Aerobic spore-forming bacteria in powdered infant formula: Enumeration, identification by MALDI-TOF mass spectrometry (MS), presence of toxin genes and rpoB gene typing
This study aimed to assess the counts and biodiversity characterization of aerobic sporeforming bacteria (ASB) in powdered infant formula (PIF). Fifty-four (n = 54) samples of PIF of three brands were analyzed for mesophilic aerobic bacteria, and ASB counts. ASB isolated from PIF were assessed for t...
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| Veröffentlicht in: | International journal of food microbiology 2022-05, Vol.368, p.109613-109613, Article 109613 |
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| creator | Mezian, Larbi Chincha, Alexandra I.A. Vecchione, Alessandra Ghelardi, Emilia Bonatto, José Matheus C. Marsaioli, Anita Jocelyne Campelo, Pedro H. Benamar, Ibrahim Moussaoui, Abd Allah Sant'Ana, Anderson S. Moussa-Boudjemaa, Boumediene |
| description | This study aimed to assess the counts and biodiversity characterization of aerobic sporeforming bacteria (ASB) in powdered infant formula (PIF). Fifty-four (n = 54) samples of PIF of three brands were analyzed for mesophilic aerobic bacteria, and ASB counts. ASB isolated from PIF were assessed for their ability to produce spoilage enzymes and hemolytic activity and further identified by MALDI-TOF mass spectrometry. Then, the isolates were subjected to rpoB gene typing and assessment of bceT, entFM, nhe (A, B, C), and hbl (A, B, C) toxin genes. The main species isolated were B. licheniformis (54%), followed by B. cereus (33%) and B. subtilis (5%). The ASB counts ranged from 1 to 4 log CFU/g, and the mean was 2.9 log CFU/g for mesophilic aerobic sporeforming bacteria (MSC) and 2.5 log CFU/g for thermophilic aerobic sporeforming bacteria (TSC). Most PIF samples presented MSC and TSC counts between 2 and 3 log CFU/g. A total of 13%, 50%, and 37% of the samples presented MSC counts from |
| doi_str_mv | 10.1016/j.ijfoodmicro.2022.109613 |
| format | Article |
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•Microbiological quality of 54 samples of powdered infant formula (PIF) was assessed.•Aerobic sporeforming bacteria (ASB) counts, pheno- and genotypically characterized•B. licheniformis, B. cereus and B. subtilis were the main species isolated from PIF.•B. cereus harbored nhe gene (100%), 60% entFM, 44% cytK, 32% bceT, 28% hbl genes.•The rpoB based phylogenetic tree provided high resolution among Bacillus species.</description><identifier>ISSN: 0168-1605</identifier><identifier>EISSN: 1879-3460</identifier><identifier>DOI: 10.1016/j.ijfoodmicro.2022.109613</identifier><identifier>PMID: 35278798</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Aerobic bacteria ; Baby foods ; Bacillus ; Bacillus cereus - genetics ; Bacteria ; Bacteria, Aerobic ; Biodiversity ; Dried foods ; Enumeration ; Food Microbiology ; Genes ; Heat resistant bacteria ; Humans ; Infant foods ; Infant Formula ; Infants ; Lecithinase ; Mass spectrometry ; Mass spectroscopy ; NHE gene ; Paenibacillus ; Phylogeny ; Powders ; RpoB protein ; Scientific imaging ; Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization ; Spectroscopy ; Spoilage ; Spore-forming bacteria ; Spores, Bacterial - genetics ; Thermophilic bacteria ; Toxin ; Toxins</subject><ispartof>International journal of food microbiology, 2022-05, Vol.368, p.109613-109613, Article 109613</ispartof><rights>2022 Elsevier B.V.</rights><rights>Copyright © 2022 Elsevier B.V. All rights reserved.</rights><rights>Copyright Elsevier BV May 2, 2022</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c405t-9314857776cf699f84e92af305aefd895fb7b615ef6297081cdb2aa9e9968fba3</citedby><cites>FETCH-LOGICAL-c405t-9314857776cf699f84e92af305aefd895fb7b615ef6297081cdb2aa9e9968fba3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.ijfoodmicro.2022.109613$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35278798$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mezian, Larbi</creatorcontrib><creatorcontrib>Chincha, Alexandra I.A.</creatorcontrib><creatorcontrib>Vecchione, Alessandra</creatorcontrib><creatorcontrib>Ghelardi, Emilia</creatorcontrib><creatorcontrib>Bonatto, José Matheus C.</creatorcontrib><creatorcontrib>Marsaioli, Anita Jocelyne</creatorcontrib><creatorcontrib>Campelo, Pedro H.</creatorcontrib><creatorcontrib>Benamar, Ibrahim</creatorcontrib><creatorcontrib>Moussaoui, Abd Allah</creatorcontrib><creatorcontrib>Sant'Ana, Anderson S.</creatorcontrib><creatorcontrib>Moussa-Boudjemaa, Boumediene</creatorcontrib><title>Aerobic spore-forming bacteria in powdered infant formula: Enumeration, identification by MALDI-TOF mass spectrometry (MS), presence of toxin genes and rpoB gene typing</title><title>International journal of food microbiology</title><addtitle>Int J Food Microbiol</addtitle><description>This study aimed to assess the counts and biodiversity characterization of aerobic sporeforming bacteria (ASB) in powdered infant formula (PIF). Fifty-four (n = 54) samples of PIF of three brands were analyzed for mesophilic aerobic bacteria, and ASB counts. ASB isolated from PIF were assessed for their ability to produce spoilage enzymes and hemolytic activity and further identified by MALDI-TOF mass spectrometry. Then, the isolates were subjected to rpoB gene typing and assessment of bceT, entFM, nhe (A, B, C), and hbl (A, B, C) toxin genes. The main species isolated were B. licheniformis (54%), followed by B. cereus (33%) and B. subtilis (5%). The ASB counts ranged from 1 to 4 log CFU/g, and the mean was 2.9 log CFU/g for mesophilic aerobic sporeforming bacteria (MSC) and 2.5 log CFU/g for thermophilic aerobic sporeforming bacteria (TSC). Most PIF samples presented MSC and TSC counts between 2 and 3 log CFU/g. A total of 13%, 50%, and 37% of the samples presented MSC counts from <2 log CFU/g, between 2 and 3 log CFU/g and between 3 and 4 log CFU/g, respectively. Among the ASB isolates, 97% had protease, 84% hydrolyzed starch, 66% had hemolytic activity, and 61% had lecithinase activity. A total of 44 out of 120 isolates harbored at least one toxin gene; 56% for B. cereus, 34% for B licheniformis, and less than 5% for B. subtilis, B pumilus, and L. sphaericus. All B. cereus isolates harbored the nhe gene, 60% entFM, 44% cytK, 32% bceT, and 28% hbl genes. Besides, 17% of B. licheniformis harbored nhe. A small proportion of B. subtilis, B. pumilus, and L. sphaericus carried toxin genes. The rpoB based phylogenetic tree provided high resolution among Bacillus species. The findings of this study provide insights into the phenotypic and genotypic biodiversity of Bacillus present in PIF.
•Microbiological quality of 54 samples of powdered infant formula (PIF) was assessed.•Aerobic sporeforming bacteria (ASB) counts, pheno- and genotypically characterized•B. licheniformis, B. cereus and B. subtilis were the main species isolated from PIF.•B. cereus harbored nhe gene (100%), 60% entFM, 44% cytK, 32% bceT, 28% hbl genes.•The rpoB based phylogenetic tree provided high resolution among Bacillus species.</description><subject>Aerobic bacteria</subject><subject>Baby foods</subject><subject>Bacillus</subject><subject>Bacillus cereus - genetics</subject><subject>Bacteria</subject><subject>Bacteria, Aerobic</subject><subject>Biodiversity</subject><subject>Dried foods</subject><subject>Enumeration</subject><subject>Food Microbiology</subject><subject>Genes</subject><subject>Heat resistant bacteria</subject><subject>Humans</subject><subject>Infant foods</subject><subject>Infant Formula</subject><subject>Infants</subject><subject>Lecithinase</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>NHE gene</subject><subject>Paenibacillus</subject><subject>Phylogeny</subject><subject>Powders</subject><subject>RpoB protein</subject><subject>Scientific imaging</subject><subject>Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization</subject><subject>Spectroscopy</subject><subject>Spoilage</subject><subject>Spore-forming bacteria</subject><subject>Spores, Bacterial - genetics</subject><subject>Thermophilic bacteria</subject><subject>Toxin</subject><subject>Toxins</subject><issn>0168-1605</issn><issn>1879-3460</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkcFu1DAQhi0EosvCKyAjLq3ULI4TOzG3ZWmh0lY9UM6W44wrRxs72A5034jHxNstCHHiZI_1jf_RfAi9KcmqJCV_N6zsYLzvR6uDX1FCaX4XvKyeoEXZNqKoak6eokVm26LkhJ2gFzEOhBBWVeQ5OqkYbTLXLtDPNQTfWY3j5AMUxofRujvcKZ0gWIWtw5P_0UOAPt-NcgkfmHmn3uMLN48QVLLenWPbg0vWWP1Q426Pr9fbj1fF7c0lHlWMOQB0Cn6EFPb49PrL2TmeAkRwGrA3OPn7nHUHDiJWrsdh8h8eSpz2Ux7pJXpm1C7Cq8dzib5eXtxuPhfbm09Xm_W20DVhqRBVWbesaRquDRfCtDUIqkxFmALTt4KZrul4ycBwKhrSlrrvqFIChOCt6VS1RKfHf6fgv80Qkxxt1LDbKQd-jpLyqm0o4zXN6Nt_0MHPweXpMsUq1tI600skjlR2FWMAI6dgRxX2siTyoFMO8i-d8qBTHnXm3tePCXM3Qv-n87e_DGyOAOSVfLcQZNT2sNLehrxu2Xv7HzG_AByduJo</recordid><startdate>20220502</startdate><enddate>20220502</enddate><creator>Mezian, Larbi</creator><creator>Chincha, Alexandra I.A.</creator><creator>Vecchione, Alessandra</creator><creator>Ghelardi, Emilia</creator><creator>Bonatto, José Matheus C.</creator><creator>Marsaioli, Anita Jocelyne</creator><creator>Campelo, Pedro H.</creator><creator>Benamar, Ibrahim</creator><creator>Moussaoui, Abd Allah</creator><creator>Sant'Ana, Anderson S.</creator><creator>Moussa-Boudjemaa, Boumediene</creator><general>Elsevier B.V</general><general>Elsevier BV</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QO</scope><scope>7QR</scope><scope>7T7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20220502</creationdate><title>Aerobic spore-forming bacteria in powdered infant formula: Enumeration, identification by MALDI-TOF mass spectrometry (MS), presence of toxin genes and rpoB gene typing</title><author>Mezian, Larbi ; Chincha, Alexandra I.A. ; Vecchione, Alessandra ; Ghelardi, Emilia ; Bonatto, José Matheus C. ; Marsaioli, Anita Jocelyne ; Campelo, Pedro H. ; Benamar, Ibrahim ; Moussaoui, Abd Allah ; Sant'Ana, Anderson S. ; Moussa-Boudjemaa, Boumediene</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c405t-9314857776cf699f84e92af305aefd895fb7b615ef6297081cdb2aa9e9968fba3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Aerobic bacteria</topic><topic>Baby foods</topic><topic>Bacillus</topic><topic>Bacillus cereus - genetics</topic><topic>Bacteria</topic><topic>Bacteria, Aerobic</topic><topic>Biodiversity</topic><topic>Dried foods</topic><topic>Enumeration</topic><topic>Food Microbiology</topic><topic>Genes</topic><topic>Heat resistant bacteria</topic><topic>Humans</topic><topic>Infant foods</topic><topic>Infant Formula</topic><topic>Infants</topic><topic>Lecithinase</topic><topic>Mass spectrometry</topic><topic>Mass spectroscopy</topic><topic>NHE gene</topic><topic>Paenibacillus</topic><topic>Phylogeny</topic><topic>Powders</topic><topic>RpoB protein</topic><topic>Scientific imaging</topic><topic>Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization</topic><topic>Spectroscopy</topic><topic>Spoilage</topic><topic>Spore-forming bacteria</topic><topic>Spores, Bacterial - genetics</topic><topic>Thermophilic bacteria</topic><topic>Toxin</topic><topic>Toxins</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mezian, Larbi</creatorcontrib><creatorcontrib>Chincha, Alexandra I.A.</creatorcontrib><creatorcontrib>Vecchione, Alessandra</creatorcontrib><creatorcontrib>Ghelardi, Emilia</creatorcontrib><creatorcontrib>Bonatto, José Matheus C.</creatorcontrib><creatorcontrib>Marsaioli, Anita Jocelyne</creatorcontrib><creatorcontrib>Campelo, Pedro H.</creatorcontrib><creatorcontrib>Benamar, Ibrahim</creatorcontrib><creatorcontrib>Moussaoui, Abd Allah</creatorcontrib><creatorcontrib>Sant'Ana, Anderson S.</creatorcontrib><creatorcontrib>Moussa-Boudjemaa, Boumediene</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>International journal of food microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mezian, Larbi</au><au>Chincha, Alexandra I.A.</au><au>Vecchione, Alessandra</au><au>Ghelardi, Emilia</au><au>Bonatto, José Matheus C.</au><au>Marsaioli, Anita Jocelyne</au><au>Campelo, Pedro H.</au><au>Benamar, Ibrahim</au><au>Moussaoui, Abd Allah</au><au>Sant'Ana, Anderson S.</au><au>Moussa-Boudjemaa, Boumediene</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Aerobic spore-forming bacteria in powdered infant formula: Enumeration, identification by MALDI-TOF mass spectrometry (MS), presence of toxin genes and rpoB gene typing</atitle><jtitle>International journal of food microbiology</jtitle><addtitle>Int J Food Microbiol</addtitle><date>2022-05-02</date><risdate>2022</risdate><volume>368</volume><spage>109613</spage><epage>109613</epage><pages>109613-109613</pages><artnum>109613</artnum><issn>0168-1605</issn><eissn>1879-3460</eissn><abstract>This study aimed to assess the counts and biodiversity characterization of aerobic sporeforming bacteria (ASB) in powdered infant formula (PIF). Fifty-four (n = 54) samples of PIF of three brands were analyzed for mesophilic aerobic bacteria, and ASB counts. ASB isolated from PIF were assessed for their ability to produce spoilage enzymes and hemolytic activity and further identified by MALDI-TOF mass spectrometry. Then, the isolates were subjected to rpoB gene typing and assessment of bceT, entFM, nhe (A, B, C), and hbl (A, B, C) toxin genes. The main species isolated were B. licheniformis (54%), followed by B. cereus (33%) and B. subtilis (5%). The ASB counts ranged from 1 to 4 log CFU/g, and the mean was 2.9 log CFU/g for mesophilic aerobic sporeforming bacteria (MSC) and 2.5 log CFU/g for thermophilic aerobic sporeforming bacteria (TSC). Most PIF samples presented MSC and TSC counts between 2 and 3 log CFU/g. A total of 13%, 50%, and 37% of the samples presented MSC counts from <2 log CFU/g, between 2 and 3 log CFU/g and between 3 and 4 log CFU/g, respectively. Among the ASB isolates, 97% had protease, 84% hydrolyzed starch, 66% had hemolytic activity, and 61% had lecithinase activity. A total of 44 out of 120 isolates harbored at least one toxin gene; 56% for B. cereus, 34% for B licheniformis, and less than 5% for B. subtilis, B pumilus, and L. sphaericus. All B. cereus isolates harbored the nhe gene, 60% entFM, 44% cytK, 32% bceT, and 28% hbl genes. Besides, 17% of B. licheniformis harbored nhe. A small proportion of B. subtilis, B. pumilus, and L. sphaericus carried toxin genes. The rpoB based phylogenetic tree provided high resolution among Bacillus species. The findings of this study provide insights into the phenotypic and genotypic biodiversity of Bacillus present in PIF.
•Microbiological quality of 54 samples of powdered infant formula (PIF) was assessed.•Aerobic sporeforming bacteria (ASB) counts, pheno- and genotypically characterized•B. licheniformis, B. cereus and B. subtilis were the main species isolated from PIF.•B. cereus harbored nhe gene (100%), 60% entFM, 44% cytK, 32% bceT, 28% hbl genes.•The rpoB based phylogenetic tree provided high resolution among Bacillus species.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>35278798</pmid><doi>10.1016/j.ijfoodmicro.2022.109613</doi><tpages>1</tpages></addata></record> |
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| ispartof | International journal of food microbiology, 2022-05, Vol.368, p.109613-109613, Article 109613 |
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| subjects | Aerobic bacteria Baby foods Bacillus Bacillus cereus - genetics Bacteria Bacteria, Aerobic Biodiversity Dried foods Enumeration Food Microbiology Genes Heat resistant bacteria Humans Infant foods Infant Formula Infants Lecithinase Mass spectrometry Mass spectroscopy NHE gene Paenibacillus Phylogeny Powders RpoB protein Scientific imaging Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization Spectroscopy Spoilage Spore-forming bacteria Spores, Bacterial - genetics Thermophilic bacteria Toxin Toxins |
| title | Aerobic spore-forming bacteria in powdered infant formula: Enumeration, identification by MALDI-TOF mass spectrometry (MS), presence of toxin genes and rpoB gene typing |
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