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Rhodococcus equi infections Patricia Muñoz M.D., Ph.D., Pablo Martín Rabadán, M.D., Emilio Bouza M.D., Ph.D.
GENERAL DESCRIPTION Rhodococcus equi infections have increased in the last years, mainly in immunocompromised patients (33, 85). Although they are particularly frequent in HIV infected patients (60, 112), they have also been described in hematological patients (2, 4, 21, 24, 30, 87, 95, 134, 135), patients with renal failure (20, 142), alcoholism (81), lung cancer (146), rheumatoid arthritis (88, 140), sarcoidosis (62), in transplant recipients (100) and even in previously healthy patients (42, 73). The most common way of infection is the airborne route (112), although it can also be acquired orally or by direct inoculation (85, 141). Dissemination from an initial site (usually the lung) has been found to be the origin of abscesses throughout the body (CNS, skin, paraspinal, bone, kidney, etc) (106, 119, 127). Diagnosis may be difficult to establish for Microbiological laboratories, and the awareness of possible mistakes in the recognition of this pathogen will contribute to a more frequent report of cases (85). Rhodococcus equi is an intracellular microorganism and its eradication requires long-term combined antimicrobial therapy and sometimes, surgical excision (33). Finally, the recent introduction of highly efficacious antiretroviral therapy in HIV positive patients (HAART) is clearly contributing to the reduction of the incidence of this infection (125). Microbiology Guided Medline Search Confirmation of infection can only be made by isolating the microorganism from clinical samples. Rhodococcus (red coccus) equi is an aerobic pleomorphic saprophyte coccobacillus that grows as mucoid, salmon-pink, colonies within 24 to 72 hours. If cultured in non-selective media, the microorganism may be overlooked or regarded as a non-pathogenic "diphtheroid" or as a saprophytic coccus (90). The use of selective culture plates such as colistine-nalidixic agar (CNA), phenyl-ethanol agar (PEA), NANAT agar or Ceftazidime-novobiocin agar, incubated aerobically at 37ºC for up to seven days may facilitate the isolation of R. equi in contaminated samples (148, 152, 154). In addition, R. equi may be mistaken as Mycobacterium species due to its partially acid-fast nature, especially on clinical samples. It can be distinguished from some mycobacterial species by the 14-day arylsulfatase test, as Rhodococcus is negative for this reaction. For all the above-mentioned reasons, the real incidence of the disease may be underestimated (56, 85, 112, 127). Regarding the susceptibility tests, the microdilution method, the disk diffusion test and the E test can provide useful results as far as the inoculum is standardized (143). However, no standard breakpoints are available. Epidemiology Guided Medline Search R. equi is a widespread organism in soil and in herbivore manure (12, 54). It is a well-known cause of lung infection in foals, and also causes submandibular adenitis in swine. Infections in other animals including calves, sheep, goats, dogs and cats have been described. In humans the route of infection is thought to be inhalation or ingestion of the microorganisms. The exposure to farm dust, animals or manure can be elicited in less than one half to up to two thirds of cases (9, 42, 49, 60, 73, 112, 127, 146), and it is less common in HIV positive patients (45% vs. 20%) (60). In 6 out of 24 cases pneumonia was acquired by HIV patients who shared room with R. equi infected patients, raising the concern of human-to-human transmission (9). Traumatic inoculation or superinfection of wounds can also lead to infection (145). The first human case was reported in 1967 in a patient receiving high dose corticosteroids (53). The first cases of R. equi pneumonia in HIV-infected patients were reported in 1986 and 87 (88, 121). Between 1967 and 1996, 115 cases of infection caused by R. equi have been published (39, 40, 60, 104) and 63 more since then (1-3, 5, 10, 11, 16, 19, 22, 23, 25, 29, 37, 41, 44, 46, 49, 55-57, 59, 61, 66, 67, 73, 75-80, 84, 87, 89, 91-93, 97, 99-102, 108, 120, 123, 124, 128, 130-132, 136, 138, 141, 144, 145, 147). In a review of 72 cases in humans, published in 1991, 86% of the patients were immunocompromised with half of those occurring in patients infected by HIV (146). More recently, a review of 72 cases in HIV positive patients was published (23). Therefore, at present the total number of R. equi human infections described is roughly around two hundred cases. Clinical Manifestations Guided Medline Search Pneumonia is the most common manifestation of R. equi infection in immunocompromised patients (23, 33, 112, 146). More than 80% of reported patients had fever and cough as presenting symptoms. Pleuritic chest pain and hemoptysis was reported in approximately 35 and 15% respectively (23). R. equi bacteremia was found in approximately one half of HIV infected patients (9, 146). Complications include the development of pleural effusion (81), endobronchial lesions (129), a pseudotumoral presentation (15, 36), cardiac tamponade (82), pneumothorax (146) or mediastinitis (25). Clinical experience and animal models have shown that clearance of R. equi is impaired in the immunocompromised host and relapses are common despite maintenance antibiotic therapy. Before HAART was available, relapses of pneumonia were described in up to 82% of cases of HIV infected patients (9). There is no published experience on the evolution of R. equi infections in HIV + patients after immune-restoration; our personal impression is that we are witnessing a sharp decrease in the incidence of R. equi infection in this particular population. Extra pulmonary disease, especially organ abscesses, has been also reported. They may be diagnosed with the initial pneumonia or during the relapses. Central nervous system abscess is the most common extra pulmonary presentation of relapsing infection (146), this complication seems especially frequent in patients with multiple relapses. In nearly all reported cases there was a concomitant or previous lung infection due to this organism (9, 47, 59, 82, 107, 108, 133, 146). Pericarditis (82), meningitis (110), mastoiditis (67, 75, 86), abscesses in the liver (82), spleen (14), kidney (133), thyroid (93), iliopsoas muscle (45), bone (46, 106) subcutaneous tissue (9), foot mycetoma (8) and adenitis (29, 45) have been observed in HIV positive patients. Intestinal involvement is known to occur in horses and it has been reported in an HIV + patient with disseminated R. equi infection and chronic diarrhea; patient’s colonoscopy revealed multiple polipoid inflammatory lesions infiltrated with R. equi (59, 141). Co-infection by R. equi and other pathogens have been occasionally found (45). The chest X rays in 102 cases of lung infection (9, 23) revealed cavities (usually single) in 73 cases, consolidation or infiltrates in 34 cases, and pleural effusions in 11. Some patients have more than one type of lesion and in some cases an interstitial pattern preceded the development of consolidation or cavity formation. In a series of 78 cases of lung cavitation identified in 73 HIV + patients, R. equi was responsible of 6 out of 69 cases (8.6%) with microbiological results, after Mycobacterium tuberculosis, Pneumocystis carinii, Pseudomonas aeruginosa, and Staphylococcus aureus (116). If patients with CD4 count above 200 and the intravenous drug users with cavitating pneumonia secondary to endocarditis were excluded from this series, R. equi accounted for approximately 10% of cases of cavitary pneumonia. Cavities usually have thick walls and sometimes an air-fluid level may be identified (151). Other presentations include mediastinal enlargement, or pulmonary nodules (151). CT scan is recommended in most patients with R. equi pneumonia to better define the extension of the disease. Laboratory Diagnosis Guided Medline Search The efficacy of sputum samples for establishing the etiological diagnosis relies on the quality of the sample (40, 41, 149) and it is usually higher in HIV positive patients. Invasive techniques may be needed (33). Blood cultures are positive in a large proportion of HIV positive patients, in a third of HIV negative patients and in 25% of solid organ recipients (40, 60, 149). Other useful samples include pleural, peritoneal or articular fluids, abscess aspirations, skin or soft tissue biopsies, lymph nodes, feces, urine or autopsy samples (60, 96, 112). Histology usually reveals a necrotizing granulomatous reaction with macrophages, neutrophils, and intracellular gram-positive organisms. Malakoplakia (sometimes spelled as malacoplakia) is an unusual inflammatory condition that usually affects the lower urinary tract and is associated with an impaired processing of microorganisms within histiocytes. Histopathologically it is characterized by accumulations of benign macrophages associated with diagnostic intracellular and extracellular calcospherites, termed Michaelis-Gutmann bodies. Lung malakoplakia is an especially rare condition with only 24 reported cases included in a 1997 review. Eighteen out of this 24 had R. equi pneumonia and 14 out of 15 were HIV positive (79). The diagnosis can be determined on biopsies, bronchial washes, bronchial aspirates or brush cytology specimens. This disease should be considered when a R. equi pneumonia persists after several months of antibiotic treatment. Pathogenesis Guided Medline Search R. equi is a facultative intracellular pathogen that infects macrophages and survives inside the lysosomes. It has a complex cell wall which contains glucosamine, muramic acid, glutamic acid and alanine (like that of Nocardia and Mycobacterium), is thought to prevent phagosome-lysosome fusion, resist the oxidative burst and cause a nonspecific degranulation of lysosomes, thereby allowing intra-histiocytic survival and chronic infection. Cortisone and cyclophosphamide impair the pulmonary clearance of R. equi (18).
SUSCEPTIBILITY IN VITRO AND IN VIVO Guided Medline Search In Vitro and In Vivo Due to the low incidence of this disease no comparative studies on antimicrobial treatment have been conducted. Present day therapeutic recommendations are based on expert opinions guided by in vitro susceptibility tests, pharmacodynamic and pharmacokinetic considerations, clinical experience on animals, experimental infection models, and rather anecdotal clinical experience in humans. Single Drug There is neither consensus nor NCCLS guidelines on the antibiotic breakpoints to be used with Rhodococcus spp isolates. The information available is based on very few number of isolates (Table 1), different laboratory procedures and different personal interpretations (9, 32, 65). Overall, similar susceptibility patterns have been found both in human and animal isolates. The interpretation of those results must take in account not only the concentration that the antimicrobials reach in serum but its penetration into the lysosomes, and the antimicrobial activity at the low pH and PO2 conditions present in this ecological niche. Furthermore, it is not clear if the intra-lysosomal survival mechanisms of Rhodococcus, in the absence of an adequate immune response, significantly modify the activity of the antimicrobials accessing the site. In a recent study performed by the CDC with 107 strains, recovered during a 17-year period, 50% of the isolates were resistant to b-lactams and clindamycin (96). Vancomycin, imipenem, erythromycin, rifampin, tetracyclines and cotrimoxazole showed an excellent in vitro activity (less than 5% resistance rate) and ciprofloxacin showed 16% of resistance. The authors found different results within different antimicrobials of the same family, so results should not be extrapolated to non-tested drugs (105). The in vitro activity of teicoplanin, meropenem and the aminoglycosides is very good (70, 72, 103). Linezolid, a new oxazolidinone antimicrobial, showed an MIC90 of 2,0 mg/mL (17). The only bactericidal drugs against R. equi were the glycopeptides, aminoglycosides, sparfloxacin, and ciprofloxacin, although this has not been confirmed in other studies (105). Combination Drugs As determined by fractional inhibitory concentration indices, four combinations were synergistic: rifampin-erythromycin, rifampin-minocycline, erythromycin-minocycline and imipenem-amikacin. However, no antibiotic combinations were synergistic with the time-kill kinetic method in one study (105). In another report, using time-kill studies of a single strain, an additive effect was observed between rifampin plus imipenem or azithromycin. Indifference was observed for the combination of vancomycin and rifampin. In vitro antagonism was demonstrated with the combination of levofloxacin and rifampin (77). In this same study, antagonism was observed with levofloxacin and azithromycin independent of the dose of levofloxacin used. There was no apparent difference in the killing rate between levofloxacin at 1 g once/day or 500 mg once/day dose. The combination of gentamicin with rifampin or erythromycin has been found antagonistic by other authors (113, 146). Studies with other bacterial genus have frequently demonstrated in vitro antagonism between clindamycin and erythromycin, probably as result of competition for the target site in the bacterial ribosome. The combination of macrolides and aminoglycosides have been found useful probably due to the fact that aminoglycosides act against the extracellular compartment and macrolides against the intracellular one (48). Animal Studies: Animal models may be more accurate than in-vitro data to analyze antimicrobial activity of single drugs and combination therapy against Rhodococcus isolates. A nude mice model of R. equi infection was established to compare the antimicrobial activity of amikacin, ciprofloxacin, erythromycin, imipenem, minocycline, rifampin and vancomycin, alone and in combination (103). Therapy was started 4 days after animals had being challenged with an intravenous suspension of one strain of R. equi. The end point of the study was the reduction in bacterial load in lung and spleen tissues after 4 or 11 days of treatment. Untreated controls were unable to clear the infection. Vancomycin, imipenem, and rifampin were the most effective agents as single therapy, while amikacin, ciprofloxacin, erythromycin, and minocycline alone were not active. The most active therapies (in descending order) were vancomycin plus rifampin, vancomycin plus imipenem, vancomycin, amikacin plus imipenem, imipenem, rifampin plus erythromycin and rifampin plus minocycline. Imipenem-resistant and amikacin-resistant mutants were detected during the treatment and also in the untreated control group. In this animal model R. equi eradication was not analyzed as an endpoint. The high activity of vancomycin may have been enhanced by the presence of a high number of extracellular bacteria. Veterinary Clinical Experience: The combination of erythromycin (25 mg/kg three times daily) and rifampin (5 mg/kg twice daily) has been used on foals since 1981 and has been considered the therapy of choice since then (63, 114). The selection was made because both drugs are lipid-soluble antibiotics capable of intracellular penetration with synergistic activity. The success of this therapy in foals has been analyzed in non-randomized studies. In a review of R. equi pneumonia in foals 20 out of 48 foals survived and 28 died or were euthanized. Thirteen of the 20 surviving foals were treated with erythromycin and/or rifampin. A decline in mortality rate was observed with the introduction of the combination of erythromycin and rifampin. None of the 17 foals treated with penicillin and gentamicin survived (137).
ANTIMICROBIAL THERAPY Smart search Drug of Choice Guided Medline Search Probably due to the absence of clear therapeutical guidelines, virtually every imaginable combination has been used (Table 2 and 3). Monotherapy was ineffective in a number of cases and is not recommended. Combinations of two or three antimicrobial agents have been usually prescribed.
The use of bactericidal drugs with extracellular activity (to reduce the
bacterial load) followed by or in combination with drugs with intracellular
activity such as Initial therapy must usually deal with a high bacterial load and frequent bacteremia, so the combination of at least two parenteral drugs with bactericidal activity is recommended. In immunocompromised patients it should include vancomycin or teicoplanin, probably in combination with imipenem (31, 33, 117). The addition of an aminoglycoside may be considered in severe cases. This parenteral therapy should be maintained during at least three weeks (33). After initial recovery (2-4 weeks), drugs with good intracellular penetration and with oral absorption are warranted and combinations including macrolides and rifampin are preferred (31, 146). Arlotti et al., recommend erythromycin plus rifampin as first choice therapy at this stage, with alternatives such as erythromycin plus ciprofloxacin, or rifampin plus ciprofloxacin (9). Azithromycin is also a promising combination due to its high tissue levels (58, 64, 69). Oral therapy should be administered for at least two months. Excision of infected tissue may be considered for refractory cases. For long-term suppressive therapy a macrolide plus rifampin is generally recommended. An effective alternative to rifampin can be a quinolone or doxycycline. Serial cultures of respiratory samples and feces to detect R. equi may be used to document persistence of infection and development of resistance. If possible, correction of underlying risk factors is warranted (112). Special Infection Guided Medline Search Very few cases of Rhodococcus equi meningitis have been described (38, 94, 110, 128, 145). Of the four cases, reviewed by DeMarais et al, only one was a patient with AIDS, and the remaining 3 did not have an underlying immunodeficiency. One patient who developed meningitis after head trauma and shunt placement was unsuccessfully treated with vancomycin and rifampin, and finally responded to levofloxacin (500 mg iv twice a day) and shunt removal. (128). No cases of endocarditis have been described. Underlying Diseases Outcome is related to host immune status and adherence to therapy. Infections are typically cured in immunocompetent hosts in contrast to relapses and chronic disease seen in the immunocompromised, especially in the first few weeks after discontinuation of suppressive therapy. Published prognostic data is available for AIDS patients, prior to the advent of potent anti-retroviral therapy. In a series of 12 cases, complete recovery (clinical, radiological and microbiological) was observed in 2/12 patients and clinical response (resolution of the signs reported on presentation) in 9/12 cases; the remaining case died within 2 weeks, without signs of improvement. The overall mortality was 58 %, with a mean survival time of 5.75 months (range 0-17 months) (40). In a series of 22 AIDS patients with follow-up data, the mean survival time was 11.4 months (range 2-24). R equi infection was considered the main cause of death in 7 of 20 fatal cases (9). In HIV positive patients, oral suppressive therapy may need to be continued for life, or at least until immune-restoration. (60, 146). However, since the advent of HAART, an impressive improvement in the prognosis of opportunistic infections has been observed in this population and will probably make unnecessary the administration of chronic suppressive therapy (5, 125). Regarding interactions, the use of rifampin is not recommended in patients receiving protease inhibitors in whom rifabutin (at half dose) is preferred. In the case of solid organ transplant recipients on cyclosporine A, rifampin should be avoided due to the risk of inducing allograft rejection due to subtherapeutic serum levels of cyclosporine A. Interaction between rifampin and methadone has also been described. Aminoglycosides should be used with precaution due to potential synergic nephrotoxicity. Alternative Therapy Guided Medline Search Most treatment options used for human therapy are summarized in tables 2 and 3. Most of them include some of the following drugs. Trimethoprim-sulfamethoxazole, used as prophylaxis of Pneumocystis carinii infection, does not seem to prevent R. equi pneumonia (4, 28) and has also been found ineffective as treatment (126). Development of resistance has been documented in humans and in horses after monotherapy with quinolones or rifampin or after prolonged two-drug combination therapy (31, 74, 118, 139). Low-level rifampin resistance has been found to be due to antibiotic inactivation (6).
Quinolones have been included as part of the multidrug therapy, but its
contribution to the patient outcome is unclear. Ciprofloxacin MICs are close
to the breakpoint for susceptibility, and, although it penetrates
intracellularly, it is only useful in some intracellular infections (such as
legionellosis) but not in others (such as brucellosis). In one case, oral
therapy failed to prevent relapse, while parenteral ciprofloxacin plus i The use of β-lactams is generally not recommended. Most authors consider that the MICs to penicillin ampicillin and cefalosporins are too high to be regarded as susceptible, and the susceptibility may decrease during therapy. In spite of this, some patients have improved with cefotaxime therapy (110). The presence of b-lactamasees has not been described in R. equi, therefore the use of a b-lactamase inhibitor such as clavulanate, sulbactam or tazobactam is not justified.
I The aminoglycosides have been successfully used in combination with bacterial wall-active antibiotics such as beta-lactams and glycopeptides in many infections including a few R. equi infections. Clindamycin has probably no place in the treatment of R. equi infections. It has failed as monotherapy and has been used with limited success in association with other antimicrobials.
(Printable Version of
Antimicrobial Therapy for
ADJUNCTIVE THERAPY Guided Medline Search Lobectomy has been employed in a number of patients when poor clinical improvement was noted after antibiotic therapy. There is no reliable data on the usefulness of this approach but it may not greatly increase the survival (9, 60). It may be considered a therapeutic option in patients with persistent immunocompromise and pneumonia refractory to prolonged antimicrobial therapy, large abscess or inflammatory pseudotumor. Drainage of empyemas and localized abscesses has been beneficial (112, 146).
ENDPOINTS FOR MONITORING THERAPY Guided Medline Search There are no clear guidelines on the duration of therapy. It probably should be individualized depending on the immunologic situation of the patient. Immunocompetent patients with R. equi pneumonia may recover completely with a short course of erythromycin while severely immunocompromised patients may relapse shortly after prolonged proper therapy is discontinued (146). As a general recommendation immunocompromised patients should receive 2 to 6 months of antibiotic therapy, or at least till cultures become negative and clinical symptoms disappear (71).
VACCINES Guided Medline Search No commercial vaccines are available.
PREVENTION OR INFECTION CONTROL MEASURES Guided Medline Search Smart search Rhodococcus equi may be isolated from soil, air and water. It has been recovered from schools and day-care centers (7). Although it can be considered a zoonosis, some authors recommend that considering the very low risk of transmission, pet contact should not be prohibited even to HIV infected patients (52). In the case of hematological patients, avoidance of exposure to domestic horses or their habitat during periods of aggressive chemotherapeutic administration seems reasonable, its efficacy has not been proven (134). Taking into account the cases of possible person-to-person transmission described, respiratory isolation of these patients is recommended if possible (9).
Table 1. Minimal Inhibitory Concentrations (MICs) of R. equi Strains+
Table 2.
Antimicrobial Therapies and Clinical Response in a Literature Review
Table 3.
Response to Maintenance Therapy
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