Transmission of Infection by Gastrointestinal Endoscopy and Bronchoscopy

Spurred in part by the acquired immunodeficiency syndrome (AIDS) epidemic, both health care workers and the lay public have become keenly interested in preventing the iatrogenic transmission of infections. Recently, reports of the transmission of infections via contaminated endoscopes have generated concern. We review the reported evidence of infections transmitted by flexible gastrointestinal and pulmonary endoscopes, the circumstances surrounding transmission of these infections, and recommended means to prevent such transmission. Methods We identified all relevant English-language articles published between 1966 and July 1992 through prominent review articles and a MEDLINE search (keywords: endoscopy, bronchoscopy, infections, transmission, and disinfection). We also manually searched bibliographies of identified articles to find additional sources. The entire search yielded 265 articles, all of which were reviewed in depth. General Considerations Flexible endoscopy is a common clinical procedure; an estimated 8.7 million gastrointestinal and 580 000 pulmonary flexible endoscopies were done in the United States in 1989 [1]. The risk for transmitting infections via these procedures depends on three factors: exposure of the endoscope to microorganisms, cleaning and disinfection procedures, and instrument design. Depending on the origin of the contaminating microorganisms, transmission of infection can be categorized as either patient-to-patient or environment-to-patient (Figure 1). During a procedure, an endoscope can be contaminated with whatever organisms are contained in patient secretions. Environmental contamination typically results from flushing or cleaning the endoscope with contaminated solutions. Whether contamination of the endoscope persists depends on the quantity and nature of the microorganisms. Some microbes are inherently more resistant to disinfectants (Figure 2), the efficacy of which depends on type, concentration, and duration of exposure. If patient material, such as blood, feces, or secretions, remains on or in the endoscope after cleaning, the effectiveness of subsequent disinfection diminishes. Figure 1. Nosocomial transmission of microorganisms via endoscopes. Figure 2. Resistance of microorganisms to disinfectants. Because endoscopes are made of fragile, heat-sensitive materials, they are routinely decontaminated by high-level disinfection, not sterilization [2]. Gastrointestinal endoscopes, with their multiple internal channels and valves (Figure 3), are more complex than the single-channeled bronchoscopes. In general, the more complex the instrument, the more crevices, joints, or surface pores there are and, hence, the more problematic cleaning and disinfection becomes [2]. Figure 3. Cross-section of typical gastrointestinal endoscope. Transmission of Specific Microorganisms Salmonella Infections Salmonella infections occur frequently in the United States; for example, more than 41 000 culture-positive patients were reported to the Centers for Disease Control (CDC) in 1989[3]. A chronic asymptomatic carrier state, defined by the continued fecal excretion of Salmonella organisms for more than 1 year, develops in approximately 3% of persons after S. typhi infection (typhoid fever) [4] and in fewer than 1% of persons after nontyphoidal Salmonella infection [5]. Both acutely infected persons and chronic carriers are thus potential sources of endoscopic contamination. Many disinfectants, including glutaraldehyde, phenolics, and iodophors, effectively kill salmonellae [2]. Transmission of Salmonella infections by endoscopy has occurred with many serotypes, including S. agona, S. kedougou, S. newport, S. oranienburg, S. oslo, S. typhi, and S. typhimurium [6-14]. Of the 84 patients reported to have developed such infections, 6 patients developed septicemia and 1 patient died. In most cases, the disinfectant (hexachlorophene, cetrimide, chlorhexidine, or quaternary ammonium compounds) used to clean the endoscopes had relatively little microbiocidal activity against salmonellae. In one outbreak, investigators identified inadequately disinfected colonic biopsy forceps as the source of infection [9]. Pseudomonas Infections Pseudomonas aeruginosa flourishes in warm, damp environments. Typical environmental reservoirs include respiratory equipment, sinks, and water bottles [15]. Most acute P. aeruginosa infections, which often involve the lungs, are nosocomially acquired. Among healthy adults, P. aeruginosa can colonize many body sites, as evidenced by isolation from throat (0% to 7%), sputum (2%), and stool (3% to 24%). Hospitalized patients, as well as patients with certain chronic lung diseases, have higher colonization rates [16]. Potential sources of endoscope contamination with Pseudomonas species thus include environmental reservoirs, acutely infected patients, and colonized patients. Like Salmonella species, P. aeruginosa is susceptible to glutaraldehyde, phenolics, and iodophors [2]. Most P. aeruginosa infections transmitted by endoscopy occurred after endoscopic retrograde cholangiopancreatography and resulted from environment-to-patient transfer of organisms. In all cases, the investigators isolated P. aeruginosa from some part of the endoscope. These infections resulted in bacteremia in 45 patients, of whom 4 died [17-26]. Most infections were caused by the use of an inadequate disinfectant [21, 22], contamination of an inner channel [18, 20], or incomplete drying of the endoscope channels before overnight storage [23, 26]. One epidemic, however, occurred despite the use of glutaraldehyde after each procedure and ceased only after replacement of the endoscope [19]. The first reports of bronchoscopic transmission of P. aeruginosa involved patients who developed Pseudomonas pneumonia [27, 28]. In a subsequent report, investigators cultured P. aeruginosa from the bronchoscopic washings of 11 patients; 1 patient, who was immunosuppressed, developed severe pneumonia [29]. The investigators isolated P. aeruginosa from the aspiration-irrigation channel of the bronchoscope, and the outbreak continued until they sterilized the bronchoscope with ethylene oxide. Mycobacteria Approximately 22 000 new cases of active tuberculosis occur in the United States each year [30], and an estimated 10 to 15 million persons carry Mycobacterium tuberculosis in its dormant phase [31]. After many years of decline, the incidence of tuberculosis in the United States began increasing dramatically in 1986 [30], predominantly because of an increasing number of cases in HIV-infected patients [32]. Infections with mycobacteria commonly found in the environment, such as M. avium-intracellulare complex, M. chelonae, and M. fortuitum, have also recently increased [33]. Unfortunately, studies determining the sensitivity of mycobacteria to various disinfectants are conflicting. In general, cetrimide, chlorhexidine, and iodophors are considered unreliable. Glutaraldehyde is widely accepted as a mycobactericidal agent, but the time required for disinfection remains undefined [34-36]. In the first reports of the bronchoscopic transmission of M. tuberculosis, the investigators, who disinfected the bronchoscopes with iodophor, advocated using a more effective disinfectant such as glutaraldehyde [37, 38]. In three subsequent cases, the patients developed clinically apparent M. tuberculosis infection despite rigorous cleaning and disinfection of the bronchoscope; the suction valve, with its spring-operated sleeve, seemed the most likely source of contamination [39]. The investigators tested this hypothesis by contaminating bronchoscopes with M. fortuitum; after they routinely cleaned and disinfected the instrument, M. fortuitum remained in all valves. Among other mycobacteria, M. chelonae has most commonly been associated with endoscopic transmission. In a large outbreak, M. chelonae was isolated from bronchial washings, brushings, or sputum in 72 patients [40]. Two patients developed clinical disease and one patient died. After recognizing the outbreak, the investigators changed from glutaraldehyde disinfection of the bronchoscopes to ethylene oxide sterilization. Nevertheless, they continued to isolate M. chelonae from clinical specimens until they discovered punctured suction channels in two of the bronchoscopes; M. chelonae was isolated from slimy material in the interior of both instruments. Hepatitis B Virus On average, more than 300 000 cases of primary hepatitis B virus (HBV) occur each year in the United States [41], and approximately 5% to 10% of patients develop persistent HBV infection. The estimated number of chronic HBV carriers in the United States ranges from 750 000 to 1 000 000 [42]. In infected persons, hepatitis B surface antigen (HBsAg) has been found in various body fluids, including serum, feces, bile, and saliva [43]. The inability to culture HBV has limited the evaluations of its environmental stability and its susceptibility to disinfectants. Alternative approaches include measuring the presence of HBsAg or inoculating chimpanzees. A study in chimpanzees showed that HBV-contaminated inanimate objects, if not properly cleaned and disinfected, can harbor and transmit the virus for up to 1 week [44]. Most of the commonly used disinfectant and sterilization procedures, however, inactivate HBV [45, 46]. Two studies have shown the potential for the endoscopic transmission of HBV. In one study, iodophor-isopropyl alcohol removed HBsAg from surfaces of endoscopes used in four HBsAg-positive patients, but not from the cytology brushes or biopsy forceps [47]. In the other study, an endoscope and a biopsy forceps were immersed for 15 minutes in gastric juice containing 1.0% serum and Iodine-125-HBsAg, and, despite subsequent disinfection with chlorhexidine and cetrimide for 15 to 20 minutes, they were both positive for Iodine-125-HBsAg [48]. One group of investigators documented the endoscopic transmission of HB