Received: 7 January 2020 Revised: 3 April 2020 Accepted: 3 April 2020

DOI: 10.1111/1541-4337.12568

COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY

Microbial quality and safety of milk and milk products in the

21st century

Vincenzina Fusco1 Daniele Chieffi1 Francesca Fanelli1 Antonio F. Logrieco1

Gyu-Sung Cho2 Jan Kabisch2 Christina Böhnlein2 Charles M. A. P. Franz2

1 Institute
of Sciences of Food Production,
National Research Council of Italy
(CNR-ISPA), Bari, Italy
2 Departmentof Microbiology and
Biotechnology, Max-Rubner Institut, Kiel,
Germany
Correspondence
Vincenzina Fusco, Institute of Sciences of
Food Production, National Research Council
of Italy (CNR-ISPA), Via Amendola 122/o,
70126 Bari, Italy.
Email: vincenzina.fusco@ispa.cnr.it
Funding information
European Community’s Horizon 2020,
Grant/Award Number: H2020-E.U.3.2-
678781; Mycokey; NextMilQ
Abstract
Milk and milk products have been utilized by humans for many thousands of years.
With the advent of metagenomic studies, our knowledge on the microbiota of milk
and milk products, especially as affected by the environment, production, and storage
parameters, has increased. Milk quality depends on chemical parameters (fat and pro-
tein content and absence of inhibitory substances), as well as microbial and somatic
cells counts, and affects the price of milk. The effects of hygiene and effective cooling
on the spoilage microbiota have shown that proteolytic and lipolytic bacteria such as
Pseudomonas or Acinetobacter spp. predominate the spoilage bacterial populations.
These bacteria can produce heat-stable proteases and lipases, which remain active
after pasteurization and thus can spoil the milk during prolonged storage. Addition-
ally, milk can become contaminated after pasteurization and therefore there is still a
high demand on developing better cleaning and sanitation regimes and equipment, as
well as test systems to (quantitatively) detect relevant pathogenic or spoilage microor-
ganisms. Raw milk and raw milk cheese consumption is also increasing worldwide
with the growing demand of minimally processed, sustainable, healthy, and local
foods. In this context, emerging and re-emerging pathogens once again represent a
major food safety challenge. As a result of global warming, it is conceivable that not
only microbiological risks but also chemical risks relating to presence of mycotoxins
or plant toxins in milk will increase. Herein, we provide an overview of the major
microbial hazards occurring in the 21st century.

KEYWORDS
milk, spoilage, microbiota, safety, pathogens

1 I N T RO D U C T I O N
The utilization of milk for human nutrition occurred some
11,000 years ago when farming in the Middle East began to
replace hunting and gathering. Cattle herders initially began
to ferment milk to yoghurt and cheese in order to break
down the milk sugar lactose, which was indigestible for adults
(Curry, 2013). Evidence from pottery in Poland has shown
that herders were producing cheese to supplement their diets
between 6,800 and 7,400 years ago (Curry, 2013; Salque et al.,
2013). Around 6,500 years ago, a genetic mutation upstream
of the gene encoding the lactase enzyme, which is respon-
sible for lactose breakdown, occurred in Europe and con-
ferred upon people the ability to produce this enzyme and
drink milk throughout adulthood (Ingram, Mulcare, Yuval,
Thomas, & Swallow, 2009; Curry, 2013). Archaeological
studies described a scenario in which bands of farmers and
herders from the Middle East swept through Europe and

Compr Rev Food Sci Food Saf. 2020;1–37. wileyonlinelibrary.com/journal/crf3 © 2020 Institute of Food Technologists® 1
2 MILK AND DAIRY MICROBIAL QUALITY…
displaced the hunter and gatherers (Curry, 2013). This appears
to have left an enduring imprint on Europe, where, unlike in
many other regions of the world, most people can tolerate
milk. There are other pockets of lactase persistence (lactase
hotspots) in West Africa (see Check, 2006), the Middle East,
and south Asia regions that are also associated with a cultural
history of milk utilization, where genetic mutations associ-
ated with the lactase gene have also been identified (Burger,
Kirchner, Bramanti, Haak, & Thomas, 2007; Ingram et al.,
2009; Gerbault et al., 2011). Thus, with the onset of farming,
milk from cows, sheep, or goats became a valuable source of
nutrients, and fermented milk products could be stored and
were thus relatively independent from seasonal variations and
harvests, helping over times of famine.
Milk is highly nutritious and in addition to the main milk
sugar lactose, it also contains proteins (caseins, whey proteins,
and minor proteins), essential amino acids, fats, minerals, and
vitamins. Its utilization may thus well have contributed to the
success of human development over the centuries. However,
milk is not only highly nutritious for humans, but also an
excellent growth substrate for microorganisms.
2 M I L K M I C RO B I OTA : M O D E R N
INSIGHTS
The interior of a healthy mammary gland is acknowledged
as a sterile environment, especially in prepubertal animals
with intact teats before colostrogenesis and initiation of milk
secretion (Tolle, 1980; Taponen et al., 2019). Around the first
parturition and after start of milking, the mammary gland
becomes a functionally open system with a direct connec-
tion to the environment (Taponen et al., 2019) and becomes
colonized by microorganisms from the teat apex, milking
equipment, feed, air, water, soil grass, and other environ-
ments (Quigley, O’Sullivan, et al., 2013). The presence of
a microbiota within the mammary gland has more recently
been hypothesized. Traditionally, it was believed that bacteria
found in milk stem from contamination from external envi-
ronment, the mammary gland skin, or the oral cavity of the
offspring (Addis et al., 2016). However, several studies sug-
gest that bacteria in milk not only stem from external colo-
nization and an endogenous route of bacterial transmission
has been proposed. Therefore, microorganisms from different
anatomical locations than the udder may somehow enter the
mammary gland. Thus, in the enteromammary pathway it was
hypothesized that bacteria can leave the intestinal lumen, trav-
eling through the mesenteric lymph nodes to the mammary
gland, likely via immune cells such as dendritic cells (Addis
et al., 2016). The intestinal bacteria transfer to the mammary
gland in cows has been reported by Young et al. (2015), who
investigating the composition and diversity of the microbiota
of feces, milk leukocytes, and blood leukocytes in healthy lac-
tating cows by metagenomics demonstrated the shared pres-
ence of a few bacterial operational taxonomic units (OTUs)
belonging to the Ruminococcus and Bifidobacterium genera
as well as the Peptostreptococcaceae family in samples from
these compartments within the same animals (Young et al.,
2015; Addis et al., 2016).
Due to its high nutritious content, milk allows the growth
of a copious and heterogeneous number of microorganisms.
Therefore, apart from its endogenous microbiota, diverse and
numerous other microorganisms originating from the teat
canal, udder skin, milking machines, tanks, and containers
used to store it, reflecting the farm and the pasture environ-
ment as well, might colonize the milk as soon as it has been
milked (Addis et al., 2016). From a microbiological point of
view, both the safety and quality of milk are relevant issues.
Thus, assessing the composition and evolution of the raw milk
microbiota and its impact on the composition and quality of
the milk and its derived products since its milking up to its
transport, storage, and transformation in dairy products and
along the phases that allow its transformation in dairy prod-
ucts is of outmost importance (Addis et al., 2016; Quigley,
O’Sullivan, et al., 2013).
2.1 Milk spoilage: Milk gone good or milk
gone bad?
It has been common knowledge that if milk is left at room
temperature, it would spontaneously sour as a result of
the growth of a major component of lactic acid bacteria
present in the milk (Wouters, Ayad, Hugenholtz, & Smit,
2002). Indeed, the lactic acid bacteria such as Lactococ-
cus, Streptococcus, Lactobacillus, Enterococcus, and Leu-
conostoc can be found in fresh raw milk, besides several
other Gram-positive genera like Bacillus, Propionibacterium,
Microbacterium, Micrococcus, and Staphylococcus (Quigley,
O’Sullivan, et al., 2013; von Neubeck et al., 2015). Improve-
ments in culture-dependent and culture-independent meth-
ods to detect microorganisms (especially the advent of the
“omics” technologies) have, however, significantly enhanced
our knowledge on the more heterogeneous and complex
than previously thought microbiota of raw milk (Oikonomou,
Machado, Santisteban, Schukken, & Bicalho, 2012; Kuehn
et al., 2013; Quigley, O’Sullivan, et al., 2013; Oikonomou
et al., 2014; von Neubeck et al., 2015; Addis et al., 2016;
Doyle, Gleeson, O’Toole, & Cotter, 2016, 2017; Ganda et al.,
2016; Kable et al., 2016; Rodrigues, Lima, Canniatti-Brazaca,
& Bicalho, 2017; Li et al., 2018; Lima, Bicalho, & Bicalho,
2018; Metzger, Hernandez, Suen, & Ruegg, 2018; Pang
et al., 2018; Porcellato et al., 2018; Kable, Srisengfa, Xue,
Coates, & Marco, 2019; Skeie, Håland, Thorsen, Narvhus,
& Porcellato, 2019; Wu et al., 2019; Zhang, Palmer, Teh,
Biggs, & Flint, 2019). Apart from the Gram-positive bac-
teria mentioned above, Gram-negative bacteria associated
MILK AND DAIRY MICROBIAL QUALITY…
with milk include Ralstonia, Pseudomonas, Sphingomonas,
Stenotrophomonas, Acinetobacter, Psychrobacter, Faecal-
ibacterium, Chryseobacterium, Bacteroides, Porphyromonas,
Comamonas, Fusobacterium, Aeromonas, Enterobacter, Haf-
nia, and Klebsiella (Oikonomou et al., 2012; Kuehn et al.,
2013; Quigley, O’Sullivan, et al., 2013; von Neubeck et al.,
2015; Addis et al., 2016).
Milk can become contaminated by a large variety of
spoilage microorganisms from many contamination sources,
which include the feed, the environment (air, water, barn,
and pasture), the cow’s udder, and milking equipment. Milk
“spoilage” by Gram-positive lactic acid bacteria, that is milk
“gone sour,” can be considered a good thing as this has actu-
ally been recognized thousands of years ago to improve the
shelf life and organoleptic properties of such products. These
days, a huge industry is involved in the production of soured
milk products such as yoghurts and cheeses, as well as for the
starter culture lactic acid bacteria used for these. Milk spoilage
can also be caused by other bacteria. Modern hygiene has dic-
tated to hold milk before and after pasteurization at tempera-
tures as low as possible and to produce milk as hygienically
as possible, trying to keep microbial counts in the milk low.
As a consequence, this led to a decline in lactic acid bacte-
rial populations in the milk and to low-temperature spoilage
by psychrophilic Gram-negative bacteria such as proteolytic
and lipolytic Pseudomonas and Acinetobacter species (von
Neubeck et al., 2015; Boor, Wiedmann, Murphy, & Alcaine,
2017; Martin, Boor, & Wiedmann, 2018). Following pasteur-
ization, milk can be spoiled by the heat-stable, proteolytic,
and lipolytic enzymes produced by Pseudomonas during cold-
adapted growth before the pasteurization step (von Neubeck
et al., 2015). Postpasteurization contamination, however, is
also still very much an issue in the milk industry, and 50%
of fluid milk can become contaminated by heat-labile bac-
teria after pasteurization (Martin et al., 2018). According to
Martin et al. (2018), there are four different groups of psy-
chrotrophic spoilage bacteria important for postpasteurization
spoilage: (a) Pseudomonas spp., (b) the coliforms, which are
a group of enterobacteria capable of utilizing lactose, (c) other
psychrophilic Gram-negative bacteria than Pseudomonas and
coliforms, and (d) Gram-positive, spore-forming bacteria. Of
these, specific species and strains of Pseudomonas as well
as the other Gram-negative and Gram-positive spore-forming
spoilage bacteria can produce lipases or proteases, which can
lead to odor and flavor defects. Moreover, some of these
contaminating microorganisms also cause milk body defects,
among which the major one is coagulation. Milk coagulation
can happen by two ways, either by acid coagulation, which
is a result of acid produced during anaerobic fermentation
of the spoilage bacteria, or by proteolysis of the milk pro-
teins, which is a nonacid coagulation also known as “sweet-
curdling.” The latter can be caused by Pseudomonas strains
as well as by some Gram-positive, spore-forming bacteria
3
(von Neubeck et al., 2015; Meng et al., 2017; Martin et al.,
2018).
The concept of milk quality relates to the amount and types
of spoilage bacteria present in the milk, as this directly relates
to the price at which the milk can be sold. There are several
levels at which spoilage is aimed to be reduced. One is to
attempt to minimize the bacterial load by preventing contam-
ination throughout the dairy chain (Boor et al., 2017). Effec-
tive temperature control from the time of milking to storage in
the raw milk bulk tank is essential; especially, as apart from
chemical indicators (freezing point, fat and protein content,
and absence of inhibitory substances), the microbial count is
one the most important quality indicators that directly affect
the milk price. Thus, in Germany and other European coun-
tries, class I raw milk according to European Regulation (EG)
no. 853/2004 should not contain more than 100,000 CFU/mL,
whereas in the United States, grade “A” milk, according to
the Pasteurized Milk Ordinance, should also not contain more
than 100,000 CFU/mL (USPHS/FDA, 2016; Martin et al.,
2018). As bacteria can enter the milk chain again as contami-
nants after pasteurization, another level for spoilage control is
by effective sanitation and cleaning-in-place regimes, as well
as improved sanitary equipment design and introduction of
mid-shift cleaning (Martin et al., 2018).
Finally, standard microbial testing in the milk industry
focuses on total mesophilic plate counting, as well as deter-
mining the numbers of enterobacteria as indicator bacte-
ria for contamination. However, as it is clear that prote-
olytic and lipolytic Pseudomonas or Acinetobacter as well
as psychrotrophic Bacillus may play a more important role
in spoilage, the development of new detection methods such
as quantitative polymerase chain reaction (qPCR) methods
(Agrimonti, Bottari, Sardaro, & Marmiroli, 2019) or loop
isothermal amplification (LAMP) is becoming more and more
important to identify contamination sources and routes and
to attempt to prevent entry of spoilage bacteria into this food
chain.
3 W H EN M ILK CAN G ET
DA NGERO US TO YO UR HEALTH
FAO/WHO (2004a) defined pasteurization as “A microbio-
cidal heat treatment aimed at reducing the number of any
pathogenic microorganisms in milk and liquid milk products,
if present, to a level at which they do not constitute a sig-
nificant health hazard. Pasteurization conditions are designed
to effectively destroy the organisms Mycobacterium tubercu-
losis and Coxiella burnetii” (FAO/WHO, 2004a). Although
historically Mycobacterium tuberculosis and Coxiella bur-
netii were some of the more important pathogens, there may
be other pathogens of concerns today (see below), which
need to be considered in the context of milk safety and
4 MILK AND DAIRY MICROBIAL QUALITY…
inactivation procedures in milk. Furthermore, in recent years,
raw milk vending has increased. In Germany, raw milk may
be sold, when produced the same day, from vending machines
located directly on the farm. A legal requirement is that
instructions to consumers to boil the milk are clearly indi-
cated. Whether or not the consumer does boil the milk, how-
ever, is left to the consumers’ discretion. In our preliminary
investigations, we asked consumers about this and approxi-
mately 76% indicated that they do not (results not shown).
In Italy, raw milk vending machines were introduced in 2004
but, following the Ordinance of the Italian Ministry of Health
(Italian Republic, 2008), a notice highlighted in red should
be attached to these notifying the consumers that the prod-
uct must be consumed only after boiling. Once again, the
consumer has the duty of sanitizing the raw milk prior to
consuming it. However, only 63 out of 100 interviewed con-
sumers consume raw milk after boiling, the remaining 37
ignored this requirement and often gave raw milk to con-
sume even to children, whereas 93 out of 100 did not use
insulated bags to transport the raw milk from the farm to
the home (D’Ascenzi et al., 2010; Giacometti, et al., 2012a).
Salmonella spp., Listeria monocytogenes, Escherichia coli
O157:H7, and other STEC, Campylobacter, Arcobacter spp.,
and coagulase-positive staphylococci have been detected in
raw milk sold by vending machines (Gelbícová & Karpísková,
2012; Giacometti et al., 2012b; Giacometti et al., 2013a; Ser-
raino et al., 2013a; Kalmus, Kramarenko, Roasto, Meremäe,
& Viltrop, 2015; Merialdi et al., 2015; Bertasi et al., 2016;
Dalzini et al., 2016; Willis et al., 2018; Faggiano, Chieffi,
Logrieco, & Fusco, 2018). Apart from the pathogens, which
have been demonstrated to survive and even proliferate at
chilling of vending machines raw milk (Tremonte et al., 2014;
Faggiano et al., 2018; Leclair, McLean, Dunn, Meyer, &
Palombo, 2019; Pannella, Messia, & Tremonte, 2019), agents
of spoilage of raw and pasteurized milk such as Pseudomonas
spp. also significantly grow under refrigeration (Faggiano
et al., 2018).
Moreover, four campylobacteriosis and two Escherichia
coli O157:H7 outbreaks and six sporadic cases of hemolytic
uremic syndrome in Italy have been traced back to the con-
sumption of vending machine raw milk (Giacometti et al.,
2012c; Giacometti et al., 2015a, 2017), whereas a potential
link between a small number of vending machines and the
spatial distribution of campylobacteriosis has been detected
in the Czech Republic (Marek, & Pászto, 2017). Six STEC-
O157 and one campylobacteriosis outbreaks occurred in Eng-
land (Butcher et al., 2016) and one of Yersinia pseudotubercu-
losis in Finland (Pärn et al., 2015). Two outbreaks of campy-
lobacteriosis occurred in the Netherlands (Heuvelink et al.,
2009), whereas in Sweden (Studahl, & Andersson, 2000) and
Denmark (Neimann, Engberg, Mølbak, & Wegener, 2003)
consumption of raw milk has been identified as a risk fac-
tor for Campylobacter infection. Indeed, raw milk vending
machines exist not only in Italy and Germany but also in Aus-
tria, Croatia, Czech Republic, Denmark, France, Greece, Ire-
land, Lithuania, the Netherlands, Poland, Romania, Serbia,
Slovakia, and others (Transparency Market Research, 2020).
In the United States, where the consumption of raw milk is
as well spread, an increase in the number of outbreaks asso-
ciated with the consumption of unpasteurized milk was reg-
istered (Mungai, Behravesh, & Gould, 2015), with Campy-
lobacter spp. as the main etiological agent (77%). Moreover,
it has been observed that in the United States, between 2009
and 2014, unpasteurized cows’ milk and cheese consumption
caused 840 times more illnesses and 45 times more hospital-
izations than pasteurized products (Costard, Espejo, Groenen-
daal, & Zagmutt, 2017). Many cheeses are indeed made from
raw milk and may become contaminated with pathogens.
The main pathogens occurring in milk and milk prod-
ucts in these times are Shiga toxin-producing Escherichia
coli (STEC), Salmonella spp., Listeria monocytogenes,
Campylobacter spp., Salmonella spp., and coagulase-positive
Staphylococcus spp. (FDA, 2013; FSANZ, 2014; EFSA &
ECDC, 2018).
Its high fatality rate (about 20%) and hospitalization rate
(>95%) make listeriosis one of the deadliest foodborne
diseases. Despite the increased surveillance and awareness,
an increasing trend in the number of listeriosis cases is being
registered in the European Union (EU) (EFSA & ECDC,
2018), whereas in the United States, an estimated 1,600
people get listeriosis each year, and about 260 die (CDC,
2020). In particular, since 2001, there has been an increased
incidence of listeriosis in the United States. Although the
reported rates of human listeriosis have remained constant
in the last years, if no changes will occur in the next few
years, the rate will exceed the Healthy People 2020 target
of 0.2 cases per 100,000 populations (Office of Disease
Prevention and Health Promotion, 2020), prompting the
need of further mitigation strategies. As shown in Table 1,
both pasteurized and unpasteurized milk and dairy products
have been involved in listeriosis outbreaks in the last 19
years, confirming the risk related to the consumption of raw
unpasteurized milk and products and also the risk related
to the faulty pasteurization and the post processing cross-
contamination. Meanwhile, atypical Listeria innocua strains
(Johnson et al., 2004), which are virulent but less so than L.
monocytogenes (Moura et al., 2019), are also emerging.
As shown in Table 2, enterotoxigenic Staphylococcus
aureus continues to be a concern in milk and dairy microbial
safety causing a large number of staphylococcal food poison-
ings (SFP).
In the last decades, staphylococcal enterotoxin (SE)-
producing strains of staphylococci other than S. aureus have
been detected, also including strains of the recently iden-
tified Staphylococcus argenteus species (previously known
as divergent Staphylococcus aureus clonal lineage), which is
MILK AND DAIRY MICROBIAL QUALITY… 5

TABLE 1 Listeriosis outbreaks traced back to consumption of milk and milk products occurred from 2000 to date
Number
Serotype Country Year Food of cases References
– USA (North Carolina) 2000 to 2001 Mexican-style fresh soft cheese 13 Boggs, Whitman, Hale, Briscoe, &
from raw milk (Queso fresco) Kahn, 2001; MacDonald et al., 2005
1/2b Japan 2001 Washed-type cheese 38 Makino et al., 2005
1/2a Sweden 2001 On-farm manufactured fresh 48 Carrique-Mas et al., 2003
cheese
4b Canada 2002 Soft and semisoft-cheese 47 Gaulin, 2003
4b Canada 2002 Pasteurized milk cheese 86 Pagotto, Ng, Clark, & Farber, 2006
1/2a Switzerland 2005 Tomme (soft cheese) 12 Bille et al., 2006
– USA 2005 Fresh cheese (Queso fresco) 9 FIOD, 2005
– Czech Republic 2006 Soft cheese 78 EFSA, 2007
4b, 1/2a, Germany 2006 to 2007 Acid curd cheese “Harzer Käse” 189 Koch et al., 2010
1/2b (made from pasteurized milk)
– USA (Massachusetts) 2007 Flavored and nonflavored fluid 5 Cumming, Kludt, Matyas, & DeMaria,
pasteurized milk 2008
– Norway 2007 Hospital/camembert cheese 17 Johnsen et al., 2010
– Canada 2008 Pasteurized milk cheese 38 Gaulin, Ramsay, & Bekal, 2012
1/2a USA 2008 Fresh cheese (Oaxaca cheese) 8 Jackson et al., 2011
– Chile 2008 Smear cheese (Brie) 91 Promed, 2008
1/2a USA (Multistate) 2009 Mexican-style cheese made from 7 Jackson et al., 2011
pasteurized milk
1/2a Austria, Germany, 2009 to 2010 Acid curd cheese “Quargel” 34 Fretz et al., 2010a, Fretz et al., 2010b
Czech Republic
4b Portugal 2009 to 2012 Fresh cheese (cured cheese and 30 Magalhaes et al., 2015
queijo fresco)
– USA (multistate) 2010 Soft cheese 30 Sauders & D’ Amico, 2016
– USA 2010 Fresh cheese (Panela, queso fresco, 5 FIOD, 2010
Requeson)
USA 2010 to 2015 Fresh cheeses 28 FIOD, 2015a
– Belgium 2011 Hard cheese 12 Yde et al., 2012
1/2b Austria–Germany 2011 to 2013 Fresh cheese 7 Schmid et al., 2014
USA 2011 Fresh cheese (Chives cheese) 2 FIOD, 2011
– USA (multistate) 2012 Ricotta salata cheese 22 Heiman et al., 2016
1/2a Spain 2012 Fresh cheese (queso fresco) 2 de Castro et al., 2012
– USA (multistate) 2013 Les Frères, Petit Frère, and Petit 6 Choi et al., 2014
Frère with Truffles cheeses
Australia 2013 Smear cheese 18 NSW, 2013
USA 2013 to 2014 Fresh cheese 4 FIOD, 2014a
USA 2014 Fresh cheese 7 FIOD, 2014b
– USA (multistate) 2013 to 2014 Quesito casero cheese 5 https://www.cdc.gov/listeria/
outbreaks/cheese-10-14/index.htm
– USA (multistate) 2014 Cheese products 8 https://www.cdc.gov/listeria/
outbreaks/cheese-02-14/index.html
USA 2015 Fresh cheese(Panela, queso fresco, 3 FIOD, 2015b
Requeson, Cotija)
– USA (multistate) 2010 to 2015 Ice cream 10 Pouillot et al., 2016
USA 2017 Smear cheese 8 CDC, 2017
6 MILK AND DAIRY MICROBIAL QUALITY…

TABLE 2 Staphylococcal food poisoning outbreaks traced back to consumption of milk and milk products occurred from 2000 to date

Staphylococcal Number
enterotoxin Country Year Food of cases References
A France 2000 Raw sheep’s milk cheese – Kèrouanton et al., 2007
A Japan 2000 Powered skim milk–based dairy products 13,420 Asao et al., 2003
A/H Japan 2000 Reconstituted milk >10,000 Ikeda, Tamate, Yamaguchi,
& Makino, 2005
– France 2001 Raw milk semihard cheese – Kèrouanton et al., 2007
A France 2001 Sliced soft cheese 2 Kèrouanton et al., 2007
A France 2001 Chocolate cake 4 Kèrouanton et al., 2007
A France 2001 Cream 10 Kèrouanton et al., 2007
A France 2002 Raw sheep’s milk cheese 43 Kèrouanton et al., 2007
A France 2002 Raw sheep’s milk cheese – Roussel et al., 2015
A France 2002 Cheese – Roussel et al., 2015
H Norway 2003 Mashed potato prepared with raw milk 8 Jørgensen et al., 2005
– France 2003 Hard cheese made from raw milk – Roussel et al., 2015
– France 2004 Semi-soft cheese made from raw milk 5 Roussel et al., 2015
– France 2004 Hard cheese made from raw milk 3 Roussel et al., 2015
A France 2004 Cheese – Roussel et al., 2015
– France 2006 Cheese 4 Roussel et al., 2015
C/D Paraguay 2007 Ultrapasteurized milk 400 Weiler et al., 2011
A/D Austria 2007 Pasteurized milk, cacao milk, and vanilla 166 Schmid et al., 2009
milk made from pasteurized milk
– France 2007 Semi-soft cheese – Roussel et al., 2015
– France 2007 Cheese made from raw milk – Roussel et al., 2015
– France 2007 Goat milk – Roussel et al., 2015
egc-encoded Switzerland 2007 Robiola cheese 5 Johler, Giannini, et al., 2015
enterotox-
ins
D France 2008 Soft cheese 5 Roussel et al., 2015
E France 2009 Soft cheese made from unpasteurized milk 3 Ostyn et al., 2010
E France 2009 Soft cheese made from unpasteurized milk 5 Ostyn et al., 2010
E France 2009 Soft cheese made from unpasteurized milk 4 Ostyn et al., 2010
E France 2009 Soft cheese made from unpasteurized milk 3 Ostyn et al., 2010
E France 2009 Soft cheese made from unpasteurized milk 3 Ostyn et al., 2010
E France 2009 Soft cheese made from unpasteurized milk 5 Ostyn et al., 2010
– France 2009 Ripened sheep’s cheese made with raw 27 Roussel et al., 2015
milk
A Germany 2013 Ice cream 13 Fetsch et al., 2014
D/J/R Romania 2013/2017 Sheep curd cheese 8 Ciupescu et al., 2018
D/G/I/J/R Romania 2013/2017 Appetizers made with soft sheep and cow 52 Ciupescu et al., 2018
cheese
H Romania 2013/2017 Raw cow milk ripened salted cheese 36 Ciupescu et al., 2018
A/D Switzerland 2014 Soft cheese from raw milk 14 Johler, Weder, et al., 2015
C Italy 2015 Semiripened sheep cheese (primosale) 2 Vitale et al., 2015
MILK AND DAIRY MICROBIAL QUALITY… 7

emerging as foodborne pathogen due to its ability to cause TABLE 3 Occurrence of MRSA in animal foods and animals
SFP (Suzuki et al., 2017; Shi & Zhang, 2018; Wakabayashi used for foods
et al., 2018). For this reason, starting from 2005 (EC reg- Country Food matrix Reference
ulations no. 2073/2005, 1441/2007), European regulations Korea Raw milk Kwon et al., 2005
require the enumeration of coagulase-positive staphylococci Italy Raw milk, pecorino Normanno et al., 2007
(CPS) at steps where the number of staphylococci is expected cheese, and
to be the highest (process hygiene criteria), and the screen- mozzarella cheese
ing of samples for the presence of SEs above well speci- Canada Pigs Golding et al., 2010
fied M (maximum limit) values (food safety criteria) (Fusco, Korea Raw meat and fish Rhee & Woo, 2010
Blaiotta, & Becker, 2018; Chieffi et al., 2020). Nevertheless, Germany Poultry based foods and Fessler et al., 2011
the incidence of SFP has increased in the last years (EFSA foods products
& ECDC, 2015a, 2015b), with SEs causing 8% of foodborne Louisiana Retail meat Pu, Wang, & Ge, 2011
outbreaks in 2016 (EFSA, 2017). This could be due to ther- USA Raw milk Haran et al., 2012
mostable nature of SEs, which may persist in a food after the Georgia Retail meat Jackson, Davis, & Barret,
vegetative cells of CPS are dead (Fusco et al., 2018; Chieffi 2013
et al., 2020), underlining the importance of testing raw milk Germany Wild boar meat Kraushaar & Fetsch, 2014
and raw milk products for coagulase-positive staphylococci. Japan Retail raw chicken meat Kitai et al., 2005
In addition, beyond classical SEs (SEA-SEE), a high num-
Greece Ovine and caprine milk Pexara et al., 2016
ber of SEs and SE-like toxins, for which no detection method
Egypt Milk and dairy products Al-Ashmawy, Sallam,
is available to date, have been discovered and most of them Abd-Elghany, Elhadidy,
have been demonstrated to cause SFP, or their genes have been & Tamura, 2016
detected in CPS strains involved in SFP cases (Chieffi et al., Iran Fishery products Arfatahery, Davoodabadi,
2020). Last but not least, enterotoxigenic strains of coagulase & Abedimohtasab, 2016
negative staphylococci, which in turn are being pinpointed as Spain Foods of animal origin Lozano, Gharsa, Ben
virulent (Chajęcka-Wierzchowska, Zadernowska, & Gajew- Slama, Zarazaga, &
ska, 2019; Heilmann, Ziebuhr, & Becker, 2019), such as S. Torres, 2016
epidermidis (Madhusoodanan et al., 2011; Podkowik, Park, Italy Raw milk Parisi et al., 2016
Seo, Bystroń, & Bania, 2013; Fusco et al., 2018; Abbondio,
Fois, Longheu, Azara, & Tola, 2019), are emerging and are
currently not even considered in the context of safety of milk. or further metabolized (Kuboka et al., 2019). It is classified
One of the greatest public health concerns is represented in group 2B by the IARC due to its demonstrated hepato-
by methicillin-resistant S. aureus (MRSA), which can cause toxic and carcinogenic effect on animals, although its toxicity
hospital-acquired and community-associated infections. is approximately one order of magnitude lower than that of
Community-associated, livestock-associated, and healthcare- AFB1 (IARC, 2012). The carry over ratio between ingested
associated MRSA, even able to produce SEs and thus to and excreted aflatoxin, which is not directly dependent on the
cause SFP, are being found in animals used for food, in food fed contamination but is influenced by the AFB1 intake per
products (Table 3), as well as in professionals working in kilogram of bodyweight (Battacone et al., 2003, 2005), usu-
the animal husbandry or in food production and processing ally ranges from 1% to 3% in ruminants, but can reach values
sectors (Jones, Kellum, Porter, Bell, & Schaffner, 2002; of 6% (EFSA, 2004). Thus, AFM1 can be detected in raw milk
Boyce & Havill, 2005; Lozano et al., 2009; van Cleef et al., and, given the heat stability of this toxin, in any dairy product
2011; Wendlandt, Schwarz, & Silley, 2013; Larsen et al., obtained by contaminated raw and even pasteurized and ultra-
2015; Shaker, 2015;). These enterotoxigenic MRSA can also high temperature milk. Maximum tolerated residue level of
act as foodborne pathogens in conditions favoring the growth AFM1 in milk for human consumption has been established,
and enterotoxin production (Jones et al., 2002; Sergelidis & ranging from 0.05 μg AFM1/kg in the EU, Africa, Asia, and
Angelidis, 2017). Latin America, to 0.5 μg/kg AFM1 in the United States, as
Besides SEs, aflatoxin (AF) M1 is an important micro- in many South American and several Asian countries (Britzi
bial toxin that may occur in human and animal milk and et al., 2013). A consistent number of reports are underlin-
dairy products. It is the hydroxylated product of AFB1, a ing the alarming % of AFM1 contamination of breast milk,
class 1 human carcinogen (IARC, 2012), mainly produced by particularly in subtropical area, which were recorded as the
Aspergillus flavus and Aspergillus parasiticus. AFB1 is bio- 82% in Nigeria (Adejumo et al., 2013), reaching the 98.1% in
transformed into AFM1 in the liver of cows, sheep, and goats Iran (Sadeghi, Almasi, Bohloli, & Mohamadi, 2013) and the
fed with AFB1-contaminated feedstuff. AFM1 is thereafter 99.5% in United Arab Emirate (Abdulrazzaq, Osman, Yousif,
absorbed into the blood and secreted in milk, urine, and bile & Al-Falahi, 2003). Levels of AFM1 in contaminated breast
8 MILK AND DAIRY MICROBIAL QUALITY…

TABLE 4 Incidence of aflatoxin M1 in raw milk samples worldwide from 2000 to date
% of samples
Positive samples/Total Amount (range) exceeding EU
Country Year samples (incidence %) (ppb) limits References
Greece 1999 to 2000 and 22/30 from December 0.005 → 0.05 3.3 and 3.6, Roussi, Govaris, Varagouli, &
2000 to 2001 1999 to May 2000 respectively Botsoglou, 2002
and 18/28 from
December 2000 to
May 2001
Brazil 2001 to 2002 10/42 0.265 to 1.998 100 Sassahara, Pontes Netto, &
Yanaka, 2005
North Africa 2002 35/49 0.03 to 3.13 97 Elgerbi, Aidoo, Candlish, &
(Libya) Tester, 2004
France 2003 3/264 <0.0026 – Boudra, Barnouin, Dragacci, &
Morgavi, 2007
Iran 2005 84/111 0.015 to 0.280 14.75 Kamkar, 2005
Syria 2005 to 2006 70/74 0.020 to 0.690 80 Ghanem & Orfi, 2009
Thailand 2006 to 2007 240/240 0.014 to 0.197 64.6 Ruangwises, & Ruangwises,
2010
Iran 2007 119/186 0.01 to 0.410 11.76 Ghiasian, Maghsood,
Neyestani, & Mirhendi, 2007
Argentina 2007 60/94 ND-0.07 11.7 Alonso et al., 2010
Iran 2008 319/319 Mean 0.0564 23 Tajkarimi et al., 2008a
Iran 2008 173/319 0.001 to 0.116 23 Tajkarimi et al., 2008b
Iran 2008 to 2009 40/60 0.011 to 0.115 37.5 Rahimi & Ameri, 2012
Egypt 2008 to 2009 19/50 0.023 to 0.073 52.6 Amer & Ibrahim, 2010
Turkey 2009 20/60 0.0054 to 0.300 8.3 Keskin, Başkaya, Karsli,
Yurdun, & Ozyaral, 2009
Brazil 2009 to 2010 635 0.012 to 0.725 10.1 Santili et al., 2015
Morocco 2009 to 2010 13/48 0.01 to 0.100 8 El Marnissi, Belkhou, Morgavi,
Bennani, & Boudra, 2012
Iran 2010 185/534 0.005 to 0.100 NS Habibipour, Khosravi,
Amirkhani, & Bayat, 2010
China 2010 281/360 0.005 to 0.123 10 Zheng et al., 2013
Iran 2011 122/122 0.004 to 0.112 14.75 Kamkar, Khaniki, & Alavi,
2011
Lebanon 2011 28/38 0.0024 to 0.126 55 Assem & Mohamad, 2011
India 2011 32/52 0.1 to 3.8 100 Siddappa, Nanjegowda, &
Viswanath, 2012
South Africa 2011 37/37 0.0 to 1.54 73% Dutton, Mwanza, de Kock, &
Khilosia, 2012
Palestine 2012 34/40 0.003 to 0.080 20 Al Zuheir & Omar, 2012
Turkey 2012 to 2015 19/90 0.011 to 0.100 3.4 Sahin, Celik, Kotay, & Kabak,
2016
Iran 2013 320/320 0.04 to 0.242 92.18 Sadeghi et al., 2013
Iran 2013 44/60 0.004 to 0.419 28 Kamkar, Yazdankhah, Nafchi,
& Nejad, 2014
Sudan 2013 35/35 0.005 → 2 100 Ali, El Zubeir, & Fadel Elseed,
2014
Kenya 2013 to 2014 NS/62 NS → 0.05 74.2 Lindahl, Kagera, & Grace,
2018
(Continues)
MILK AND DAIRY MICROBIAL QUALITY… 9

TABLE 4 (Continued)
% of samples
Positive samples/Total Amount (range) exceeding EU
Country Year samples (incidence %) (ppb) limits References
Italy 2013 to 2018 63/31,702 (0.2) NS → 0.05 0.20 Serraino et al., 2019
Iran 2014 145/312 0.012 to 0.198 15.4 Fallah, Fazlollahi, & Emami,
2016
Turkey 2014 53/176 0.025 to 1.010 17 Golge, 2014
Tanzania 2014 31/37 0.026 to 2.007 16.1 Mohammed, Munissi, &
Nyandoro, 2016
Iran 2015 204/254 0.011 to 0.321 56.7 Fallah, Barani, & Nasiri, 2015
Serbia 2015 to 2016 984/1,408 0.005 to 1.100 31 Milićević et al., 2017
Kosovo 2016 74/192 0.00 to 0.083 5.7 Camaj, Meyer, Berisha,
Arbneshi, & Haziri, 2018
Iran 2016 89/168 0.00 to 0.100 30 Hashemi, 2016
India 2019 86/150 (57.3) <0.052 (LOD) 21 Sharma, Jadhav, & Garg, 2020
→ 0.5
India 2019 9/168 (13.2) ND → 0.5 1.2 Moudgil, Bedi, Aulakh, & Gill,
2019
Egypt 2019 20/20 (100) 0.02 to 0.19 70 Abdallah, Girgin, & Baydar,
2019
Iran 2019 123/257 (47.8) 0.051 to 0.5 1.5 Khaneghahi Abyaneh, Bahonar,
Noori, Yazdanpanah, &
Shojaee Aliabadi, 2019

milk are often similar to or higher than those considered safe
in animal milk for human consumption (Adejumo et al., 2013;
Cherkani-Hassani, Mojemmi, & Mouane, 2016). In Serbia,
a high percentage of contaminated colostrum (85%) and all
samples of breast milk collected 4 to 8 months after delivery
had AFM1 concentration above maximum allowable concen-
tration required by Regulation on Health Safety of Dietetic
Products (Radonić et al., 2017). Such finding underlines the
high exposure risk of infants, who are at the early stage of
development and vulnerable to toxic contaminants. Several
measures are being developed to mitigate the occurrence in
milk of this aflatoxin (Prandini et al., 2009; Benkerroum,
2016; Assaf et al., 2019), and a number of microorganism
or enzymes have been identified with AFM1-degrading activ-
ity (Loi et al., 2016). Nevertheless, numerous studies report a
widespread AFM1 contamination in milk (Table 4) and milk
products (Table 5), particularly in the developing countries,
where climatic conditions (hot and humid) are mostly favor-
able for AFB1 contamination in crops and where a regula-
tion on AFB1 in food and feed and AM1 in milk has not yet
been set. Tolerable limits of aflatoxin with regard to food and
feed contamination as well as of AFM1 in milk are being,
or have been, not yet setted (Iqbal, Jinap, Pirouz, & Ahmad
Faizal, 2015). However, also in developed countries climate
change is expected to worsen AFB1 and AFM1 contamination
landscape. Indeed, Battilani et al. (2016) estimated that the
aflatoxin contamination in maize and wheat crops in Europe
within the next 100 years, especially under the most proba-
ble +2 ◦ C climate change scenario, will be a concern. East-
ern Europe, Balkan Peninsula, and the Mediterranean regions
will be the most affected regions (Battilani et al., 2016). Using
a full chain modeling approach, Van der Fels-Klerx, Ver-
meulen, Gavai, and Liu (2019) have determined that by using
maize grown in Eastern Europe and imported to the Nether-
lands as a component of the dairy cow feed, an increase of
up to 50% of maximum mean of AFM1 in milk by 2030 can
be expected. It is therefore crucial to monitor and regulate the
level of AFM1 in milk and milk products through the control
of animal feed/food quality also in developing countries.
Campylobacter spp. is one of the four key global causes
of diarrheal diseases (WHO, 2018a). Campylobacteriosis
is sporadic in nature but outbreaks can occur worldwide
(Table 6). Milk, especially raw unpasteurized milk, is among
the main incriminated foods, where Campylobacter may
occur mainly through cross-contamination, as they inhabit the
intestinal tract of a broad range of animals. Although C. coli
and C. jejuni are the most incriminated species, the taxon-
omy of Campylobacter is evolving continuously with several
novel species described (Foster et al., 2004; Debruyne, On,
De Brandt, & Vandamme, 2009; Zanoni, Debruyne, Rossi,
Revez, & Vandamme, 2009; Debruyne et al., 2010a, 2010b;
Gilbert, Kik, Miller, Duim, & Wagenaar, 2015; Piccirillo
et al., 2016; Van, Elshagmani, Gor, Scott, & Moore, 2016;
Cáceres, Muñoz, Iraola, Díaz-Viraqué, & Collado, 2017;
 10

TABLE 5 Incidence of aflatoxin M1 in dairy products worldwide from 2000 to date

Positive samples/Total Amount (range in % of samples
Country Year Dairy product samples (incidence %) ppb) exceeding EU limits References
Turkey 2001 Cheese 50/57 0.040 to 0.810 NS Oruc & Sonal, 2001
Turkey 2001 to 2002 White, kashar, and processed 10/200, 12/200, and 0.202 to 0.366 100 Yaroglu, Oruc, & Tayar, 2005
cheese 8/200
Iran 2003 to 2004 Feta cheese 66/80 0.15 to 2.05 100 Kamkar, 2006
North Africa 2004 White soft cheese 15/20 0.011 to 0.050 – Elgerbi et al., 2004
Turkey 2004 Cheese and yogurth 11/39, 32/40 <50 to 0.188 28 and 100 Gürbay, Engin, Çağlayan, & Şahin,
2006
Slovenia 2004 to 2005 Curd, soft, salted, or nonsalted 4/40 0.051 to 0.223 7.5 Torkar & Vengušt, 2008
cheese and semihard cheese
Kuwait 2005 to 2007 White cheese 32/40 0.024 to 0.452 30 Dashti et al., 2009
Turkey 2006 Surk cheese 72/120 0.016 to 1.043 60 Aygun, Essiz, Durmaz, Yarsan, &
Altintas, 2009
Turkey 2006 White brined cheese 159/193 0.052 to 0.860 100 Ardic, Karakaya, Atasever, &
Adiguzel, 2009
Turkey 2007 to 2008 Kashar cheese 109/132 0.01 to 0.630 27.3 Tekinşen & Eken, 2008
Iran 2007 to 2008 White cheese and cream cheese 93/116 and 68/94 0.052 to 0.785 100 Fallah, Jafari, Fallah, & Rahnama,
2009

Brazil 2008 Minas Frescal cheese and 6/24 and 7/24 0.037 to 0.313 21 and 25 Oliveira, Franco, Rosim, & Fernandes,
Minas Padrão cheese 2011
(Continues)
MILK AND DAIRY MICROBIAL QUALITY…
TABLE 5 (Continued)
Positive samples/Total Amount (range in % of samples
Country Year Dairy product samples (incidence %) ppb) exceeding EU limits References
Italy 2008 cheese 44/265 0.050 to 0.250 – Montagna, Napoli, De Giglio, Iatta, &
Barbuti, 2008
Egypt 2008 to 2009 Soft, hard, and processed 20/50, 19/50, and 11/50 0.052 to 0.088, 100, 100, and 100 Amer & Ibrahim, 2010
cheese 0.052 to 0.182,
and 0.052 to 0.054
MILK AND DAIRY MICROBIAL QUALITY…

Brazil 2010 Cheese, yogurt and dairy drinks 49/58, 25/53, and 10/10 0.010 to 0.304 29.3, 13.2, none Iha, Barbosa, Okada, & Trucksess,
2011
Italy 2010 cheese 85/102 <50 → 150 56.7 Anfossi et al., 2012
Worldwide 2011 Blue-venied cheese and 0/89 – – Fontaine et al., 2015
blue-white mold cheeses
Iran 2011 to 2012 Yoghurt, cheese, and ice-cream 48/60, 69/80, and 34/60 0.014 to 0.572 13.7 (cheese) and 5 Rahimi, 2014
(yogurt), none in
ice-cream
Turkey 2012 White pickled cheese, yogurth 50/50, 50/50 0.040-0.131, 20, 20 Temamogullari & Kanici, 2014
0.041-0.72
Italy 2012 Milk cream and cheese 10/24 ≤0.003 to 0.018 none Santini et al., 2013
Lebanon 2012 Processed and imported cheese 75/111 0.006 to 0.315 32.4 Elkak, El Atat, Habib, & Abbas, 2012
Costa Rica 2012 to 2014 Fresh cheese, Sour cream 26/70 and 0/70 0.031 to 0.276, none 18.6 Chavarría, Granados-Chinchilla,
Alfaro-Cascante, & Molina, 2015
Iran 2013 White and Lighvan cheese 39/82 ND-0.31 12 Mohajeri et al., 2013
Iran 2014 to 2015 Cheese samples 52/100 0.050 to 0.424 100 Sharifzadeh, Ghasemi-Dehkordi,
Foroughi, Mardanpour-Shahrekordi,
& Ramazi, 2017
Turkey 2014 to 2016 Ezine cheese, cheese halva 60/120 and 7/120 0.019 to 0.158 and – Eker, Muratoglu, & Eser, 2019
0.050 to 0.213
Iran 2015 Yogurt, white cheese, and 15/18, 6/10, and 10/10 0.008 to 0.012 0.006 none Sohrabi & Gharahkoli, 2016
butter to 0.021 0.005 to
0.017
Qatar 2018 Yogurt, cheese, butter, and 16/21, 39/46, 12/18, and 0.002 to 0.220 None, 74, none, none Hassan et al., 2018
laban 19/25
11
12 MILK AND DAIRY MICROBIAL QUALITY…

TABLE 6 Outbreaks due toCampylobacter spp. traced back to milk and dairy products occurred from 2000 to date
Number
Species Country Year Food of cases References
C. jejuni USA 2001 Unpasteurized milk 75 Harrington, Archer, Davis,
(Wisconsin) Croft, & Varma, 2002
C. jejuni Spain 2003 Custard made with UHT milk 81 Jiménez et al., 2005
C. jejuni USA (Utah) 2002 Raw milk 13 Peterson, 2003
C. jejuni The Netherlands 2005 Raw milk 22 Heuvelink et al., 2009
C. jejuni USA (California) 2006/2007 Milk, postpasteuriza- 1.644/8 Jay-Russell et al., 2013
tion/commercial raw milk
and raw chocolate colostrum
C. jejuni USA (Kansas) 2007 Unpasteurized milk and cheese 19 Hunt, Ocfemia, Neises,
Hansen, & Aghoghovbia,
2009
C. jejuni USA (California) 2007 Raw milk or colostrum 8 CDPH, 2008
C. jejuni The Netherlands 2007 Raw milk 16 Heuvelink et al., 2009
C. jejuni USA (Multistate) 2012 Unpasteurized milk 148 Longenberger et al., 2013
C. jejuni Pennsylvania 2013 Raw (unpasteurized) milk 6 CDC, 2013
C. jejuni California 2015 Raw goat milk 3 FIOD, 2015c
C. jejuni Utah 2014 Raw milk 99 Davis et al., 2016
C. jejuni Sweden 2014 Raw (unpasteurized) milk 11 Lahti et al., 2017
C. jejuni Colorado 2016 Raw (unpasteurized) milk 12 Burakoff et al., 2018
C. fetus The Netherlands 2017 Unripened chees from 6 Koppenaal et al., 2017
unpasteurized sheep’s milk

Gilbert et al., 2017, 2018), and other amended (Wang et al.,
2002; Duim et al., 2004; Miller et al., 2005), prompting the
need of (re)validating the species-specific detection and iso-
lation assays available for these species (On et al., 2013) in
order to investigate their occurrence and the related potential
risks associated with the milk (products).
Salmonella is another of the four key global causes of diar-
rheal diseases (WHO, 2018b) and it causes annually 93.8
million cases of foodborne illness and 155,000 deaths (Eng
et al., 2015). Being ubiquitous bacteria, salmonellae may
enter milk and the dairy environment from many sources.
However, because adequate pasteurization of milk and hur-
dles such as those used in ripened hard cheeses inactivates
Salmonella, salmonellosis outbreaks related to dairy products
have mainly involved raw milk and fresh raw milk cheeses
(Table 7). Although Salmonella taxonomy and nomenclature
have been subject to debate since their discovery in 1855 (Tin-
dall, Grimont, Garrity, & Euzéby, 2005; Ryan, O’Dwyer, &
Adley, 2017), more than 2,500 different serotypes or serovars
have been identified to date within the Salmonella bon-
gori and Salmonella enterica species, with S. Enteritidis, S.
Typhimurium, S. Infantis, S. Newport, S. Agona, S. Kentucky,
S. Derby, S. Stanley, and S. Virchow as the most frequent
serovars in reported confirmed cases of human salmonellosis
in the EU (EFSA & ECDC, 2018). Moreover, (multi)drug
resistance and novel genetic repertoires for pathogenicity and
adaptations have been noted to occur within certain serovars
(Olsen et al., 2004; Reen et al., 2005; Cummings et al., 2010;
Moreno Switt et al., 2012; Yap, Gan, The, Chai, & Thong,
2014; Giner-Lamia et al., 2019; Gong et al., 2019; Mangat
et al., 2019; Sekhon, Chander, Mayilraj, & Rishi, 2019).
Although E. coli includes commensal strains of the micro-
biota of healthy humans and other mammals, certain strains
of this bacterium have evolved into highly versatile pathogens
that are able to cause serious and lethal diseases with
significant economic losses and public health burdens world-
wide. Among these, Shiga toxin-producing E. coli (STEC)
may cause bloody diarrhea, which in 5 to 15% of pediatric
patients flows into potentially fatal hemolytic uremic syn-
drome (Bruyand et al., 2019). STEC include E. coli-producing
Stx1 and/or Stx2 toxins, with O103, O146, O157, O111,
O113, and O126 serogroups as the mostly detected in milk
and dairy products in the EU (EFSA & ECDC, 2018), whereas
E. coli O157:H7 is the most associated to milk- and dairy-
borne outbreaks worldwide since the start of the 21st century
(Table 8). However, non-O157 STEC strains mainly belong-
ing to the O26, O45, O91, O103, O111, O121, O145, and
O146 serogroups are emerging as foodborne pathogens caus-
ing sporadic cases of illness and outbreaks worldwide (Math-
usa, Chen, Enache, & Hontz, 2010; Castro, Carvalho, Conte-
Junior, & Figuiredo, 2017; EFSA & ECDC, 2018; Valilis,
Ramsey, Sidiq, & DuPont, 2018).
Apart from the abovementioned ongoing and emerging
microbial threats, other pathogens are newly emerging in milk
MILK AND DAIRY MICROBIAL QUALITY… 13

TABLE 7 Salmonellosis outbreaks traced back to milk and dairy products consumption occurred from 2000 to 2019
Number
Serotype Country Year Food of cases References
S. Typhimurium USA (Pennsylvania and 2000 Milk contaminated after 93 Olsen et al., 2004
New Jersey) pasteurization
S. Enteritidis France 2001 Cantal cheese made from raw 215 Haeghebaert et al., 2003
milk
S. Stanley Switzerland 2006 to 2007 Local soft cheese 82 Pastore et al., 2008
S. Typhimurium France 2008 Unpasteurized goat’s cheese 25 van Cauteren et al., 2009
S. Montevideo France 2006 Soft cheese made with raw 23 Dominguez et al., 2009
milk from cows
S. Newport USA (Illinois) 2006 to 2007 Unpasteurized Mexican-style 85 Austin et al., 2008
aged cheese
S. Agona France 2005 Powdered infant formula 141 Brouard et al., 2007
S. Typhimurium USA (multistate) 2002 Raw milk 62 Mazurek et al., 2004
S. Typhimurium 2006 to 2007 Ripened hard cheese made 224 Van Duynhoven et al., 2009
from raw milk
S. Typhimurium USA (Pennsylvania) 2007 Raw milk and raw milk cheese 29 Lind et al., 2007
S. Give France 2008 Infant milk formula 6 Jourdan et al., 2008
S. Enteritidis USA (multistate) 2012 Mexican-style fast food 68 CDC, 2012
restaurant chain (77% of the
ill people reported eating
cheese)
S. Dublin France 2012 Saint-Nectaire (bovine 103 Ung et al., 2019
raw-milk cheese)
S. Stanley USA (multistate) 2013 to 2014 Raw Cashew Cheese 17 CDC, 2014
S. Dublin France 2015 Reblochon (bovine raw-milk 34 Ung et al., 2019
cheese)
S. Agona France, Spain and 2017 Infant formula 39 EFSA & ECDC, 2018
Greece
S. Poona France 2018 to 2019 Infant formula 33 Jones et al., 2019

and dairy products. Among these, Arcobacter butzleri, whose
taxonomy has been recently suggested to be emended to
the Aliarcobacter butzleri comb. nov. (Perez-Cataluña et al.,
2018a, 2018b), is an emerging foodborne enteropathogen that
is being associated with enteritis, severe diarrhea, bacteremia,
and septicemia in humans and enteritis, mastitis, abortion, and
stillbirth in cows, sheep, and pigs (Fanelli et al., 2019, 2020).
For this reason, the International Commission on Microbi-
ological Specifications for Foods, on 2002, included it in
the list of microbes considered as serious hazard to human
health (ICMSF, 2002). Several studies investigated the pres-
ence of Arcobacter spp. in bulk tank raw cow’s and buf-
falo’s milk, reporting from low to high prevalence rates in
diverse countries (Table 9). Moreover, their occurrence and
survival in milk and dairy products and environments have
been demonstrated (Pianta, Thompsen Passos, Hepp, & de
Oliveira, 2007; Giacometti et al., 2014; Giacometti, Losio,
et al. 2015; Scarano et al., 2014; Serraino & Giacometti, 2014;
Tremonte et al., 2014; De Cesare et al., 2016; Piva et al., 2017;
Ferreira, Oleastro, & Domingues, 2017).
Even though it is widespread in retail meat products and
the intestine of food animals and insight into its virulence
and antibiotic resistance has been recently provided (Fanelli
et al., 2019, 2020), the significance of Arcobacter as food-
borne pathogen is unclear. Surveillance programs assessing
the prevalence of this emerging pathogen in the various foods
should be undertaken and rapid and reliable methods to detect
it should be developed. Moreover, the substantial lack of infor-
mation on its virulence mechanisms should be fulfilled by
appropriate pathogenesis studies mainly explaining its role in
gastrointestinal disease.
Yersinia enterocolitica is an important enteropathogen
that causes gastrointestinal diseases leading to severe com-
plications such as osteoarthritis, mesenteric lymphadeni-
tis, pseudoappendicular syndrome, hematuria, splenitis,
nephritis, purulent hepatitis, myocarditis, and also chronic
immunological sequelae (Chlebicz & Śliżewska, 2018).
Yersiniosis is third most commonly reported bacterial food-
borne zoonosis reported in the EU, with milk and dairy prod-
ucts among the most incriminated foods (Ackers et al., 2000;
14 MILK AND DAIRY MICROBIAL QUALITY…

TABLE 8 Outbreaks due to pathogenic E. coli traced back to milk and dairy products occurred from 2000 to 2019
Number
Serotype Country Year Food of cases References
O157:H7 Canada (Alberta) 2002 Unpasteurized gouda 13 Honish et al., 2005
cheese
O157 Slovakia 2003 Unpasteurized cow’s milk 9 Liptakova et al., 2004
O157:H- Denmark 2003 to 2004 Organic Jersey milk 25 Jensen et al., 2006
O157 France 2004 Unpasteurized goat’s cheese 2 Espiè et al., 2006
O157:H7 USA (Washington 2005 Raw milk 18 Bhat et al., 2007
and Oregon)
O157:H7 USA (Pacific 2005 Raw milk 18 Denny, Bhat, & Eckmann,
Northwest) 2008
O157:H7 USA (California) 2006 Raw (unpasteurized) cow 6 Schneider, Mohle-Boetani,
milk Vugia, & Menon, 2008
O92:H33 Italy 2006 Pecorino cheese mad with 24 Scavia et al., 2008
unpasteurized sheep milk
O145; O26 Belgium 2007 Ice cream from pasteurized 12 De Schrijver et al., 2008
milk
O157 USA (Connecticut) 2008 Raw milk 14 Guh et al., 2010
O157:H7 USA (multistate) 2010 Bravo Farm cheese 38 CDC, 2010
O26:H11 Italy and Romania 2013 Dairy products 20 Germinario et al., 2016
O157:H7 Scotland 2016 Unpasteurized cows’ milk 20 HPS, 2016
cheese (Dunsyre Blue)
STEC O157 Europe 2016 Dairy products 25 EFSA, 2016
and O26 (multi-country)
O157:H7 England 2017 Raw drinking milk 7 Treacy et al., 2019
O26 France 2019 Raw cow’s milk soft cheese 16 Jones et al., 2019

Longenberger et al., 2014; EFSA & ECDC, 2018). Several
studies are reporting the occurrence of this pathogen in milk
and dairy products (Table 10) where it can survive, even in
the viable but unculturable state, and proliferate also at refrig-
erated temperatures (Bozkurt & Erkmen, 2001;De Lamo-
Castellví et al., 2005; Tamagnini, de Sousa, González, Revelli,
& Budde, 2005; Bari, Hossain, Isshiki, & Ukuku, 2011; Han-
ifian, & Khani, 2012a; Yehualaeshet et al., 2013; Kowalik,
& Lobacz, 2015; Zadernowska, Chajęcka-Wierzchowska, &
Ogryzek, 2015; Abdollahi & Hanifian, 2016; Bursová, Neci-
dová, Haruštiaková, & Janštová, 2017).
However, many Y. enterocolitica strains isolated from milk
can also be apathogenic. Six serovars can be distinguished
in Y. enterocolitica, that is, serovars 1A, 1B, 2, 3, 4, and 5.
Although strains of the serovars 1B to 5 possess a virulence
plasmid (pYV) and virulence factors (e.g., enterotoxin YstA),
these are considered pathogenic. Strains of serovar 1A, on
the other hand, do not possess the virulence plasmid but do
produce a different subtype of the heat stable enterotoxin
(YstB), which can also contribute to diarrhea. It was shown
that in some cases, biovar-1A-strains can cause similar gas-
troenteritis symptoms to pathogenic serovars and may thus
be considered as opportunistic pathogens. Research is needed
on (a) where these strains originate from, (b) why often high
numbers of such apathogenic strains occur in milk, (c) which
conditions promote their prevalence, and (d) which virulence
factors can occur in these strains. Other Yersinia species,
such as Y. pseudotuberculosis, are emerging as milk-borne
pathogens able to cause yersiniosis (Quigley, O’Sullivan,
et al., 2013; Ruusunen et al., 2013; Yehualaeshet et al., 2013;
McAuley, McMillan, Moore, Fegan, & Fox, 2014; Darwish,
Asfour, & Allam, 2015; Pärn et al., 2015; Jamali, Paydar,
Radmehr, & Ismail, 2015; Bonardi et al., 2018; Castro
et al., 2019).
Mycobacterium avium subsp. paratuberculosis (MAP), the
etiological agent of paratuberculosis (also referred to as
Johne’s disease) in domestic and wild ruminants, is also
debated as agent of Crohn’s disease in humans, with raw milk
and its derivatives serving as the main routes of transmis-
sion in humans (Robertson et al., 2017). Contamination of
milk by MAP takes place by both direct shedding of the bac-
terium within the udder of an infected animal and also indi-
rectly through fecal contamination; the degree of the latter
very much depends on care taken to ensure udder hygiene
during the milking process (Okura, Nielsen, & Toft, 2013;
Rani, Beaver, Schukken, & Pradhan, 2019). Some studies
performed in experimental conditions mimicking the actual
commercial pasteurization of milk have demonstrated the
MILK AND DAIRY MICROBIAL QUALITY… 15

TABLE 9 Occurrence of Arcobacter spp. in milk and dairy Helicobacter pylori, a pathogenic bacterium that can cause
products severe diseases such as gastric and duodenal ulcers with a
Country Source Reference high morbidity and mortality rate, has been detected and was
Ireland Raw milk Scullion, Harrington, & demonstrated to survive in raw cow, sheep, goat, buffalo, and
Madden, 2006 camel milk and dairy products (Table 12) (Dore et al., 2001;
Turkey Raw milk Ertas, Dogruer, Gonulalan, Elhariri, Hamza, Elhelw, & Hamza, 2018), suggesting these
Guner, & Ulger, 2010 food matrices as reservoirs or vehicles in the transmission of
Italy Water buffalo milk Giacometti, Salas-Massó, this pathogen. However, further investigations are needed to
Serraino, & Figueras, verify the transmission of H. pylori via milk and dairy con-
2015 sumption.
Italy Raw milk, ricotta cheese, Giacometti, Lucchi, et al., Powdered infant formula, whose main ingredient is mostly
mozzarella cheese, and 2013 milk powder, has been identified as source of Cronobacter
conditioning liquid
spp., especially C. sakazakii (Franz et al., 2018), previously
Italy Cow and water buffalo Giacometti, Serraino, et al., known as Enterobacter sakazakii and reassigned to the novel
raw milk and ricotta 2013
genus on 2008 (Iversen et al., 2008), which with an estimated
cheese
infection dose lower than 3 CFU/100 g (FAO/WHO, 2004b)
Italy Raw milk Giacometti, Lucchi, et al.,
could be fatal to neonates, infants, and immunocompromised
2015
adults. C. sakazakii, C. malonaticus, C. turicensis, C. muyt-
Italy Ricotta cheese Giacometti, Lucchi, et al.,
jensii, C. condimenti, C. universalis, and C. dublinensis (Lu
2015
et al., 2019) are species of this genus. They can be grouped, on
Malaysia Raw milk Shah, Saleha, Murugaiyah,
Zunita, & Memon, 2012
the basis of their clinical relevance, into Group I, comprising
C. sakazakii and C. malonaticus, which represent the major-
Italy In-line milk filters Serraino et al., 2013b
ity of isolates in all age groups; Group 2, which comprises C.
Turkey Cow milk, water buffalo Yesilmen, Vural, Erkan, &
turicensis and C. universalis, which have been rarely reported;
milk, and fresh village Yildirim, 2014
cheese and Group 3, which includes C. dublinensis, C. muytjensisii,
Italy Raw milk Caruso et al., 2019
and C. condimenti that have little or no clinical significance
(Forsythe, 2018). Several outbreaks have been traced back
Italy Raw milk and dairy De Cesare et al., 2016
products to the consumption of infant formulae contaminated with C.
sakazakii (reviewed by Parra-Flores et al., 2018; Yong et al.,
2018; Lepuschitz et al., 2019; Henry & Fouladkhah, 2019).
The concern was so high that it lead the Codex Alimentarius
inactivation of MAP (Pearce et al., 2001; Stabel, & Lam- Commission (CAC) and World Health Organization (WHO)
bertz, 2004; Lynch, Jordan, Kelly, Freyne, & Murphy, 2007) to assess and mitigate the microbiological risks by improving
and many studies demonstrated the survival of MAP after the microbiological criteria recommendations and revising
simulated milk pasteurization (Gao, Mutharia, Chen, Rahn, the advice on the preparation of infant feeds (FAO/WHO
& Odumeru, 2002; Grant, Hitchings, McCartney, Ferguson, 2004a, 2004b, 2006, 2008; WHO, 2007; CAC, 2008).
& Rowe, 2002; Stabel, & Lambertz, 2004; Grant, Williams, Brucellosis is caused by Gram-negative bacteria of the
Rowe, & Muir, 2005). Moreover, a quantitative model devel- genus Brucella, of which B. melitensis and B. abortus are
oped by Cerf, Griffiths, and Aziza (2007) has revealed that the major pathogens, which can be transmitted from sheep
the probability to detect MAP in 50 mL of pasteurized milk and goats and from cattle and other Bovidae, respectively.
is lower than 1%, thus implying that the presence of MAP in In the EU, brucellosis has been eradicated from livestock in
pasteurized milk could be due to either pasteurization failure most member states leading to the status officially free of
or postpasteurization contamination rather than to MAP sur- bovine brucellosis caused by B. abortus (officially brucellosis
vival. However, the quantification methods used until 2007 free [OBF]) as well as officially free of ovine and caprine
were less sensitive than those employed from 2007 to date brucellosis caused by B. melitensis (officially B. melitensis
more (e.g., phage assay or PMS-phage assay or qPCR) (Stan- free [ObmF]) (EC, 2003; Jansen, Linard, Noll, Nöckler, &
ley et al., 2007; Slana, Kralik, Kralova, & Pavlik, 2008; Fod- Al Dahouk, 2019). However, at the end of 2016, Bulgaria,
dai, Elliott, & Grant, 2009; Irenge et al., 2009; Slana, Liapi, Croatia, Cyprus, Greece, Hungary, Italy, Portugal, Spain, and
Moravkova, Kralova, & Pavlik, 2009; Foddai, & Grant, 2017), the United Kingdom (Channel Islands Jersey and Guernsey)
leading to a certain uncertainty in the conclusions of Cerf et al. were not yet OBF (EFSA and ECDC, 2017; Jansen et al.,
(2007). Moreover, in the last two decades, several studies have 2019). Brucella was also found to occur in raw cow’s milk
reported the presence of this pathogen in raw and pasteurized from the central Anatolian region of Turkey in 2016, where
milk and dairy products (Table 11). 35 of 202 raw cow’s milk samples (17.32%) were identified
16 MILK AND DAIRY MICROBIAL QUALITY…

TABLE 10 Occurrence of Yersinia enterocolitica in milk and dairy products

Country Source Reference
USA Pasteurized milk Ackers et al., 2000
Turkey Raw milk Yeşim Özbaş, Lehner, & Wagner, 2000
Germany Camembert cheese Maoz et al., 2002
Iran Raw and pasteurized milk Soltan-Dallal, Tabarraie, & MoezArdalan, 2004
USA Raw milk Jayarao et al., 2006
USA Pasteurized whole milk Myers, Gaba, & Al-Khaldi, 2006
Turkey Raw milk and cheese Yucel & Ulusoy, 2006
Egypt Sheep’s milk, goat’s milk, pasteurized milk, Abd El Aal & Atta, 2009
white soft cheese, plain yoghurt, and fruit
yoghurt
India Raw milk Subha, Ramakrishnan, & Suganthi, 2009
Iran Raw milk Hanifian & Khani, 2012b
Mexico Raw milk Bernardino-Varo, Quiñones-Ramírez, Fernández,
& Vázquez-Salinas, 2013
China Refrigerated and frozen dairy products Ye, Ling, Han, & Wu, 2014
Iran Traditional and commercial dairy products Rahimi, Sepehri, Safarpoor Dehkordi, Shaygan,
& Momtaz, 2014
Egypt Raw milk, cheese, ice cream, yogurt, and whey Ali, Attiah, & Aly, 2015
Egypt Buffaloes, goats and she-camels milk Darwish et al., 2015
Malaysia Raw milk Jamali et al., 2015
Turkey Raw, fermented and pasteurized milk, and cheese Özdemir & Arslan, 2015
Algeria Raw milk Hadef, Medjahdi, Beldjilali, Benamar, &
Moussa, 2016
South Africa Raw milk Ntuli, Njage, & Buys, 2016
Iran Raw sheep and goat milk Alavi, Rahimi, & Tajbakhsh, 2018
Sweden Raw milk Artursson, Schelin, Thisted Lambertz, Hansson,
& Olsson Engvall, 2018
Italy Raw milk Bonardi et al., 2018
USA Raw milk Drake, Davis, Khatiwada, & Williams, 2018;
Egypt Raw and pasteurized milk, fermented milk, and Ahmed, Tahoun, Abou Elez, Abd El-Hamid, &
ripened salted cheese Abd Ellatif, 2019
Brazil Raw milk Bertolini et al., 2019

as presumptive B. abortus (Babaoglu et al., 2018). Jansen
et al. (2019) investigated the presence of Brucella DNA in
cheeses mainly declared by processors as “raw milk cheeses”
and found 20.5% (41 of 200) samples on the German market
to be Brucella positive. No live cultures could, however, be
obtained from molecular positive samples using classical cul-
turing. The authors found that Brucella could be detected in
cheese samples from Bulgaria, France, Greece, and Turkey
and that, in contrast to the vendor information, essentially
only three of the PCR-positive cheese samples were made
from raw milk. Moreover, positive samples clustered at cer-
tain vendors, which indicates large-scale illegal imports of the
cheeses, leading to the conclusion that Brucella in imported
raw milk cheese seems to be still a food safety issue in the
EU, and that especially the uncontrolled importation of dairy
products from endemic regions may explain human Brucella
infections acquired in the nonendemic EU countries (Jansen
et al., 2019).
4 M ILK SA F ET Y IN TH E AG E OF
G E NOM I C S
Several methods are to date available to detect and char-
acterize milk- and dairy-borne pathogens. However, con-
ventional methods, also including serotyping, antimicrobial
susceptibility testing, and mass spectrometry-based methods
(reviewed by van Belkum et al., 2007 and Fusco & Quero,
2014), are time-consuming and provide low taxonomic res-
olution, whereas nonamplification- and amplification-based
genetic analyses are focused on only a small fragment of bac-
terial genome and usually require species-specific protocols.
These drawbacks are overcome by whole genome sequencing
MILK AND DAIRY MICROBIAL QUALITY… 17

TABLE 11 Example studies on the presence of Mycobacterium avium subsp. paratuberculosis in milk and dairy products
Country Source Reference
United Kingdom Raw and pasteurized milk Grant, Ball, & Rowe, 2002
Norway Raw goat milk Djønne, Jensen, Grant, & Holstad, 2003
India Raw goat milk Singh & Vihan, 2004
Czech Republic Pasteurized milk Ayele, Svastova, Roubal, Bartos, & Pavlik, 2005
USA Pasteurized milk Ellingson et al., 2005
Greece and the Soft, hard, and semihard cheeses (from pasteurized Ikonomopoulos et al., 2005
Czech Republic milk)
India Raw and pasteurized milk, and pasteurized milk Shankar et al., 2010
products
Brazil Pasteurized milk Carvalho, Pietralonga, Schwarz, Faria, &
Moreira, 2012
Argentina Pasteurized milk Paolicchi, Cirone, Morsella, & Gioffré, 2012

Cyprus Powdered infant formula Botsaris et al., 2016

Iran Raw milk Eftekhari & Mosavari, 2016
Italy Goat and sheep raw milk cheeses Galiero et al., 2016
Italy Raw milk Ricchi et al., 2016
India Fresh cottage cheese Stephen et al., 2016
Brazil Raw milk Feitosa de Albuquerque et al., 2017
England Semi-skimmed pasteurized milk Gerrard et al., 2018
Brazil Coalho cheese Albuquerque et al., 2019

(WGS)-based typing, which provides a bulk of information
from which it is possible to reconstruct the identification,
phylogeny, epidemiology, distribution, virulence, and mul-
tidrug resistance of a single strain.
WGS costs in the last decades decreased over time, whereas
the improvement in the techniques, single-molecule real-time
sequencing and long reads-based platform, increased the
output. WGS provides an unprecedented resolution for geno-
typing and this approach has become particularly relevant in
the identification of multidrug-resistant pathogens in clinical
environment, leading to the implementation of WGS-based
analysis as routine tool for the monitoring and the early detec-
tion of outbreaks in several countries. The reliability of WGS
has grown concurrently with the development of dedicated
pipeline for the analysis of pathogenicity determinants imple-
mented in the standard workflow of the analysis. Considering
that milk is one of the greatest reservoirs of pathogens
(Burgess, 2013), the application of WGS is determinant to
define genomic variations or epidemiological characteristics
among isolates associated with milk-borne-disease (Revez
et al., 2014; Dai et al., 2019; Hanson et al., 2019; Qian et al.,
2019).
WHO (2018c) published a landscape paper highlighting
the importance of WGS in foodborne disease surveillance.
The higher resolution of these method compared to the
traditional standard typing (pulsed-field gel electrophoresis
and multilocus carriable number tandem repeat analysis)
has been reported for Salmonella Enteritidis by den Bakker
et al. (2014) and for Listeria monocytogenes by Kwong et al.
(2016), whereas Dallman et al. (2015) reported no significant
difference between WGS and multilocus variable-number tan-
dem repeat analysis (MLVA) in timeliness of cluster detection
for Shiga toxin-producing Escherichia coli (STEC) O157.
WGS analysis can also permit the monitoring and predic-
tion of emerging threats linked to the rise of novel virulent
clones or novel allelic variants of a specific cluster among a
population of pathogens. These data can speed the surveil-
lance and management of emerging threats, and even if the
European Committee on Antimicrobial Susceptibility Testing
(EUCAST, 2016) does not yet support the use of WGS alone
in the decision-making process, it does not exclude that this
method would replace phenotypic testing for surveillance pur-
poses in the near future. On the contrary, WGS-based antimi-
crobial resistance (AMR) surveillance was introduced in the
United States at State and local public health departments and
universities within the framework of The National Antimi-
crobial Resistance Monitoring System (NARMS). The WGS-
based surveillance implementation has made available a
plethora of foodborne pathogens genomes (GenomeTrakr and
PulseNet networks have sequenced over 343,000 foodborne
isolates [FDA, 2020], which also constitute a base of standard-
ized output to be used for the development of phylogenomic
pipelines to characterize the variation among a set of
isolates).
18 MILK AND DAIRY MICROBIAL QUALITY…

TABLE 12 Presence of Helicobacter pylori in milk and dairy on this basis, be viewed as a way to increase the gut bacterial
products diversity. On the other hand, however, raw milk is clearly a
Country Source Reference possible source of serious bacterial pathogens such as STEC
Japan Raw milk Fujimura, Kawamura, Kato, and Campylobacter, which have low infectious doses. This
Tateno, & Watanabe, raises the question whether selling the milk with the (legally
2002 required) instruction to boil the milk is sufficient in terms
Turkey Raw sheep milk Turutoglu & Mudul, 2002 of food safety. Clearly, in the case of raw milk that is sold,
Italy Raw goat, sheep and Quaglia et al., 2008 the responsibility currently lies solely with the consumer and
cow milk the producer’s responsibility is only to clearly indicate to the
Greece Raw milk Angelidis et al., 2011 consumer that he/she should boil the milk. With pasteurized
Iran Raw milk Safaei, Rahimi, Zandi, & milk, such responsibility clearly is already with the producer,
Rashidipour, 2011 who has to ensure that the milk is safe for consumption after
Iran Bovine, buffalo, camel, Rahimi & Kheirabadi, 2012 the pasteurization process. Because in a small survey among
ovine, and caprine raw milk customers we determined that many consumers buy
milk the milk because they prefer it in the raw state (unpublished
Iran Rawa milk and cheeses Mousavi, Dehkordi, & results), the question is what should be done to protect the
Rahimi, 2014 public health. One possibility would be to legally curb the
Italy Raw milk Bianchini et al., 2015 sale of raw milk, or to regulate the sale of raw milk such
Sudan Raw milk Osman et al., 2015 that the producer is held responsible for selling a safe product.
Iran Cows, sheep, goats, Talaei, Souod, Momtaz, & Such decisions clearly need to be made by politicians and gov-
camels and buffalo Dabiri, 2015 ernment. Labeling consumer warnings regarding the higher
raw milk chances of serious infection in the young, old, and immune-
Iran Cow, sheep, goat, camel, Saeidi & Sheikhshahrokh, impaired subgroups of the population should also be adopted.
and buffalo milk 2016 As a minimum, the consumer needs to be informed of the
Egypt Raw milk and traditional Khaji, Banisharif, & Alavi, risks associated with raw milk consumption. Last, should the
dairy products 2017
trend of selling raw milk via vending machines increase, it
Algeria Raw milk Guessoum, Guechi, & would be of advantage if national or international norms were
Adnane, 2018
defined for the hygienic design and operation of such equip-
Iran Raw milk Ranjbar, Farsani, & ment. Very recently, a new DIN norm (Food Hygiene–Milk
Dehkordi, 2018
vending machines–Hygiene requirements) has become avail-
Iran Traditional dairy Ranjbar, Yadollahi Farsani,
able by the German Institute for Norming (European Com-
products & Safarpoor Dehkordi,
mission, 2020).
2019
Regarding the determinations of milk quality, it has become
evident that there has been a shift in milk spoilage micro-
biota from souring lactic acid bacteria to psychrophilic and
With particular reference to milk, Butcher et al. (2016) protein- and fat-degrading enzyme-producing pseudomonads
demonstrated that the use of WGS improved the case and acinetobacters. Although these bacteria would not survive
ascertainment in an outbreak of Shiga toxin-producing pasteurization, the proteases and lipases produced by pseu-
Escherichia coli O157 associated with raw drinking milk. domonads and acinetobacters are heat stable and can over pro-
The same conclusions were recently reported by Treacy et al. longed storage produce enzymatic damage to the milk. The
(2019) who demonstrated the usefulness of WGS in outbreak question, therefore, is whether the determination of micro-
detection and characterization, exploiting its highly discrimi- bial counts as stipulated by regulation (EC) 853/2004, which
natory strain typing. determines the number of mesophilic bacteria by plate count-
ing on plate count agar and incubating for 72 hr at 30 ◦ C
(ISO 4833-1:2013), is still adequate or whether this regula-
5 BRAND N E W P RO B L E MS FOR tion needs to be updated to account for growth of the more
AN ANCIENT P RO D U C T cold-tolerant spoilage bacteria. Furthermore, we should think
about developing methods to selectively detect and quantify
Based on metagenomic studies, the milk microbiota was such psychrotrophic bacteria in milk and to trace contamina-
shown to be more complex than initially thought. As current tion routes in cases of postpasteurization contamination.
gut microbial research indicated that a higher gut diversity of Emerging pathogens are also a concern in the context
gut bacteria appears to be positively associated with health of milk safety, especially in the light of climate change,
(Rinninella et al., 2019), the consumption of raw milk could, where increases in ambient temperatures affect feed
MILK AND DAIRY MICROBIAL QUALITY…
availability, production, cooling, and hence safety of milk.
Emerging pathogens such as Arcobacter butzleri, Yersinia
parahaemolyticus and pseudotuberculosis, coagulase-
negative staphylococci, and Campylobacter species should
be continually monitored and methods for culturing need to
be improved. Factors that may affect the specific detection of
such pathogens include the fact (i) that many cells can enter
the viable but nonculturable state that cannot be detected
by culturing, and (ii) that at cold temperatures and in the
substrate milk, some pathogens may die and decrease quickly,
which is a problem in the sampling process. This makes the
specific detection and the accurate determination of the levels
of the pathogenic bacteria present in milk samples incredibly
difficult. Methods such as next-generation sequencing-based
metagenomics, qPCR, or LAMP PCR can, however, be
developed to counteract these problems.
As the example of the investigation of Brucella in cheeses
on the German market (Jansen et al., 2019) has shown,
the hygienic status of milk with respect to such important
pathogens as B. melitensis or B. abortus (and potentially other
pathogens) differs among the EU and non-EU countries. With
fast air and road travel these days, the possibility that prod-
ucts made with raw milk that contain pathogenic bacteria from
endemic countries enter the EU and pose a risk to the EU con-
sumers is a reality. Such risk should become more cognizant
to food inspection and custom services among EU border to
assist consumer protection.
Finally, climate change can also be anticipated to affect
milk quality. As temperatures in northern Europe can be
expected to rise and periods with short but heavy rain fall
may be expected to increase, carryover problems with plant or
mold toxins may become a problem. For example, expansion
of the Datura plant originating from eastern and southeast-
ern Europe to eastern Bavarian and eastern German fields has
been reported to occur. These plants contain tropane alkaloids
which, when ending up in cow feed, might be carried over
into the milk. The same concern exists for mycotoxin B1, as
reported by Walte, Schwake-Anduschus, Geisen, and Fritsche
(2016) and Battilani et al. (2016). Thus, we need studies on the
potential for carryover of these and possibly also other plant
toxins that may, as a result of climate change, spread north
and contaminate feed, leading to novel problems with regard
to milk safety.
Humans and milk have a history that spans for centuries.
Yet we still have safety and quality issues with milk as a result
of changes in agriculture, processing methods, and climate
change. As milk is a highly nutritious food, we will always
also be in competition with our biggest competitors, which
are the smallest forms of life, that is, bacteria, prompting us
to explore new ways to improve the quality and safety of milk
in a changing setting. Thus, predictably, the subject of milk
safety and quality will be a current topic as long as we utilize
milk as a food.
19
ACKNOW LEDGMENTS
The authors would like to acknowledge the input of Dr. Karin
Knappstein and Dr. Hans-Georg Walte obtained from talks
and discussions regarding this subject. This review was in part
prepared within the European Community’s Horizon 2020
program under the MycoKey project (EU Project H2020-
E.U.3.2-678781). The authors would also like to thank the
German Ministry of Nutrition and Agriculture for funding
of the project “Anpassung mikrobiologischer Qualitätsbes-
timmung bei Rohmilch an moderne Produktionsbedingungen
durch Entwicklung und Integration innovativer Schnellmeth-
oden (NextMilQ).” The opinions expressed in this manuscript
are solely the opinions of the authors and do not reflect any
governmental opinions.
AUTH O R CONTRIBUTIO NS
VF and CF conceived the work, wrote the manuscript, revised
the overall manuscript, and were responsible of the overall
review quality control. DC, FF, and AFL assisted in drafting
the sections on milk safety and genomics. JK and CB assisted
in drafting the sections on milk quality and on milk micro-
biota. GS-C contributed to the milk microbiota section. GS-C
and DC reviewed the literature. All the authors contributed
to the revision of the manuscript and read and approved the
submitted manuscript.
O RC I D
Vincenzina Fusco https://orcid.org/0000-0002-5608-7657
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How to cite this article: Fusco V, Chieffi D,
Fanelli F, et al. Microbial quality and safety
of milk and milk products in the 21st cen-
tury. Compr Rev Food Sci Food Saf. 2020;1–37.
https://doi.org/10.1111/1541-4337.12568