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      Bacillus cereus Induces Severe Infections in Preterm Neonates: Implication at the Hospital and Human Milk Bank Level

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          Abstract

          Human breast milk (HBM) is a source of essential nutrients for infants and is particularly recommended for preterm neonates when their own mother’s milk is not available. It provides protection against infections and decreases necrotizing enterocolitis and cardiovascular diseases. Nevertheless, HBM spoilage can occur due to contamination by pathogens, and the risk of a shortage of HBM is very often present. B. cereus is the most frequent ubiquitous bacteria responsible for HBM being discarded. It can contaminate HBM at all stages, from its collect point to the storage and delivery. B. cereus can induce severe infection in newborns with very low birth weight, with sometimes fatal outcomes. Although the source of contamination is rarely identified, in some cases, HBM was suspected as a potential source. Even if the risk is low, as infection due to B. cereus in preterm infants should not be overlooked, human milk banks follow strict procedures to avoid contamination, to accurately identify remaining bacteria following pasteurization and to discard non-compliant milk samples. In this review, we present a literature overview of B. cereus infections reported in neonates and the suspected sources of contamination. We highlight the procedures followed by the human milk banks from the collection of the milk to its microbiological characterization in Europe. We also present improved detection and decontamination methods that might help to decrease the risk and to preserve the public’s confidence in this vital biological product for infants whose mothers cannot breastfeed.

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          Most cited references78

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          The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2017

          (2018)
          Abstract This report of the European Food Safety Authority and the European Centre for Disease Prevention and Control presents the results of zoonoses monitoring activities carried out in 2017 in 37 European countries (28 Member States (MS) and nine non‐MS). Campylobacteriosis was the commonest reported zoonosis and its EU trend for confirmed human cases increasing since 2008 stabilised during 2013–2017. The decreasing EU trend for confirmed human salmonellosis cases since 2008 ended during 2013–2017, and the proportion of human Salmonella Enteritidis cases increased, mostly due to one MS starting to report serotype data. Sixteen MS met all Salmonella reduction targets for poultry, whereas 12 MS failed meeting at least one. The EU flock prevalence of target Salmonella serovars in breeding hens, laying hens, broilers and fattening turkeys decreased or remained stable compared to 2016, and slightly increased in breeding turkeys. Salmonella results on pig carcases and target Salmonella serovar results for poultry from competent authorities tended to be generally higher compared to those from food business operators. The notification rate of human listeriosis further increased in 2017, despite Listeria seldom exceeding the EU food safety limit in ready‐to‐eat food. The decreasing EU trend for confirmed yersiniosis cases since 2008 stabilised during 2013–2017. The number of confirmed shiga toxin‐producing Escherichia coli (STEC) infections in humans was stable. A total of 5,079 food‐borne (including waterborne) outbreaks were reported. Salmonella was the commonest detected agent with S. Enteritidis causing one out of seven outbreaks, followed by other bacteria, bacterial toxins and viruses. The agent was unknown in 37.6% of all outbreaks. Salmonella in eggs and Salmonella in meat and meat products were the highest risk agent/food pairs. The report further summarises trends and sources for bovine tuberculosis, Brucella, Trichinella, Echinococcus, Toxoplasma, rabies, Coxiella burnetii (Q fever), West Nile virus and tularaemia.
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            Bacillus cereus, a volatile human pathogen.

            Bacillus cereus is a Gram-positive aerobic or facultatively anaerobic, motile, spore-forming, rod-shaped bacterium that is widely distributed environmentally. While B. cereus is associated mainly with food poisoning, it is being increasingly reported to be a cause of serious and potentially fatal non-gastrointestinal-tract infections. The pathogenicity of B. cereus, whether intestinal or nonintestinal, is intimately associated with the production of tissue-destructive exoenzymes. Among these secreted toxins are four hemolysins, three distinct phospholipases, an emesis-inducing toxin, and proteases. The major hurdle in evaluating B. cereus when isolated from a clinical specimen is overcoming its stigma as an insignificant contaminant. Outside its notoriety in association with food poisoning and severe eye infections, this bacterium has been incriminated in a multitude of other clinical conditions such as anthrax-like progressive pneumonia, fulminant sepsis, and devastating central nervous system infections, particularly in immunosuppressed individuals, intravenous drug abusers, and neonates. Its role in nosocomial acquired bacteremia and wound infections in postsurgical patients has also been well defined, especially when intravascular devices such as catheters are inserted. Primary cutaneous infections mimicking clostridial gas gangrene induced subsequent to trauma have also been well documented. B. cereus produces a potent beta-lactamase conferring marked resistance to beta-lactam antibiotics. Antimicrobials noted to be effective in the empirical management of a B. cereus infection while awaiting antimicrobial susceptibility results for the isolate include ciprofloxacin and vancomycin.
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              From soil to gut: Bacillus cereus and its food poisoning toxins.

              Bacillus cereus is widespread in nature and frequently isolated from soil and growing plants, but it is also well adapted for growth in the intestinal tract of insects and mammals. From these habitats it is easily spread to foods, where it may cause an emetic or a diarrhoeal type of food-associated illness that is becoming increasingly important in the industrialized world. The emetic disease is a food intoxication caused by cereulide, a small ring-formed dodecadepsipeptide. Similar to the virulence determinants that distinguish Bacillus thuringiensis and Bacillus anthracis from B. cereus, the genetic determinants of cereulide are plasmid-borne. The diarrhoeal syndrome of B. cereus is an infection caused by vegetative cells, ingested as viable cells or spores, thought to produce protein enterotoxins in the small intestine. Three pore-forming cytotoxins have been associated with diarrhoeal disease: haemolysin BL (Hbl), nonhaemolytic enterotoxin (Nhe) and cytotoxin K. Hbl and Nhe are homologous three-component toxins, which appear to be related to the monooligomeric toxin cytolysin A found in Escherichia coli. This review will focus on the toxins associated with foodborne diseases frequently caused by B. cereus. The disease characteristics are described, and recent findings regarding the associated toxins are discussed, as well as the present knowledge on virulence regulation.
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                Author and article information

                Journal
                Toxins (Basel)
                Toxins (Basel)
                toxins
                Toxins
                MDPI
                2072-6651
                07 February 2021
                February 2021
                : 13
                : 2
                : 123
                Affiliations
                [1 ]Micalis Institute, INRAE, AgroParisTech, Université Paris-Saclay, 78350 Jouy-en-Josas, France; delphine.cormontagne@ 123456inrae.fr (D.C.); jasmina.vidic@ 123456inrae.fr (J.V.); francesco.rizzotto@ 123456inrae.fr (F.R.)
                [2 ]Région Île-de-France Human Milk Bank, Hôpital Necker-Enfants Malades, Assistance Publique-Hôpitaux de Paris, 75015 Paris, France; virginie.rigourd@ 123456aphp.fr
                [3 ]Department of Clinical Microbiology, Necker Enfants-Malades Hospital, AP-HP, 75015 Paris, France; emmanuelle.bille@ 123456aphp.fr
                [4 ]INSERM U1151-CNRS UMR 8253, Institut Necker-Enfants Malades, Université de Paris, 75015 Paris, France
                Author notes
                [* ]Correspondence: nalini.ramarao@ 123456inrae.fr
                [†]

                These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0001-9037-7490
                https://orcid.org/0000-0002-8549-8199
                https://orcid.org/0000-0001-6045-8521
                Article
                toxins-13-00123
                10.3390/toxins13020123
                7915446
                33562185
                d9e203fa-0b71-45a0-9af5-ba656aa58732
                © 2021 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 15 December 2020
                : 02 February 2021
                Categories
                Review

                Molecular medicine
                bacillus cereus,human breast milk,preterm neonates
                Molecular medicine
                bacillus cereus, human breast milk, preterm neonates

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