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Pantoea Agglomerans: a Mysterious Bacterium of Evil and Good

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Pantoea Agglomerans: a Mysterious Bacterium of Evil and Good Annals of Agricultural and Environmental Medicine 2016, Vol 23, No 2, 197–205 REVIEW ARTICLE www.aaem.pl Pantoea agglomerans: a mysterious bacterium of evil and good. Part III. Deleterious effects: infections of humans, animals and plants Jacek Dutkiewicz1, Barbara Mackiewicz2, Marta Kinga Lemieszek3, Marcin Golec1, Janusz Milanowski2 1 Department of Biological Health Hazards and Parasitology, Institute of Rural Health, Lublin, Poland 2 Department of Pneumonology, Oncology and Allergology, Medical University, Lublin, Poland 3 Department of Medical Biology, Institute of Rural Health, Lublin, Poland Dutkiewicz J, Mackiewicz B, Lemieszek MK, Golec M, Milanowski J. Pantoea agglomerans: a mysterious bacterium of evil and good. Part III. Deleterious effects: infections of humans, animals and plants. Ann Agric Environ Med. 2016; 23(2): 197–205. doi: 10.5604/12321966.1203878 Abstract Pantoea agglomerans, a bacterium associated with plants, is not an obligate infectious agent in humans. However, it could be a cause of opportunistic human infections, mostly by wound infection with plant material, or as a hospital-acquired infection, mostly in immunocompromised individuals. Wound infection with P. agglomerans usually follow piercing or laceration of skin with a plant thorn, wooden splinter or other plant material and subsequent inoculation of the plant-residing bacteria, mostly during performing of agricultural occupations and gardening, or children playing. Septic arthritis or synovitis appears as a common clinical outcome of exogenous infection with P. agglomerans, others include endophthalmitis, periostitis, endocarditis and osteomyelitis. Another major reason for clinical infection with P. agglomerans is exposure of hospitalized, often immunodeficient individuals to medical equipment or fluids contaminated with this bacterium. Epidemics of nosocomial septicemia with fatal cases have been described in several countries, both in adult and paediatric patients. In most cases, however, the clinical course of the hospital-acquired disease was mild and application of the proper antibiotic treatment led to full recovery. Compared to humans, there are only few reports on infectious diseases caused by Pantoea agglomerans in vertebrate animals. This species has been identified as a possible cause of equine abortion and placentitis and a haemorrhagic disease in dolphin fish Coryphaena( hippurus). P. agglomerans strains occur commonly, usually as symbionts, in insects and other arthropods. Pantoea agglomerans usually occurs in plants as an epi- or endophytic symbiont, often as mutualist. Nevertheless, this species has also also been identified as a cause of diseases in a range of cultivable plants, such as cotton, sweet onion, rice, maize, sorghum, bamboo, walnut, an ornamental plant called Chinese taro (Alocasia cucullata), and a grass called onion couch (Arrhenatherum elatius). Some plant-pathogenic strains of P. agglomerans are tumourigenic, inducing gall formation on table beet, an ornamental plant gypsophila (Gypsophila paniculata), wisteria, Douglas-fir and cranberry. Recently, a Pantoea species closely related to P. agglomerans has been identified as a cause of bacterial blight disease in the edible mushroom Pleurotus eryngii cultivated in China. The genetically governed determinants of plant pathogenicity in Pantoea agglomerans include such mechanisms as the hypersensitive response and pathogenicity (hrp) system, phytohormones, the quorum-sensing (QS) feedback system and type III secretion system (T3SS) injecting the effector proteins into the cytosol of a plant cell. Key words Pantoea agglomerans, infections, humans, vertebrate animals, arthropods, plant pathogen, genetic determinants Causative agent of opportunistic infections in humans et al. [14] found in a retrospective study that all 9 patients with 1–2 months of ineffective treatment of post-traumatic Pantoea agglomerans is not an obligate infectious agent in wounds showed the presence of foreign bodies of plant origin humans. However, it could be a cause of the opportunistic infected with Pantoea agglomerans. Removal of the foreign (occasional) human infections, mostly in 2 situations: 1) bodies led to rapid healing of the wounds in 2–3 days. Septic wound infection with plant material, and 2) hospital-acquired arthritis or synovitis appears as a common clinical outcome infection. Cases which do not fall into these 2 categories are of exogenous infection with P. agglomerans (Figs. 1–2) [4, less numerous. 5, 7, 9, 10, 11, 12, 13], others include endophthalmitis [3, 6, Wound infection with P. agglomerans could follow 15, 16], acute unilateral dacryocystitis, peculiar by the kind piercing or laceration of skin with a plant thorn, wooden of eye contaminant – not a plant material but dog feces splinter or other plant material, usually during performing [17], corneal infiltrate in an agricultural worker after rice of agricultural occupations [1, 2], during gardening [3, 4, 5, husk injury, caused by Pantoea ananatis, a species closely 6] or children playing [7, 8, 9, 10, 11, 12, 13], and subsequent related to P. agglomerans [18], periostitis [8], endocarditis inoculation of the plant-residing bacteria. Recently, Vaiman [19], osteomyelitis after injury with rose thorn [20] or after closed fracture [21], tibial osteitis after an open grade IIIB Address for correspondence: Prof. Jacek Dutkiewicz, Department of Biological tibial shaft fracture [22], and a tumour-like muscle cyst of Health Hazards and Parasitology, Institute of Rural Health, Jaczewskiego 2, 20-090 Lublin, Poland the thigh [2]. E-mail: [email protected] Exposure of hospitalized, often immunocompromised Received: 08 March 2016; accepted: 20 April 2016 individuals, to medical equipment or fluids contaminated with 198 Annals of Agricultural and Environmental Medicine 2016, Vol 23, No 2 Jacek Dutkiewicz, Barbara Mackiewicz, Marta Kinga Lemieszek, Marcin Golec, Janusz Milanowski. Pantoea agglomerans: a mysterious bacterium of evil and good. Part III… in patients seen at a children’s hospital in Houston, USA, over 6 years. Isolates included 23 from the bloodstream, 14 from abscesses, 10 from joints/bones, 4 from the urinary tract, and 1 each from the peritoneum and the thorax. Infections were mostly polymicrobial, mortality equaled to 5.7%. P. agglomerans was most associated with penetrating trauma by vegetative material and catheter-related bacteraemia. The other cases of hospital-acquired P. agglomerans infection with identified source of contamination include: pneumonia in a heart-lung transplant recipient following transplantation (Fig. 3) [26], a ventilator-associated pneumonia in a patient with chronic renal failure [32], septicaemia after blood transfusion [27], septicaemia in oncologic patients due to infected catheters [33], and endocarditis in a patient with mitral valve leaflet prolapse [34]. Figure 1. A case of plant thorn synovitis of the hand joint caused by P. agglomerans in an adult male. Photomicrograph is showing a large plant thorn spike and the surrounding synovial reaction. According to Olenginski et al. [4], with permission Figure 2. A case of the knee arthritis caused by P. agglomerans in a 14-year-old boy, following penetration by a palm tree thorn. Foreign body with approximate length of 8 mm (the palm thorn) is seen (between the black arrows) in the posterior lateral aspect of the knee. According to Kratz et al. [11], with permission P. agglomerans [23, 24, 25, 26, 27, 28] is another major reason for clinical infections with this bacterium. The greatest nosocomial (hospital-borne) epidemic caused by P. agglomerans and other enterobacteria, which occurred in the USA between 1970–1971 and resulted in 378 cases of septicemia (of which 152 caused solely by P. agglomerans) with 13.4% mortality, was proved to have been spread by the factory-contaminated screw-caps of bottles with intravenous fluids [23]. Contamination of the screw-caps of the bottles containing the intravenous fluid with P. agglomerans and Enterobacter cloacae also caused the epidemic of nosocomial sepsis with 6.3% mortality among 63 Greek infants and children [24]. More recently, there was described in Malaysia an outbreak of septicemia with respiratory failure, with a very high mortality (87.5%) among neonates in an intensive care unit caused by parenteral nutrition solutions infected with Pantoea spp. [25, 29]. Bicudo et al. [30] described a nosocomial outbreak of P. agglomerans sepsis with gastrointestinal symptoms in 6 paediatric patients in Figure 3. A case of pneumonia caused by P. agglomerans in a heart-lung transplant recipient. (A) Patient’s chest radiograph shows bilateral lower lobe consolidation Brazil, caused by contaminated transference tube used for on the day of diagnostic bronchoscopy, and (B) interval improvement in bilateral intravenous rehydration. Boszczowski et al. [28], also in lobe consolidation 10 days after initiation of appropriate antimicrobial therapy. Brazil, reported an outbreak of P. agglomerans bacteraemia in According to Shubov et al. [26], with permission. 7 patients receiving haemodialysis or plasmapheresis, caused by contamination of an anticoagulant citrate-dextrose 46% Some infections with P. agglomerans associated with the solution produced by the hospital’s compound pharmacy. stay in hospital cannot be traced to any documented way of Cruz et al. [31] described 53 paediatric cases of Pantoea infection and are defined as ‘endogenous’, ‘spontaneous’ or agglomerans infections cultured from
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