St-Gelais J Ferreira G Kuznetsov JF Hendrich bacteria Volponi M Ferguson Human milk microbiome Miguindou-Mabiala B Jayarao Schneider As with bacteria, the extent of the fungal population in raw milk and dairy products is often underestimated. Mauriello & Vaughan EE (, Randazzo Pseudomonas spp., which are commonly found in raw milk, are the most common cause of milk spoilage (Ercolini etal., 2009). Ross KL K O In recent years, there has been considerable focus on the action of the S-layer protein (SLP) of lactic acid bacteria as an antiviral component. Garrigues Many LAB isolated from raw milk produce putative bacteriocin-like compounds and exhibit activity against L.monocytogenes, S.aureus, C.tyrobutyricum, C.sporogenes, E.faecalis, E.faecium and E.durans (Alegra etal., 2010; Ortolani etal., 2010; Perin etal., 2012). TP Franzetti Millire Spinnler G & Mahon BE (, Latorre Human milk may be stored at neonatal units and used as a life-saving therapy to high-risk infants (Silvestre etal., 2006). Some of these nutrients are directly available to all microorganisms, while others are provided following the metabolism of major components by specific populations to release components and metabolites that are used by others (Frank, 1997). Fernndez BA Y Milk is typically stored at refrigeration temperatures that reduce the growth of most bacteria, with the exception of psychrotolerant microorganisms that can proliferate under these conditions and become a major cause of milk spoilage (Eddy, 1960; Morita, 1975; De Jonghe etal., 2011). M Yeasts can play a major role in dairy fermentations due to a number of their physiological and biochemical characteristics, including the ability to utilise lactose or galactose, for example, in D.hansenii (Van den Tempel & Jakobsen, 2000); high proteolytic or lipolytic activity, for example, in Yarrowia lipolytica and G.candidum (Sacristn etal., 2012); and the ability to grow at low temperatures and to tolerate high salt concentrations. & Coppola S (, Ercolini A Fornasari Sasamoto Sorensen Murphy (, Foulqui Moreno Van Landschoot A & Swinne D (, Lamendella SJ & Stiles ME (, Fricker Lactobacillus rhamnosus LB 1.5 and Lactobacillus paracasei LB6.4: Innocuous bacteria, antimicrobial activity, adherence to Caco-2 cells, and coaggregation properties, E Typically, this concern is removed with pasteurisation, but remains a problem in instances where raw milk is still consumed daily (Coker etal., 2006; De la Rua-Domenech, 2006). G Horrevorts & Caggia C (, Ranieri Lynch EG Schnrer MP In dairy products, the presence of bifidobacteria results in increased levels of lactate and acetate but does not influence sensory or textural properties (Dinakar & Mistry, 1994). F Abeer When a model cheese system was employed to assess the consequences of the presence of some of these Gram-negative bacteria, it was established that the majority had little influence on colour, odour and volatile compounds (Delbs-Paus etal., 2011). G Rossetti H Jimenez HA cremoris, L.helveticus, L.fermentum, L.rhamnosus, L.paracasei and L.acidophilus (Muguerza etal., 2006). Crohn's disease and the mycobacterioses: a quarter century later. & Tsakalidou E (, Marchand AM Scott While the milk, sourced from a variety of commercial producers throughout Ireland, was dominated by Lactococcus, Pseudomonas and Leuconostoc, we also detected a number of anaerobic taxa, including Bacteroides, Faecalibacterium, Prevotella and Catenibacterium, which are more typically associated with the gut microbiota and may be entering the milk through faecal contamination. & Labrie S (, Le Bourhis Alegria C Breen Many human milk lactobacilli and bifidobacteria can contribute to infant digestion by aiding in the breakdown of complex foods such as proteins and sugars; some lactobacilli increase the production of functional metabolites such as butyrate, which is utilised as an energy source and can improve intestinal function (Asakuma etal., 2011; Zivkovic etal., 2011; Gil-Campos etal., 2012), while various bifidobacteria have positive effects on health, including prevention of infection by pathogenic bacteria (e.g. Zoumpopoulou cremoris SK11 strain contains a number of unique plasmids, pSK11A, pSK11B, pSK11L and pSK11P, which encode important traits related to dairy adaptation and utilisation, including lactose utilisation, a complex proteolytic system and an oligopeptide permease system (Siezen etal., 2005). Barbour & Molenaar D (, Beecher A Thus, high-throughput sequencing approaches can provide a detailed insight into the bacterial composition of milk, and it is likely that these technologies will be used increasingly in future to investigate the factors that influence the composition of cows' milk. C Corcos ME Delgado Andrighetto G M I A Revol-Junelles cremoris, S.thermophilus, Enterococcus faecalis, Enterococcus durans and Weissella cibaria as being among the most common species in yak milk (Watanabe etal., 2008; Yu etal., 2011). & Tavassoli M (, Monnet Buckley A were detected in milk over 40years ago (Jayne-Williams & Skerman, 1966) and have also been found on the teat surface and throughout the farm environment (Vacheyrou etal., 2011; Braem etal., 2012). M Penaud Verbist Chamberlin Y However, molecular methods based on PCR and quantitative PCR allow the rapid detection and classification of phages from different dairy matrices (Binetti etal., 2008). Palmer Angulo & Brasca M (, de Garnica A This suggests that the timing of bacterial arrival in the gut is very important in shaping the gut microbiome. Leveau Cintas Ahmadova J & Rodrguez JM (, Ferrario & Engels WJM (, Sun EG A recent study of isolates from milk and cheese revealed 17 CNS species. Fresno (, Astobiza *Sheep milk NGS information was extrapolated from data relating to naturally ripened cheeses manufactured using raw sheep milk. The other species of dairy Propionibacterium are usually isolated from milk and different cheese types (Meile etal., 2008). V Sasaki Leuconostoc spp. Ramos M Lactobacilli can be found in rich, carbohydrate-containing niches, including those associated with plants, animals, silage and raw milk (Bernardeau etal., 2008). Human milk on the other hand is typically dominated by Streptococcus, Staphylococcus, Lactobacillus and Bifidobacterium spp. L JZ Di Palo Brucella was present in milk in Africa at 010%, increasing with increasing farming intensity (Oliver & Murinda, 2011). D AG S Streptococcus thermophilus strain ND03, isolated from naturally fermented yak milk, contains unique genes not previously found in other strains. & Singer RS (, Duthoit Salminen Dimanche-Boitrel Leuconostoc spp. & Dellaglio F (, Vacheyrou J China (, Swenson Suwandhi Follador ML P Valdivia Between 1% and 6% is excreted in milk as aflatoxin M1. Van Swam M L R Z & Montel M-C (, Mora M T Many microbial communities are complex; that is, they are comprised of many different taxonomical groups of microorganisms. Urashima Whole-genome sequencing of S.thermophilus has revealed that this bacterium exhibits 80% similarity with other streptococci, indicating that it shares a substantial part of its overall physiology and metabolism with its pathogenic relatives. Indeed, clostridia have been identified in raw milk quite frequently (Herman etal., 1995; Lopez-Enriquez etal., 2007; Cremonesi etal., 2012) and can contribute to the spoilage of subsequent cheese products by causing a late blowing defect, which is particularly associated with C.tyrobutyricum, leading to off-flavours and textural defects in cheese (Cocolin etal., 2004; Le Bourhis etal., 2005). These populations, which are often referred to as nonstarter LAB (or NSLAB), have an ability to adapt to the conditions of cheese ripening, where many nutrients are depleted, pH is reduced, and moisture content is low. The maternal gut is the principal source of commensal bacteria in the infant gut during the lactation stage, where breast milk acts as an intermediary for the transfer of Genome sequencing has also revealed the presence of more than 50 insertion sequences, which have shaped the genome and, in part, are associated with genes involved in the adaptation of the species to milk. L Foschino Traditional culture-based methods have indicated that staphylococci, LAB and propionibacteria dominate in human milk with a significant Bifidobacterium population also present (Table4; Martin etal., 2009). Desmasures Constantinidou K Tessier & Montel MC (, Duthoit AL Lactobacillus in the Dairy Industry: From Natural Diversity to The most common LAB genera in milk include Lactococcus, Lactobacillus, Leuconostoc, Streptococcus and Enterococcus. Ranieri S & Demberel S (, Wegmann RP Leigh RP F L JY Forney & Alvarez MA (, Lafarge MD M (20%), Streptococcus macedonicus (10%) and Lactococcus lactis (10%; Fig. etal. I Brahmbhatt & Marwaha SS (, Albesharat Silva Jnior It has been suggested that S.dysgalactiae present in the mammary gland degrades the proteose peptones of milk prior to milking and consequently results in a reduced ability of milk to coagulate during fermentations (Merin etal., 2008). An African dairy isolate, Streptococcus infantarius ssp. Van Driessche S Verdier-Metz A great majority of the flavour compounds produced in yogurt result from the activity of microorganisms in starter cultures. Rouault & Leitner G (, Meslier B This milk is employed in many ways, including direct consumption and the manufacture of dairy products and milk powders. WebLactobacillus Lactobacillus SPP. A L In 2010, Yersinia incidence in raw milk and low-heat-treated milk products was low, with only two positive results reported within the EU (European Food Safety Authority, 2012). A B Andrighetto Cavazza Yu Lactococcus lactis ssp. These include L.casei, Lactobacillus paracasei, L.plantarum/paraplantarum, Lactobacillus rhamnosus and Lactobacillus curvatus, L.brevis, Lactobacillus sake, Lactobacillus pentosus, Lactobacillus acidophilus, Lactobacillus reuteri, Lactobacillus johnsonii, Lactobacillus crispatus, L.fermentum, L.buchneri and Lactobacillus gasseri. Labiad Yang Maubois & Jan G (, Cremonesi Fresno E Paul Debaryomyces hansenii and Y.lipolytica may also be emerging dairy pathogens. A-C Latif CM A M C Isolation and Identification of lactobacilli from raw milk M C & Alatossava T (, Murphy K While many dairy bacteria can be infected by phage, there are a number of industrially important strains that have inherent resistance to phage. Dolci S V Sonnen E G Sequencing of Corynebacterium casei UCMA 3821, Corynebacterium variable DSM 44702 and Chryseobacterium bovis DSM 20583 has revealed genes involved in iron acquisition and uptake, an important feature of cheese surface bacteria. (, Bolotin G S A Where birth was by nonelective caesarean section, the bacterial profile was more comparable with milk from mothers who had a natural labour than that of milk from mothers who underwent elective caesarean section. & Ibrahim A (, Achemchem M J Vigiis 101 Lactic Acid Bacteria Capsules is a commercially available product for Lactobacillus paracasei subspecies paracasei NTU 101 (NTU 101) is a strain of Lactobacillus isolated from the intestinal tract of newborns in Taiwan. PA Sylven Beresford J These studies reveal the high biodiversity of Gram-negative bacteria among raw milk and dairy products and suggest that they may play a role in dairy fermentations. Lactobacillus spp. S etal. Traditionally, standard microbiological methods were employed. M Janstova Bugnard University of Turin, Dronero (CN), Italy, Impact of Gram-negative bacteria in interaction with a complex microbial consortium on biogenic amine content and sensory characteristics of an uncooked pressed cheese, A PCR method for detection of bifidobacteria in raw milk and raw milk cheese: comparison with culture-based methods, Nisin and its uses as a food preservative, Monitoring the microbiology of high quality milk by monthly sampling over 2years, Antibiotic resistance and microbial composition along the manufacturing process of Mozzarella di Bufala Campana, Antimicrobial resistance: challenges and perspectives, Silage and the safety and quality of dairy foods: a review, Bacterial community dynamics during production of registered designation of origin Salers cheese as evaluated by 16S rRNA gene single-strand conformation polymorphism analysis, Relationships between sensorial characteristics and microbial dynamics in Registered Designation of Origie' Salers cheese, The use and meaning of the term psychrophilic', Environmental bacteria and childhood asthma, Potential use of lactic acid bacteria for reduction of allergenicity and for longer conservation of fermented foods, Bacteriophage: Genetics and Molecular Biology, Horizon Scientific Press/Caister Academic Press, The potential of a polyphasic PCR-DGGE approach in evaluating microbial diversity of natural whey cultures for water-buffalo mozzarella cheese production: bias of culture-dependent and culture-independent analyses, PCR-DGGE fingerprints of microbial succession during a manufacture of traditional water buffalo mozzarella cheese, Molecular identification of mesophilic and psychrotrophic bacteria from raw cow's milk, Remake by high-throughput sequencing of the microbiota involved in the production of water buffalo mozzarella cheese, Lactic acid bacteria from raw milk as potentially beneficial strains to prevent bovine mastitis, Scientific Report of EFSA and ECDC. & Sorokin A (, Bonizzi E Mastitis can be a common disease, with incidence rates of up to 33% in lactating mothers (Foxman etal., 2002; the issue of bovine mastitis is addressed later in the review). JH Belzacq The presence of these microorganisms impairs milk quality and the quality of subsequent products (Barbano etal., 2006). Salomskiene E Bardowski etal. It is hypothesised that this key phenotype has been gained by dairy isolates through lateral gene transfer (Ferrario etal., 2012). M-T CL JM J Importantly, food isolates of E.faecalis lack a large number of genes, which are present in clinical isolates. N G This trait appears to increase in occurrence through the cold chain transportation of raw milk (Munsch-Alatossava & Alatossava, 2007). P Introduction. etal. Yang Enterococci contribute to fermentations due to their proteolytic activity; ability to hydrolyse milk fat; and contribution to the development of flavour compounds, including acetaldehyde, acetoin and diacetyl (Franz etal., 1999). ACE-inhibitory drugs are commonly used to control arterial blood pressure. Marchioni Benjouad Lang etal. C D These standard methods are legislated and accredited by National and International Accreditation Boards (e.g. (, Callon PD Despite the beneficial impact of many milk-associated microorganisms from a flavour, technological or health-related perspective, it is clear that there can be significant risks associated with the consumption of raw milk and raw milk-derived products or, more specifically, of the pathogens that can be found therein. Arthrobacter arilaitensis is perhaps the most important cheese-associated species, and genome sequencing of strain Re117 reveals the presence of several genes that reflect its adaptation to growth in dairy/cheese environments including salt tolerance, galactose metabolism and enzymes for catabolism of fatty acids, amino acids and lactate. Awasthi The Nutrition Source Collado C Saffar If confirmed, further investigations will be required to determine whether overall microbial load or specific components of the microbial population are responsible. E Similarly, S.agalactiae is a major causative agent associated with mastitis in cows. A Korakli Lactobacillus Similarly, several studies have demonstrated the transfer of Staphylococcus, Lactobacillus, Bifidobacterium as well as Enterococcus spp. A number of psychrotrophic spore-forming species have also been identified and will be discussed in the next section. Jarvinen G J These microorganisms enter milk from a variety of sources and, once in milk, can play a number of roles, such as facilitating dairy fermentations (e.g. & Budde C (, Teh The renninangiotensinaldosterone system is a key factor in the maintenance of arterial blood pressure. JB Pot Ganguly & Oerther DB (, Langer F Laursen http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2005:338:0001:0026:EN:PDF; http://www.inab.ie/). P The microbial composition of milk can also have health-related implications in that the consumption of raw milk contaminated with pathogens can lead to, in some cases, severe illness (Oliver etal., 2009). Torriani Corynebacterium spp. Other strains of non-LAB genera are also encountered in milk, as well as various yeasts and moulds (Quigley etal., 2011). The genus Lactobacillus is very diverse and, according to the most recent estimations, consists of 174 different species and 27 subspecies (www.bacterio.cict.fr). Although Lactococcus raffinolactis is typically not used by the dairy industry because of a lack of caseinolytic activity (Holler & Steele, 1995), a recent study observed synergism between L.raffinolactis and Lactococcus lactis strains, whereby L.raffinolactis improved acid production thanks to its ability to utilise metabolic products generated by Lactococcus lactis (Kimoto-Nira etal., 2012), presumably thanks to the presence of a complete set of genes for lactate fermentation and genes responsible for an oligopeptide ABC transporter (Meslier etal., 2012b;). C They are gram-positive, oxidase- and catalase-negative, and asporogenous, and belong to the order Lactobacillales ( Mattarelli et al., 2014 ). & Steele JL (, Cocco & Tornadijo ME (, Sanchez DK L M Ripening and flavor production, Quantitative risk assessment of listeriosis due to consumption of raw milk, Characterization of the fungal microflora in raw milk and specialty cheeses of the province of Quebec, Development and validation of PCR primers to assess the diversity of, Food safety: unpasteurized milk: a continued public health threat, Comparative genomic hybridization analysis of, Lactic acid bacteria as functional starter cultures for the food fermentation industry, Antifungal effect of dairy propionibacteria contribution of organic acids, Antifungal compounds from cultures of dairy propionibacteria type strains, High-throughput bacterial genome sequencing: an embarrassment of choice, a world of opportunity, Milk contamination and resistance to processing conditions determine the fate of, Quantitative and qualitative microbial analysis of raw milk reveals substantial diversity influenced by herd management practices, Isolation and identification of bacterial flora from milk of apparently health buffalocows, Comparison of the incidence of virulence determinants and antibiotic resistance between, Seasonal influence on heat-resistant proteolytic capacity of, Flavours of cheese products: metabolic pathways, analytical tools and identification of producing strains, The commensal microflora of human milk: new perspectives for food bacteriotherapy and probiotics, Results from raw milk microbiological tests do not predict the shelf-life performance of commercially pasteurized fluid milk, Cultivation-independent assessment of the bacterial diversity of breast milk among healthy women, Polyphasic study of microbial communities of two Spanish farmhouse goats' milk cheeses from Sierra de Aracena, Aflatoxin M1 in raw and ultra high temperature-treated milk commercialized in Portugal, Characterization of bacterial populations in Danish raw milk cheeses made with different starter cultures by denaturating gradient gel electrophoresis and pyrosequencing. K lactis (the latter two species will be referred to as L.bulgaricus and Lactobacillus lactis hereafter). V MA S E DF Thanellas Finally, a decision has to be made regarding the genes to be targeted. Thus, lactobacilli numerically overshadow all other genera, including Bifidobacterium, in colonizing neonatal mucosal and skin surfaces at birth during passage though the vagina and its Lactobacillus -rich microbiota, and then after labour during feeding, with the mothers breast milk containing high numbers of lactobacilli [ 5 ]. Ruiz-Zarzuela D MA BM P WebSimilar to other genera in the family, Lactobacillus are characterized by their ability to produce lactic acid as a by-product of glucose metabolism. etal. GM Hantsis-Zacharov & Montel MC (, anek Majheni Streptococcus uberis is an animal pathogen and one of the major causes of bovine mastitis worldwide (Bradley etal., 2007). JA AG Human milk has the potential to protect a newborn against infectious disease through the provision of active components including immunoglobulins, immunocompetent cells, fatty acids, oligosaccharides and glycoproteins (Saaverda, 2002; Newburg, 2005). F (Mathieu etal., 1993; Casaus etal., 1997; Giraffa & Carminati, 1997; Achemchem etal., 2006; Izquierdo etal., 2009; Mirhosseini etal., 2010) and are active against many spoilage and pathogenic microorganisms. cremoris can dominate in raw milk, cheese and other (unheated) dairy products. Daga J & Martinez-Bueno M (, Masoud M Fitzgerald T E Pattono Finally, the significance of coagulase-negative staphylococci (CNS) with respect to dairy fermentations has been the subject of much debate. Ricci B Reinheimer Phenotypic methods are those which have been traditionally employed and involve the growth of microorganisms in microbiological media (either general or selective) supplemented with morphological, biochemical or physiological characterisation (Quigley etal., 2011). Also, in silico analysis predicted the existence of a limited number of cell wallbound and extracellular proteins, which could contribute to direct contact between L.bulgaricus and S.thermophilus (van de Guchte etal., 2006). Mastitis results in the inflammation of the mammary lobules, usually due to the presence of staphylococci, streptococci or corynebacteria. Santos Pepe Lopez M F Bonnarme lactobacilli and bifidobacteria) or causing disease (e.g. Y The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2011, What happened to the streptococci: overview of taxonomic and nomenclature changes, Comparative phenotypic and molecular genetic profiling of wild, The human milk microbiota: origin and potential roles in health and disease, Probiotic and technological properties of facultatively heterofermentative Lactobacilli from Greek traditional cheeses, Novel lactic Acid Bacteria in raw cow's milk from highland farms, Phenotypic typing, technological properties and safety aspects of, Isolation of microbial pathogens of subclinical mastitis from raw sheep's milk of Epirus (Greece) and their role in its hygiene, The role and application of enterococci in food and health, Lactation mastitis: occurrence and medical management among 946 breastfeeding women in the United States, Presence of enterococci in raw cow's milk and Puzzone Di Moena cheese, Food Microbiology Fundamental and Frontiers. The species typically isolated from milk include Staphylococcus equorum, Staphylococcus xylosus and Staphylococcus carnosus. & Gavini F (, Delgado bacteria A Messens R Lactobacillus Atun MG While a relatively small number of yeast species occur in raw milk, they are persistent and can be detected at relatively high levels, that is, 102104CFUmL1 (Lagneau etal., 1996). bulgaricus and L.delbrueckii ssp. C IF Arroyo Cotter etal. Garg Microorganisms in Milk Dairy Science and Technology eBook Purswani Valina IS GF Lactobacillus Bacteria in Breast Milk 1. Here, they are able to carry out proteolysis and lipolysis to produce many end products that contribute to flavour and texture development of cheese (Smit etal., 2005). B Staphylococcus aureus can be transferred to milk through the teat canal, equipment, the environment or human handling (Rosengren etal., 2010) and cause illness through the production of heat-stable enterotoxins, which can withstand pasteurisation (Balaban & Rasooly, 2000). Offek These bacteria can become the predominant microorganisms in raw milk stored at low temperatures, constituting up to 7090% of the microbial population (Sorhaug & Stepaniak, 1997). P Kleerebezem Alegra G However, it is still important to assess the frequency with which antibiotic-resistant isolates occur in milk. de Blas The bovine teat surface can contain a high diversity of bacteria (Braem etal., 2012; Monsallier etal., 2012; Verdier-Metz etal., 2012). Notably, aflatoxin B1 is the only mycotoxin with significant carry-over into milk. lactis (Giraffa etal., 2008). These include malty aromas as well as alcohol and fruity odours in cheese, although some strains have been linked with sweat, faecal and rotten-fruit-associated flavours (Marilley & Casey, 2004). & Bouton Y (, van de Guchte Reviriego H & Jordan KN (, Kim Although pasteurisation will kill Y.enterocolitica, if insufficient pasteurisation or recontamination occurs, the bacterium can multiply under refrigeration temperatures (Schiemann & Toma, 1978). Rollando Marin Isolation, Screening and Characterization of Lactobacilli from Cow AM Staphylococcal toxins were detected in 18.4% of cheeses assessed across the EU in 2010 (European Food Safety Authority, 2012). Acidophilus (Lactobacillus acidophilus), a bacterium found in the mouth, intestine and vagina, is used as a probiotic. (, Hickey K E Frontiers | The Composition and Concordance of Lactobacillus Breast milk is a natural food for infants and young children. It is defined as homofermentive lactic acid bacteria & Pavlik I (, Slattery V Studies assessing the impact of storing sheep milk at refrigeration temperature highlighted increases in psychrophiles, but also in mesophiles. R Gram-negative bacteria are very common in dairy foods. S E Many other psychrotolerant microorganisms are present in milk but are generally less important than Pseudomonas with respect to milk spoilage. These include genes encoding a lactose phosphotransferase operon, a protein predicted to function in d-lactate utilisation, a system for uptake of oligopeptides generated from casein degradation as well as oligopeptidases, which allow this strain to utilise casein as a nitrogen source (Fallico etal., 2011). Low pH inhibits the growth of pathogenic bacteria. P (Shakd etal., 2009), have also been detected in raw milk. M Messens Larriestra M Caravelli Vogensen (, Georgalaki Stessl The presence of high numbers of Gram-negative bacteria in milk has been noted in situations where hygiene standards are low and generally reflect poor udder preparation, poor sanitation or deficiencies with respect to the hygiene of equipment. Thus, it is estimated that these phenotypically similar subspecies diverged c.17million years ago (Bolotin etal., 2004). It was first isolated over a century ago from an Emmental cheese and contributes to hole or eye formation and flavour formation in these cheeses (Langsrud & Reinbold, 1973). L Genome sequencing of Lactococcus lactis ssp. 2). & Jordan K (, Irlinger lactis and Lactococcus lactis ssp. Lactococcus lactis strains isolated from raw milk and raw milk products are capable of producing nisin with activity against L.monocytogenes as well as other pathogens including E.coli and Staphylococcus spp.
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