First case of a renal cyst infection caused by Desulfovibrio: a case report and literature review

Abstract

Background

Genus Desulfovibrio species is a sulphate-reducing anaerobic gram-negative rod that resides in the human oral cavity and intestinal tract. It was reported as the causative pathogen of bacteraemia and abdominal infections, but not renal cyst infection, and Desulfovibrio fairfieldensis has higher pathogenicity than other Desulfovibrio species.

Case presentation

A 63-year-old man was on haemodialysis for end-stage renal failure due to autosomal dominant polycystic kidney disease. On admission, he had a persistent high-grade fever, right lumbar back pain, and elevated C-reactive protein levels. His blood and urine cultures were negative. He received ciprofloxacin and meropenem; however, there was no clinical improvement. Contrast-enhanced computed tomography and plain magnetic resonance imaging revealed a haemorrhagic cyst at the upper pole of the right kidney. The lesion was drained. Although the drainage fluid culture was negative, D. fairfieldensis was detected in a renal cyst using a polymerase chain reaction. After the renal cyst drainage, he was treated with oral metronidazole and improved without any relapse.

Conclusions

To the best of our knowledge, this is the first reported case of a renal cyst infection with Desulfovibrio species. D. fairfieldensis is difficult to detect, and polymerase chain reaction tests can detect this bacterium and ensure better management for a successful recovery.

Background

Genus Desulfovibrio is an anaerobic gram-negative rod and a type of sulphate-reducing bacteria belonging to more than 30 species residing in the human oral cavity, intestinal tract, and nature, including soil, sewage, and brackish water [1]. Desulfovibrio fairfieldensis has higher pathogenicity and more antimicrobial resistance than other Desulfovibrio species [1,2,3,4]. It may be the causative pathogen of bacteraemia and abdominal infections, such as abscesses and cholecystitis [1]. There are several reports of infections such as brain abscesses, meningitis, intra-abdominal abscesses, and bacteraemia caused by Desulfovibrio species [1,2,3, 5,6,7], but not renal cyst infection. Here, we report a case of renal cyst infection caused by D. fairfieldensis; this is the first such report.

Case presentation

A 63-year-old man, who was a glass craftsman and a sewer cleaner, on haemodialysis for 19 years due to autosomal dominant polycystic kidney disease (ADPKD), was referred by his family doctor for suspicion of renal cyst infection after presenting with a persistent fever of approximately 38 °C, right lumbar back pain, and elevated C-reactive protein (CRP) levels for the past 14 days. Although he had received intravenous ceftriaxone for two days and meropenem and levofloxacin for 12 days, he displayed no clinical improvement. On admission, he had a fever of 38.4 °C and negative blood and urine cultures (Fig. 1a). His blood tests revealed leucocytosis (9280/μL), thrombocytopenia (77000/μL), elevated CRP levels (11.09 mg/dL), and elevated procalcitonin levels (0.94 ng/mL). Plain computed tomography (CT) revealed a right renal cyst infection. Although treatment with intravenous ciprofloxacin (0.4 g/day) had been started, his clinical findings did not improve. Therefore, his treatment was changed to meropenem (0.5 g/day) on Day 9 to cover extended-spectrum β-lactamase-producing bacteria since meropenem had been reported to provide poor penetration into infected cysts but clinical improvement [8]. Contrast-enhanced CT and plain magnetic resonance imaging (MRI) were also performed (Fig. 1b). They revealed a haemorrhagic cyst at the upper pole of the right kidney, which was suspected to be the cause of the infection; percutaneous drainage of the renal cyst was performed on Day 13, and 200 mL of fluid was drained. The subsequent drainage volume was approximately 20 mL daily for 1 week. After drainage, the patient’s body temperature reduced to approximately 36.7 °C. In addition, the leucocytosis, thrombocytopenia, elevated CRP, and procalcitonin levels were resolved. The drainage fluid culture was negative for bacteria, including anaerobes and fungi. Therefore, a polymerase chain reaction (PCR) test of 16S rDNA using 27FN (AGAGTTTGATCMTGGCTCAG) and 1525R (AAAGGAGGTGATCCAGCC) primers was performed for purified DNA from the drainage fluid. On Day 30, it turned out that the obtained sequences were 99.7% identical (1500/1505 bp) to that of D. fairfieldensis ATCC 700045^T(U42221). Therefore, on Day 31, his treatment was changed to oral metronidazole (1 g/day). The volume of drained fluid decreased to 0–2 mL on Day 34, and contrast-enhanced CT performed on Day 35 showed shrinkage of the renal cysts. His clinical findings normalised, and the drainage tube was removed on Day 36. The Japanese guidelines for treating renal cyst infection in patients with ADPKD recommend a treatment period of at least 4 weeks with antimicrobial agents [9]. Therefore, on Day 38, he was discharged and asked to continue oral metronidazole for 4 weeks. After that, there was no relapse of the infection.

Fig. 1

a Chart of patient’s clinical course after admission. The lower graph shows the patient’s body temperature, white blood cell count, and C-reactive protein levels during hospitalisation. Renal cyst drainage was performed on Day 13, and the fluid drained initially was 200 mL. A PCR test performed on Day 30 revealed that the causative bacteria was Desulfovibrio fairfieldensis. The middle graph shows the volume of fluid drained. The drained fluid volume could not be measured for two days after the initial drainage. The upper bar shows the antibacterial drug administered, the dose, and the timing of switching; BT, body temperature; CIP, ciprofloxacin; CRP, C-reactive protein; MEM, meropenem; MNZ, oral metronidazole; PCR, polymerase chain reaction; WBC, white blood cell count. b Diffusion-weighted imaging of plain abdominal magnetic resonance imaging (MRI) on Day 9 of admission. White arrow: a renal haemorrhagic cyst

Discussion and conclusions

Genus Desulfovibrio was first described in 1895 [10], and a human infection (bacteraemia associated with cholecystitis) with D. desulfuricans was first reported in 1987 [11]. However, it was later considered to be D. fairfieldensis in 2005 because the strain was positive for catalase and nitrate. Optical and electron micrographs of D. fairfieldensis were published in 1996 and 1997 [6, 12], and the first human infection with D. fairfieldensis was reported in Fairfield, Australia; it presented as a liver abscess [6]. Subsequently, we searched PubMed and Google scholar and 71 reported human cases of infection with Desulfovibrio species, including D. desulfuricans, D. fairfieldensis, D. piger, and D. legalli, were found in 26 articles (Table 1). D. fairfieldensis has been isolated from several sites of infection, including blood [2,3,4, 7, 12], peritoneal fluid [4], periodontal pockets [29, 30], the pelvis and colon [4], liver abscesses [6], and urine [5]. This report describes the first case of renal cyst infection caused by the genus Desulfovibrio. When our case is added to those previously reported, D. fairfieldensis infection is the most common (26 cases, 36%), followed by D. desulfuricans (24 cases, 33%), with bacteraemia and intra-abdominal infection being the commonest presentations (Table 2).

Table 1 Characteristics of 72 cases infected with Desulfovibrio species in 27 articles

Table 2 Summary of clinical characteristics of cases of infection with Desulfovibrio species in 27 articles

Because renal cyst infections in patients with ADPKD are frequent and refractory and patients on haemodialysis are immunocompromised [31], identification and eradication of the causative organism are essential [32]. The causative organisms of renal cyst infections have only been identified in 49% of cases, and the most common causative organisms are gram-negative rods from the intestinal tract [32, 33]. Therefore, the actual infection rate by Desulfovibrio species may be underestimated because of the difficulty in identifying anaerobic bacteria [3, 17] and the actual number of infections by anaerobic bacteria, including Desulfovibrio species, maybe much higher. No strain was cultured in this patient’s blood, urine, or renal cyst fluid, but D. fairfieldensis was detected in the renal cyst fluid by PCR testing. PCR is useful in identifying organisms that cannot be grown in vitro or in cases where existing culture techniques are not sensitive enough and/or require long incubation times due to its tremendous sensitivity, specificity, and amplification speed [34]. In previous reports, PCR tests using 16S rDNA were used to identify 87% of Desulfovibrio species, while biochemical methods were used in 13% (Table 2). Matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS) was also used in only 5.6% of the cases (Table 2); however, its use for organism identification is expected to increase because it is a novel method that can rapidly identify bacteria and be as accurate as 16S rDNA. In addition, 72% of the cases were identified after 3 days in cultures, and 24% were identified after 7 days (Table 2). Therefore, if the causative bacteria are unknown, performing the culture for a longer period is necessary.

In this case, contrast-enhanced CT and plain MRI identified the infected renal cyst, but 18-fluorodeoxyglucose positron emission tomography/CT (18FDG PET/CT) has been reported to be useful in the diagnosis of renal cyst infection [35, 36]. However, this method is not commonly used in Japan due to cost, where the national health insurance system allows the use of 18FDG PET/CT for malignant tumours mainly.

The routes of renal cyst infection include hematogenous routes and retrograde infection from the urinary tract. In the literature review, bloodstream infection was the most common among Desulfovibrio infection, followed by intra-abdominal infection, while urinary tract infection was less common at 3.6% (Table 2). He was in regular contact with soil and sewage, which are dwelling sites of the bacteria, due to his occupation. Since most of the Desulfovibrio species are also found in the environment, and since haemodialysis patients have reduced urine volume and are unable to cleanse themselves through urination, we suspected that the bacteria had entered the urinary tract and caused the infection retrogradely. However, it has been reported that D. fairfieldensis survives only in the human intestinal tract [4, 25], and we thought that it was more likely that the infection was haematogenous.

Infected cysts need early percutaneous cyst drainage, which provides the best treatment results because antibiotics alone do not usually treat the infection [33, 37]. In this case, the patient’s condition improved after drainage was performed.

For antimicrobial treatment of renal cyst infections, lipid-permeable antimicrobials with high penetration are recommended as first-line agents [32, 37]. Therefore, we also used ciprofloxacin as a quinolone, but with poor improvement. Then, we used meropenem which has been reported to have clinical improvement for cyst infection despite the poor penetration [8], but there was no improvement. The other antimicrobial agents for this patient were used as empirical treatments.

Optimal antimicrobial therapy for D. fairfieldensis remains controversial. One study showed that metronidazole had the highest antibacterial activity, while imipenem was effective against it [1]. Another study showed that imipenem, ciprofloxacin, clindamycin, chloramphenicol, and beta-lactams, except carbapenems, were ineffective [2]. Lipid-permeable antimicrobials such as metronidazole and clindamycin increase the concentrations of the antimicrobials in the renal cyst fluid [38]. Therefore, oral metronidazole was used for this patient. In addition, D. fairfieldensis may be more resistant to antimicrobial agents and have higher pathogenicity than other Desulfovibrio species [1,2,3]. Metronidazole was effective with good blood levels in the renal cysts of patients with ADPKD, including those on haemodialysis [38]. Summarising the previous reports of Desulfovibrio species infection, metronidazole showed the highest susceptibility (78%), and clindamycin was also effective (Table 3). However, metronidazole was used in only 23% of the patients; given that D. fairfieldensis is more resistant to antimicrobial agents and more pathogenic than other Desulfovibrio species [1,2,3,4], identifying the Desulfovibrio species, especially in D. fairfieldensis, by PCR tests, and using metronidazole, are essential for patient prognosis. In addition, because 54% of the patients with Desulfovibrio infection were complicated with other bacteria, there is concern that Desulfovibrio species can manifest when antimicrobial agents which are susceptible to other bacteria but resistant to Desulfovibrio are used (Table 2). The prognosis of Desulfovibrio infection was 11% of death, and treatment should be carefully selected, including appropriate drainage and antimicrobial agents.

Table 3 Summary of antimicrobial susceptibility of Desulfovibrio species and actual antibiotic therapy

The essential recommendations for the general treatment of renal cyst infection, including Desulfovibrio species, are as follows: if the bacteria of renal cyst infection are unknown, focus on long-term culture studies, consider identification of the organism by 16S rDNA or MALDI-TOF MS, consider the possibility of multiple bacterial complications. Some bacteria have a high mortality rate, and drainage should be performed first if possible and appropriate antimicrobials should be administered according to the organism.

To conclude, this is the first report of a renal cyst infection with the genus Desulfovibrio species to the best of our knowledge. D. fairfieldensis has higher pathogenicity and more antimicrobial resistance than other Desulfovibrio species and is difficult to detect. PCR tests can detect this bacterium and ensure better management for a successful recovery.