Abstract
A 75-year-old man was diagnosed with probable Campylobacter jejuni prosthetic knee infection after a diarrheal illness. Joint aspirate and operative cultures were negative, but PCR of prosthesis sonicate fluid was positive, as was stool culture. Nineteen additional cases of Campylobacter prosthetic joint infection reported in the literature are reviewed.
CASE REPORT
A 75-year-old man from Minnesota presented with a 6-day history of right knee pain and swelling. He had a history of bilateral knee arthroplasties performed 4 years prior, hypertension, and papillary thyroid cancer. Two years prior, he developed culture-negative right prosthetic knee joint infection (PJI), which was managed at another facility with two-stage resection-reimplantation of his right knee prosthesis. He had been doing well since then. One day before his current onset of knee pain, he developed acute, nonbloody diarrhea. He worked on a cattle farm but had no direct contact with animals, had no recent travel, did not recall consuming undercooked meats, and had no ill contacts. He was evaluated by his local doctors 3 days into his diarrheal illness. Stool was positive for Campylobacter antigen (ImmunoCard STAT! CAMPY; Meridian Bioscience, Cincinnati, OH). He was treated with oral azithromycin for 3 days. His diarrhea improved, but knee pain persisted and was associated with subjective fevers and chills. On the fifth day of illness, he presented to his local orthopedic surgeon and underwent right knee aspiration, which showed 27,900 leukocytes/μl (88% neutrophils).
The following day, he presented to our facility with a warm and tender right knee and a large effusion. Right knee aspiration yielded 127 ml of “brown murky” fluid with 42,681 leukocytes/μl (92% neutrophils). The C-reactive protein (CRP) level and erythrocyte sedimentation rate (ESR) were 239 mg/liter and 47 mm/h, respectively. Gram stain of the aspirated fluid was negative, as were bacterial cultures (aerobic cultures on sheep blood and chocolate agar, anaerobic cultures in thioglycolate broth and on CDC sheep blood agar, and Campylobacter cultures under microaerophilic conditions on cefoperazone-vancomycin-amphotericin B [CVA] and buffered charcoal yeast extract [BCYE] agar) at 42°C and fungal and mycobacterial cultures, along with blood cultures. The patient underwent resection arthroplasty with placement of a vancomycin- and gentamicin-impregnated antibiotic spacer. Acute inflammation was present in periprosthetic tissue. Aerobic, anaerobic, and microaerophilic cultures (at 42°C) performed on two periprosthetic tissues and prosthesis sonicate fluid (1) were negative. A previously described Campylobacter jejuni/Campylobacter coli real-time PCR assay targeting cadF and designed for testing stool (2) was performed on sonicate fluid. The PCR assay was positive, with a crossing point value of 37.6 cycles (positive-control crossing point, 32.0 cycles). He was treated with intravenous meropenem (1 g every 8 h) and oral azithromycin (500 mg daily) for 6 weeks. The Campylobacter antigen-positive stool specimen collected at his local health care facility was forwarded to the Minnesota Department of Health, where Campylobacter jejuni was isolated. The isolate exhibited a positive hippurate hydrolysis reaction and was susceptible by the Etest to ciprofloxacin and erythromycin but resistant to tetracycline (3). Using National Antimicrobial Resistance Monitoring System (NARMS) criteria, the isolate was also susceptible to nalidixic acid, clindamycin, gentamicin, chloramphenicol, and azithromycin (4). After completion of meropenem and azithromycin, he was maintained on azithromycin for another 7 weeks, and then observed off therapy for 4 weeks prior to reimplantation arthroplasty. Bacterial cultures and cadF PCR of three tissue specimens obtained at the time of reimplantation were negative, although histopathology showed residual acute inflammation. Postreimplantation, he was treated with meropenem for 2 weeks, and thereafter, chronic suppressive therapy with oral azithromycin at 1,200 mg weekly was administered. The patient remained well at 3 months of follow-up.
By 2030, the yearly number of combined knee and hip arthroplasties is estimated to reach 4 million (5), and recent data have shown that laboratory-confirmed campylobacteriosis increased by 14% in 2012, compared to 2006 to 2008 (6). While Campylobacter PJI is an uncommon entity, the convergence of two factors—an increased numbers of persons with prosthetic joints and the prominence of food-borne infections despite stringent regulatory measures (5, 42)—makes it likely that clinicians will continue to encounter PJIs caused by enteropathogens (7, 8).
We reviewed the literature regarding Campylobacter PJI. Twenty cases (including our case) have been reported (9–20) (Table 1). One case reported as “Campylobacter intestinalis” was excluded as we were unable to obtain further details (21). The predominance of C. fetus is in keeping with its propensity to cause bacteremia, possibly related to its relative resistance to the bactericidal activity of serum (22).
TABLE 1.
Campylobacter prosthetic joint infections reported in the literaturea
Species | No. of cases | Median patient age, yr (range) | No. (%) of male patients | Relevant exposure (no.) | No. (%) immunocompromised | Joint (no.) | Time of onset of PJI from arthroplasty | Acuity (no.) | Diarrheal illness | Culture result (no.) |
Surgery (no.) | No. (%) with combination therapyb | Duration of treatmentc | No. (%) with chronic suppression | Outcome (no.) | Duration of follow-up | Reference(s) | ||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Blood | Stool | Joint | |||||||||||||||||
C. fetus | 13 | 72 (52–88) | 6 (46) | Cattle farmer (1) | 9 (69)d | Knee (5),e hip (8) | 1 mo–∼8 yrf | Acute (4), chronic (8), Unk (1) | Yes (4), no (4), Unk (5) | Pos (5), Neg (6), Unk (2) | Pos (4), Neg (4), ND (2), Unk (3) | Pos (13)h | 1SR (3), 1SR and DAIR (1), 2SR (1), DAIR (3), explantation (1), no surgery (3), NR (1) | 12 (92) | 4–12 wk | 4 (31)j | Recovered (11), death (2)k | 6 mo–5 yr (8 cases) | 9–15 |
C. jejuni | 3 | 75 (60–77) | 3 (100) | Cattle farmer (1) | 1 (33)d | Knee (2) Hip (1) | 2–9 yrg | Acute (2), chronic (1) | Yes (2), Unk (1) | Pos (1), Neg (2) | Pos (1), Neg (1), ND (1) | Pos (2), Neg (1)i | 1SR (1), 2SR (1), no surgery (1) | 3 (100) | 8–22 wk | 1 (33)i | Recovered (3) | 7 wk–8 yr | 9, 16; this report |
C. coli | 1 | 60 | 1 (100) | Consumed raw oysters (1) | 0 | Hip | 6 yr | Acute | Yes | Neg | ND | Pos | DAIR | 0 | 6 wk | 0 | Recovered | NR | 17 |
C. gracilis | 1 | 74 | 1 (100) | Cattle farmer who handled septic abortion (1) | 0 | Knee | 3 yr | Acute | Yes | Pos | Neg | Pos | DAIR | 1 | ∼8 wk | 0 | Recovered | 6 mo | 18 |
C. lari | 1 | 81 | 1 (100) | 0 | Hip | 4 yr | Acute | No | Pos | Neg | Pos | DAIR | 1 | NA | NA | Death from sepsis at 2 days | NR | 19 | |
C. upsaliensis | 1 | 24 | 1 (100) | 1 (100)d | Knee | 1 yr | Acute | Yes | Neg | Neg | Pos | No surgery | 1 | 30 wk | 0 | Recovered | 34 mo | 20 |
Abbreviations: PJI, prosthetic joint infection; Pos, positive; Neg, negative; Unk, unknown; ND, not done; 1SR, one-stage reimplantation arthroplasty; 2SR, two-stage reimplantation arthroplasty; DAIR, débridement, antibiotics, and implant retention; NR, not recorded; NA, not applicable.
Combination therapy represents simultaneous treatment with two or more classes of antimicrobials at any time point.
Excluding patients placed on chronic antibiotic suppression.
These comprised: C. fetus (liver cirrhosis, 3; lung cancer, 1; renal transplant, 1; rheumatoid arthritis on immunosuppressants, 2; chronic leukemia, 2); C. jejuni (AIDS and liver cirrhosis); and C. upsaliensis (tibial osteoblastic osteosarcoma).
Bilateral prosthetic knee joints were involved in one case.
Data from seven cases with onsets of PJI of 1, 5, and 11 months and 3 (Alain Meyer, personal communication), 4, 7, and ∼8 years.
Data from two cases.
Two specimens comprised drainage from wound and a bone biopsy specimen.
This is the present case. PCR for cadF was positive, but cultures were negative.
Two patients underwent DAIR, two patients did not undergo surgery, and one patient underwent a two-stage revision.
One death from an unrelated cause.
There has been a male preponderance (65%) of Campylobacter PJI, with patients having a median age of 72 years (range, 24 to 88 years), and with cases relatively equally distributed between hip and knee prostheses. Seventy percent of patients with C. fetus PJI have been immunocompromised (three with liver cirrhosis, two each with chronic leukemia and rheumatoid arthritis on immunosuppressive therapy, and one each with lung cancer and renal transplant). Interestingly three patients with Campylobacter PJI (including our patient) were cattle farmers, suggesting zoonotic transmission. Onset of PJI following arthroplasty has been as short as 1 month (in a patient who had campylobacteriosis perioperatively, with positive blood and stool cultures) and as long as 9 years (median, 3 years). Among patients with available data, 53% (10/19) presented acutely, the remainder having more protracted symptoms, and 69% (9/13) reporting a diarrheal illness preceding their episode of PJI. Together, these data suggest that Campylobacter PJI likely arises following hematogenous seeding of the site of the prosthetic joint after a gastrointestinal illness, which may or may not be symptomatic. Of the 20 cases, 8 (40%) and 5 (25%) had positive blood and stool cultures, respectively, although results of these cultures were not obtained and/or not reported in all cases. The yield of stool cultures may be low for certain Campylobacter spp.: C. fetus and C. upsaliensis may be inhibited by cephalothin-containing Campylobacter selective media, and C. fetus may not grow well at the 42°C incubation temperature routinely used for isolation of C. jejuni (23). With the exception of our case, all reported cases of Campylobacter PJI have had positive cultures from the affected joint, including cultures of synovial fluid, bone, tissue, or wound drainage.
A variety of surgical strategies (including one- or two-stage resection arthroplasties or débridement, antibiotics, and implant retention [DAIR]) and antimicrobial regimens have been employed for the management of Campylobacter PJI, with most cases of C. fetus and C. jejuni PJIs treated with a combination of antimicrobials. Overall, the usage of the various antimicrobial classes has included the following: β-lactams (including β-lactam/β-lactam inhibitor combinations and carbapenems), 60%; aminoglycosides, 55%; macrolides, 45%; fluoroquinolones, 25%; clindamycin, 25%; and tetracyclines, 10%. Despite heterogeneous treatment, most cases have had a successful outcome, although the duration of follow-up has been variable (Table 1).
Five cases were managed with no surgery and seven with DAIR. Of these, one patient with Campylobacter lari PJI (19) managed with DAIR succumbed to sepsis on the second day of hospital admission, and a second patient with C. fetus PJI managed with antimicrobial agents alone died of an unrelated cause 2 months following presentation. While these numbers are too small to draw firm conclusions, it is interesting that the remaining 10 cases were successfully managed, with four patients (2 each managed with DAIR and no surgery) being maintained on chronic suppressive antimicrobial therapy.
Our case highlights several points. First, special growth requirements may preclude Campylobacter spp. from being routinely isolated. Thus, when there is a compatible clinical syndrome (i.e., preceding diarrhea), clinicians should alert the clinical microbiology laboratory to the possibility of Campylobacter infection so that appropriate culture media and incubation conditions are used. Studies on extra-articular specimens (e.g., blood and stool cultures, stool antigen testing, and PCR) may be useful adjuncts in diagnosing campylobacteriosis. Although early treatment of gastrointestinal disease may prevent hematogenous dissemination and subsequent PJI, antimicrobial agents can render cultures obtained for diagnosis of PJI negative. Recent Infectious Diseases Society of America (IDSA) guidelines (24) recommend avoiding antimicrobial agents if feasible or holding them for at least 2 weeks prior to collection of cultures for PJI diagnosis. It may not be possible to administer antimicrobial agents so as to idealize both scenarios.
Second, molecular testing, in this case using a real-time PCR assay on sonicate fluid, may be useful in defining the etiology of PJI. Arguably, the mere detection of bacterial DNA in sonicate fluid may not amount to definitive evidence for PJI (25), as DNA of urogenital and enteric pathogens (Chlamydia and Yersinia species, respectively) has been detected in synovial fluid of patients with reactive arthritis (26). However, our patient fulfilled the IDSA criteria for PJI (given gross purulence of synovial fluid and acute inflammation on histopathology) (24) and also had a concurrent stool culture positive for C. jejuni. Pre- and intraoperative cultures from his joint may have been rendered negative due to antecedent antimicrobial therapy. Thus, the positive cadF PCR in our patient corroborates a probable diagnosis of C. jejuni PJI. Nevertheless, it cannot be definitely concluded that C. jejuni was the cause of the PJI, since no viable isolate was recovered from the site of his prosthetic joint. Microorganisms associated with PJI are found in biofilms; thus, methods such as implant vortexing and sonication, which sample the prosthesis surface, provide improved sensitivity for PJI diagnosis compared to conventional periprosthetic tissue cultures (1). Molecular methods further improve the sensitivity of biofilm-directed diagnostic approaches. We recently compared results from a PCR panel of 10 individual PCR assays targeting (at the genus or group level) the most common bacteria that cause PJIs, performed on biofilms dislodged from explanted hip and knee arthroplasties, and found that the sensitivities of tissue culture, sonicate fluid culture, and sonicate PCR were 70.1, 72.9, and 77.1%, respectively (27). We have also investigated PCR-electrospray ionization mass spectrometry (28) and 16S rRNA gene real-time PCR (29) on sonicate fluid for the diagnosis of PJI and found both techniques to be at least as sensitive as (29) or superior to (28) culture-based methods, with improved turnaround time.
Finally, based on our review of the literature, we propose that clinicians promptly diagnose and probably treat campylobacteriosis and other enteric bacterial infections in patients with prosthetic joints, as their implants may be considered “locus minoris resistentiae” (30, 31). As illustrated in the report by Prendki et al. of two postoperative Campylobacter PJI cases occurring after recent gastroenteritis (9), consideration should be given to postponing elective arthroplasty surgery in patients who have had a recent episode of bacterial gastroenteritis. PJIs caused by non-Campylobacter enteric pathogens have included Yersinia enterocolitica (32–34), Salmonella species (over 20 cases reported) (35), and Clostridium difficile (36–39). Although current treatment recommendations for campylobacteriosis limit treatment to those with severe illness, protracted symptoms (>1 week), and the immunocompromised (40, 41), based on the findings reported herein, treatment might also be considered for those with prosthetic joints because patients with prosthetic joints may have a predilection to developing PJI after what may initially seem like an innocuous gastrointestinal illness. Future studies should address the risk of PJI in patient who have a prosthetic joint and an infection with a bacterial enteric pathogen, including Campylobacter species.
ACKNOWLEDGMENTS
Robin Patel is supported by research grants from the National Institutes of Health (R01 AR056647 and R01 AI91594).
Robin Patel has received research grant support from Pfizer, Pocared, Pradama, Astellas, 3M, and Tornier. She has patents for a pertussis PCR assay, an antibiofilm substance, and a method/device for sonication. She has relinquished her rights to receive royalties for the sonication device.
We thank Alain Meyer for providing further clinical details from a case he reported (15).
Footnotes
Published ahead of print 12 February 2014
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