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Saudi Journal of Kidney Diseases and Transplantation
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CASE REPORT Table of Contents   
Year : 2003  |  Volume : 14  |  Issue : 4  |  Page : 511-515
Vascular Steal Syndrome and Shewanella alga Infection Requiring Amputation in a Hemodialysis Patient


1 Department of Internal Medicine, University of Texas Medical Branch at Galveston, Texas, USA
2 Division of Nephrology, University of Texas Medical Branch at Galveston, Texas, USA

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   Abstract 

Shewanella alga is a rare gram-negative marine bacterium. Its role as a pathogenic organism is gradually evolving with sporadic cases being reported in humans. We report a case of vascular steal syndrome secondary to a polytetrafluoroethylene (PTFE) graft in the upper extremity of an end-stage renal disease (ESRD) patient on maintenance hemodialysis, which was complicated by infection with S. alga. This resulted in extensive myonecrosis requiring amputation of the limb. To our knowledge this is the fourth case of primary S. alga infection, and the first case in a hemodialysis patient reported in the medical literature from the United States. We also discuss the biochemical tests for identification and differentiation of S. alga from a closely related strain S. putrefaciens.

Keywords: Shewanella alga, Shewanella putrfaciens, End-stage renal disease, Hemodialysis.

How to cite this article:
Jammula P, Gupta R, Agraharkar M. Vascular Steal Syndrome and Shewanella alga Infection Requiring Amputation in a Hemodialysis Patient. Saudi J Kidney Dis Transpl 2003;14:511-5

How to cite this URL:
Jammula P, Gupta R, Agraharkar M. Vascular Steal Syndrome and Shewanella alga Infection Requiring Amputation in a Hemodialysis Patient. Saudi J Kidney Dis Transpl [serial online] 2003 [cited 2019 Sep 20];14:511-5. Available from: http://www.sjkdt.org/text.asp?2003/14/4/511/32988

   Introduction Top


Shewanella spp. is widely distributed in nature, with soil and water being its natural habitat. [1]  Shewanella putrefaciens Scientific Name Search  is the major species, and was initially considered to be a colonizer or a saprophyte thriving on previously damaged tissue. [2] There have been numerous reports associating this bacterium with otitis media, ulcers of the lower extremities and hands, infective endocarditis, arthritis, peritonitis and systemic infections in patients with liver disease, malignancy and severe debility. [3],[4],[5],[6],[7],[8],[9],[10],[11],[12] Shewanella alga is a newly discovered strain that is being increasingly implicated in human disease. [13],[14] We report a case of vascular steal syndrome in a hemodialysis (HD) patient complicated by S. alga infection and septi­cemia that ultimately required amputation of the limb.


   Case Report Top


A 58-year-old African-American male pre­sented with the complaints of pain in the left forearm and hand. He had end-stage renal disease (ESRD) from hypertensive nephro­sclerosis, and was receiving maintenance HD. He had a history of thrombosis of multiple polytetrafluoroethylene (PTFE) grafts placed for vascular access for HD. Another PTFE graft had been placed three months before, in the left arm. He complained of worsening of the pain in the left hand along with nausea, vomiting and abdominal discomfort. The patient was a resident of Galveston Island and enjoyed fishing. His vital signs recorded at the time of admission showed a blood pressure of 132/88 mm Hg; pulse rate of 94/min; respi­ratory rate of 20/min; and a temperature of 38.6 °C. Physical examination at admission revealed an anxious person in moderate pain. The left hand had a dusky appearance. It was edematous, cold, and tender to touch and the radial artery pulsation was impalpable. A palpable thrill and an audible bruit were recorded over the PTFE graft. Rest of the physical examination was unremarkable.

Initial laboratory data demonstrated an elevated white cell count (WBC) of 35,100/ml with a differential count of 77% neutrophils and 14% lymphocytes; hemoglobin was 11.1 g/dl; and the platelet count was 161,000/ml. Serum chemistry revealed a blood urea nitrogen (BUN) of 21.1 mmol/L and serum creatinine of 1016.6 µmmol/L The liver function tests and radiography of the left forearm was normal. Arteriogram of the left upper extremity showed severe atherosclerosis in the brachial and radial arteries, with occlu­sion of the ulnar and interosseous arteries. Injection of the dye into the graft caused minimal opacification of the distal vascu­lature suggesting the presence of a vascular steal syndrome [Figure - 1].

On the third day of admission, necrotic ulcers, bullous lesions, and a foul odor became evident in the left hand and forearm. The PTFE was ligated and surgical exploration of left forearm and hand, and aspiration of the bullous lesions was performed. Blood cultures demonstrated a growth of gram-negative rods, which were subsequently identified as Shewanella alga. The organism was identified using the commer­cially available API 20 NE system. Standard sensitivity testing was not used for deter­mination of sensitivity for this organism and instead we used the Sensititer® (Trek Diagnostics, UK) system for determining the sensitivity for Shewanella alga. The anti­biogram revealed sensitivity to amikacin, gentamicin, tobramycin, ampicillin/sulbactam, piperacillin, ticarcillin/clavunate, cefepime, ceftazidime, ciprofloxacin, imipenem and trimethoprim/sulfamethoxazole [Table - 1].

Aspirate of bullous lesions and tissue culture also demonstrated the growth of S. alga. The gangrene in the left upper extremity worsened and the patient subsequently underwent an amputation of the left forearm. He was treated with cefepime resulting in clinical improvement and subsequent blood cultures were sterile.


   Discussion Top


Shewanella alga is a recently discovered non­fermentative, motile, gram negative, mesophilic marine bacterium closely related to the more psychrotolerant Shewanella putrefaciens. [15] It is capable of reducing Fe (III) in anaerobic conditions and may play an important role in the turnover of inorganic material. [16],[17] S. alga usually does not grow at temperatures below 5°C. A Danish study, however, reported its detection at water temperature above 13°C. They also demonstrated its survival in cold water with regrowth after increase in water temperature. [18]

Prior to the identification of S. alga, most of the human infections caused by Shewanella species were believed to be caused by S. putrefaciens which was first reported in clinical isolates by King. [19] In 1990, Simidu et al proposed the name S. alga for a tetro­dotoxin producing isolate that was recovered from red algae. [20] Later, Nozue et al demon­strated that strains of S. putrefaciens with high guanine and cytosine (G+C) content (52-54 mol%) were genetically related to S. alga.[21] Of the 40 clinical isolates of S. putrefaciens reidentified by Nozue et al, 33 (83%) were found to be S. alga based on the DNA homology and phenotypic criteria. Later, Vogel et al found that 16 of the 19 human isolates of Shewanella strains, that were studied by them, belonged to S. alga group, based on the 16S rRNA sequencing, ribotyping and whole cell protein profiles. [15] Studies on mice by Khashe and Janda have also reported similar results. [22] The above studies suggest that S. alga may be the predominant human pathogen in this genus.

S. alga can be differentiated from S. putre­faciens by its ability to grow at 42°C and 6% NaCl, and its inability to grow at 4°C. Addi­tionally, it produces acid oxidatively from D-glucose and D-ribose but not from L­arabinose or maltose. It grows on  Salmonella More Details- Shigella agar and exhibits β-hemolysis on sheep and bovine blood agars. S. alga was also noted to produce tetrodotoxin. [23] Finally, the percentage of G+C contents differentiate S . alga (52-54 mol %) from S. putrefaciens (43-47 mol %). [21]

There are very few case reports of primary S.alga infection. Strains identified as S. putre­faciens in the past may have factually belonged to S. alga. Dominguez et al, in 1996, reported the first two Danish patients with S. alga bacteremia and lower extremity ulcers. Exten­sive myonecrosis was found in one of the patients. [13] Iwata et al in 1999, reported the first Japanese case of primary septicemia in a patient on HD. [14] Our patient had primary S. alga induced infection of the skin and soft tissues including the musculature involving the hand and forearm, with septicemia. Skin defects and contact with seawater predisposes to infection with S. alga. [13] Noticeably, case reports with this organism have been from geographic areas with long shorelines. [13],[14] We attribute contact with the marine environ­ment during fishing expeditions as the source of infection in our patient. Our case supports the previously expressed notion that this organism may have predilection for tissues with poor circulation. [13] The myonecrosis in our patient was possibly due to the combined effect of vascular insufficiency and infection. The spread of infection was rapid and our patient had to undergo amputation. To our knowledge, this is the fourth case of primary S. alga septicemia and probably the second case of primary S. alga sepsis in a patient on HD, the first being the case reported by Iwata et al. This may be the first case of primary S. alga septicemia in a HD patient being reported from the United States.

Susceptibility of S. alga to cephalosporins, aminoglycosides, quinolones, ampicillin and tetracyclines was reported by Dominguez. [13] A good clinical response to levofloxacin, cefpirome and minocycline was observed by Iwata. [14] S. alga in our patient was sensitive to penicillins, cephalosporins, aminoglycosides, fluoroquinolones and trimethoprim/ sulfame­ thoxazole [Table - 1]. We treated our patient with cefepime, and clindamycin was added to provide anaerobic coverage. Despite signi­ficant morbidity, mortality from S. alga infections has so far not been reported.

There is a growing evidence of S. alga infection in patients in contact with marine environment. Immunocompromised patients such as those with ESRD may be more susceptible. However, further studies regarding bacterial virulence factors and host immune response are required to clarify its patho­genic role in humans.


   Conclusion Top


We conclude that S. alga is a rare human pathogen acquired through contact with sea water that can cause septicemia and tissue necrosis in immunocompromised hosts in the setting of vascular insufficiency.

 
   References Top

1.Kueh CS, Kutarski P, Brunton M. Contaminated marine wounds--the risk of acquiring acute bacterial infection from marine recreational beaches. J Appl Bacteriol 1992;73:412-20.  Back to cited text no. 1  [PUBMED]  
2.Debois J, Degreef H, Vandepitte J, Spaepen J. Pseudomonas putrefaciens as a cause of infection in humans. J Clin Pathol 1975;28:993-6.  Back to cited text no. 2  [PUBMED]  [FULLTEXT]
3.Brink AJ, van Straten A, van Rensburg AJ. Shewanella (Pseudomonas) putrefaciens bacteremia. Clin Infect Dis 1995;20:1327-32.  Back to cited text no. 3  [PUBMED]  
4.Chen YS, Liu YC, Yen MY, et al. Skin and soft-tissue manifestations of Shewanella putrefaciens infection. Clin Infect Dis 1997;25:225-9.  Back to cited text no. 4  [PUBMED]  
5.Gilardi GL. Infrequently encountered Pseudomonas species causing infection in humans. Ann Intern Med 1972;77:211-5.  Back to cited text no. 5  [PUBMED]  
6.Holmes B, Lapage SP, Malnick H. Strains of Pseudomonas putrefaciens from clinical material. J Clin Pathol 1975;28:149-55.  Back to cited text no. 6  [PUBMED]  [FULLTEXT]
7.Kim JH, Cooper RA, Welty-Wolf KE, Harrell LJ, Zwadyk P, Klotman ME. Pseudomonas putrefaciens bacteremia. Rev Infect Dis 1989;11:97-104.  Back to cited text no. 7  [PUBMED]  
8.Yohe S, Fishbain JT, Andrews M. Shewanella putrefaciens abscess of the lower extremity. J Clin Microbiol 1997; 35:3363.  Back to cited text no. 8  [PUBMED]  [FULLTEXT]
9.Leong J, Mirkazemi M, Kimble F. Shewanella putrefaciens hand infection. Aust N Z J Surg 2000;70:816-7.  Back to cited text no. 9  [PUBMED]  
10.Dhawan B, Chaudhry R, Mishra BM, Agarwal R. Isolation of Shewanella putrefaciens from a rheumatic heart disease patient with infective endocarditis. J Clin Microbiol 1998;36:2394.  Back to cited text no. 10  [PUBMED]  [FULLTEXT]
11.Levy PY, Tessier JL. Arthritis due to Shewanella putrefaciens. Clin Infect Dis 1998;26:536.  Back to cited text no. 11    
12.Bhandari S, Pan TL, Horvath J, Tiller D. CAPD, swimming in Shewanella. Nephrol Dial Transplant 2000;15:1484-5.  Back to cited text no. 12  [PUBMED]  [FULLTEXT]
13.Dominguez H, Vogel BF, Gram L, Hoffmann S, Schaebel S. Shewanella alga bacteremia in two patients with lower leg ulcers. Clin Infect Dis 1996;22:1036-9.  Back to cited text no. 13    
14.Iwata M, Tateda K, Matsumoto T, Furuya N, Mizuiri S, Yamaguchi K. Primary Shewanella alga septicemia in a patient on hemodialysis. J Clin Microbiol 1999; 37:2104-5.  Back to cited text no. 14  [PUBMED]  [FULLTEXT]
15.Vogel BF, Jorgensen K, Christensen H, Olsen JE, Gram L. Differentiation of Shewanella putrefaciens and Shewanella alga on the basis of whole-cell protein profiles, ribotyping, phenotypic chara­cterization, and 16S rRNA gene sequence analysis. Appl Environ Microbiol 1997; 63:2189-99.  Back to cited text no. 15    
16.Caccavo F Jr, Blakemore RP, Lovley DR. A hydrogen oxidizing Fe(III)-reducing microorganism from the Great Bay estuary, New Hampshire. Appl Environ Microbiol 1992;58:3211-16.  Back to cited text no. 16    
17.Rossello MR, Caccavo F Jr, Springer N, et al. Isolation and taxonomic characterization of a halotolerant facultatively iron-reducing bacterium. Syst Appl Microbiol 1994; 17:569-73.  Back to cited text no. 17    
18.Gram L, Bundvad A, Melchiorsen J, Johansen C, Fonnesbech Vogel B. Occurrence of Shewanella alga in Danish coastal water and effects of water temperature and culture conditions on its survival. Appl Environ Microbiol 1999; 65:3896-900.  Back to cited text no. 18  [PUBMED]  [FULLTEXT]
19.King EO. The identification of unusual pathogenic gram-negative bacteria. National Communicable Disease Center, Atlanta 1964.  Back to cited text no. 19    
20.Simidu U, Kita-Tsukamoto K, Yasumoto T, Yotsu M. Taxonomy of four marine bacterial strains that produce tetrodotoxin. Int J Syst Bacteriol 1990;40:331-6.  Back to cited text no. 20  [PUBMED]  
21.Nozue H, Hayashi T, Hashimoto Y, et al. Isolation and characterization of Shewanella alga from human clinical specimens and emendation of the description of S. alga Simidu et al., 1990, 335. Int J Syst Bacteriol 1992;42:628-34.  Back to cited text no. 21    
22.Khashe S, Janda JM. Biochemical and pathogenic properties of Shewanella alga and Shewanella putrefaciens. J Clin Microbiol 1998;36:783-7.  Back to cited text no. 22  [PUBMED]  [FULLTEXT]
23.Semple KM, Duran JL, Westlake DS. DNA relatedness of oil-field isolates of Shewanella putrefaciens. Can J Microbiol 1989;35:925-31.  Back to cited text no. 23    

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Correspondence Address:
Mahendra Agraharkar
Department of Medicine, Nephrology Division, University of Texas Medical Branch, 4200 John Sealy Annex, 301 University Boulevard, Galveston, Texas 77555-0562
USA
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PMID: 17657124

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