of the left forearm; forearm irrigation and debridement (I&D); and open carpal tunnel release within 2 hours of the initial evaluation (Fig. 2). Multiple seropurulent “dishwater pus” fluid collections were noted, consistent with NF. Intraoperative cultures were obtained. After the surgery, the infectious disease team was consulted, and an antibiotic regimen consisting of ciprofloxacin, piperacillin or tazobactam, and vancomycin was continued.
      Figure thumbnail gr2
      Figure 2Index complete fasciectomy and open carpal tunnel release of the left volar, dorsal, and mobile wad compartments.
      On hospital day (HD) 1, the patient was taken back to the operating room for repeat 3-compartment I&D of the left forearm, with extension of debridement into the volar aspect of the palm and dorsal aspect of the hand and index finger. There was diffuse edema in the fourth extensor compartment. However, the underlying fascia appeared healthy and did not require excision. On HD 2, the patient was again taken back to the operating room for repeat I&D, with partial closure and placement on negative-pressure wound therapy (Fig. 3). The initial operative cultures exhibited gram-negative rods that speciated to P. damselae, and the initial pathology was determined to be “fibroadipose tissue and skeletal muscle with fibrinopurulent debris and necrosis.” The antibiotic coverage was then narrowed to piperacillin or tazobactam and ciprofloxacin. The patient underwent repeat I&D and adjustment of wound VAC on HDs 5 and 8, with placement of an Integra dermal allograft during the latter. The patient was discharged for home on HD 10 without complication. At the time of discharge, the patient was transitioned to oral ciprofloxacin, with the antibiotic therapy discontinued at the time of follow-up at the infectious disease clinic 22 days after the initial presentation. The patient’s operative course was completed 29 days after the index procedure, with outpatient I&D, debridement of the olecranon bursa, and forearm split-thickness skin grafting of the left forearm (Fig. 4).
      Figure thumbnail gr3
      Figure 3Secondary debridement, with extension into the volar aspect of the palm and dorsal aspect of the hand or index finger.
      Figure thumbnail gr4
      Figure 4Split-thickness skin grafting of the left forearm.
      The patient has continued to follow-up at a hand clinic and has been participating in hand therapy. During the initial follow-up period, there was failure of the split thickness skin grafting at the site of the original abrasion on the dorsal aspect of the forearm, which led to chronically delayed wound closure. This was managed with wound care and in-clinic debridement. The wound has now progressed to complete healing (Fig. 5). The patient has had continued postoperative therapy and has regained significant function in the surgical extremity (Fig. 6). These most recent functional data recorded by the hand therapy team can be seen in the Table.
      Figure thumbnail gr5
      Figure 5Initial failure of split-thickness skin grafting because of chronic delayed wound closure due to long-term healing secondary to wound care treatment.
      Figure thumbnail gr6
      Figure 6Functionality and range of motion of the left upper extremity and hand after surgery.
      TableRange of Motion 5 Months After Initial Debridement
      Active Range of MotionDegrees (Contralateral)Left Hand StrengthWeight (lbs.) (Contralateral)
      Left elbowGrip strength15 (35)
       Extension25 (15)Left pinch strength
       Flexion150 (150)Lateral5 (9)
      Left forearmTripod2.5 (7)
       Pronation65 (75)Tip2 (5.5)
       Supination55 (80)
      Left wrist
       Extension50 (65)
       Flexion30 (65)
       Radial deviation10 (15)
       Ulnar deviation5 (30)
      Left hand
       Thumb CMC passive abduction35 (40)
       Thumb MCP arc0/55
       Thumb IP arc+10/65
       Index finger MCP arc0/60
       Index finger PIP arc0/95
       Index finger DIP arc5/50
       Middle finger MCP arc15/70
       Middle finger PIP arc0/95
       Middle finger DIP arc0/65
       Ring finger MCP arc20/75
       Ringer finger PIP arc0/90
       Ring finger DIP arc0/70
       Small finger MCP arc15/55
       Small finger PIP arc5/55
       Small finger DIP arc5/40
      Of note, contralateral right hand with full digital fisting and extension.
      CMC, carpometacarpal; DIP, distal interphalangeal; IP, interphalangeal; MCP, metacarpophalangeal; PIP, proximal interphalangeal.

      Discussion

      Vibrio damselae is a facultatively anaerobic, motile, gram-negative, halophilic bacterium that has been reclassified as Photobacterium damsela subsp. damselae.
      • Goodell K.H.
      • Jordan M.R.
      • Graham R.
      • Cassidy C.
      • Nasraway S.A.
      Rapidly advancing necrotizing fasciitis caused by Photobacterium (Vibrio) damsela: a hyperaggressive variant.
      ,
      • Howard R.J.
      • Bennett N.T.
      Infections caused by halophilic marine Vibrio bacteria.
      Halophilic marine vibrio species account for 31% of the total bacterial population in marine waters. They have been isolated from warm ocean waters around the world but are most common in the waters of Florida.
      • Howard R.J.
      • Bennett N.T.
      Infections caused by halophilic marine Vibrio bacteria.
      Inoculation typically results from direct subcutaneous tissue exposure to contaminated seawater. In this case, the likely exposure was evident; however, in many cases, the exact exposure is uncertain.
      • Howard R.J.
      • Bennett N.T.
      Infections caused by halophilic marine Vibrio bacteria.
      Historically, the virulence of P. damsela subsp. damselae was correlated with its capacity to produce damselysin, a heat-labile cytolytic toxin with activity against mouse and sheep erythrocytes in vitro.
      • Kreger A.S.
      • Bernheimer A.W.
      • Etkin L.A.
      • Daniel L.W.
      Phospholipase D activity of Vibrio damsela cytolysin and its interaction with sheep erythrocytes.
      Damselysin, coded for by the dly gene, has phospholipase D activity against sphingomyelin and hemolytic activities, which is distinct from cytotoxins produced by other vibrios.
      • Osorio C.R.
      • Romalde J.L.
      • Barja J.L.
      • Toranzo A.E.
      Presence of phospholipase-D (dly) gene coding for damselysin production is not a pre-requisite for pathogenicity in Photobacterium damselae subsp. damselae.
      However, it has been shown that the dly gene is not directly indicative of pathogenicity and that there is synergistic activity between damselysin and 2 other HlyA hemolysins.
      • Rivas A.J.
      • Balado M.
      • Lemos M.L.
      • Osorio C.R.
      Synergistic and additive effects of chromosomal and plasmid-encoded hemolysins contribute to hemolysis and virulence in Photobacterium damselae subsp. damselae.
      The full hemolytic potential is reached when all 3 cytotoxins are present in bacterial strains that carry the plasmid pPHDD1.
      • Rivas A.J.
      • Balado M.
      • Lemos M.L.
      • Osorio C.R.
      Synergistic and additive effects of chromosomal and plasmid-encoded hemolysins contribute to hemolysis and virulence in Photobacterium damselae subsp. damselae.
      Photobacterium damselae is the first reported gram-negative bacterium involved in synergistic hemolysis occurring within the same species, which might be of special relevance in the severity of its pathogenesis.
      • Rivas A.J.
      • Balado M.
      • Lemos M.L.
      • Osorio C.R.
      Synergistic and additive effects of chromosomal and plasmid-encoded hemolysins contribute to hemolysis and virulence in Photobacterium damselae subsp. damselae.
      Few cases of NF caused by P. damselae have been reported in the literature. It is associated with an especially aggressive course, with severe systemic illness as well as high morbidity and mortality. Of 14 previous cases, 10 were fatal and 1 survivor required amputation at the level of the shoulder.
      • Martin D.P.
      • Barron O.A.
      • Wu C.H.
      Photobacterium damsela necrotizing fasciitis of the arm.
      The patient in this study remained hemodynamically stable throughout the duration of her hospital stay and was discharged without complication on HD 10.
      There are many possible reasons why the patient in this study remained hemodynamically stable throughout admission. First, a suspected diagnosis of NF was made, and surgical debridement was performed within 2 hours of the presentation at our institution and within roughly 24 hours of the onset of the symptoms. It is well established that there are higher rates of morbidity and mortality when treatment is initiated greater than 24 hours after seeking care.
      • Schecter W.
      • Meyer A.
      • Schecter G.
      • Giuliano A.
      • Newmeyer W.
      • Kilgore E.
      Necrotizing fasciitis of the upper extremity.
      Additionally, although the patient in this study was 75 years of age, she did not have other medical comorbidities that increased her risk of severe disease and worse outcomes.
      • Flevas D.A.
      • Syngouna S.
      • Fandridis E.
      • Tsiodras S.
      • Mavrogenis A.F.
      Infections of the hand: an overview.
      ,
      • McDonald L.S.
      • Bavaro M.F.
      • Hofmeister E.P.
      • Kroonen L.T.
      Hand infections.
      ,
      • Angoules A.G.
      • Kontakis G.
      • Drakoulakis E.
      • Vrentzos G.
      • Granick M.S.
      • Giannoudis P.V.
      Necrotising fasciitis of upper and lower limb: a systematic review.
      Additionally, it is possible that her disease was caused by a less virulent strain of P. damselae, which did not contain the plasmid pPHDD1, which is responsible for synergistically amplified hemolysis.
      Necrotizing fasciitis is a true surgical emergency, with literature-reported mortality rates greater than 20%.
      • Angoules A.G.
      • Kontakis G.
      • Drakoulakis E.
      • Vrentzos G.
      • Granick M.S.
      • Giannoudis P.V.
      Necrotising fasciitis of upper and lower limb: a systematic review.
      Early source control is imperative to successful treatment, with patients often requiring 3–4 surgical debridement procedures.
      • Angoules A.G.
      • Kontakis G.
      • Drakoulakis E.
      • Vrentzos G.
      • Granick M.S.
      • Giannoudis P.V.
      Necrotising fasciitis of upper and lower limb: a systematic review.
      If multiple debridement procedures fail to control the infection, amputation of the affected extremity is required. Thus, clinical suspicion should remain high even if the patient remains aseptic, as was the case in this scenario. At the time of admission, the patient in this study was normotensive, with mild leukocytosis and mildly elevated levels of inflammatory markers. On examination, there was no palpable crepitus, and the initial computed tomography scan was read as “diffuse subcutaneous edema, likely representing cellulitis… No discrete fluid collection or soft tissue gas appreciated.” Thus, the focus should be placed on the timeline of symptomatic progression and clinical examination. The patient in this report underwent six I&Ds, on HD 0 (within 2 hours of presentation), 1, 2, 5, 8, and in the outpatient setting 29-days post-index procedure and had a successful outcome.
      Empiric broad-spectrum intravenous antibiotics should be administered emergently to support debridement. Necrotizing fasciitis is typically caused by virulent, toxin-producing bacteria.
      • Flevas D.A.
      • Syngouna S.
      • Fandridis E.
      • Tsiodras S.
      • Mavrogenis A.F.
      Infections of the hand: an overview.
      ,
      • McDonald L.S.
      • Bavaro M.F.
      • Hofmeister E.P.
      • Kroonen L.T.
      Hand infections.
      ,
      • Angoules A.G.
      • Kontakis G.
      • Drakoulakis E.
      • Vrentzos G.
      • Granick M.S.
      • Giannoudis P.V.
      Necrotising fasciitis of upper and lower limb: a systematic review.
      Extremities are primarily infected by Staphylococcus aureus and Streptococcus pyogenes; however, other common bacterial isolates include Clostridium species, anaerobes, and polymicrobial infections.
      • Flevas D.A.
      • Syngouna S.
      • Fandridis E.
      • Tsiodras S.
      • Mavrogenis A.F.
      Infections of the hand: an overview.
      ,
      • McDonald L.S.
      • Bavaro M.F.
      • Hofmeister E.P.
      • Kroonen L.T.
      Hand infections.
      ,
      • Angoules A.G.
      • Kontakis G.
      • Drakoulakis E.
      • Vrentzos G.
      • Granick M.S.
      • Giannoudis P.V.
      Necrotising fasciitis of upper and lower limb: a systematic review.
      More recently, Vibrio vulnificus was recognized to cause a distinctive clinical syndrome characterized by rapidly progressive NF, septicemia, and death.
      • Angoules A.G.
      • Kontakis G.
      • Drakoulakis E.
      • Vrentzos G.
      • Granick M.S.
      • Giannoudis P.V.
      Necrotising fasciitis of upper and lower limb: a systematic review.
      In this case, the initial operative cultures grew P. damselae and the antibiotic coverage was subsequently narrowed to piperacillin or tazobactam and ciprofloxacin per the guidance of the infectious disease consulting service.
      Because the bacterium is known to inhabit warm waters, more cases may be encountered as global climate changes continue to affect ocean currents and temperatures. An increasing incidence of atypical bacteria and associated atypical presentations of NF would introduce further diagnostic uncertainties. Thus, clinicians should maintain a high index of suspicion for atypical presentations of NF because rapid diagnosis and treatment are crucial in the management of these patients.
      In conclusion, NF is a surgical emergency, often requiring multiple debridements. However, despite a clear-cut treatment algorithm, the clinical course may differ depending on the offending microorganism. Thus, the suspicion for NF should remain high when a patient presents with soft-tissue infection even if the patient remains clinically aseptic because atypical microorganisms may exhibit clinical courses that differ from those of commonly offending organisms. This case demonstrates that early diagnosis in the setting of atypically presenting NF caused by an atypical microorganism is of critical importance because early surgical intervention and medical management can lead to a successful outcome.

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