Less Commonly Encountered Nonenteric Gram-Negative Bacilli

Less Commonly Encountered Nonenteric Gram-Negative Bacilli

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Commonly Encountered Nonenteric 151 Less Gram-Negative Bacilli Michael T. Brady and Amy Leber

MICROBIOLOGY AND EPIDEMIOLOGY Several genera of nonglucose-fermenting gram-negative rods are infrequent opportunistic human pathogens. As a group, most are nonfastidious, aerobic, catalase-positive organisms; motility, oxidase activity, and growth on MacConkey agar are variable. Those organisms that grow on

MacConkey agar typically produce colorless colonies. Identification of organisms has depended on phenotypic and biochemical characteristics. Matrix-assisted laser-desorption ionization–time of flight (MALDITOF) mass spectrometry has been used more recently.1–3 The utility of MALDI-TOF mass spectrometry improves as databases are expanded. Taxonomy continues to undergo significant changes based on DNA

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homology studies and 16S ribosomal RNA (rRNA) gene sequencing. The organisms are widely distributed in natural environments including plant material, soil, and water, as well as in the environment in healthcare facilities. Some species can colonize mammalian mucosal surfaces.1,2,4 In many ways, these organisms resemble Pseudomonas spp. including Pseudomonas aeruginosa. This chapter focuses on select taxonomic family groups not discussed in other chapters. Pseudomonadaceae.  Certain organisms in the family Pseudomonadaceae have been reclassified. An earlier classification scheme grouped the pseudomonads into 5 homology groups based on similarities in 16S rRNA gene sequence. At present, only the former members of rRNA homology group I are retained in the amended genus Pseudomonas. The most common Pseudomonas spp. isolated from human clinical specimens are the fluorescent pseudomonad group organisms, P. aeruginosa, P. putida, and P. fluorescens. P. stutzeri, P. mendocina, P. alcaligenes, P. pseudoalcaligenes, P. luteola, and P. oryzihabitans are isolated less frequently (see Chapter 154). Both P. luteola (formerly Chryseomonas luteola) and P. oryzihabitans (formerly Flavimonas oryzihabitans) are catalase-positive, oxidase-negative, motile, gram-negative bacilli that form yellow-pigmented, often wrinkled colonies on blood and MacConkey agar. The negative oxidase reaction of these organisms is unique among Pseudomonas spp. P. luteola can be differentiated from P. oryzihabitans on the basis of its ability to hydrolyze esculin and orthonitrophenyl-β-d-galactopyranoside.4 rRNA homology group II organisms now are designated Burkholderia spp., Ralstonia spp., Cupriavidus spp., Pandoraea spp., and related organisms in the family Burkholderiaceae; rRNA homology group III contains Comamonas spp., Delftia spp., and Acidovorax spp. in the family Comamonadaceae; rRNA homology group IV pseudomonads are now classified as Brevundimonas spp. in the family Caulobacteraceae; and rRNA homology group V pseudomonads are now Stenotrophomonas spp.1 Alcaligenaceae.  Both Achromobacter and Alcaligenes spp., along with the closely related Bordetella spp., currently are grouped together within the family Alcaligenaceae. The clinically relevant Achromobacter and Alcaligenes spp. include Alcaligenes faecalis, Achromobacter piechaudii, Achromobacter denitrificans, and Achromobacter xylosoxidans.2,5 The first 3 organisms listed are asaccharolytic and biochemically are similar to Bordetella spp. and Oligella ureolytica, also members of this family.6 Achromobacter xylosoxidans is saccharolytic and biochemically is similar to several organisms of uncertain taxonomic position, including Achromobacter groups B, E, and F and Ochrobactrum anthropi; the former Achromobacter groups A, C, and D are biovars of O. anthropi.7 Ochrobactrum spp. have been placed in the family Brucellaceae. The genus Oligella contains 2 species of clinical significance, O. urethralis and O. ureolytica.6 O. urethralis (formerly Moraxella urethralis) is nonmotile, shares several characteristics with Moraxella spp., and is thought to be a commensal of the genitourinary tract. O. ureolytica is motile and biochemically is similar to Bordetella bronchiseptica, including the property of rapid hydrolysis of urea. Caulobacteraceae.  Several Brevundimonas spp. have been named, but only B. diminuta and B. vesicularis are of human clinical significance. These species currently are placed in the family Caulobacteraceae. All these organisms are aerobic, oxidase-positive, motile, gram-negative bacilli that can be isolated in the laboratory on blood or chocolate agar; most but not all strains also grow on MacConkey agar. Some isolates produce a yellow or tan-brown pigment. Comamonadaceae.  Current members of the family Comamonadaceae include the following: Comamonas testosteroni and C. terrigena; Delftia acidovorans (formerly Comamonas acidovorans) and D. tsuruhatensis; and 3 Acidovorax spp.—A. facilis, A. delafieldii, and A. temperans. Flavobacteriaceae.  The family Flavobacteriaceae has undergone extensive revision and now contains many genera including Chryseobacterium, Elizabethkingia, Flavobacterium, Weeksella, Bergeyella, Empedobacter, and Myroides. Elizabethkingia meningoseptica (formerly Chryseobacterium meningosepticum and Flavobacterium meningosepticum) and Chryseobacterium indologenes are the most common human isolates of this group.1,2,5,6 E. meningosepticum produces large, smooth colonies on blood and chocolate agar within 24 hours, but most isolates do not grow on MacConkey agar. Gram stain of agar isolates reveals long, thin rods that can be filamentous. Isolates are encapsulated and produce proteolytic enzymes including elastase, a potential virulence factor. Ribotyping demonstrates heterogenicity among strains of E. meningoseptica.4

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Other Chryseobacterium spp. produce colonies of similar appearance; some produce yellow-pigmented colonies on blood agar, but pigment production may be negative or weak, except for the deep-yellow pigment produced by C. indologenes.1 Flavobacterium breve has been reclassified as Empedobacter brevis. Organisms formerly classified as F. odoratum are now classified as 2 distinct species, Myroides odoratus and M. odoratimimus. Weeksella zoohelcum has been reclassified as Bergeyella zoohelcum, and Weeksella virosa remains as the single species in the genus. Unlike the other flavobacteria that are environmental organisms, W. virosa and B. zoohelcum are found on mucosal surfaces of humans and other mammals.1,2,4,5 Colonies of W. virosa are mucoid, adherent to agar, and can develop a tan appearance, whereas colonies of B. zoohelcum can be sticky and tan in appearance. Useful tests to differentiate these organisms include the following: hydrolysis of gelatin, starch, and esculin; DNase and urease production; nitrate reduction; and susceptibility to penicillin and polymyxin B.1,2,4,5 Methylobacteriaceae.  Methylobacterium spp. and Roseomonas spp., members of the family Methylobacteriaceae, are oxidase positive and produce characteristic pink- or coral-pigmented colonies on a variety of media, including blood, Sabouraud, Thayer-Martin, and buffered charcoal–yeast extract agar. These are environmental organisms that also can be found in the healthcare environment. Colonies of Methylobacterium spp. generally appear dry, and Gram stain shows large, highly vacuolated, pleomorphic bacilli; growth on MacConkey agar at temperatures higher than 40°C usually is negative. In contrast, colonies of Roseomonas spp. are mucoid in culture and show nonvacuolated, coccoid bacilli on Gram stain; these organisms usually grow on MacConkey agar at temperatures up to 42°C.4 Rhizobiaceae.  Rhizobium spp. and Agrobacterium spp. are members of the family Rhizobiaceae and are natural inhabitants of soil and wellknown pathogens of plants. Rhizobium radiobacter (formerly Agrobacterium radiobacter and A. tumefaciens) is the only medically important species in the family.8 Colonies of the organism can appear mucoid and pink on MacConkey agar, resembling colonies of Klebsiella spp. Sphingomonadaceae.  The family Sphingomonadaceae contains numerous species, but only 2 species are considered to be of human clinical significance, Sphingomonas paucimobilis (formerly Pseudomonas paucimobilis) and S. parapaucimobilis. S. paucimobilis grows slowly and produces yellow colonies; however, in contrast to Sphingobacterium spp., most isolates of S. paucimobilis are urease negative and susceptible to polymyxin B.2 Sphingobacteriaceae.  The family Sphingobacteriaceae contains several former Flavobacterium spp., but only 2 species are considered of human clinical significance, Sphingobacterium multivorum and S. spiritivorum. Sphingobacterium spp. generally are yellow pigmented, urease positive, and resistant to polymyxin B; this last property is shared with Burkholderia spp., Chryseobacterium spp., and a few other genera of nonfermentative gram-negative bacilli.2 Shewanellaceae.  The genus Shewanella, family Shewanellaceae, has more than 20 species, but only S. putrefaciens and S. algae are thought to be of clinical importance. S. algae is a halophilic and asaccharolytic organism and thought to be the more common human isolate, whereas S. putrefaciens is nonhalophilic and saccharolytic and more commonly isolated from the environment. Among nonfermentative gram-negative bacilli, these organisms have the unique property of producing hydrogen sulfide in Kligler or triple sugar iron agar.2 Acetobacteraceae.  Acetic acid bacteria belonging to the family Acetobacteraceae have been associated with human infection relatively recently. Relevant clinical genera in this family include Asaia, Gluconobacter, and Granulibacter.2 These organisms oxidize alcohols or sugars, thus producing acetic acid. They are found in soil or associated with plants and have been used to convert wine to vinegar. Asaia spp. include a group of pink-pigmented gram-negative rods. Colonies are pale pink with scant to moderate growth on sheep blood agar, and they are oxidase negative. Relevant clinical species include A. bogorensis, A. lannensis and A. siamensis. Gluconobacter are gram-negative, catalase-positive, oxidase-negative rods. Granulibacter are oxidase-negative, coccobacillary, gram-negative rods.

CLINICAL MANIFESTATIONS AND TREATMENT As a group, these organisms are opportunistic pathogens that cause relatively few human infections. Most infections occur in people with

Less Commonly Encountered Nonenteric Gram-Negative Bacilli

underlying medical conditions or indwelling medical devices. For many organisms, no standardized methods are available for in vitro antimicrobial susceptibility testing or interpretation of results. Empiric management rests on clinical experience and published reports. In vitro testing should establish antimicrobial minimum inhibitory concentrations to guide definitive therapy. Disk diffusion testing can be unreliable. An in vitro test result of “resistant” indicates a likely treatment failure, but a result of “susceptible” may not predict treatment success. Device removal and surgical debridement when relevant are primary treatments.

Acidovorax, Brevundimonas, Comamonas, and Delftia Species Single cases of Acidovorax spp. bloodstream infection (BSI) and implanted port- or catheter-related infections have been reported.9,10 Brevundimonas vesicularis infections in children have included septic arthritis in a healthy toddler,11 as well as BSIs in a patient undergoing hemodialysis, in a child with sickle cell disease,12 and in 2 premature neonates.13,14 Infections with B. vesicularis in adults have included infective endocarditis,15 keratitis after laser surgical procedures,16 and BSIs following bone marrow transplantation,17 open heart surgery,18 and ambulatory peritoneal dialysis.19 B. vesicularis typically is susceptible to meropenem, piperacillintazobactam, and aminoglysosides.20 Susceptibility is less common for ceftazidime and trimethoprim-sulfamethoxazole.20 B. diminuta has been associated with BSI and vascular catheter infections primarily in patients with cancer, peritonitis associated with chronic ambulatory peritoneal dialysis, and cutaneous infections in immunocompetent people.19,21–22 Comomonas testosteroni and C. kerstersii infections commonly are polymicrobial and occur most often in the abdomen including following perforation of the appendix.23,24 C. testosteroni was reported to cause catheter-associated BSI, endocarditis, and meningitis in a patient with recurrent cholesteatoma.25–30 Delftia acidovorans has caused catheterassociated BSI, endocarditis associated with intravenous drug use, conjunctivitis, and otitis externa.31–34 Delftia tsuruhatensis has caused catheter-associated BSI.35 Antibiotic susceptibility of this group of organisms is variable, but most isolates are susceptible to broad-spectrum cephalosporins, carbapenems, and fluoroquinolones. B. diminuta, however, is intrinsically resistant to fluoroquinolones,21 and susceptibility to aminoglycosides is variable.

Achromobacter and Alcaligenes Species Achromobacter and Alcaligenes spp. are opportunistic human pathogens causing sporadic cases of pneumonia, septicemia, peritonitis, and urinary tract and other infections.36–39 Achromobacter xylosoxidans and Alcaligenes faecalis are the most common isolates and agents of disease, but little is known about factors promoting virulence. Whereas BSI, meningitis, and pneumonia are reported most commonly, sites of isolation also include peritoneal fluid in chronic ambulatory peritoneal dialysis, joint fluid, bone, and urine.36–40 Infections have been associated with contaminated medical supplies and devices, such as transducers, topical medications, nuclear medicine tracers, deionized water used for hemodialysis, and fluids from incubators and humidifiers.38,41,42 In patients with cancer, the gastrointestinal tract can be the source of infection.37 A. xylosoxidans has been recovered from blood and cerebrospinal fluid (CSF) of neonates with nosocomial infection, in maternal BSI, and from bone after penetrating nail injury in older children.36,38,42 Clinical illness resulting from A. xylosoxidans BSI is indistinguishable from that of other gram-negative bacilli.43 Intravascular catheters frequently are predisposing factors to infection, but neutropenia is not a major risk factor.37 A. xylosoxidans and A. faecalis can colonize the respiratory tract of intubated children and patients with cystic fibrosis.40,44 A. xylosoxidans is a “late colonizer” in up to 8.7% of patients with cystic fibrosis and can contribute to exacerbation of pulmonary disease.45,46 A. xylosoxidans has been reported to cause lymphadenitis in patients with chronic granulomatous disease and hyperimmunoglobulin M syndrome.47,48 The antimicrobial susceptibility pattern of these organisms is variable.37,49 Isolates of A. xylosoxidans and A. faecalis produce several types of β-lactamases that hydrolyze a variety of the penicillins and cephalosporins. Ceftazidime generally retains good in vitro activity against A. xylosoxidans; meropenem and trimethoprim-sulfamethoxazole

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typically also are active. Resistance to aminoglycosides and aztreonam is expected; activity of ureidopenicillins, ticarcillin−clavulanic acid, and the fluoroquinolones is variable. Monotherapy is probably sufficient in most cases of infection, but 2 agents may be required to eradicate the organism in patients with severe, deep-seated infections such as endocarditis. Removal of a contaminated venous catheter or other device often is necessary to clear infections.

Rhizobium radiobacter Virtually all reported cases of human infections with members of the Rhizobiaceae family are caused by Rhizobium radiobacter and have occurred in immunocompromised hosts or in patients with medical devices, especially central venous catheters (CVCs), chronic ambulatory peritoneal dialysis catheters, or implanted biomedical prostheses.50–58 The ability of this organism to adhere to silicone and other inert surfaces may explain these associations. Approximately 20% of cases of human infections have occurred in people ≤16 years of age. More than 50% of infections required antibiotic therapy and removal of the device for resolution. R. radiobacter also has caused native valve endocarditis and urinary tract infection.50–58 The antimicrobial susceptibility is variable, and many isolates are multiply resistant because of production of antibiotic-inactivating enzymes. Most strains are inhibited by ceftriaxone (but not ceftazidime), gentamicin (but not tobramycin), trimethoprim-sulfamethoxazole, piperacillin-tazobactam, ciprofloxacin, and carbapenems. Although R. radiobacter infections typically are of low virulence, variable antibiotic susceptibility and lack of optimal therapeutic regimens make them difficult to treat.50–52

Chryseobacterium, Elizabethkingia, Bergeyella, Weeksella, Myroides, and Empedobacter Species Members of the genera Chryseobacterium, Elizabethkingia, Bergeyella, Weeksella, Myroides, and Empedobacter spp., all once classified as Flavobacterium spp., are responsible for infrequent infections. Elizabethkingia (formerly Flavobacterium) meningoseptica is of greatest medical importance. Although recovered from patients with community-acquired infections, E. meningoseptica is most frequently an opportunistic nosocomial pathogen of infants ≤3 months of age, who account for >75% of reported cases.59,60 E. meningoseptica has caused numerous nursery outbreaks of infection, especially BSI and meningitis.61 Approximately one half of reported cases of meningitis caused by E. meningoseptica in neonates have occurred during nursery outbreaks.62 Outbreaks have been associated with contamination of solutions and equipment in the hospital environment, including containers of antiseptic solutions, vials of intravenous drugs, chlorinated water sources, and respiratory care equipment.62 Infants become colonized with E. meningoseptica in the nose, throat, or gastrointestinal tract before development of invasive infection. The clinical course of BSI or meningitis is similar to that of infection with other gram-negative bacilli; meningitis can have either an early or a late onset. The onset of disease can be insidious, and CSF evaluation can be unremarkable initially.61 The mortality rate of neonatal meningitis caused by E. meningoseptica is >50%, and survivors frequently have severe neurologic sequelae, including hydrocephalus. Development of hydrocephalus is significantly associated with administration of intrathecal antibiotics or positive CSF cultures for >10 days.61 E. meningoseptica rarely causes infection in immunocompetent children beyond the neonatal period, but infections in immunocompromised people occur as outbreaks in intensive care units or as isolated cases; >90% of cases are nosocomially acquired.60 Pneumonia is the most common infection, accounting for 40% of reported cases. The mortality rate in immunocompromised patients is >60%. Other reported E. meningoseptica infections include endocarditis, ophthalmologic infections, cellulitis, pyogenic arthritis related to an elbow joint prosthesis, abdominal abscesses, and burn wound sepsis.63,64 Prolonged antibiotic therapy may predispose patients to infection. Although Chryseobacterium indologenes is the most common human isolate within this group, recovery of the organism is not always associated with infection. C. indologenes primarily causes BSI in immunocompromised patients and in patients with indwelling intravascular devices,

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but it also has been implicated in cellulitis, bacteremia, pneumonia, meningitis, pyomyositis, and keratitis.65–69 Weeksella virosa is recovered primarily from urine and urogenital tract specimens, but its clinical significance is questioned. Bergeyella zoohelcum is an inhabitant of the oropharynx of dogs and cats and has been recovered in bite wound infections and in a case of meningitis that followed multiple bites.70–73 Bergeyella sp. was recovered from amniotic fluid of a mother delivering a preterm infant, but its significance was unclear.74 The 2 current Myroides spp., M. odoratus and M. odoratimimus, are uncommon human isolates from urine, respiratory tract, and rarely blood. Empedobacter brevis also is reported rarely as an agent of human disease. E. meningoseptica and other related species can be resistant to antimicrobial agents routinely prescribed for gram-negative infections including third- and fourth-generation cephalosporins, carbapenems, aztreonam, and the aminoglycosides. E. meningoseptica, however, may be susceptible in vitro to agents generally active against gram-positive organisms including rifampin, vancomycin, and clindamycin. Antibiotics with the most consistent in vitro activity against both E. meningoseptica and C. indologenes are minocycline, rifampin, and levofloxacin. Ciprofloxacin, trimethoprim-sulfamethoxazole, and piperacillin-tazobactam are less active.60,61,75–78 In vitro test results may not correlate with clinical efficacy. Both W. virosa and B. zoohelcum are susceptible to a wide variety of antimicrobial agents. Disk diffusion susceptibility testing of Chryseobacterium spp. and related agents can be unreliable.76,77 Optimal therapy for serious infections, including meningitis, caused by E. meningoseptica is not well established. Minimum inhibitory concentrations of vancomycin are high for almost all isolates. A study of 4 E. meningoseptica isolates recovered from neonatal CSF demonstrated synergy in vitro between vancomycin and rifampin in 3 of 4 isolates, as well as additive interaction between vancomycin and ciprofloxacin and antagonism between vancomycin and meropenem in all 4 isolates.79 High-dose vancomycin and rifampin may be the optimal therapy for management of central nervous system infections.79 Minocycline for patients ≥8 years of age, trimethoprim-sulfamethoxazole, or a fluoroquinolone is a treatment option, based on susceptibility testing, for infections outside the central nervous system.

Methylobacterium and Roseomonas Species Methylobacterium mesophilica and Roseomonas gilardii are the most frequently isolated species. Both organisms have been reported as agents of BSI, primarily in association with an indwelling CVC, hemodialysis catheter, and contaminated endoscope. Other reported infections include peritonitis related to chronic ambulatory peritoneal dialysis, septic arthritis, endophthalmitis, cellulitis, bacteremia, keratitis, ventilatorassociated pneumonia, and urinary tract infection.80–90 These organisms generally are susceptible to carbapenems, aminoglycosides, tetracycline, and fluoroquinolones.91–93 Roseomonas mucosa strains typically are more resistant than are strains of R. gilardii.

Ochrobactrum Species Ochrobactrum anthropi is the most common Ochrobactrum sp. causing disease. O. anthropi colonizes the respiratory tract and wounds and subsequently can cause a variety of opportunistic infections including CVC-associated BSI, prosthetic valve endocarditis, septic arthritis, osteomyelitis, peritonitis, BSI, and meningitis.52,94–110 Other Ochrobactrum spp. including O. haematophilum and O. pseudogrignonense have been isolated rarely from human clinical specimens.111 The closely related Achromobacter-like groups B, E, and F organisms have been recovered most commonly from blood cultures of patients with CVCs.112 Most isolates of these Achromobacter-like groups and O. anthropi are susceptible to aminoglycosides, carbapenems, fluoroquinolones, and trimethoprim-sulfamethoxazole.113

Oligella Species The 2 Oligella spp. of clinical significance, O. urethralis and O. ureolytica, have been recovered primarily from the urogenital tract and rarely as agents of urosepsis or pyogenic arthritis.114,115 O. urethralis has an antibiotic susceptibility pattern similar to that of Moraxella spp. Antibiotic susceptibility of O. ureolytica is variable.

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Pseudomonas luteola and Pseudomonas oryzihabitans Both P. luteola and P. oryzihabitans are found in natural environments such as soil, water, and damp environments including rice paddies, as well as in the hospital environment in sinks and respiratory therapy equipment. Infections with both organisms are found most commonly in patients with medical devices or immunosuppressive conditions,116–121 and they include osteomyelitis, peritonitis, endocarditis, meningitis after a neurologic procedure, leg ulcer in a patient with sickle cell disease, endophthalmitis following cataract operation, polymicrobial BSI, cellulitis, abscesses, and wound infections.122–129 Published data are insufficient to recommend treatment regimens. P. luteola and P. oryzihabitans are susceptible to most extended-spectrum penicillins, third-generation cephalosporins, fluoroquinolones, and aminoglycosides, but they usually are resistant to ampicillin and first- and second-generation cephalosporins.116–119 Because of the low virulence of P. oryzihabitans, patients can recover spontaneously from infection after removal of foreign material.121

Sphingobacterium, Sphingomonas, and Shewanella Species Sphingobacterium multivorum and S. spiritivorum are the most commonly recovered species from clinical specimens, usually from blood and urine. Isolates generally are resistant to the aminoglycosides and polymyxins, are susceptible to fluoroquinolones and trimethoprim-sulfamethoxazole, and have variable susceptibility to β-lactam agents.130–132 Sphingomonas paucimobilis and other Sphingomonas spp. have been recovered from blood, CSF, urine and urogenital sites, and wounds; these organisms have caused sporadic or community-acquired infections including BSI, osteomyelitis, pyogenic arthritis, meningitis, urinary tract infection, and wound infection.133–139 Infections follow acquisition from the environment or nosocomially from contaminated fluids or equipment.129–131 A single case of BSI caused by S. mucosissima in a patient with sickle cell disease was reported.139 Most isolates are susceptible to aminoglycosides, fluoroquinolones, and trimethoprim-sulfamethoxazole; susceptibility to β-lactam agents is variable.134 Shewanella algae and S. putrefaciens have clinical importance. Shewanella spp. have been recovered in association with BSI, CVC-associated BSI, ventilator-associated pneumonia, tonsillitis, cerebellar abscess, ventriculoperitoneal shunt infection, peritonitis, osteomyelitis, pyogenic arthritis, and external ear and skin and soft tissue infections following trauma.140–151 These organisms generally are susceptible to a wide variety of antimicrobial agents, except for first-generation penicillins and cephalosporins.140–151

Granulibacter, Asaia, and Gluconobacter Species A few acetic acid bacteria have been reported to cause human infections. Granulibacter bethesdensis can cause fever and necrotizing lymphadenitis in patients with chronic granulomatous disease.152,153 Biopsy can reveal necrotizing granulomatous inflammation, negative Gram stain but growth within 3 weeks on Middlebrook 7HII, buffered charcoal–yeast extract, or fungal media. These reported infections required surgical treatment and prolonged antimicrobial therapy for resolution,152 and recurrence or relapse is possible. Granulibacter organisms typically are multiresistant. Susceptibility testing is difficult because of poor growth. Ceftriaxone, aminoglycosides, doxycycline, and trimethoprim-sulfamethoxazole can be active against these organisms in vitro. Ceftriaxone may be the preferred agent.152 G. bethesdensis has been shown to persist in monocytes in patients with chronic granulomatous disease as a result of resistance to oxygen-independent microbicides in monocytes; this organism requires intact reduced nicotinamide adenine dinucleotide phosphate (NADPH) oxidase for clearance.154 Infections with Asaia spp. primarily have consisted of catheterassociated BSI, peritonitis related to peritoneal dialysis, and BSI in an intravenous drug user.155–158 Identification in clinical specimens usually requires 165 rRNA gene sequence analysis. Antimicrobial therapy and catheter removal have been successful as treatment. Asaia spp. are multidrug resistant, with susceptibility in reported cases limited to tobramycin and tetracyclines.

Key Points: Diagnosis and Management of Less Commonly Encountered Nonenteric Gram-Negative Bacilli MICROBIOLOGY

DIAGNOSIS

• Nonglucose-fermenting nonenteric gram-negative rods • Nonfastidious, aerobic, and catalase-positive organisms • Motility, oxidase activity, and growth on MacConkey agar variable

• Organisms recoverable by standard culture methods • Antibiotic resistance testing required because of the considerable strain susceptibility variation

EPIDEMIOLOGY

TREATMENT

• Environmental organisms (plant material, soil, water, and healthcare facilities) that rarely cause infections in normal hosts • Some species able to colonize mammalian mucosal surfaces

• Empiric antimicrobial treatment should include agents with broad spectrum activity against gram-negative bacilli. • Definitive therapy is based on antimicrobial susceptibility test results.

CLINICAL MANIFESTATIONS • Commonly associated with indwelling devices • May be present in respiratory samples taken from patients with cystic fibrosis during respiratory exacerbations; but role frequently is unclear

Acetic acid bacteria such as Gluconobacter, Acetobacter, and Asaia spp. have been isolated from sputum of patients with cystic fibrosis, in whom a liquid acidic environment likely is relevant.99,159 The role of these bacteria in clinical symptoms is unclear. Association with intravenous drug abuse may reflect the use of acidic substances (vinegar or lemon juice) to dilute heroin and the possible contamination of compounds used.158–162 All references are available online at www.expertconsult.com.

KEY REFERENCES 1. LiPuma JJ, Currie BJ, Peacock SJ, Vandamme PA. Burkholderia, Stenotrophomonas, Ralstonia, Cuprividus, Pandoraea, Brevundimonas, Comamonas, Delftia, and Acidovorax. In: Jorgensen JH, Pfaller MA, Carroll KC, et al. (eds) Manual of Clinical Microbiology, 11th ed. Washington, DC, ASM Press, 2015, pp 791–812.

2. Vaneechoutte M, Nemic A, Kampfer P, et al. Acinetobacter, Chryseobacterium, Moraxella, and other nonfermentative gram-negative rods. In: Jorgensen JH, Pfaller MA, Carroll KC, et al. (eds) Manual of Clinical Microbiology, 11th ed. Washington, DC, ASM Press, 2015, pp 813–837. 47. Kanellopoulou M, Pournaras S, Iglezos H, et al. Persistent colonization of nine cystic fibrosis patients with an Achromobacter (Alcaligenes) xylosoxidans clone. Eur J Clin Microbiol Infect Dis 2004;23:335–339. 84. Sanders JW, Martin JW, Hooke M, Hooke J. Methylobacterium mesophilicum infection: case report and literature review of an unusual opportunistic pathogen. Clin Infect Dis 2000;30:936–938. 88. Shokar NK, Shokar GS, Islam J, Cass AR. Roseomonas gilardii infection: case report and review. J Clin Microbiol 2002;40:4789–4791.

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REFERENCES 1. LiPuma JJ, Currie BJ, Peacock SJ, Vandamme PA. Burkholderia, Stenotrophomonas, Ralstonia, Cuprividus, Pandoraea, Brevundimonas, Comamonas, Delftia, and Acidovorax. In: Jorgensen JH, Pfaller MA, Carroll KC, et al. (eds) Manual of Clinical Microbiology, 11 th ed. Washington, DC, ASM Press, 2015, pp 791–812. 2. Vaneechoutte M, Nemic A, Kampfer P, et al. Acinetobacter, Chryseobacterium, Moraxella, and other nonfermentative gram-negative rods. In: Jorgensen JH, Pfaller MA, Carroll KC, et al. (eds) Manual of Clinical Microbiology, 11th ed. Washington, DC, ASM Press, 2015, pp 813–837. 3. Marko DC, Saffert RT, Cunningham SA, et al. Evaluation of the Bruker Biotyper and Vitek MS matrix-assisted laser desorption ionization-time of flight mass spectrometry systems for identification of nonfermenting gram-negative bacilli isolated from cultures from cystic fibrosis patients. J Clin Microbiol 2012;50:2034–2039. 4. Winn W, Allen SD, Janda WM, et al. 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