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Evaluation of eight cases of confirmed Bordetella bronchiseptica infection and colonization over a 15-year period

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Abstract

Clin Microbiol Infect 2011; 17: 201–203 We describe eight human cases of Bordetella bronchiseptica infection and colonization over a 15-year period. Amongst the eight patients, seven had significant underlying disease. Cat exposure was documented in three cases. Symptoms ranged from asymptomatic carriage to severe pneumonia. We could not identify a homogeneous pattern of clinical disease among symptomatic patients. Although B. bronchiseptica infection remains a rare clinical condition among humans, it should be considered as potentially pathogenic when found in airways of immunocompromised patients.

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... Bordetella bronochiseptica is closely related to B. pertussis but does not express pertussis toxin and is not considered a primary human pathogen [1]. However, an increasing number of B. bronchoseptica human infections have been reported recently [7][8][9]. Immunocompromised patients are affected by the pathogen most commonly [10,11]. A large series of patients with cancer with B. bronchiseptica infections was recently published [12]. ...
... Pneumonia is the most common manifestation in human beings, however, reports on other infections such as one patient with liver cirrhosis and spontaneous bacterial peritonitis caused by B. bronchiseptica are available [9]. There is evidence that transmission through animal vectors plays a key role [7,8,[13][14][15][16]. Register et al. [8] documented transmission of B. bronchiseptica from a cat to a patient with cystic fibrosis. ...
... Redelmann-Sidid et al. [13] reported recently a patient with glioblastoma on temozolomide therapy with kitten-transmitted B. bronchoseptica infection. Wernli et al. [7] summarized recently eight cases of B. bronchoseptica infection in human beings, the majority of whom had severe underlying disease and three of whom had been exposed to cats. Our patient is only the eleventh reported patient with cancer and the first with malignant disease of the liver with B. bronchiseptica infection. ...
Article
Background: Although Bordetella bronchiseptica is primarily an animal pathogen, cases of human disease caused by this pathogen have been published recently, most frequently pneumonia in immunocompromised patients. In human disease, transmission through animal vectors may play a key role. Although no standardized sensitivity testing is available for this pathogen in human disease, animal isolates are sensitive to most β-lactam antibiotics. Case Report: A 62-year-old Caucasian male with Child-Pugh class A cirrhosis caused by chronic hepatitis C infection underwent uneventful left lateral segmentectomy for a 3 cm cholangiocarcinoma. Within 48 h, he developed altered mental status, temperature of 39.4°C, leukocytosis (white blood cell count: 13,000/mm³), and dyspnea followed by hypotension requiring vasopressor support and intubation. Computed tomography (CT) scan demonstrated left lower lobe pneumonia. Empiric antibiotic therapy including vancomycin (1 g every 12 h) and piperacillin-tazobactam (3.5 g every 6 h) was initiated and his signs of sepsis resolved within two days. Bordetella bronchiseptica was cultured from sputum. Upon questioning, the patient reported close contact with several pet cats on the days prior to admission. Antibiotics were continued for a total of seven days and he was discharged in good condition doing well at his six-month follow-up. Conclusions: Immunocompromised patients may develop infection with Bordetella bronchiseptica especially if they are in close contact with animals known to be a reservoir of this pathogen. If diagnosed early and treated appropriately, the outcome is favorable. Bordetella bronchiseptica is a small, gram negative, rod-shaped bacterium of the genus Bordetella [1]. Rarely reported in human beings, it is a common cause of respiratory disease in farm, wild, and pet animals [2,3]. Cats, dogs, rabbits, pigs, cattle, polar bears, sloths, and rodents may harbor this organism [4–6]. Bordetella bronochiseptica is closely related to B. pertussis but does not express pertussis toxin and is not considered a primary human pathogen [1]. However, an increasing number of B. bronchoseptica human infections have been reported recently [7–9]. Immunocompromised patients are affected by the pathogen most commonly [10,11]. A large series of patients with cancer with B. bronchiseptica infections was recently published [12]. Pneumonia is the most common manifestation in human beings, however, reports on other infections such as one patient with liver cirrhosis and spontaneous bacterial peritonitis caused by B. bronchiseptica are available [9]. There is evidence that transmission through animal vectors plays a key role [7,8,13–16]. Register et al. [8] documented transmission of B. bronchiseptica from a cat to a patient with cystic fibrosis.
... In both animals and humans, the respiratory tract is the predominant site of B. bronchiseptica infections. In humans, the clinical significance of B. bronchiseptica isolation from the respiratory tract varies between individuals as the disease pattern ranges from asymptomatic colonization to severe pneumonia [8]. However, anecdotal data suggest a potential pathogenic role of B. bronchiseptica in the respiratory tract of immunocompromised patients. ...
... Human infections caused by B. bronchiseptica have been rarely reported in the literature [7,8]. A potential explanation for the rarity of human B. bronchiseptica infections is that cross-immunity may be conferred by B. pertussis vaccination, although immunocompromised individuals may remain susceptible due to a diminished immune response [9]. ...
... A potential explanation for the rarity of human B. bronchiseptica infections is that cross-immunity may be conferred by B. pertussis vaccination, although immunocompromised individuals may remain susceptible due to a diminished immune response [9]. The pathogenicity of B. bronchiseptica in humans is not well established but should be considered as a true clinical pathogen when isolated from the lower respiratory tract of immunocompromised patients [8,10]. While we acknowledge the possibility that B. bronchiseptica may have represented airway colonization in our patient, her immunosuppressed status and clinical presentation suggest that it played a pathogenic role. ...
Article
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Bordetella bronchiseptica infections may be overlooked by clinicians due to the uncommon encounter of this pathogen in humans and common isolation of co-pathogens. However, the isolation of B. bronchiseptica in immunocompromised individuals may represent a true infection. We report our experience with the fatal case of a stem cell transplant recipient, co-infected with SARS-CoV-2 and B. bronchiseptica, who was considered fully vaccinated (two doses) at the time of her case in spring 2021. Future studies are needed to evaluate the incidence of bacterial co-infections in immunosuppressed individuals with SARS-CoV-2 and clinicians should remain cognizant of the potential pathogenic role of uncommon pathogens isolated in these individuals.
... Bordetella (B.) bronchiseptica is primarily a zoonotic respiratory pathogen, with close resemblance to B. pertussis, causative agent of whooping cough [1]. B. bronchiseptica is common inhabitant of upper respiratory tract of various domestic and wild animals including rodents, swine, household pets, voles, seals and captive koalas [1,2]. ...
... Bordetella (B.) bronchiseptica is primarily a zoonotic respiratory pathogen, with close resemblance to B. pertussis, causative agent of whooping cough [1]. B. bronchiseptica is common inhabitant of upper respiratory tract of various domestic and wild animals including rodents, swine, household pets, voles, seals and captive koalas [1,2]. Human infections are rarely reported, despite frequent exposure to animals infected with this pathogen. ...
... The exact prognosis associated with this infection is difficult to establish because of scarcity of the literature. Wernli et al. reported mortality of 12.5% in his case series [1]. ...
Article
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Bordetella (B.) bronchiseptica is primarily a zoonotic pathogen, which is often found in upper respiratory tract of various domestic and wild animals. Human infections are rarely reported in immunocompromised patients and are associated with a wide spectrum of presentation ranging from mild cough, tracheobronchitis to sepsis and death. Here, we describe a case of B. bronchiseptica pneumonia that led to the diagnosis of human immunodeficiency virus infection. The diagnosis of B. bronchiseptica infection can be challenging, as there are no distinctive imaging features. This infection mimics Pneumocystis jiroveci infection and unless a detailed evaluation of an unusual presentation is done it may be missed, resulting in increased morbidity and mortality. This case emphasizes the importance of a systematic detailed investigation of patients with unusual pneumonia presentations.
... 9 Wernli et al. described eight cases of BB that caused infection or colonization in human beings over a 15-year period. 16 Those researchers showed that seven of their patients had underlying diseases and that only three had been in contact with domestic animals. The patients' symptoms ranged from no symptoms to severe pneumonia. ...
... It was not possible to establish a homogeneous pattern regarding clinical disease among the symptomatic patients. 16 A study by García-de-la-Fuente et al. in 2015 showed that most of the patients from whom BB was isolated presented a compromised immune system as well as an underlying disease, and 82% presented respiratory symptoms. 17 Respiratory tract diseases are the major cause of morbidity and mortality among AIDS patients. ...
... 18 Although B. bronchiseptica is only rarely isolated in humans, it should be considered to be potentially pathogenic when found in samples from the respiratory tract in patients with a compromised immune system. [4][5][6]16 Sputum culturing and investigation of exposure to animals are recommended. 9,16 It became known that the patient in Report 2 had been in contact with 25 domestic dogs. ...
Article
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Context and objective: Bordetella bronchiseptica (BB) is a Gram-negative coccobacillus responsible for respiratory diseases in dogs, cats and rabbits. Reports on its development in humans are rare. However, in immunosuppressed patients, especially in those with the immunodeficiency virus (HIV), BB can cause severe pulmonary infections. We report on two cases of pneumonia caused by BB in HIV-positive male patients in a university hospital. Case report: The first case comprised a 43-year-old patient who was admitted presenting chronic leg pain and coughing, with suspected pneumonia. BB was isolated from sputum culture and was successfully treated with trimethoprim/sulfamethoxazole in association with levofloxacin. The second case comprised a 49-year-old patient who was admitted presenting fever, nausea, sweating and a dry cough, also with suspected pneumonia. BB was isolated from sputum culture, tracheal secretions and bronchoalveolar lavage. The disease was treated with ciprofloxacin but the patient died. Conclusion: BB should be included in the etiology of pneumonia in immunodeficient HIV patients. As far as we know, these two were the first cases of pneumonia due to BB to occur in this university hospital.
... La identificación de B. bronchiseptica puede resultar difícil con los métodos automatizados convencionales, ya que con estos sistemas se puede clasificar erróneamente el microorganismo como otro bacilo Gram negativo no fermentador; a pesar de esto, en algunos estudios se sugiere que una manera confiable y útil de identificarlo, es usar el sistema automatizado VITEK2, además de la prueba de oxidasa positiva (15). ...
... El paciente recibió 14 días de tratamiento con imipenem de acuerdo con las recomendaciones, y dada la necesidad de administrar un medicamento de amplio espectro en un paciente inmunosuprimido con otras infecciones concomitantes y la efectividad reportada de este carbapenémico frente a B. bronchiséptica. Aunque la recomendación es administrarlo durante, al menos, dos semanas (15,17), las recurrencias son frecuentes. En este caso, se presentó una nueva bacteriemia a pesar de los resultados negativos en los hemocultivos y de la evolución clínica satisfactoria, lo que sugiere que puede requerirse un tratamiento antibiótico más prolongado para disminuir el riesgo de recurrencia. ...
Article
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Se reporta un caso de bacteriemia recurrente por Bordetella bronchiseptica en un paciente inmunocomprometido con antecedentes de trasplante alogénico de medula ósea por síndrome mielodisplásico, quien ingresó al hospital por síndrome febril. Bordetella bronchiseptica es un agente patógeno veterinario poco común en humanos que afecta principalmente a pacientes inmunocomprometidos y es causa poco frecuente de bacteriemia.
... Although this pathogen rarely infects humans, certain reports have indicated that B. bronchiseptica can infect immunocompromised patients or those with underlying respiratory diseases (2)(3)(4). The respiratory infections caused by this zoonotic pathogen could also become chronic, although with few or no symptoms (5,6). The persistence of B. bronchiseptica in hosts seems to be facilitated through modification of the expression of bacterial constituents mainly controlled by a two-component regulatory system encoded by the bvgAS locus (7,8). ...
... Therefore, the identification of appropriate bacterial components for the development of a new vaccine is still needed. In this search, the characteristic constituents of the avirulent phase could be included in evaluations, since this phase seems to be involved in the infectious process (6,8,17). ...
Article
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Bordetella bronchiseptica, a Gram-negative bacterium, causes chronic respiratory tract infections in a wide variety of mammalian hosts, including humans (albeit rarely). We recently designed Bordetella pertussis and Bordetella parapertussis experimental vaccines based on outer membrane vesicles (OMVs) derived from each pathogen, and we obtained protection against the respective infections in mice. Here, we demonstrated that OMVs derived from virulent-phase B. bronchiseptica (OMVBbvir⁺) protected mice against sublethal infections with different B. bronchiseptica strains, two isolated from farm animals and one isolated from a human patient. In all infections, we observed that the B. bronchiseptica loads were significantly reduced in the lungs of vaccinated animals; the lung-recovered CFU were decreased by ≥4 log units, compared with those detected in the lungs of nonimmunized animals (P < 0.001). In the OMVBbvir⁺-immunized mice, we detected IgG antibody titers against B. bronchiseptica whole-cell lysates, along with an immune serum having bacterial killing activity that both recognized B. bronchiseptica lipopolysaccharides and polypeptides such as GroEL and outer membrane protein C (OMPc) and demonstrated an essential protective capacity against B. bronchiseptica infection, as detected by passive in vivo transfer experiments. Stimulation of cultured splenocytes from immunized mice with OMVBbvir⁺ resulted in interleukin 5 (IL-5), gamma interferon (IFN-γ), and IL-17 production, indicating that the vesicles induced mixed Th2, Th1, and Th17 T-cell immune responses. We detected, by adoptive transfer assays, that spleen cells from OMVBbvir⁺-immunized mice also contributed to the observed protection against B. bronchiseptica infection. OMVs from avirulent-phase B. bronchiseptica and the resulting induced immune sera were also able to protect mice against B. bronchiseptica infection. IMPORTANCE Bordetella bronchiseptica, a Gram-negative bacterium, causes chronic respiratory tract infections in a wide variety of mammalian hosts, including humans (albeit rarely). Several vaccines aimed at preventing B. bronchiseptica infection have been developed and used, but a safe effective vaccine is still needed. The significance and relevance of our research lie in the characterization of the OMVs derived from B. bronchiseptica as the source of a new experimental vaccine. We demonstrated here that our formulation based on OMVs derived from virulent-phase B. bronchiseptica (OMVBbvir⁺) was effective against infections caused by B. bronchiseptica isolates obtained from different hosts (farm animals and a human patient). In vitro and in vivo characterization of humoral and cellular immune responses induced by the OMVBbvir⁺ vaccine enabled a better understanding of the mechanism of protection necessary to control B. bronchiseptica infection. Here we also demonstrated that OMVs derived from B. bronchiseptica in the avirulent phase and the corresponding induced humoral immune response were able to protect mice from B. bronchiseptica infection. This realization provides the basis for the development of novel vaccines not only against the acute stages of the disease but also against stages of the disease or the infectious cycle in which avirulence factors could play a role.
... Bordetella bronchiseptica is a Gram-negative cocco-bacillary aerobe well known for its role in animal disease, particularly kennel cough in dogs (3) and atrophic rhinitis in swine (4). To date, its pathogenic role in human disease remains poorly understood; it is infrequently encountered, with few published studies available to guide antimicrobial therapy (5,6). The cases of B. bronchiseptica previously reported primarily describe respiratory tract infections in immunocompromised hosts, with or without known animal contacts (5,7). ...
... There appears to be only intermediate susceptibility to fluoroquinolones and sulfamethoxazole. Interestingly, B. bronchiseptica is the only species in the genus Bordetella that is consistently resistant to macrolides (6,16). ...
Article
Bordetella bronchiseptica is a respiratory pathogen rarely encountered in human hosts. We describe a case of bacteremia and pancreatic abscess caused by this organism. To our knowledge, this is the first reported case of B. bronchiseptica causing intra-abdominal infection in the form of an abscess. Copyright © 2015, American Society for Microbiology. All Rights Reserved.
... Dogs and cats are not uniformly vaccinated against this pathogen as it is most often encountered in daycare/kennel settings where it can cause an outbreak as it is highly contagious. Exposure to the family pet even if not participating in group activities such as day care can lead to zoonotic transmission highlighting the need to counsel the immunocompromised patients on how to minimize their risk [1,2,[5][6][7]. ...
... Realize that unlike other Bordetella spp, this pathogen is not typically responsive to erythromycin and is often resistant to ampicillin and cephalosporins so may break through typical neutropenic fever coverage [4] (an antipseudomonal cephalosporin and azithromycin). Duration of therapy can range from two weeks to several months depending on the degree of immunocompromise and is generally guided by the resolution of radiological abnormalities [1,5,8]. Most patients eventually recover appropriately, however there have been few reported deaths from sepsis [3]. ...
Article
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Bordetella bronchiseptica is a pleomorphic gram-negative coccobacillus that commonly causes respiratory tract infections in canines, felines, and swine. Human infections are rare. We report a case of Bordetella bronchiseptica pneumonia in a 67-year-old immunocompromised host. His past medical history included multiple myeloma treated with autologous bone marrow transplant followed by a chimeric antigen receptor cell therapy for relapse. He was admitted with unrelenting diarrhea due to HHV-6 pancolitis. During the hospital course he developed high-grade fever (102.3°F), cough and respiratory failure requiring mechanical ventilation. Chest imaging demonstrated bilateral opacities most pronounced at lung bases and worsening mediastinal lymphadenopathy. Bronchoalveolar lavage cultures grew Bordetella bronchiseptica. He was treated with piperacillin/tazobactam, but developed progressive multiorgan failure, transitioned to comfort care, and expired in the hospital. Bordetella bronchiseptica is an organism that do not cause serious infection in immunocompetent persons but can sometimes cause serious illness in immunocompromised populations. It causes “kennel cough” in dogs and spready by respiratory droplets. Dogs and cats are not uniformly vaccinated against this pathogen. Therefore, transmission through animal contact is becoming increasingly common. Realize that unlike other Bordetella spp, this pathogen is not typically responsive to erythromycin and is often resistant to ampicillin and cephalosporins so the typical neutropenic fever coverage with an antipseudomonal cephalosporin and azithromycin might not be effective. Given the increasing recognition of this zoonosis as a threat to the immunocompromised, it is essential to educate immunocompromised patients to minimize zoonotic exposure, as immunization of pets might not confer protection to humans.
... Our patient was successfully treated with a 19-day course of antibiotics and temporary CSF diversion. It is presumed that his exposure to B. bronchiseptica occurred during his volunteer activities at local animal shelters, but it is unknown whether he was colonized with B. bronchiseptica, as previous studies support B. bronchiseptica colonization of the human respiratory tract [10,14]. Both his advanced age and infliximab therapy may have contributed to his immunocompromised status and increased susceptibility to infection. ...
Article
Full-text available
Background Bordetella bronchiseptica is a gram-negative, obligate aerobic coccobacillus known to cause disease in domesticated animals and pets. In humans, B. bronchiseptica commonly leads to respiratory infections like pneumonia or bronchitis, and animal contact usually precedes the onset of symptoms. Case presentation We report a case of post-traumatic B. bronchiseptica meningitis without recent surgery in the setting of immunosuppression with a monoclonal antibody. Our case concerns a 77-year-old male with ulcerative colitis on infliximab who sustained a mechanical fall and developed a traumatic cerebrospinal fluid leak complicated by meningitis. He received meropenem then ceftazidime during his hospital course, and temporary neurosurgical drain placement was required. His clinical condition improved, and he was discharged at his baseline neurological status. Conclusions B. bronchiseptica is an unusual cause of meningitis that may warrant consideration in immunocompromised hosts with known or suspected animal exposures. To better characterize this rare cause of meningitis, we performed a systematic literature review and summarized all previously reported cases.
... This study found that the prevalence of B. bronchiseptica infection was higher than CDV in asymptomatic dogs, which is consistent with the present findings. Also, in the current study, the prevalence of B. bronchiseptica in apparently healthy dogs was higher than that reported in the study by Lavan (22). Moreover, Decaro et al. (9) in 2016 performed a molecular study to detect the etiology of CIRD among animals with clinical CIRD, healthy dogs, and animals with the preliminary stages of CIRD. ...
Article
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Background: Canine distemper virus (CDV) is an extremely contagious pathogen that causes deadly diseases in carnivores worldwide. Objectives: Considering the effect of CDV on the host immune system and the increased risk of other infections, the present study aimed to investigate the incidence of coinfection with CDV and Bordetella bronchiseptica, using genomic and serological methods. Methods: In this study, 50 blood samples, eye samples, respiratory swabs, and gastrointestinal tract swabs were taken from dogs, which showed symptoms of respiratory and gastrointestinal tract involvement, suggesting CDV infection. Also, 50 seemingly healthy dogs were included in this study. The animals were referred to Isfahan clinics between the spring of 2018 and the winter of 2019. For the initial diagnosis of CDV by immunological methods, a rapid CDV immunochromatography kit was used. To investigate for the genomes of both pathogens, after DNA and RNA extraction and reverse transcription of the extracted RNA samples, a PCR assay was performed using specific primers. Results: Based on the results of the RT-PCR assay, of 50 samples taken from dogs with suspected CDV infection, 37 were positive for the presence of CDV nucleic acids, and 20 were positive for the presence of B. bronchiseptica nucleic acids. Also, of 50 samples taken from seemingly healthy dogs, three were positive for CDV, and 15 were positive for B. bronchiseptica nucleic acids. Conclusions: In the present study, of 100 samples taken from dogs with suspected CDV infection and apparently healthy dogs, 15 showed coinfection (12 samples from dogs with symptoms of CDV and three from seemingly healthy dogs). However, no significant relationship was found between CDV and B. bronchiseptica infections. It seems that future studies with a larger sample size can provide us with more accurate results.
... Several human cases of Bordetella bronchiseptica infections have been reported in immunocompromised individuals, especially organ transplant recipients and cancer patients who had been exposed either to dogs or cats that can be healthy carriers of this emerging zoonotic pathogen [44]. Symptoms ranged from asymptomatic carriage to severe pneumonia [45]. Although B. bronchiseptica infection remains a rare clinical condition among humans, it should be considered as potentially pathogenic when found in airways of immunocompromised patients. ...
Article
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Simple Summary Dogs and cats have been sharing our environment for a long time and as pets they bring major psychological well-being to our modern urbanized society. However, they still can be a source of human infection by various pathogens, including viruses, bacteria, parasites, and fungi. Abstract Since the middle of the 20th century, pets are more frequently considered as “family members” within households. However, cats and dogs still can be a source of human infection by various zoonotic pathogens. Among emerging or re-emerging zoonoses, viral diseases, such as rabies (mainly from dog pet trade or travel abroad), but also feline cowpox and newly recognized noroviruses or rotaviruses or influenza viruses can sicken our pets and be transmitted to humans. Bacterial zoonoses include bacteria transmitted by bites or scratches, such as pasteurellosis or cat scratch disease, leading to severe clinical manifestations in people because of their age or immune status and also because of our closeness, not to say intimacy, with our pets. Cutaneous contamination with methicillin-resistant Staphylococcus aureus, Leptospira spp., and/or aerosolization of bacteria causing tuberculosis or kennel cough are also emerging/re-emerging pathogens that can be transmitted by our pets, as well as gastro-intestinal pathogens such as Salmonella or Campylobacter. Parasitic and fungal pathogens, such as echinococcosis, leishmaniasis, onchocercosis, or sporotrichosis, are also re-emerging or emerging pet related zoonoses. Common sense and good personal and pet hygiene are the key elements to prevent such a risk of zoonotic infection.
... In case of food poisoning by clostridium, oral rehydration or intravenous fluids and electrolyte therapy in severe cases, can be applied; antibiotics are not recommended [74]. In other antibiotic therapy includes use of clindamycin, vancomycin, carbapenem etc. however sporadic resistance against clindamycin, cephalosporins, erythromycin and fluoroquinolones has been reported in recent times [75][76][77]. ...
Article
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Emergence of multidrug resistance (MDR), extensively drug resistance (XDR) and pandrug resistance (PDR) strains of bacteria in communicable diseases of zoonotic and reverse zoonotic importance is the major hurdle of one health concept. Increasing level of resistance against antibiotics among bacterial population throughout the world, slow pace of new antibacterial drug discovery and enhanced pace of resistance development by pathogenic bacteria possess major challenges for human and animal health as well as life in future. Alternative management strategy in terms of improved prophylactic vaccine; early, easy and effective diagnostics and therapeutic drugs against those resistant bacteria is the need of the hour. In this context nanomedicine can fit into the multi-faceted demands as an effective prophylactic and theranostic alternative to control the communi-cable diseases in a cost effective manner in the era of microbial resistance. The current review is focused towards delineating the application of nanomaterials as vaccine or drug delivery system, diagnostics and directly acting antimicrobial therapeutic agents in combating the important zoonotic and reverse zoonotic bacterial diseases in recent scenario along with their potential benefits, limitations and future prospects to formulate successful eradication strategies.
... A few cases of human exposure were reported from dogs and cats, and immunosuppression has been reported to play a vital role in the colonization by this organism. Macrolide antibiotics, Colistin and Morepenem were reported as the most active antibiotics against this bacteria [36,37]. Therefore, isolation of these pathogens in snakes makes it a potentially important zoonotic pathogen of concern especially for veterinarians, pet snake owners and zoo keepers. ...
Article
Aim: Captivity of non-venomous snakes such as python and boa are common in zoos, aquariums and as pets in households. Poor captivity conditions expose these reptiles to numerous pathogens which may result in disease conditions. The purpose of this study was to investigate the common bacteria isolated from necropsied captive snakes in Malaysia over a five year period. Materials and methods: A total of 27 snake carcasses presented for necropsy at the Universiti Putra Malaysia (UPM) were used in this survey. Samples were aseptically obtained at necropsy from different organs/tissues (lung, liver, heart, kindey, oesophagus, lymph node, stomach, spinal cord, spleen, intestine) and cultured onto 5% blood and McConkey agar, respectively. Gram staining, morphological evaluation and biochemical test such as oxidase, catalase and coagulase were used to tentatively identify the presumptive bacterial isolates. Results: Pythons had the highest number of cases (81.3%) followed by anaconda (14.8%) and boa (3.7%). Mixed infection accounted for 81.5% in all snakes and was highest in pythons (63%). However, single infection was only observed in pythons (18.5%). A total of 82.7%, 95.4% and 100% of the bacterial isolates from python, anaconda and boa, respectively were gram negative. Aeromonas spp was the most frequently isolated bacteria in pythons and anaconda with incidences of 25 (18%) and 8 (36.6%) with no difference (p > 0.05) in incidence, respectively, while Salmonella spp was the most frequently isolated in boa and significantly higher (p < 0.05) than in python and anaconda. Bacteria species were most frequently isolated from the kidney of pythons 35 (25.2%), intestines of anacondas 11 (50%) and stomach of boa 3 (30%). Conclusion: This study showed that captive pythons harbored more bacterial species than anaconda or boa. Most of the bacterial species isolated from these snakes have public health importance and have been incriminated in human infections worldwide.
... Bordetella bronchiseptica is a zoonotic bacterium and it can cause infection in most of the mammalian species such as cat, dog, horse, rabbit, and pig. In humans, B. bronchiseptica infection is not common (2). If a human is infected, it is thought that this infection comes from an infected animal with B. bronchiseptica (3). ...
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Introduction: Bordetella bronchiseptica is an aerobic, Gram-negative pleomorphic coccobacillus. It can infect various mammals including cats, dogs, and pigs. Bordetella bronchiseptica rarely infect humans. Infants, immunosuppressed and HIV infected persons, and patients with comorbidities constitute the risk group for B. bronchiseptica infections. Bordetella bronchiseptica may lead to disseminated infection, cavitary pneumonia, and rarely fatal tracheobronchitis and sepsis. Case Presentation: A patient who was in follow-up due to acquired immunodeficiency syndrome (AIDS) was admitted to our hospital with persistent dry cough and fever for 4 weeks. The clinical history revealed the presence of classical anti-retroviral resistant HIV infection, and the development of blindness in the right eye because of retinitis. The case was considered as febrile neutropenia; the meropenem therapy was started empirically. Even though we were able to get fever response with empirical therapy, cough remained persistent. Throat culture was inoculated into 5% sheep blood agar and incubated at 37°C. Gram-negative coccobacillus was detected in the examination. Then, the colonies were loaded to MALDI-TOF-VITEK MS and the disease factor was determined as B. bronchiseptica. We stopped meropenem therapy on 7th day and administered clarithromycin 2 × 500mg orally for 14 days. Conclusions: In AIDS patients with chronic cough, B. bronchiseptica should be considered as a pathogen causing opportunistic infection. In this manuscript, we report a case of tracheobronchitis caused by B. bronchiseptica in an AIDS patient
... El potencial zoonótico de la infección por B. bronchiseptica es importante y es común en niños y adultos inmunocomprometidos. Tienen mayor riesgo las personas cuya inmunosupresión se relaciona con afección maligna hematológica, terapia con glucocorticoides a largo plazo y embarazo, también tienen riesgo de infectarse quienes se someten a traqueotomía o intubación con sonda endotraqueal; las personas con enfermedad respiratoria preexistente como bronquitis crónica y neumonía son particularmente susceptibles (Abhishek et al., 2008: Mazumder y Cleveland, 2010Werli et al., 2011). ...
... 6,8,27,28 This phenomenon has also been demonstrated for Bordetella bronchiseptica, whilst most other clinically significant Bordetella species are generally susceptible to macrolides. 29,30 Unfortunately, our genomic analyses did not identify any mutations that could explain elevated MIC to erythromycin in tested isolates. It is still otherwise an open question over whether patients should indeed be treated with antibiotics upon detection of B. hinzii. ...
Article
Bordetella hinzii has emerged as an unusual cause of infection in immunocompromised patients, previously linked to zoonotic transmission. Antimicrobial susceptibility and genetic diversity of B. hinzii are poorly understood. This study reports phenotypic and genomic characteristics of the first four Australian isolates of B. hinzii obtained from elderly immunocompromised patients. Bordetella hinzii isolates were identified by MALDI-TOF and whole genome sequencing (WGS). Antibiotic susceptibility testing was performed using disk diffusion or E-test. Genomes of B. hinzii were analysed in global context. A phylogenetic tree was constructed of all isolates using Roary and maximum-likelihood tree was generated from the core-snp alignment. Bordetella hinzii minimum inhibitory concentrations (MICs) were largely uniform with high MICs to ampicillin, ceftriaxone and ciprofloxacin and low MICs to meropenem and piperacillin-tazobactam. Genomic analysis of isolate sequences divided strains analysed into two phylogenetically distinct groups, with one Australian B. hinzii isolate (AUS-4) assigned to Group 1, and the remaining isolates (AUS1-AUS3 and AUS-5) to Group 2. Single nucleotide polymorphism (SNP) analysis revealed two isolates, AUS-1 and AUS-2, were closely related with 14 SNP differences between them. All other Australian isolates were unrelated to each and all other isolates from the international dataset. Bordetella hinzii appears to pose a risk to immunocompromised individuals but remains susceptible to extended spectrum β-lactam and carbapenem antibiotics. Genomic analysis suggested a dissemination of genetically distinct strains.
... 63,64 Most people with Bordetella species infections are infected by Bordetella pertussis, but some individuals, particularly immunocom promised people, can be infected with B bronchiseptica. 65,66 Cats with cough and systemic evidence of bacterial infection such as fever might occasionally be infected with Y pestis and/or F tularensis, if living in endemic areas; these agents can be transmitted from cats to humans in respiratory secretions. 53,67,68 (See Panelists' advice 16.) Humans are the principal natural hosts for Streptococcus group A (Streptococcus pyogenes) bacteria, which cause 'strep throat' in people. ...
Article
Aim The overarching purpose of the 2019 AAFP Feline Zoonoses Guidelines (hereafter referred to as the ‘Guidelines’) is to provide accurate information about feline zoonotic diseases to owners, physicians and veterinarians to allow logical decisions to be made concerning cat ownership. Scope and accessibility The Panelists are physicians and veterinarians who worked closely together in an attempt to make these Guidelines a document that can be used to support the International One Health movement. This version of the Guidelines builds upon the first feline zoonosis panel report, published in 2003 ( catvets.com/guidelines ), and provides an updated reference list and recommendations. Each of the recommendations received full support from every Panelist. Primary recommendations are highlighted in a series of ‘Panelists’ advice’ boxes.
... Antimicrobial susceptibility testing revealed that B. bronchiseptica and B. pseudohinzii had almost similar antimicrobial profiles, reflecting the close phylogenetic relationships between the two bordetellae. The only antimicrobial susceptibility variance between B. bronchiseptica and B. pseudohinzii was observed using the macrolide; erythromycin, where it was ineffective against B. bronchiseptica although it was reported to be effective for the treatment of most Bordetella clinical infections [31], including B. pseudohinzii in this study. Resistance to erythromycin could be an innate phenotype of B. bronchiseptica as this was also observed among B. bronchiseptica isolates from pigs with respiratory diseases in China [33]. ...
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Rodents have historically been associated with zoonotic pandemics that claimed the lives of large human populations. Appropriate pathogen surveillance initiatives could contribute to early detection of zoonotic infections to prevent future outbreaks. Bordetella species are bacteria known to cause mild to severe respiratory disease in mammals and, some have been described to infect, colonize and spread in rodents. There is a lack of information on the population diversity of bordetellae among Malaysian wild rodents. Here, bordetellae recovered from lung tissues of wild rats were genotypically characterized using 16S rDNA sequencing, MLST and nrdA typing. A novel B. bronchiseptica ST82, closely related to other human-derived isolates, was discovered in three wild rats (n=3) from Terengganu (5.3333° N, 103.1500° E). B. pseudohinzii, a recently identified laboratory mice inhabitant, was also recovered from one rat (n=1). Both bordetellae displayed identical antimicrobial resistance profiles, indicating the close phylogenetic association between them. Genotyping using the 765-bp nrdA locus was shown to be compatible with the MLST-based phylogeny, with the added advantage of being able to genotype non-classical bordetellae. The recovery of B. pseudohinzii from wild rat implied that this bordetellae has a wider host range than previously thought. The findings from this study suggest that bordetellae surveillance among wild rats in Malaysia has to be continued and expanded to other states to ensure early identification of species capable of causing public health disorder.
... A maioria dos casos corresponde a infeção respiratória, nomeadamente tosse convulsa, pneumonia, bronquite, sinusite, laringotraqueíte ou tosse prolongada, sendo raras outras apresentações, como meningite. [20][21][22][23][24][25] No caso descrito, um lactente previamente saudável apresentou sintomatologia clássica de tosse convulsa, achados laboratoriais típicos, evoluindo favoravelmente sob antibioterapia com macrólido e terapêutica de suporte, sem necessidade de suporte ventilatório. Desconhece-se contacto com animal possivelmente infetado. ...
... Evidence supporting the role of B. bronchiseptica in reducing BPmediated asthma and allergies includes the following: 1) B. bronchiseptica, a Gram-negative bacterium that synthesizes LPS endotoxin, is well known to infect domesticated and farm mammals such as dogs, cats, pigs, cows, sheep and horses [116,117], 2) B. bronchiseptica and BP share a close genetic relationship [118] and several key virulence factors including filamentous haemagglutinin (FHA) [119], pertactin [120], dermonecrotic toxin [121], and lipopolysaccharide [114], 3) living on a farm and having household animals increases human exposure to B. bronchiseptica as these infections are common in animals, e.g., 18.6% of lung samples from pigs with respiratory disease [122] and 10% of cats [114] test positive for B. bronchiseptica, 4) although not a primary host, and investigations are limited, humans can be infected and colonized by B. bronchiseptica [114,[123][124][125], usually as a result of contact with animals [123,126], and perhaps most importantly, 5) by stimulating host TLR4 mucosal responses, B. bronchiseptica endotoxin "protects against Bordetella pertussis colonization" in rodents [127]. ...
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Decades of peer reviewed evidence demonstrate that: 1) Bordetella pertussis and pertussis toxin are potent adjuvants, inducing asthma and allergic sensitization in animal models of human disease, 2) Bordetella pertussis often colonizes the human nasopharynx, and is well documented in highly pertussis-vaccinated populations and 3) in children, a history of whooping cough increases the risk of asthma and allergic sensitization disease. We build on these observations with six case studies and offer a pertussis-based explanation for the rapid rise in allergic disease in former East Germany following the fall of the Berlin Wall; the current asthma, peanut allergy, and anaphylaxis epidemics in the United States; the correlation between the risk of asthma and gross national income per capita by country; the lower risk of asthma and allergy in children raised on farms; and the reduced risk of atopy with increased family size and later sibling birth order. To organize the evidence for the pertussis hypothesis, we apply the Bradford Hill criteria to the association between Bordetella pertussis and asthma and allergic sensitization disease. We propose that, contrary to conventional wisdom that nasopharyngeal Bordetella pertussis colonizing infections are harmless, subclinical Bordetella pertussis colonization is an important cause of asthma and diseases of allergic sensitization.
Article
Pertussis is a highly infectious vaccine-preventable cough illness that continues to be a significant source of morbidity and mortality around the world. The majority of human illness is caused by Bordetella pertussis , and some is caused by Bordetella parapertussis . Bordetella is a Gram-negative, pleomorphic, aerobic coccobacillus. In the past several years, even countries with high immunization rates in early childhood have experienced rises in pertussis cases. Reasons for the resurgence of reported pertussis may include molecular changes in the organism and increased awareness and diagnostic capabilities, as well as lessened vaccine efficacy and waning immunity. The most morbidity and mortality with pertussis infection is seen in infants too young to benefit from immunization. Severe infection requiring hospitalization, including in an intensive care setting, is mostly seen in those under 3 months of age. As a result, research and public health actions have been aimed at better understanding and reducing the spread of Bordetella pertussis . Studies comparing the cost benefit of cocooning strategies versus immunization of pregnant women have been favorable towards immunizing pregnant women. This strategy is expected to prevent a larger number of pertussis cases, hospitalizations, and deaths in infants <1 year old while also being cost-effective. Studies have demonstrated that the source of infection in infants usually is a family member. Efforts to immunize children and adults, in particular pregnant women, need to remain strong.
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Bordetella bronchiseptica frequently causes nonfatal tracheobronchitis, but its role in fatal pneumonia is less recognized. Our study evaluated histologic identification of cilia-associated bacteria as a method for diagnosis of B. bronchiseptica pneumonia. Cases of fatal bronchopneumonia were studied retrospectively, excluding neonates and cases of aspiration pneumonia, minor lung lesions, or autolysis. The study population comprised 36 canine and 31 feline cases of bronchopneumonia. B. bronchiseptica was identified in 8 of 36 canine and 14 of 31 feline cases based on immunohistochemistry (IHC) using serum from a rabbit hyperimmunized with pertactin, PCR testing (Fla2/Fla12), and/or bacterial culture data when available. Of these, IHC was positive in 4 canine and 7 feline cases, PCR was positive in 8 canine and 14 feline cases, and B. bronchiseptica was isolated in 2 of 5 canine and 3 of 9 feline cases tested. Examination of histologic sections stained with hematoxylin and eosin revealed bronchial cilia-associated bacteria in 4 of 36 canine and 5 of 31 feline cases; these were all positive by IHC and PCR. The presence of cilia-associated bacteria had been noted in the pathology report for only 2 of these 9 cases. Thus, the presence of cilia-associated bacteria seems frequently overlooked by pathologists, but is a diagnostically significant feature of B. bronchiseptica pneumonia. A specific diagnosis of B. bronchiseptica pneumonia is important because it suggests primary or opportunistic bacterial pneumonia rather than aspiration pneumonia, and because of the risk of animal-to-animal transmission of B. bronchiseptica, the availability of vaccines for disease prevention, and the potential zoonotic risk to immunocompromised pet owners.
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Investigations of five misidentification cases of Brucella species using commercial identification techniques prompted a retrospective analysis of previously published misidentifications of Brucella infections in China and elsewhere. Brucella causes a notifiable communicable zoonotic disease. The misidentifications of Brucella as other genetically similar Gram-negative pathogens may result in inappropriate treatment of the patient as well as risk of laboratory-acquired infections. We summarize the microbiological identification methods, reasons and possible influence of misidentification of Brucella infection in humans.
Article
Background: The genus Bordetella consists of 9 species of small gram-negative coccobacilli, of which 4 are known to cause disease in humans: Bordetella pertussis, Bordetella parapertussis, Bordetella holmesii, and Bordetella bronchiseptica. Bordetella bronchiseptica is a commensal and a cause of respiratory tract disease in many wild and domestic animals but has rarely been implicated as a cause of infection in humans. Methods: PubMed search for Bordetella bronchiseptica in humans, in English literature. Case: We present a case of a 54-year-old man who underwent elective back surgery and developed complications leading to prolonged intubation. He began to have spiking fevers with profuse sputum production and had evidence of pneumonia on chest radiograph. He was started on broad-spectrum antibiotics, but continued having high fevers. His sputum revealed a gram-negative, nonenteric oxidase-positive organism, which was later identified as B. bronchiseptica, likely transmitted from his puppy, which had been diagnosed with kennel cough. Both the patient and his best friend received effective antibiotics with a full recovery. Results: Sixty-two human cases of B. bronchiseptica have been published in the English literature; 84% had pneumonia/bronchitis. The majority of the patients were immunocompromised, most commonly with HIV/AIDS, or had underlying lung disease, mainly cystic fibrosis. Sixty-five percent of the patients had known animal contact prior to becoming ill. The most common animal was a dog.
Article
Bordetella bronchiseptica is a bacterial pathogen usually isolated from animals and rarely causes human infections. There are, however, some reports that B. bronchiseptica causes human respiratory infections in immunocompromised patients or those with underlying respiratory diseases, although there is a lack of treatment guidelines. An 80-year-old woman was admitted to our hospital to treat anti-neutrophil cytoplasmic antibodies-associated vasculitis. On the 16th day after admission, she complained of a productive cough with right pleuritic pain and had low-grade fever. After chest CT scans, we diagnosed pneumonia. Gram stain of her sputum revealed moderate levels of gram-negative coccobacilli, which was later identified as B. bronchiseptica by mass spectrometry. According to the result of minimum inhibitory concentration, we successfully treated the pneumonia with minocycline. This case suggests that B. bronchiseptica pneumonia can be treated by minocycline if the minimum inhibitory concentration is less than 0.25 μg/mL.
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Bordetella bronchiseptica is a facultative pathogen bacterium located in the upper respiratory tract of mammals, and plays a key role in the aetiology of canine kennel cough. Significant molecules of infection (flagellin, fimbria and adenylate cyclase) were investigated on B. bronchiseptica strains originated from dogs and from human illnesses. By polymerase chain reaction followed by restriction fragment length polymorphism analysis (PCR-RFLP), fimbrial genes proved to be uniform, while flagellin genes were grouped to 3 different types. Only twenty percent of the strains possessed the adenylate cyclase gene that showed remarkable diversity. Although the Hungarian canine B. bronchiseptica strains were uniform in several assays, the similarity found between the foreign canine and human strains draws the attention to the risk of zoonosis.
Article
Objective To assess knowledge, attitudes and practices in relation to zoonoses among pet owners.Methods Questionnaire completed by 81 clients attending a small animal practice in Sydney, Australia.ResultsMost (64.5%) clients reported that they were not concerned about contracting a disease from their pet, but 7.9% and 3.9% of clients were a little or very concerned, respectively; 23.7% of clients stated that they had not considered the possibility. Although respondents indicated that they had heard of a number of zoonoses, knowledge of animal sources and exposure pathways was generally low, particularly for the more important zoonoses in Australia such as toxoplasmosis, psittacosis and Q fever. Only 37.0%, 12.3% and 11.1%, respectively, of clients had heard of these diseases. Most respondents (84.1%) indicated that they viewed veterinarians as having the primary responsibility for providing information about zoonoses, yet less than half (48.1%) recalled ever getting information from their veterinarian. Likewise, many respondents (48.1%) indicated that medical professionals played a role in providing information about zoonoses, yet less than one-quarter (23.5%) recalled ever getting information from their doctor.Conclusion The low level of knowledge among pet owners about sources and exposure pathways indicates a need to strengthen communication between veterinarians, doctors and their clients around the possible risks of zoonoses and appropriate prevention strategies.
Article
PvuII ribotyping and MLST are each highly discriminatory methods for genotyping Bordetella bronchiseptica, but a direct comparison between these approaches has not been undertaken. The goal of this study was to directly compare the discriminatory power of PvuII ribotyping and MLST, using a single set of geographically and genetically diverse strains, and to determine whether subtyping based on repeat region sequences of the pertactin gene (prn) provides additional resolution. One hundred twenty-two isolates were analyzed, representing 11 mammalian or avian hosts, sourced from the United States, Europe, Israel and Australia. Thirty-two ribotype patterns were identified; one isolate could not be typed. In comparison, all isolates were typeable by MLST and a total of 30 sequence types was identified. An analysis based on Simpson's Index of Diversity (SID) revealed that ribotyping and MLST are nearly equally discriminatory, with SIDs of 0.920 for ribotyping and 0.919 for MLST. Nonetheless, for ten ribotypes and eight MLST sequence types, the alternative method discriminates among isolates that otherwise type identically. Pairing prn repeat region typing with ribotyping yielded 54 genotypes and increased the SID to 0.954. Repeat region typing combined with MLST resulted in 47 genotypes and an SID of 0.944. Given the technical and practical advantages of MLST over ribotyping, and the nominal difference in their SIDs, we conclude MLST is the preferred primary typing tool. We recommend the combination of MLST and prn repeat region typing as a high-resolution, objective and standardized approach valuable for investigating the population structure and epidemiology of B. bronchiseptica.
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Bordetella bronchiseptica, an emerging zoonotic pathogen, infects a broad range of mammalian hosts. B. bronchiseptica-associated atrophic rhinitis incurs substantial losses to the pig breeding industry. The true burden of human disease caused by B. bronchiseptica is unknown, but it has been postulated that some hypervirulent B. bronchiseptica isolates may be responsible for undiagnosed respiratory infections in humans. B. bronchiseptica was shown to acquire antibiotic resistance genes from other bacterial genera, especially Escherichia coli. Here, we present a new B. bronchiseptica lytic bacteriophage—vB_BbrP_BB8—of the Podoviridae family, which offers a safe alternative to antibiotic treatment of B. bronchiseptica infections. We explored the phage at the level of genome, physiology, morphology, and infection kinetics. Its therapeutic potential was investigated in biofilms and in an in vivo Galleria mellonella model, both of which mimic the natural environment of infection. The BB8 is a unique phage with a genome structure resembling that of T7-like phages. Its latent period is 75 ± 5 min and its burst size is 88 ± 10 phages. The BB8 infection causes complete lysis of B. bronchiseptica cultures irrespective of the MOI used. The phage efficiently removes bacterial biofilm and prevents the lethality induced by B. bronchiseptica in G. mellonella honeycomb moth larvae.
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Background: Veterinary practice is a hazardous work environment with high levels of occupation‐related injuries and illness reported compared to general practitioners of human medicine (Nienhaus and others 2005). There are occupational hazards that veterinary staff may face when performing veterinary anaesthesia and so it's important to know how to minimise the risks. Aim of the article: This article outlines the physical, biological, chemical and potential psychological hazards encountered in veterinary anaesthesia, and examines what can be done to minimise the risks to those involved.
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The objective of the study was to access microbial load and microorganism found in swine house depending on the sample site and to compare between the conventional and molecular methods (MEGA 6a rDNA sequencing) of characterization of swine house isolates. The antimicrobial spectrum, growth/ killing kinetics of the isolates using Ultraviolet spectrophotometer signatures were also evaluated. The sample were taken at the pig house from the wall [w] and at a distance of 2km and body[B] and floor[F] using sterile swap stick. The sample underwent serial dilution and a pure isolate was sub-cultured using nutrient agar and also biochemical test was conducted as a preliminary test. From the preliminary test, the following organism were identified, Mycobacterium tuberculosis, Bacillus spp Bacillus anthracis, Bacillus cereus, Staphylococcus aureus, Clostridium sp. In addition the samples were tested for antibiotics susceptibility test (Amtibiogram) using Kirby-bauer antibiotic susceptibility disc. All isolates were found to be susceptible to Ciprofloxacin, Levofloxacin, Gentamycin, Rifampicin, Streptomycin, Erythromycin and Amoxyl. Isolates were resistant to Norflaxacin, Chloramphenicol and Ampiclox. Molecular sequencing were performed on three isolates for a confirmatory test. It was observed that Shigella flexneri and Enterococcus faecalis. Growth rate and death rate / killing time of isolates using ultraviolet spectrophotometer from the swine house were measured. It was observed, At, wavelength 480λ. Bacillus spp has the highest growth rate of 0.525λ and Bacillus subtilis have the lowest growth rate of 0.001λ. At 84th hour, bacillus spp has the lowest death rate of 0.307 λ and Bacillus cereus have the highest death rate of 0.227λ, growth dynamic and killing time of bacteria isolates and addition of ciprofloxacin antibiotic at 24th hour using ultraviolet spectrophotometer. it was observed that at 0 hour, Bacillus subtilis has the highest growth rate of 0.251λ and Bacillus cereus have the lowest growth rate of 0.019λ. At the 84th hour, Bacillus kaustophilus has the lowest death rate of 0.152λ and Bacillus subtilis have the highest death rate of 0.097. Proper sanitation of pig house as well as the animals can help minimize the possible organisms found in the swine house which may serve as a major health hazards for people that consume pig and farmers in the pig house. It can also serve as food-borne pathogen posing potential health hazard when pork from infected animals are consumed.
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This review provides a state-of-the-art description of the performance of Sanger cycle sequencing of the 16S rRNA gene for routine identification of bacteria in the clinical microbiology laboratory. A detailed description of the technology and current methodology is outlined with a major focus on proper data analyses and interpretation of sequences. The remainder of the article is focused on a comprehensive evaluation of the application of this method for identification of bacterial pathogens based on analyses of 16S multialignment sequences.
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Introduction: Pertussis is a highly contagious respiratory infection caused by Bordetella pertussis and to minor extent B. parapertussis. Despite high vaccination coverage, epidemics persist worldwide. Laboratory testing with the capacity to support increasing demand and generate fast and accurate results is needed to promptly provide treatment to mitigate symptoms, prevent transmission and thus impact infection control and disease surveillance. Areas covered: This review will describe the features of the Simplexa™ Bordetella Direct Assay and compare this technology with other existing assays. Unmet needs and future directions will be discussed. Expert commentary: Resurgence of pertussis highlights the importance of reliable and accurate diagnosis. The Simplexa™ Bordetella Direct Assay provides an easy workflow, reduced hand-on time, less risk of contamination and rapid turnaround time. The use of efficient molecular assays in routine clinical laboratory is valuable for increasing demand, improvement of infection control and surveillance.
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Bordetella bronchiseptica is a gram-negative coccobacillus that infects animals, but rarely affects humans. B. bronchiseptica has been reported to cause disease in immunocompromised hosts. We present a case of a 61-year-old man with a renal transplant who developed B. bronchiseptica bacteremia likely as a result of close contact between dogs and his skin cancer biopsy sites. The patient was successfully treated with 2 weeks of oral levofloxacin. This case alerts physicians to B. bronchiseptica as a cause of bacteremia in solid organ transplant patients with exposure to animals.
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Découverte en 1995, Bordetella holmesii est une bactérie méconnue qui s’apparente à celle qui cause la coqueluche, Bordetella pertussis. A l’inverse de cette dernière, B. holmesii ne cause pas uniquement des infections respiratoires mais également des infections invasives, comme des méningites, endocardites ou arthrites. Sa non-identification est problématique, notamment lors d’infections respiratoires. En effet, en cas de coqueluche, les outils diagnostiques utilisés ne permettent pas de distinguer B. holmesii de B. pertussis. Cette erreur systématique biaise les analyse d’efficacité du vaccin contre la coqueluche, car celui-ci ne protège pas contre B. holmesii. Puisque toutes les infections respiratoires à B. holmesii sont actuellement diagnostiquées comme dues à B. pertussis, elles peuvent potentiellement être interprétées comme un échec vaccinal. Ce travail de thèse a donc pour but de résumer la littérature disponible sur B. holmesii afin de sensibiliser à sa problématique et de chercher si B. holmesii circule également en Suisse.
Article
A 24-year-old man with a history of HIV and large B cell lymphoma (currently in remission) presented with fever, dry cough and dizziness. His CD4+ count was undetectable, and the HIV viral load was 109 295 cop/mL. Physical examination revealed fever, hypotension and tachycardia with coarse breath sounds in the middle and lower chest zones bilaterally. Chest imaging showed diffuse abnormal micronodular and patchy infiltrates, without focal consolidation. A cavitary lesion was noted measuring 5×2 cm in axial dimensions within the left lower lobe and multiple small cystic lesions in the background. Bronchoalveolar lavage fluid culture grew Bordetella bronchiseptica . The patient was empirically treated with vancomycin and piperacillin–tazobactam for multifocal pneumonia with concerns for sepsis and was started on combined antiretroviral therapy (cART) with abacavir/dolutegravir/lamivudine. Symptoms improved after day 3 of therapy, and the patient was discharged home on 2 weeks of moxifloxacin, in addition to the cART and appropriate chemoprophylaxis.
Article
Objective: To investigate the clinical manifestations, microbiological data, and outcomes of Bordetella bronchiseptica (Bb) infections in patients with cancer. Methods: Review of electronic medical records of 24 patients with Bb infection, from 2000 to 2013. An infection was considered to be associated with Bb if both clinical manifestations plus microbial growth from infected sites were present. Results: Ten patients (42%) had a monomicrobial infection, whereas multiple pathogens in addition to Bb were isolated from the rest (14 patients, 58%). The most frequent sites of infection were the respiratory tract (18 patients, 75 %) and bloodstream (17%). The most frequently associated conditions were lymphopenia (71%), tobacco use (42%), and chemotherapeutic or immunosuppressive agents (33% each). Animal exposure was established in four patients. Overall, the response rate to treatment was 100% for monomicrobial and 79% for polymicrobial infections, respectively. Conclusions: Bb is an uncommon pathogen even in immunosuppressed patients. Predominant sites of infection are the respiratory tract and bloodstream. Bb should be considered pathogenic in immunocompromised hosts, particularly with history of zoonotic exposure, even if accompanied by co-pathogens. Therefore, contact with potential animal sources should be minimized. The infection ranges from mild to severe and has no specific clinical or radiographic manifestations.
Article
Antimicrobial Resistance in Bordetella bronchiseptica, Page 1 of 2 Abstract Bordetella bronchiseptica is involved in respiratory tract infections mainly in dogs and pigs but may also cause infections in humans. Valid and representative data on antimicrobial susceptibility of B. bronchiseptica is rare. Approved antimicrobial susceptibility testing methods have been published, but very few clinical breakpoints are available. The MIC values are low for most agents but high for β-lactam antibiotics and macrolides. Information on the genetic basis of resistance is scarce. For a small number of isolates that are resistant or show elevated MICs, the molecular basis of resistance was identified. Three tetracycline resistance genes, tet(A), tet(C), and tet(31), coding for major facilitator superfamily efflux pumps, were identified. Two other major facilitator superfamily exporter genes confer resistance to chloramphenicol (cmlB1) or to chloramphenicol and florfenicol (floR). Two class B chloramphenicol acetyltransferase genes (catB1 and catB3), which confer resistance to nonfluorinated phenicols by enzymatic inactivation, have been identified in B. bronchiseptica. Like the trimethoprim resistance genes dfrA1 and dfrB1, which code for trimethoprim-insensitive dihydrofolate reductases, the genes catB1 and catB3 were located on gene cassettes and found in class 1 integrons also harboring the sulfonamide resistance gene sul1. In addition, the gene sul2 has also been detected. Both sul1 and sul2 code for sulfonamide-insensitive dihydropteroate synthases. A gene cassette harboring the β-lactamase gene bla OXA-2 was also identified, whereas β-lactam resistance in B. bronchiseptica seems to be more likely due to reduced influx in combination with the species-specific β-lactamase encoded by bla BOR-1. The resistance genes were mostly located on conjugative plasmids.
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Outbreaks of hospital infections caused by multidrug resistant Acinetobacter baumannii strains are of increasing concern worldwide. Although it has been reported that particular outbreak strains are geographically widespread, little is known about the diversity and phylogenetic relatedness of A. baumannii clonal groups. Sequencing of internal portions of seven housekeeping genes (total 2,976 nt) was performed in 154 A. baumannii strains covering the breadth of known diversity and including representatives of previously recognized international clones, and in 19 representatives of other Acinetobacter species. Restricted amounts of diversity and a star-like phylogeny reveal that A. baumannii is a genetically compact species that suffered a severe bottleneck in the recent past, possibly linked to a restricted ecological niche. A. baumannii is neatly demarcated from its closest relative (genomic species 13TU) and other Acinetobacter species. Multilocus sequence typing analysis demonstrated that the previously recognized international clones I to III correspond to three clonal complexes, each made of a central, predominant genotype and few single locus variants, a hallmark of recent clonal expansion. Whereas antimicrobial resistance was almost universal among isolates of these and a novel international clone (ST15), isolates of the other genotypes were mostly susceptible. This dichotomy indicates that antimicrobial resistance is a major selective advantage that drives the ongoing rapid clonal expansion of these highly problematic agents of nosocomial infections.
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The molecular epidemiology of multidrug-resistant Acinetobacter baumannii was investigated in two intensive care units of the V. Monaldi university hospital in Naples, Italy, from May 2006 to December 2007. Genotype analysis by pulsed-field gel electrophoresis (PFGE), trilocus sequence-based typing (3LST), and multilocus sequence typing (MLST) of A. baumannii isolates from 71 patients identified two distinct genotypes, one assigned to PFGE group A, 3LST group 1, and ST2 in 14 patients and the other to PFGE group B, 3LST group 6, and ST78 in 71 patients, that we named ST2/A and ST78/B, respectively. Of these, ST2/A corresponded to European clone II identified in the same hospital during 2003 and 2004; ST78/B was a novel genotype that was isolated for the first time in May 2006 but became prevalent during 2007. The ST78/B profile was also identified in five patients from two additional hospitals in Naples during 2007. The ST2/A and ST78/B isolates were resistant to all antimicrobials tested, including carbapenems, but were susceptible to colistin. Both ST2/A and ST78/B isolates possessed a plasmid-borne carbapenem-hydrolyzing oxacillinase gene, blaOXA-58, flanked by ISAba2 and ISAba3 elements at the 5′ and 3′ ends, respectively. The selection of the novel ST78/B A. baumannii clone might have been favored by the acquisition of the blaOXA-58 gene.
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To assess dissemination of OXA-23-producing strains of Acinetobacter baumannii, we obtained 20 carbapenem-resistant, OXA-23-producing isolates from different regions. Their clonal relationship was assessed by pulsed-field gel electrophoresis and multilocus sequence typing. We identified 8 sequence types, including 4 novel types. All except 2 strains belonged to 2 main European clonal lineages. The blaOXA-23 gene was either located on the chromosome or on plasmids and associated with 4 genetic structures.
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Although B. bronchiseptica efficiently infects a wide range of mammalian hosts and efficiently spreads among them, it is rarely observed in humans. In contrast to the many other hosts of B. bronchiseptica, humans are host to the apparently specialized pathogen B. pertussis, the great majority having immunity due to vaccination, infection or both. Here we explore whether immunity to B. pertussis protects against B. bronchiseptica infection. In a murine model, either infection or vaccination with B. pertussis induced antibodies that recognized antigens of B. bronchiseptica and protected the lower respiratory tract of mice against three phylogenetically disparate strains of B. bronchiseptica that efficiently infect naïve animals. Furthermore, vaccination with purified B. pertussis-derived pertactin, filamentous hemagglutinin or the human acellular vaccine, Adacel, conferred similar protection against B. bronchiseptica challenge. These data indicate that individual immunity to B. pertussis affects B. bronchiseptica infection, and suggest that the high levels of herd immunity against B. pertussis in humans could explain the lack of observed B. bronchiseptica transmission. This could also explain the apparent association of B. bronchiseptica infections with an immunocompromised state.
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Although Bordetella bronchiseptica can infect and colonize immunocompromised humans, its role as a primary pathogen in pneumonia and other respiratory processes affecting those patients remains controversial. A case of cavitary pneumonia caused by B. bronchiseptica in an AIDS patient is presented, and the basis of the seemingly enhanced pathogenic potential of this isolate (designated 814) is investigated. B. bronchiseptica was the only microorganism recovered from sputum, bronchoalveolar lavage fluid, and samples taken through the protected brush catheter. Unlike previous work reporting the involvement of B. bronchiseptica in cases of pneumonia, antibiotic treatment selected on the basis of in vitro antibacterial activity resulted in clearance of the infection and resolution of the pulmonary infiltrate. Although isolate 814 produced reduced amounts of several major antigens including at least one Bvg-activated factor (pertactin), the molecular basis of this deficiency was found to be BvgAS independent since the defect persisted after the bvgAS locus of isolate 814 was replaced with a wild-type bvgAS allele. Despite its prominent phenotype, isolate 814 displayed only a modest yet a significant deficiency in its ability to colonize the respiratory tracts of immunocompetent rats at an early time point. Interestingly, the antibody response elicited by isolate 814 in these animals was almost undetectable. We propose that isolate 814 may be more virulent in immunocompromised patients due, at least in part, to its innate ability to produce low amounts of immunogenic factors which may be required at only normal levels for the interaction of this pathogen with its immunocompetent natural hosts.
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Bordetella respiratory infections are common in people (B. pertussis) and in animals (B. bronchiseptica). During the last two decades, much has been learned about the virulence determinants, pathogenesis, and immunity of Bordetella. Clinically, the full spectrum of disease due to B. pertussis infection is now understood, and infections in adolescents and adults are recognized as the reservoir for cyclic outbreaks of disease. DTaP vaccines, which are less reactogenic than DTP vaccines, are now in general use in many developed countries, and it is expected that the expansion of their use to adolescents and adults will have a significant impact on reducing pertussis and perhaps decrease the circulation of B. pertussis. Future studies should seek to determine the cause of the unique cough which is associated with Bordetella respiratory infections. It is also hoped that data gathered from molecular Bordetella research will lead to a new generation of DTaP vaccines which provide greater efficacy than is provided by today's vaccines.
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In this study a multilocus sequence typing (MLST) scheme for Acinetobacter baumannii was developed and evaluated by using 40 clinical A. baumannii isolates recovered from outbreaks in Spanish and German hospitals during the years 1990 to 2001, as well as isolates from other European hospitals and two DSMZ reference strains of A. baumannii. For comparison, two isolates of Acinetobacter species 13 (sensu Tjernberg and Ursing), two clinical isolates, and three DSMZ strains of A. calcoaceticus (both belonging to the A. calcoaceticus-A. baumannii complex) were also investigated. Primers were designed for conserved regions of housekeeping genes, and 305- to 513-bp internal fragments of seven such genes—gltA, gyrB, gdhB, recA, cpn60, gpi, and rpoD—were sequenced for all strains. The number of alleles at individual loci ranged from 6 to 12, and a total of 20 allelic profiles or sequence types were distinguished among the investigated A. baumannii strains. The MLST data were in high concordance with the epidemiologic typing results generated by pulsed-field gel electrophoresis and amplified fragment length polymorphism fingerprinting. The MLST scheme provides a high level of resolution and an excellent tool for studying the population structure and long-term epidemiology of A. baumannii.
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Bordetella bronchiseptica (BBS) est un agent fréquent d'infections du tractus respiratoire des mammifères. Une revue en référençait 25 cas chez l'homme en 1991. Soixante douze isolements de 52 patients dont 10 pédiatriques ont pu être colligés en France. Tous intéressent l'arbre respiratoire. Dans 25 cas sur 28 on retrouve une pathologie favorisante broncho-pulmonaire ou immuno-dépression acquise. BBS se comporte comme un pathogène opportuniste chez l'homme. Dans tous les cas se manifeste une pathologie bronchitique et parenchymateuse dans la moitié environ. BBS synthétise toutes les toxines de B. pertussis à l'exception de la toxine de pertussis. BBS possède une résistance naturelle à de nombreuses bêtalactamines dont le céfotaxime, la ceftriaxone et les C3G orales. L'imipénème, les macrolides en C 14 (érythromycine), en C 15 (azithromycine) sont très actifs mais ceux en C 16 (josamycine) sont sans action. La minocycline, le cotrimoxazole et le chloramphénicol sont actifs sur la plupart des souches. L'amendement des signes respiratoires est long, les rechutes nombreuses. Les études sérologiques chez les sujets en contact avec les animaux de rente ou de compagnie montrent la fréquence des réponses sérologiques confirmant la circulation de BBS chez l'homme. Les infections humaines respiratoires à BBS constituent une entité réelle particulière, certes rare. La poursuite de leur étude reste du plus grand intérêt tant pour leur meilleure connaissance en elle-même que pour les renseignements comparatifs importants que l'on peut en tirer vis-à-vis de B. pertussis, agent de la coqueluche (physiopathologie, antibiothérapie, antigènes vaccinaux).
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In this study, multilocus sequence typing (MLST) was used to describe the genetic backgrounds of carbapenem-resistant Acinetobacter baumannii (CRAB) and carbapenem-susceptible A. baumannii (CSAB) from multiple cities of China. One hundred and fifty-two CRAB and 74 CSAB isolates obtained from 16 cities of China were selected for molecular characterization by MLST. eBURST was used to cluster sequence types (STs) into clonal complex (CCs) and infer evolutionary descent. PCR was used to detect carbapenemase-encoding genes and bla(AmpC) with the upstream element ISAba1. CSAB showed more diverse genetic backgrounds than CRAB since 36 distinct STs were identified in CSAB while only 8 STs were identified in CRAB. ST22 and its three single-locus variants, all clustered into CC22, were the most prominent STs, accounting for 86.8% of CRAB and 45.9% of CSAB, distributed in all 16 cities and possessing more noticeable antibiotic resistance than other STs. PCR amplification was positive for bla(OXA-23) in most CRAB isolates but negative in CSAB isolates. The presence of ISAba1 upstream of bla(AmpC) was variable in distinct STs of CRAB. eBURST reveals that CC22 is the largest group in the Pubmlst database, which also contains ST6 previously identified in a European clone II isolate as a member of a subgroup of CC22. We describe the wide dissemination of CRAB CC22 in China. The close relatedness between CC22 and European clone II implies the probable global spread of CC22. It is inferred that ST22-CSAB evolves to ST22-CRAB through acquiring bla(OXA-23) as a determinative factor.
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We have investigated the molecular epidemiology and distribution of carbapenemase genes in 492 imipenem-non-susceptible Acinetobacter baumannii worldwide isolates (North and Latin America, Europe, Asia, South Africa and Australia). MICs were determined by broth microdilution and Etest. The presence of carbapenemase-encoding genes was investigated by PCR. Molecular epidemiology was performed by repetitive sequence-based PCR (rep-PCR; DiversiLab), sequence-type multiplex PCR and PFGE. Imipenem non-susceptibility was associated with ISAba1 upstream of the intrinsic bla(OXA-51-like) or the acquired carbapenemase bla(OXA-23-like), bla(OXA-40-like) or bla(OXA-58-like). Isolates were grouped into eight distinct clusters including European clones I, II and III. European clone II was the largest (246 isolates) and most widespread group (USA, pan-Europe, Israel, Asia, Australia and South Africa). The global dissemination of eight carbapenem-resistant lineages illustrates the success this organism has had in epidemic spread. The acquired OXA enzymes are widely distributed but are not the sole carbapenem resistance determinant in A. baumannii.
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This study examines the potential of Bordetella bronchiseptica to act as a human pathogen. After encountering two patients from whom B. bronchiseptica was isolated, we searched the literature and found 23 reports in which a human infection was reported in association with B. bronchiseptica. As a basis for evaluating these cases, we summarize the literature about the current microbiological status of B. bronchiseptica, the pathology and pathogenic mechanisms associated with the microorganism, and the likelihood of it acting as a commensal or colonizer. From this review we conclude that B. bronchiseptica has been rarely isolated from humans despite their considerable exposure to animal sources. Evidence suggests that B. bronchiseptica may be rarely encountered as a commensal or colonizer of the respiratory tract of humans and rarely in association with infection. When found as a probable pathogen, most infections have been respiratory tract in origin and have occurred in severely compromised hosts.
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One hundred and fifty-two predominantly feline isolates of Bordetella bronchiseptica were tested for their susceptibility to seven antimicrobial agents using an agar dilution method. The majority of isolates tested by the agar dilution method were resistant to trimethoprim (MIC90 500 micrograms/ml) and ampicillin (MIC90 > 32 micrograms/ml) but sensitive to tetracycline, doxycycline and enrofloxacin (MIC90 2 micrograms/ml for all three agents). The isolates showed a spectrum of susceptibility to sulphadiazine and clavulanate potentiated amoxycillin. The MIC's of twenty-nine of the 152 isolates were then compared for five of the antimicrobial agents using the E-test (AB Biodisk, Sweden), a recently introduced method for measuring the MIC's of antimicrobial agents based on the diffusion of a pre-defined antibiotic gradient from a plastic strip. Comparisons with the E-test demonstrated an overall agreement (+/- 1 log2 dilution) with the agar dilution method of 79.4% and an agreement within +/- 2 log2 dilutions of 96.2%.
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Bordetella bronchiseptica are small, pleomorphic Gram-negative coccobacilli which are commensal organisms in the upper respiratory tract of many wild and domestic animals ('kennel cough' in dogs). While it is common for health care providers to ask about exposure to ill family/friends, most do not routinely inquire about the health or immunization status of household pets. We report two cases of B. bronchiseptica pneumonia in lung transplant recipients [cystic fibrosis (CF); ages 10 and 15 yr; one male] who contracted B. bronchiseptica from pet dogs. We compared their course and outcome to four children (two CF, one congenital heart disease and one Duchenne's muscular dystrophy; four males, age range 6 months to 14 yr) with B. bronchiseptica cultured from the respiratory tract. Two of the four patients also acquired their illnesses from pet dogs and two from unknown sources. One lung transplant recipient expired from progressive respiratory failure. We conclude that B. bronchiseptica can cause serious infections in both immunosuppressed and immunocompetent children. We speculate that a detailed history of exposure to ill pets (particularly dogs), and the immunization status of all pets should be included in the routine evaluation of all pediatric transplant recipients.
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A recent resurgence in the number of cases of whooping cough, and other respiratory diseases caused by members of the bordetellae, in vaccinated populations has demonstrated the need for a thorough understanding of vaccine-induced immunity to facilitate more intelligent vaccine design. In this work, we use a murine model of respiratory infection using the highly successful animal pathogen, Bordetella bronchiseptica. Since previously infected animals have been shown to resist re-infection by B. bronchiseptica, we sought to examine the differences between vaccine-induced immunity and infection-induced immunity. Both prior infection and vaccination conferred nearly complete protection in the lungs, however, only prior infection resulted in significant protection in the upper respiratory tract. While immunity induced by prior infection offered significant protection even in the absence of complement or FcgammaRs, vaccination-induced protection required both complement and FcgammaRs. Although vaccination induced higher titers of B. bronchiseptica-specific antibodies, this serum was less effective than infection-induced serum in clearing bacteria from the lower respiratory tract. Together these findings highlight substantial differences between the mechanisms involved in vaccine- and infection-induced protective immunity.
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Representatives (n = 31) of outbreak strains of Acinetobacter baumannii from five countries fell into three clear groups, designated Groups 1-3, based on their ompA (outer-membrane protein A), csuE (part of a pilus assembly system required for biofilm formation) and bla(OXA-51-like) (the intrinsic carbapenemase gene in A. baumannii) gene sequences. With the exception of the closely related alleles within the Group 1 clonal complex, alleles at each locus were highly distinct from each other, with a minimum of 14 nucleotide differences between any two alleles. Isolates within a group shared the same combination of alleles at the three loci, providing compelling evidence that the outbreak strains investigated belonged to three clonal lineages. These corresponded to the previously identified European clones I-III. Sequence differences among the alleles were used to design multiplex PCRs to rapidly assign isolates belonging to particular genotypes to sequence groups. In the UK, genotypes belonging to the Group 1 clonal complex have been particularly successful, accounting for the vast majority of isolates referred from hospitals experiencing problems with Acinetobacter.
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Bordetella spp. are not normally included when considering the opportunistic bacterial species that are typically involved in respiratory tract infections in individuals with cystic fibrosis (CF). By using a combination of bacterial genotyping and 16S rDNA sequencing, Bordetella spp. were identified in cultures obtained from 43 individuals with CF. Most (n = 23) patients were infected with Bordetella bronchiseptica/parapertussis; five were infected with Bordetella hinzii, four with Bordetella petrii, three with Bordetella avium, and eight with unidentified Bordetella spp. Consideration should be given to the presence of these organisms in the evaluation of CF sputum cultures.
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To further expand the limited multilocus sequence typing (MLST) database for Acinetobacter baumannii, 53 clinical isolates from various outbreaks in Europe and the USA, collected between 1991 and 2004, plus the A. baumannii reference strain ATCC 19606(T) and 20 clinical Acinetobacter genomic species 13TU isolates from the same period, were analyzed using a new MLST scheme based on fragments of the gltA, gyrB, gdhB, recA, cpn60, gpi and rpoD genes. Data were compared with typing results generated using pulsed-field gel electrophoresis (PFGE) and randomly amplified polymorphic DNA (RAPD)-PCR. In total, 50 sequence types (STs) were distinguished among the A. baumannii isolates investigated, and the MLST data were in high concordance with the PFGE and RAPD-PCR results. Only five clonal complexes were identified by eBURST analysis, including the 21 STs listed in a previous study, suggesting high diversity among the A. baumannii isolates. With one exception, there was no relatedness among isolates from outbreaks in different countries (Europe) or regions (USA). No intercontinental spread was revealed. Acinetobacter genomic species 13TU isolates could also be analyzed using the A. baumannii MLST scheme (18 different STs) and could be distinguished from A. baumannii isolates according to characteristic sequences. It was concluded that the MLST scheme provides a high level of resolution and is a promising tool for studying the epidemiology of A. baumannii and Acinetobacter genomic species 13TU.
eBURST: infer-ring patterns of evolutionary descent among clusters of related bac-terial genotypes from multilocus sequence typing data
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Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. eBURST: infer-ring patterns of evolutionary descent among clusters of related bac-terial genotypes from multilocus sequence typing data. J Bacteriol 2004; 186: 1518–1530.
Population genetics of bacterial patho-gens Molecular medical microbiology
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Spratt BG, Feil EJ, Smith NH. Population genetics of bacterial patho-gens. In: Sussman M, ed. Molecular medical microbiology. London: Academic Press, 2001; 445–484.