Successful Liver Transplantation from Donor with Plesiomonas shigelloides Sepsis after Freshwater Drowning: Case Report and Review of Literature on Gram-Negative Bacterial Aspiration during Drowning and Utilization of Organs from Bacteremic Donors

Abstract

Background:

Plesiomonas shigelloides is a freshwater, non-fermentative gram-negative bacillus associated with diarrheal disease. Rare cases of invasive infection in human beings usually involve immunosuppressed individuals.

Methods:

We report a patient who underwent successful liver transplantation (LT) using a graft from a 14-year-old boy who had drowned in a freshwater lake. PUBMED was searched for both reported drowning victims with sepsis and outcomes of LT using organs from infected donors.

Results:

Our patient received prophylactic piperacillin-tazobactam, which was switched to cefepime one day after transplantation when gram-negative bacteria grew in blood cultures of the donor. The next day, the organism was identified as P. shigelloides resistant to third- and fourth-generation cephalosporins; ciprofloxacin was given for seven days, and surveillance cultures remained negative. After an uneventful course the patient was discharged on day 10 after LT without signs of infection and is alive with a well-functioning graft. Literature review revealed one case of P. shigelloides in a potential allograft, in which the organism was isolated from heart valves of a drowning victim; the organs were discarded. Reports of freshwater drowning show that bacteremia is universally found post-mortem. Isolated pathogens correspond to specimens from the drowning site, with Aeromonas spp. being the most common and many other microorganisms described anecdotally. Livers from infected donors have been used, in most cases with good results if the recipient and, when possible, donor were treated appropriately; however, cases of fatal pathogen transmission have been reported.

Conclusion:

This is the first reported case of a LT using a graft from a donor with P. shigelloides sepsis. Drowning victims should be considered potentially infected with rare pathogens and therefore represent extended-criteria donors.

Because of the shortage of available organs, liver transplants (LTs) are being performed with extended-criteria donor allografts [1]. Old age, high body mass index, prolonged intensive care treatment, and many other conditions have been proposed to define extended-criteria donors [2]. For obvious reasons, infection and, in particular, bacteremia in the donor also is considered an extension criterion [3]. On the other hand, several case reports demonstrate that such grafts may be used if the causative pathogen is known [4], whereas if such an infection is not diagnosed and the pathogen is not covered by the empiric prophylactic antimicrobial regimen, the infection can be fatal [5].

Drowning victims frequently suffer severe asphyxia and therefore brain death. In most cases, these individuals are young and otherwise healthy, making them ideal donors [6]. However, drowning commonly is associated with aspiration of microorganisms and subsequent blood stream invasion by pathogens [7 –9]. Therefore, these organs should be considered potentially infected, and a unique spectrum of pathogens should be expected, different from that in other donors with sepsis [9 –11].

Plesiomonas shigelloides is a non-fermentative gram-negative bacillus that is abundant in fresh water. The organism usually is associated with both sporadic and epidemic diarrheal illness, but can cause invasive infection [12 –14]. Many reported cases have occurred in immunosuppressed individuals, including one transplant recipient [15, 16]. Lee et al. reported a pediatric stem cell recipient with P. shigelloides sepsis [15]. In their review of the literature, they found that Plesiomonas sepsis frequently was found in neonatal infants and carried a high mortality rate. In an animal model, Haralambie and Schmidt-Weinmar found selective decontamination of the bowel using non-absorbable antibiotics helped reduce Plesiomonas sepsis in dogs undergoing bone marrow transplantation [17]. In contrast to Aeromonas, Plesiomonas has not been associated with disease after aspiration of fresh water during drowning, despite the fact that both pathogens inhabit lakes and ponds [12,18,19]. However, Vehmeyer et al. said that they discarded human homografts from a drowning victim after they cultured Aeromonas from various tissues and the blood and P. shigelloides from the pulmonary and aortic valves [9]. We report successful utilization of a cadaveric liver from a donor with P. shigelloides sepsis who acquired the infection during a drowning accident.

Patients and Methods

PUBMED was searched for reported drowning and near-drowning victims with pneumonia or sepsis caused by gram-negative bacilli. MedLine also was searched for reports on the outcome of LT using organs from donors with bacteremia and infections that could be associated with undetected blood stream infection.

Case Report

Our patient is a 51-year-old man with hepatitis B virus (HBV)-associated liver cirrhosis. His hepatitis B had been treated with lamivudine and tenofovir with a negative viral load for 11 months prior to the transplant. He was listed for LT with a model of end-stage liver disease (MELD) score of 12. Major co-morbidities included diabetes mellitus, which was treated with metformin. The liver donor was a teenage boy who had drowned in a freshwater lake in a neighboring state.

No intraoperative complications occurred. The perioperative antibiotic prophylaxis included piperacillin-tazobactam per program protocol. Trimethoprim-sulfamethoxazole was started for Pneumocystis jirovecci pneumonia prophylaxis within 24 h after LT. On Day 1 after LT, we were informed that gram-negative bacilli were growing in blood cultures taken from the donor prior to organ procurement; piperacillin-tazobactam was replaced with cefepime for treatment of potential gram-negative sepsis. On Day 2, however, the organism was identified as P. shigelloides resistant to third- and fourth-generation cephalosporins but sensitive to ciprofloxacin, which was given for seven days; surveillance cultures remained negative. Prophylactic immunosuppression included tacrolimus, mycophenolate mofetil, and rapidly tapered steroids. Antiviral prophylaxis with anti-hepatitis B virus (HBV) hyperimmunoglobulin and lamivudine and adefovir was started. After an uneventful course, the patient was discharged on Day 10 after LT without any signs of infection. The patient was alive with a well-functioning graft after one year.

Literature Review

Five articles were found that reported the microbiology of drowning victims [7,8,20 –22]. Pathogens isolated from the lung or blood stream of drowning and near-drowning victims usually correspond to pathogens isolated from the accident site, which should be considered when initiating antimicrobial therapy. Not unexpectedly, environmental gram-negative organisms frequently are associated with drowning and near-drowning events; however, gram-positive bacteria and fungi also have been implicated. Six victims from the tsunami in Thailand of December 2004 developed melioidosis; fortunately, all survived because of accurate diagnosis. In another case series, five patients developed Francisella philomiragia infection after near drowning [23 –26]. One article reported a drowning victim who was evaluated for tissue donation [9]. Because P. shigelloides was cultured from the aortic and pulmonary valves, the organs were not used [9]. Aeromonas spp. are the predominant pathogens reported in association with drowning accidents [18,19,27 –32]. Table 1 summarizes papers that report patients with infections caused by gram-negative bacilli after drowning and near drowning.

Table 1.

Microbiologic Findings in Drowning and Near-Drowning Victims

Authors	Organism	Comments
Auerbach et al. [7]	Various	Freshwater pathogens commonly resistant to low-end antibiotics
Auerbach et al. [8]	Various	For some saltwater pathogens, no test systems are available commercially
Ender and Dolan [21]	Various	Pneumonia caused by rare organisms common in near-drowning victims
Vehmeyer et al. [9]	Plesiomonas shigelloides, Aeromonas hydrophila	Tissue donor rejected because of contamination; both organisms isolated from heart valves
Beckert et al. [20]	Various	Injuries in fresh water commonly associated with gram-negative infections
Lucci and Cirnelli [22]	Various	In drowning victims, fecal organisms can almost always be recovered from the blood; organisms also can be isolated from drowning site
Bonatti et al. (present paper)	P. shigelloides	Multi-organ donor
Rosenthal et al. [24]	Pseudomonas putrefaciens	Pathogen isolated from sputum also was isolated at drowning site
Wenger et al. [26]	Francisella philomiragia	Rare pathogen isolated from five drowning victims
Tokuda et al. [25]	Legionella pneumophilia	Fatal pneumonia and lung abscess
Chierakul et al. [23]	Burkholderia pseudomallei	Prognosis is good with early diagnosis
Reines and Cook [31]	A. hydrophilia	In near-drownings, one survived, one died of acute respiratory distress syndrome (ARDS) and sepsis
Outin et al. [30]	A. hydrophilia	Three cases of septicemia, including 51-year-old patient who died after a few days with ARDS
Gaussorgues et al. [28]	A. hydrophilia	No details available
Lecler et al. [29]	A. hydrophilia	No details available
Ender et al. [18]	A. hydrophilia	Sepsis common in near-drowning victims; should they receive prophylactic antibiotics?
Vázquez Piloto et al. [32]	A. hydrophilia	Drunk driver nearly drowned in irrigation ditch but survived
Miyake et al. [19]	A. hydrophilia	Patient also had severe sepsis
Bossi-Kupfer et al. [27]	A. veronii	Nineteen-year-old man with tracheobronchitis after near-drowning in river known to be contaminated with A. veronii biovar sobria

Table 2 summarizes 16 publications on LT using organs from donors with systemic infection. Nine articles focused on donors with documented bacteremia, including individuals with endocarditis [3 –5,10,11,33 –36]. Another five papers included donors with serious bacterial infections, such as meningitis, who had the potential to have unrecognized bacteremia [2,37 –40]. Three major review articles were found, the most recent from the special transplant infection issue of the American Society of Transplantation [41 -43]. Kumar et al. reported on transmission of Pseudomonas aeruginosa to three organ recipients, including one LT recipient. They suspected spillage from the stapled trachea during lung procurement to be the source of infection, which resulted in graft loss secondary to anastomotic infections in all recipients [44].

Table 2.

Publications on Use of Liver Allografts from Bacteremic or Potentially Bacteremic Donors

Authors	Organism	Bacteremic?	No. Recipients	No. Donors	Liver Transplants	Other Organs	Transmission?	Comments
Little et al. [11]	Various	Yes	19	8	6	Kidney, pancreas, heart-lung	No	Donor meningitis/epiglottitis
Caballero et al. [33]	Enterococcus faecalis	Yes	3	1	1	Kidney	No	Donor endocarditis; negative blood culture
Freeman et al. [10]	Various	Yes	212	95	55	Kidney, pancreas, heart, lung	No	Single-center series; no donor-transmitted infections or poor outcomes
Zibari et al. [40]	Various	Some yes	179	599 donors; 46 bacteremic	9	Kidney, heart	3 heart recipients	State data; donor-transmitted infection rare
Lumbreras et al. [3]	Various	Yes	408 liver; 161 heart	29/569	18	Heart	No	No donor-derived infections or adverse outcomes in recipients of organs from bacteremic donors
Satoi et al. [38]	Streptococcus pneumoniae (4); Haemophilus influenzae (1); other streptococci (2)	Potentially	34	33	34	NA	No	Donor bacterial meningitis
Angelis et al. [43]	Various (review)	NA	NA	NA	NA	NA	NA	Effect of pathogen transmission on liver function, morbidity, mortality rate
Kumar et al. [44]	Pseudomonas aeruginosa	No	5	1	1	Lung, liver, kidney, spleen-pancreas-kidney	4 of 5	Intraoperative spillage from stapled trachea; transmission to three recipients caused graft loss from anastomotic infection
Pauly et al. [35]	Staphylococcus aureus	Yes	3	1	1	Kidney	No	Severe sepsis
Gonzalez-Segura et al. [34]	Various	Yes	143; detailed data provided for 95	52	40	Kidney, heart, lung, pancreas	No	Positive blood cultures in donors; >50% coagulase-negative staphylococci
Cerutti et al. [5]	Various	Yes	128	128	128	NA	11	128 bacteremic liver donors and 189 other donors with positive cultures; Candida albicans common
Cohen et al. [4]	Acinetobacter baumannii	Yes	12	3	2	Kidney, lung, heart	No	Septic shock
Tector et al. [2]	NA	Potentially	NA	2	2	None	No	Donors with meningitis included in other series
Len et al. [37]	Various	Potentially	292	211 infected donors; 38 bacteremic	2	Kidney, lung	5	S. aureus most common pathogen; lung allografts most likely to transmit infection
Sözen et al. [36]	Klebsiella; A. baumannii	Yes	8	2	3 (one split graft)	Kidney, heart	No	Two donors with gram-negative sepsis; one heart not used because of infection but livers and kidneys used
Wu et al. [39]	Various	Potentially	34/72	59	59	None	No	S. aureus most common; lung most commonly infected site
Grossi and Fishman [42]	Various (review)	NA	NA	NA	NA	NA	NA	Summarizes risks of infection with grafts
Fischer and Avery [41]	Various (review)	NA	NA	NA	NA	NA	NA	Guidelines for donor screening

NA, not available.

Data from more than 400 donors and more than 300 LTs are available (Table 2). Staphylococcus aureus is the most common organism to colonize or infect donors. In general, the lung is the site most commonly infected. Data from large registries suggest that the outcome of LT using grafts from infected donors is not poorer than after LT using non-infected donor allografts, as neither a higher infection risk nor worse graft function was observed. Risk factors for bacteremia in donors include long-term ventilation, advanced age, burns, and requirement for large doses of vasopressors.

Drowning victims should be considered potentially infected; rare pathogens may be transmitted from such donors to organ recipients [45]. However, drowning does not necessarily preclude organ donation; McNamee et al. reported on successful utilization of a lung allograft from a drowning victim [46].

Discussion

To our knowledge, this is only the second case of P. shigelloides sepsis reported after drowning and the first case of LT using a graft from a donor who suffered from such a systemic infection. This organism is an emerging pathogen that is widespread in the aquatic environment and responsible for intestinal diseases and extra-intestinal infections in humans and animals [47 –50].

Because of the limited knowledge of its genetic diversity, population structure, and evolution, epidemiologic control of P. shigelloides has been limited. Salerno et al. recently analyzed 77 epidemiologically unrelated strains from several countries and ecological sources using multilocus sequence typing [51]. They found that P. shigelloides exhibits a high rate of recombination, which is more similar to that of Streptococcus pneumoniae than to other Enterobacteriaceae such as Salmonella enterica, Escherichia coli, or Yersinia enterocolitica.

Plesiomonas may be found as a normal commensal of many animals, and colonization patterns have been well studied in pets, birds, fish, and maritime invertebrates [52 –55]. This pathogen has the ability to modulate host protective responses through inhibiting cathepsins involved in antigen processing and presentation [56] and can produce hemolysins and other exotoxins [57].

Contaminated water serves as a reservoir for P. shigelloides-associated diarrheal disease. Filter-feeding invertebrates along the coast of California and many other geographic areas have been found to concentrate fecal bacteria flowing from land to sea, including P. shigelloides, pointing to the impact of human interventions on coastal ecosystems and the environmental niches of fecal bacteria [58]. Two large case series from Southeast Asia have shown that whereas Plesiomonas diarrhea is more common in children than in adults, adults tend to have more severe disease [59,60]. Moreover, co-infection with other enteric pathogens may occur. The infection is self-limited in most cases, and fluoroquinolones appear to be the preferred treatment option for severe infection [59,60]. Importantly, P. shigelloides appears to be resistant to ceftazidime and cefepime [61,62]. Woo et al. analyzed seven cases of P. shigelloides sepsis and found biliary tract disease to be a major risk factor [14]. These patients did not present with enteric infection but rather with cholangitis. Other reported rare infections caused by P. shigelloides include proctitis in a bisexual man that led to fatal sepsis, neonatal meningitis, necrotizing fasciitis, osteomyelitis, ophthalmitis, and intra-abdominal abscesses; an impaired immune system is a common finding [63 –69]. Humphreys et al. described a patient with liver cirrhosis and spontaneous infection of the pleural space with sepsis [70]. Only two cases of pneumonia attributed to P. shigelloides were reported, one of them fatal [71,72]. No case of aspiration in cases of near drowning has been reported, which is surprising, given the fact that P. shigelloides is such a frequent isolate from marine environments. However, in a drowning victim, the pathogen was cultured from the aortic and pulmonary valves but no other sites [9]. In this case, the tissue was not used for transplantation. Whole organs are more valuable, and most reports on donor bacteremia suggested that the risk of transmission of pathogens to the recipient is low. Also, blood cultures may become positive only after the organ has already been implanted, such as in our case.

Whereas for gram-negative bacilli, there may be a low risk of transmission, for S. aureus, this hypothesis may not apply. Common pathogens to be considered in drowning accidents are Aeromonas and Pseudomonas; however, many less common pathogens also have been reported, including Legionella pneumophila, Shewanella putrefaciens, Burkholderia pseudomallei, Vibrio, F. philomiragia, and zygomycetes among many others [7,8,18,20,21,23 –26,73 –76]. With increasing fecal pollution and global warming, many uncommon or new pathogens, such as Naegleria fowleri, may cause more waterborne illnesses [77]. Lucci and Cirnelli reported that almost all drowning victims have positive blood cultures on postmortem examination and that pathogens found in blood corresponded to those isolated from the aquatic environments where drowning took place [22].

From a practical point of view, when managing near-drowning victims, close microbiological monitoring, including tracheal secretions and blood cultures, should be performed; and rare pathogens should be anticipated. In terms of donor management, special attention should be drawn to such rare pathogens in drowning victims. This situation is unique for this special entity of donors, and therefore, they should be considered extended criteria.

Author Disclosure Statement

No conflicting financial interests exist.

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