1 s2.0 S095869461500120X Main

International Dairy Journal 50 (2015) 32e44
Contents lists available at ScienceDirect
International Dairy Journal

journal homepage: www.elsevier.com/locate/idairyj
Review
A review of the microbiological hazards of dairy products made from

raw milk
C. Verraes a, *, G. Vlaemynck b, S. Van Weyenberg b, L. De Zutter c, d, G. Daube c, e,
M. Sindic c, f, M. Uyttendaele c, g, L. Herman b, c
a
Staff Direction for Risk Assessment, DG Control Policy, Federal Agency for the Safety of the Food Chain (FASFC), Kruidtuinlaan 55, 1000 Brussels, Belgium
b
Institute of Agricultural and Fisheries Research (ILVO), Brusselsesteenweg 370, 9090 Melle, Belgium
c
Scientific Committee, Federal Agency for the Safety of the Food Chain (FASFC), Kruidtuinlaan 55, 1000 Brussels, Belgium
d
Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
e
Faculty of Veterinary Medicine, University of Liege, Boulevard de Colonster 20, 4000 Li ege, Belgium
f
Gembloux Agro-bio Tech, University of Li ege, Passage des Deport
es 2, 5030 Gembloux, Belgium
g
Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, Belgium
a r t i c l e i n f o a b s t r a c t
Article history: This review concentrates on information concerning microbiological hazards possibly present in raw
Received 7 April 2015 milk dairy products, in particular cheese, butter, cream and buttermilk. The main microbiological hazards
Received in revised form of raw milk cheeses (especially soft and fresh cheeses) are linked to Listeria monocytogenes,
21 May 2015
verocytotoxin-producing Escherichia coli (VTEC), Staphylococcus aureus, Salmonella and Campylobacter.
Accepted 25 May 2015
Available online 14 June 2015
L. monocytogenes, VTEC and S. aureus have been identified as microbiological hazards in raw milk butter
and cream albeit to a lesser extent because of a reduced growth potential compared with cheese. In
endemic areas, raw milk dairy products may also be contaminated with Brucella spp., Mycobacterium
bovis and the tick-borne encephalitis virus (TBEV). Potential risks due to Coxiella burnetii and Myco-
bacterium avium subsp. paratuberculosis (MAP) are discussed. Pasteurisation ensures inactivation of
vegetative pathogenic microorganisms, which increases the safety of products made thereof compared
with dairy products made from raw milk. Several control measures from farm to fork are discussed.
© 2015 Elsevier Ltd. All rights reserved.
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
2. Occurrence of human pathogenic microorganisms in raw milk and dairy products made from raw milk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
3. Reported human cases and outbreaks due to the consumption of dairy products made from raw milk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
4. Growth and survival of pathogenic microorganisms during production and storage/ripening of dairy products made from raw milk . . . . . . . . . . . . . 38
5. Identification of main microbiological hazards in dairy products made from raw milk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
6. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
7. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42
1. Introduction
Consumers' attitudes show a trend towards increased con-

sumption of foods that are not or only minimally processed such as
* Corresponding author. Tel.: þ32 2 211 87 00. raw milk and dairy products made from raw milk. Cheeses made
E-mail address: [email protected] (C. Verraes). from raw cow, sheep and goat milk are the most frequently
http://dx.doi.org/10.1016/j.idairyj.2015.05.011
0958-6946/© 2015 Elsevier Ltd. All rights reserved.
C. Verraes et al. / International Dairy Journal 50 (2015) 32e44 33
consumed type of dairy products made from raw milk; however, collected for Europe and are shown in Table 1, where the detection
other types of dairy products made from raw milk are also frequency, the type of food, the method of analysis and the country
consumed such as mozzarella made from raw buffalo milk, as well are given.
as raw milk butter made from cow milk. The consumption of raw Frequencies of occurrence were found for several raw milk
milk can hold a risk for the consumer, due to the possible presence cheeses, butter and cream. No frequencies were found for butter-
of human pathogenic microorganisms. The risks and benefits of the milk made from raw milk as such products are less often produced.
consumption of raw cow milk were described in a review by Claeys No Salmonella has been detected in any tested samples of raw milk
et al. (2013) and the nutritional and health benefits of the con- cheeses, butter and cream with the exception of one publication
sumption of raw milk from animal species other than cows were where the prevalence in cheese was 4.3% (n ¼ 70 samples; Almeida
described in a review by Claeys et al. (2014). The microbiological et al., 2007). Concerning VTEC in raw milk cheeses, E. coli strains
hazards of raw milk from animal species other than cows were with virulence genes are detected with frequencies between 0 and
described in a review by Verraes et al. (2014). Also EFSA evaluated 55.3%. Farrokh et al. (2013) stated that the prevalence of vtx genes,
the public health risk from the consumption of raw drinking milk detected by PCR, does not necessarily reflect the occurrence of a
(EFSA, 2015). viable E. coli isolate containing those genes. VTEC was also detected
In the present review, a collation is made of available informa- in butter (Messelh€ ausser, Beck, Gallien, Schalch, & Busch, 2008). As
tion in the scientific literature concerning the microbiological illustrated in Table 1, L. monocytogenes was detected in raw milk
hazards of dairy products made from raw milk, in particular cheese, cheeses, butter and cream with frequencies varying between 0 and
butter, cream and buttermilk. Dairy products made from raw milk 41.9%, 3.6 and 29.9%, and 0.7 and 8.3% respectively, although in
from cows, sheep and goats are taken into account. Dairy products some cases the numbers were lower than 100 cfu g1. Of 70 cheese
made from raw milk from other animal species are less relevant in samples, 11.4% were positive for L. monocytogenes per 25 g, whereby
Europe, with the exception of mozzarella made from raw buffalo 1.4% contained counts higher than 200 cfu g1 and 10.0% lower than
milk. Only zoonotic human pathogenic microorganisms and path- 100 cfu g1 (Almeida et al., 2007). Of 474 cheese samples and 519
ogens originating from the environment have been taken into butter samples, respectively, 0.6% and 0.2% of the samples that were
consideration. Pathogenic agents originating from human taken in Belgium by the sector of small cheese producers in the
contamination due to human illness, e.g., Salmonella Typhi, Shigella Walloon region had counts higher than 100 cfu g1 (Sci Com, 2015).
spp. and noroviruses are not covered in this review. No Campylobacter were detected in 199 tested raw milk cheeses,
which contrasts the higher reporting in raw milk (0e12%) (EFSA,
2. Occurrence of human pathogenic microorganisms in raw 2015; Verraes et al., 2014). As indicated in Table 1, S. aureus was
milk and dairy products made from raw milk found in raw milk products with frequencies between 5 and 100%
in cheeses, and between 1.6 and 20.3% in butter, but the possibility
In general, pathogenic microorganisms can contaminate raw of the strains to produce enterotoxins varies and the share of such
milk in two ways. The first way is an endogenous contamination strains is difficult to deduce from the available information.
where the milk is contaminated by a direct transfer from the blood Jørgensen, Mørk, and Rørvik (2005) also detected S. aureus in sour
(systemic infection) to the milk or via an infection in the udder cream. B. cereus was detected in 28% of 25 samples of cheeses made
called mastitis. The second way is an exogenous contamination, from raw milk of several animal species. All strains were able to
where the milk is contaminated during or after milking by the produce enterotoxins (Williams & Withers, 2010). MAP was
faeces, the exterior of the udder and teats, the skin, the environ- detected in 4.2 and 20% of raw milk cheese samples using PCR
ment, etc. (Stephan, Schumaher, Tasara, & Grant, 2007; Williams & Withers,
Based on recent review documents (Claeys et al., 2013; EFSA, 2010). C. burnetii was detected with PCR in 57.0% of unpasteurised
2015; Sci Com, 2011, 2013; Verraes et al., 2014), the following hu- cheese samples and in one of two cream samples, but the relation
man pathogenic microorganisms are considered as the main of these PCR results with the presence of infectious strains is not
microbiological hazards associated with raw milk consumption clear (Eldin, Angelakis, Renvoise , & Raoult, 2013).
from cows, goats and sheep: Bacillus cereus, Campylobacter coli and
Campylobacter jejuni, enterotoxin-producing Staphylococcus aureus, 3. Reported human cases and outbreaks due to the
Helicobacter pylori, human pathogenic verocytotoxin-producing consumption of dairy products made from raw milk
Escherichia coli (VTEC), human pathogenic Yersinia, Leptospira, Lis-
teria monocytogenes, Salmonella spp., Streptococcus agalactiae, The development of a disease after consumption of contami-
Streptococcus equi subsp. zooepidemicus, Clostridium botulinum, nated dairy products made from raw milk depends on several
Brucella spp., Mycobacterium bovis, Cryptosporidium parvum and factors such as the pathogenicity of the strain, the number of
Toxoplasma gondii. Some microbiological hazards are indicated as ingested microorganisms, the physiological state of the microor-
hypothetical because they are still not confirmed, but have the ganism, the health condition of the consumer at the moment of
hypothetical potential to be pathogenic for humans (Mycobacte- ingestion, etc. Persons belonging to the YOPI group (young, old,
rium avium subsp. paratuberculosis; MAP) or to be foodborne pregnant, immunodeficient) have a higher risk of infection for
(Coxiella burnetii). certain pathogens such as L. monocytogenes and healthy persons
Limited systematic data were available on prevalences of human can also be infected. The likelihood of developing a disease follows
pathogenic microorganisms in dairy products made from raw milk. a doseeresponse curve with a higher number of cells increasing the
In a baseline study (EFSA, 2013b) performed at a European level, 1 chance of developing a disease. This relationship was categorised
sample from 476 raw milk cheese samples exceeded 100 cfu g1 for by the EFSA BIOHAZ Panel in the framework of a risk ranking ex-
L. monocytogenes. The EU summary report mentioned that non- ercise of foods of non-animal origin as follows: score 1 stands for a
compliance of L. monocytogenes primarily occurred in soft and doseeresponse curve where the pathogen has to grow to high
semi-soft cheeses made from raw or low heat-treated cows' milk numbers (often higher than 5 log cfu g1) to produce toxins and
(EFSA & ECDC, 2015). In addition, studies in the scientific literature cause illness; score 2 stands for a doseeresponse curve where the
describing detection frequencies of human pathogenic microor- pathogen must grow to cause illness; and score 3 stands for a
ganisms in dairy products made from raw milk provide an indica- doseeresponse curve where the pathogen can cause illness in low
tion of prevalences. Data of such frequencies of occurrence were numbers (Da Silva et al., 2015; EFSA, 2013a). Salmonella,
34 C. Verraes et al. / International Dairy Journal 50 (2015) 32e44
Table 1
Reported frequencies of occurrence of human pathogenic microorganisms in/on dairy products made from raw milk in Europe.a
Dairy product made Frequency of Number of Comments Country References

from raw milk occurrence (%) samples
Salmonella
Cheese 0.0 71 Belgium De Reu, Debeuckelaere, Botteldoorn, De
Block, and Herman (2002)
0.0 20 Belgium De Reu, Grijspeerdt, and Herman (2004)
0.0 334 Germany Hahn, Walte, Coenen, and Teufel
(1999a)
0.0 75 Ireland Coveney, Fitzgerald, and Daly (1994)
4.3 70 Portugal Almeida et al. (2007)
0.0 25 Scotland Williams and Withers (2010)
0.0 429 Belgium DiversiFerm (pers. comm.)
0.0 582 Belgium FASFC (pers. comm.)
Butter 0.0 64 Belgium De Reu et al. (2004)
0.0 518 Belgium DiversiFerm (pers. comm.)
Cream 0.0 132 Belgium FASFC (pers. comm.)
Verocytotoxin-producing Escherichia coli (VTEC)

Cheese 5.6 71 IMS, VIDAS O157 Belgium De Reu et al. (2002)
assay and PCR
0.0 20 IMS, VIDAS O157 Belgium De Reu et al. (2004)
assay and PCR
0.0 334 1.5% VTEC Germany Hahn et al. (1999a)
4.0 25 Enrichment; 1 stx2- Italy Volponi et al. (2012)
positive strain
13.1 1039 PCR France Vernozy-Rozand, Montet, Berardin,
Bavai, and Beutin (2005)
5.7 1502 PCR Switzerland Zweifel et al. (2010)
0.0 739 IMS Scotland Coia, Johnston, Steers, and Hanson
(2001)
8.9 180 - Vero cell assay France Fach et al. (2001)
30.6 - PCR-ELISA
4.8 83 Isolation Spain Caro and García-Armesto (2007)
30.4 112 - PCR-ELISA Italy , and
Auvray, Lecureuil, Dilasser, Tache
27.7 - RT-PCR Derzelle (2009)
2.7 - Colony hybridisation
4
- .5 143 - PCR vtx1 gene Italy Civera et al. (2007)
3.8 - PCR vtx2 gene
0.8 - PCR eae gene
2.1 - PCR ehxA gene
0.0 - Isolation
0.0 1313 Isolation of E. coli O157; Italy Conedera et al. (2004)
also butter
4.9 - 796 - PCR Switzerland Stephan et al. (2008)
41.0 - 39 - Non-O157 VTEC strains
0.0 70 IMS Portugal Almeida et al. (2007)
29.8 400 - PCR vtx gene France Madic et al. (2011)
37.3 - PCR eae gene
55.3 - At least one of O26,
6.5 O103, O111, O145 and
O157 genetic markers
- Combinations of above
0.0 25 Isolation of E. coli O157 Scotland Williams and Withers (2010)
10.0 10 Also butter Germany Messelh€ausser et al. (2008)
0.8 1042 PCR Belgium FASFC (pers. comm.)
Butter 0.0 64 IMS, VIDAS O157 Belgium De Reu et al. (2004)
assay and PCR
0.0 366 PCR Belgium FASFC (pers. comm.)
Cream 0.0 131 PCR Belgium FASFC (pers. comm.)
Listeria monocytogenes
Cheese 0.0 55 Sweden Rosengren et al. (2010)
0.8 122 Norway Jakobsen, Heggebø, Sunde, and
Skjervheim (2011)
2.8 71 Belgium De Reu et al. (2002)
0.0 20 Belgium De Reu et al. (2004)
2.4 334 Germany Hahn et al. (1999a)
0.0 17 Ireland Coveney et al. (1994)
11.4 70 1.4% > 2.3 log cfu g1; Portugal Almeida et al. (2007)
10.0% < 2 log cfu g1
19.0 42 Italy Rantsiou, Alessandria, Urso, Dolci, and
Cocolin (2008)
0.0 252 Portugal Kongo, Malcata, Ho, and Wiedmann
(2006)
Table 1 (continued )
Dairy product made Frequency of Number of Comments Country References

from raw milk occurrence (%) samples
0.0 51 Spain Arrese and Arroyo-Izaga (2012)

4.0 25 Scotland Williams and Withers (2010)
41.9 31 Sweden Loncarevic et al. (1995)
0.0 230 Austria Schoder et al. (2011)
12.2 474 0.6% > 2 log cfu g1 Belgium DiversiFerm (pers. comm.)
Butter 18.7 64 Belgium De Reu et al. (2004)
29.9 519 0.2% > 2 log cfu g1 Belgium DiversiFerm (pers. comm.)
12.4 259 Belgium De Reu and Herman (2004); De Reu,
Herman, De Boosere, and De Ville
(2006, 2007); De Reu, Herman, and De
Ville (2008)
Cream 5.0 20 Belgium De Reu and Herman (2004)
8.3 60 Croatia
Frece, Markov, Cvek, Kolarec, and Delas
(2010)
4.2 48 England & Wales Greenwood et al. (1991)
Campylobacter
Cheese 0.0 66 Ireland Whyte et al. (2004)
0.0 10 Germany Messelha€usser et al. (2008)
Staphylococcus aureus
Cheese 69.0 55 Coagulase-positive Sweden Rosengren et al. (2010)
staphylococci; 10.9% > 5
log cfu g1; 0% enterotoxins
67.5 122 Average of cheese stages Norway Jakobsen et al. (2011)
19.7 71 >3 log cfu g1; 7.1% (14) Belgium De Reu et al. (2002)
Enterotoxins
5.0 20 0% Enterotoxins Belgium De Reu et al. (2004)
13.1 245 >4 log cfu g1 Germany Hahn, Walte, Coenen, and Teufel
(1999b)
100.0 33 42.4% Enterotoxins Italy Cremonesi et al. (2007)
80.4 46 Average of cheese stages; Italy Poli et al. (2007)
100% enterotoxins
36.0 25 7 of 18 Examined strains Scotland Williams and Withers (2010)
from 2 cheeses able
to produce enterotoxin C
8.3 737 >5 log cfu g1 Belgium FASFC (pers. comm.)
Butter 1.6 64 0% Enterotoxins Belgium De Reu et al. (2004)
Bacillus cereus
Cheese 28.0 25 100% Enterotoxins Scotland Williams and Withers (2010)
Mycobacterium avium subsp. paratuberculosis

Cheese 4.2 143 PCR; no viable cells Switzerland Stephan et al. (2007)
20.0 25 PCR Scotland Williams and Withers (2010)
Coxiella burnetii
Cheese 57.0 68 France Eldin et al. (2013)
Butter 0.0 Not given France Eldin et al. (2013)
Cream 50.0 2 France Eldin et al. (2013)
a
Abbreviations are: IMS, immunomagnetic separation; PCR, polymerase chain reaction; PCR-ELISA, polymerase chain reaction enzyme-linked immunosorbent assay.
Campylobacter, VTEC and the tick-borne encephalitis virus (TBEV) non-exhaustive list is shown of reported human cases and out-
were in the framework of the present study allocated a score 3; breaks in Europe, the United States and Canada related to the
L. monocytogenes, Brucella, M. bovis and pathogenic species of consumption of dairy products made from raw milk found in sci-
Streptococcus have to grow to cause illness and have score 2; and entific literature or reported by official organisations. Only out-
S. aureus and B. cereus have to grow to numbers of several log units breaks due to the consumption of raw milk cheeses were found and
to be able to produce sufficient toxins to cause illness and therefore one outbreak was ascribed to the consumption of raw milk cream
they have a score of 1. For MAP and C. burnetii the foodborne and linked to infection with E. coli O157:H7 (CDSC, 1998a). Outbreaks
zoonotic potential is not known. due to the consumption of raw milk butter or buttermilk were not
The consumption of dairy products made from raw milk has found. From a report from EFSA (EFSA & ECDC, 2014), it seems that
already caused several human cases and outbreaks. In Table 2, a in 2012 no outbreaks were reported in the EU due to the
Table 2
Reported human cases and outbreaks in Europe, the United States and Canada due to the consumption of dairy products made from raw milk.
Pathogenic agent Dairy product made from Country Year Cases References
raw milk
Salmonella enteric Muenster Cheddar cheese from Canada 1982 Not given D'Aoust, Warburton,
unpasteurised milk and Sewell (1985); van
Cauteren et al. (2009)
Salmonella Typhimurium PT10 Cheddar cheese from Canada 1984 >1700 confirmed cases D'Aoust et al. (1985)
unpasteurised milk
Salmonella Farm raw milk cheese Finland 1985 35 cases Huchot, Bohnert, Cerf,
Farrokh, and Lahellec
(1993)
Salmonella Typhimurium Raw milk vacherin mont Switzerland 1985 215 cases Anonymous (1986)
d'or cheese
Salmonella Dublin Soft stilton cheese from England and Wales 1989 42 cases Maguire et al. (1992)
unpasteurised milk
Salmonella Paratyphi B Raw goat milk cheese France 1990 277 cases Grimont and Bouvet
(1991)
Salmonella Paratyphi B Raw goat milk cheese France 1993 273 cases, 1 dead Desenclos et al. (1996)
Salmonella Berta Farm soft cheese from Canada 1994 35 confirmed cases Ellis et al. (1998)
unpasteurised milk
Salmonella Dublin Raw cow milk mont d'or France and 1995 25 cases, 12 hospitalised, 5 Vaillant et al. (1996)
cheese Switzerland dead
Salmonella Dublin Raw cow milk mont d'or France 1996 14 cases, 1 dead Infuso, Vaillant, and
cheese Desenclos (1997)
Salmonella Typhimurium Raw milk morbier cheese France 1997 113 cases De Valk et al. (2000)
PT12 atypical
Salmonella Typhimurium Unpasteurised Mexican- United States 1997 31 confirmed cases Cody et al. (1999)
var Copenhagen phage style cheese (outbreak 1); 79 cases
type DT104 (outbreak 1) (outbreak 2)
and non-var Copenhagen
phage type DT 104b
(outbreak 2)
Salmonella Typhimurium DT104 Unpasteurised Mexican- United States 1997 54 confirmed cases Villar et al. (1999)
style cheese
Salmonella Newport Raw milk cheese United States 2001 27 cases, 12 hospitalised CDC (2014)
Salmonella Enteritidis phage type 8 Raw milk cantal cheese France 2001 215 cases Haeghebaert et al.
(2003)
Salmonella Typhimurium Unpasteurised queso-fresco United States 2003 50 cases, 7 hospitalised CDC (2014)
cheese
Salmonella Typhimurium Unpasteurised queso-fresco United States 2004 12 cases, 1 hospitalised and CDC (2014)
cheese 1 dead
Salmonella Unpasteurised queso-fresco United States 2005 2 cases CDC (2014)
cheese
Salmonella Typhimurium Unpasteurised queso-fresco United States 2006 20 cases, 2 hospitalised CDC (2014)
cheese
Salmonella enterica Newport Unpasteurised Mexican- United States 2006e2007 85 cases (but no significant CDC (2008)
style aged cheese association)
Salmonella Typhimurium Raw milk cheese and raw United States 2007 29 cases CDC (2007)
milk
Salmonella enteric Muenster Unpasteurised goat cheese France 2008 25 laboratory-confirmed van Cauteren et al.
cases, 4 hospitalised (2009)
Escherichia coli O119:B14 (vtx2) Farm fresh cheese from raw France 1992e1993 4 cases, 4 HUS, 1 dead Casenave et al. (1993)
cow and goat milk
E. coli O157 (PT28, vtx2) Farm raw milk cheese Scotland 1994 22 cases, 1 HUS Ammon (1997)
E. coli O103 Farm fresh cheese from raw France 1994 4 cases, 4 HUS Decludt (1995)
goat milk
E. coli O110:H- Raw milk cheese Germany 1996 3 cases, 0 HUS Bockemühl and Karch
(1996)
E. coli O157:H7 Fresh cheddar cheese curds United States 1998 63 cases, 55 laboratory- CDC (2000)
confirmed, 24 hospitalised
E. coli O157:H7 Unpasteurised cream England 1998 7 cases CDSC (1998a)
E. coli O157 (PT2, vtx2) Cheese from unpasteurised England 1998 10 cases, 1 HUS case CDSC (1998b)
milk
E. coli O157 Unpasteurised farm cheese Scotland 1998 4 cases Strachan et al. (2006)
E. coli O157 (PT21, PT28) Homemade raw goat milk Scotland 1999 27 cases, 1 HUS Curnow (1999)
cheese
E. coli O157:H7 Unpasteurised gouda hard Canada 2002e2003 13 cases, 2 HUS Honish et al. (2005)
cheese
E. coli O157:H7 Unpasteurised queso-fresco United States 2004 3 cases, 2 hospitalised CDC (2014)
cheese
E. coli O157:H7 Raw milk cheese Canada 2004 3 cases MAPAQ (2004)
E. coli O157 (vtx2, eae) Farm fresh unpasteurised France 2004 3 cases, 2 HUS et al. (2006)
Espie
goat cheese
E. coli O26, O80 (vtx2, eae) Raw milk brie France 2005 6 HUS INVS (2007)
E. coli O157:H7 Raw milk cheese Canada 2008e2009 16 cases Gaulin et al. (2012)
E. coli O157:H7 Aged raw milk gouda United States 2010 38 cases, 15 hospitalised McCollum et al. (2012)
cheese
Pathogenic agent Dairy product made from Country Year Cases References
raw milk
E. coli O157:H7, E. coli O157:NM(H-) Unpasteurised cheeses United States 2010 15 cases CDC (2014)
E. coli O157:H7 and Unpasteurised gouda United States 2010 38 cases, 15 hospitalised, 1 CDC (2014)
Listeria monocytogenes cheese HUS
Listeria Vacherin mont d'or cheese Switzerland 1983e1987 122 cases, 33 dead Bille (1989)
from unpasteurised milk
Listeria meningitis Anari raw goat milk soft England 1988 1 case Azadian, Finnerty, and
cheese Pearson (1989)
Listeria monocytogenes Serovar 4b Raw milk brie de meauw France 1995 36 cases, 4 dead, 7 foetal/ Vaillant, Maillot,
cheese neonatal cases Charley, and Stainer
(1998)
Listeria monocytogenes Serovar 4b Raw milk livarot, pont- France 1997 14 cases Jacquet, Saint-Cloment,
ve
l'e ^que cheese Brouille, Catimel, and
Rocourt (1998)
Listeria monocytogenes Fresh Mexican-style raw United States 2000e2001 13 cases, 11 pregnant CDC (2001);
milk cheese women (5 stillbirths, 3 MacDonald et al. (2005)
premature deliveries, 3
infected newborns)
Listeria monocytogenes Unpasteurised queso-fresco United States 2003 12 cases, 12 hospitalised, 1 CDC (2014)
cheese dead
Listeria monocytogenes Unpasteurised queso-fresco United States 2005 12 cases, 12 hospitalised, CDC (2014)
cheese 0 dead
Brucella melitensis Home-made fresh cottage Spain 1996 81 cases Castell Monsalve,
cheese from unpasteurised Rull
an, and CallizoNiet-
milk Sandoval Alcolea
(1996)
Brucella Homemade unpasteurised United States 2001 4 cases, 0 dead CDC (2014)
cheese
Brucella melitensis serovar 3 Unpasteurised raw goat Spain 2002 11 brucellosis cases Mendez Martínez et al.
milk cheese (2003)
Brucella Unpasteurised queso-fresco United States 2005 2 cases, 2 hospitalised, CDC (2014)
cheese 0 dead
Brucella Unpasteurised goat cheese United States 2006 5 cases, 3 hospitalised, CDC (2014)
0 dead
Brucella Unpasteurised queso-fresco United States 2007 3 cases, 1 hospitalised, CDC (2014)
cheese 0 dead
Brucella abortus Raw milk cheese France 2012 1 case (child) Bronner, Henaux,
, Hendrikx, and
Fortane
Calavas (2014)
Campylobacter jejuni Homemade unpasteurised United States 2000 18 cases, 0 hospitalised, CDC (2014)
cheese 0 dead
Campylobacter jejuni Unpasteurised cheese United States 2003 18 cases, 0 hospitalised, CDC (2014)
0 dead
Campylobacter jejuni Homemade unpasteurised United States 2006 58 cases, 2 hospitalised, CDC (2014)
cheese 0 dead
Campylobacter jejuni Fresh raw milk cheese United States 2007 68 cases CDC (2009)
Campylobacter jejuni Unpasteurised queso-fresco United States 2009 10 cases, 0 hospitalised, CDC (2014)
cheese 0 dead
Staphylococcus aureus Farm raw sheep milk France 1983 20 cases De Buyser, Janin, and
enterotoxins A and D cheese Dilasser (1985)
Staphylococcus aureus enterotoxins A Raw sheep milk cheese Scotland 1984 27 cases Bone, Bogie, and
Morgan-Jone (1989)
Staphylococcus aureus Stilton cheese from England 1988 155 cases Maguire et al. (1991)
unpasteurised milk
Staphylococcal enterotoxin type E Soft cheese from France 2009 6 outbreaks, 23 cases Ostyn et al. (2010)
unpasteurised milk
Streptococcus equi, Mexican-style soft raw milk United States 1983 16 cases, 5 hospitalised, 3 Altekruse et al. (1998);
Streptococcus zooepidemicus cheese (queso fresco) dead CDC (1983)
(group C)
Tick-borne encephalitis virus Cheese from raw cow and Austria 2008 6 cases Holzmann et al. (2009)
goat milk
consumption of dairy products made from raw milk and in 2013 linked to the majority of the VTEC outbreaks, but also other sero-
one outbreak was reported due to VTEC O157 contamination of types have been implicated (Farrokh et al., 2013). C. jejuni (in the
unpasteurised cheese (EFSA & ECDC, 2015). United States), L. monocytogenes and Brucella spp. were relatively
The majority of the outbreaks (22 out of 64) due to the con- often linked to raw milk cheese outbreaks, respectively 5, 8 and 7
sumption of raw milk cheeses was caused by Salmonella, followed out of 64 outbreaks. Dairy products made from raw milk can be a
by VTEC. Consumption of contaminated soft and semi-soft cheeses transmission route of Brucella spp. (EFSA & ECDC, 2014). In Medi-
is often implicated in outbreaks with VTEC, especially when they terranean countries not officially free from brucellosis, it is
are made of unpasteurised cow or goat milk. VTEC O157:H7 is assumed that the consumption of raw sheep and goat milk as well
as cheese made from raw sheep and goat milk is the main source of It can be concluded from Table 3 that during the production of
contamination (FASFC, WIV, & CODA, 2011). Magwedere et al. hard cheeses, some bacteria can survive, such as Salmonella,
(2011) have shown that raw goat milk, home-made goat cheese L. monocytogenes, S. aureus and MAP, albeit without subsequent
and coffee served with raw goat milk, as well as contact with goats growth. The number of E. coli can increase during the cheese pro-
can be a source of human cases of brucellosis. Enterotoxin- duction, which is due to a combination of a concentration effect
producing S. aureus, Streptococcus spp. and the TBEV were also during the formation of the curd as well as due to real growth of the
linked to the consumption of raw milk cheeses. Three of the four pathogen (Farrokh et al., 2013). In hard cheeses several pathogens
outbreaks of S. aureus occurred more than 20 years ago, and two can be inactivated during storage. Salmonella, E. coli,
were caused by cheese made from raw sheep milk. Concerning L. monocytogenes and MAP may decrease in numbers, but can still
Streptococcus, one outbreak occurred in the United States due to be detected after long ripening periods. During the production of
Mexican-style soft raw milk cheese in 1983. In 1997e2008, 64 cases semi-hard cheeses, some bacteria can grow, such as Salmonella,
of tick-borne encephalitis in patients that consumed unpasteurised E. coli and S. aureus. L. monocytogenes and MAP that survive the
milk and cheese made from sheep milk were reported in the Czech production process. During the ripening and storage of semi-hard
Republic (Krí
z, Benes, & Daniel, 2009). cheeses, most bacteria will decrease in numbers, but Salmonella,
E. coli and S. aureus can still be detected. L. monocytogenes and MAP
4. Growth and survival of pathogenic microorganisms during can survive the ripening and storage. During the production of soft
production and storage/ripening of dairy products made from cheeses, E. coli, L. monocytogenes and Brucella spp. can grow. During
raw milk the ripening and storage, E. coli and Brucella spp. can survive, but
L. monocytogenes can possibly grow in and on soft cheeses,
The circumstances of production and storage of dairy products depending on the ripening stage and the circumstances. The
made from raw milk determine the behaviour (i.e., growth, survival growth of L. monocytogenes in butter does not occur or is limited
or inactivation) of the microorganisms that are potentially present (De Reu & Herman, 2004).
in the raw milk. The pathogens can grow, survive or be inactivated.
Some of these important influencing factors are summarised as 5. Identification of main microbiological hazards in dairy
follows for raw milk cheeses. The growth of the fermenting bacteria products made from raw milk
reduces the growth possibilities of the pathogens by, on the one
hand, competition and, on the other hand, a decline of the pH. The The information on the possible presence of human pathogenic
effect of starter cultures producing bacteriocins and the addition of microorganisms in raw milk, frequencies of occurrence of human
potassium or sodium nitrate is especially aimed at inhibiting the pathogenic microorganisms in dairy products made from raw milk
growth of butyric acid bacteria. The outgrowth of L. monocytogenes in Europe, outbreaks resulting from consumption of dairy products
could also be influenced due to the presence of bacteriocins (Dal made from raw milk in Europe, the United States and Canada and
Bello et al., 2012) while the outgrowth of B. cereus may be the worst case scenario of the behaviour in dairy products made
ascribed to potassium or sodium nitrate inhibiting spore germi- from raw milk is summarised in Table 4.
nation (Avila, Go mez-Torres, Hernandez, & Garde, 2014). The The main microbiological hazards linked to raw milk cheese are
coagulation of the milk followed by sineresis of the curd, concen- L. monocytogenes, human pathogenic VTEC, Salmonella,
trates the pathogens in the curd. Some herbs used in the cheeses enterotoxin-producing S. aureus and Campylobacter. These patho-
may have a bacteriostatic effect (Leuschner & Ielsch, 2003). gens can be present in raw milk and as there is no heat treatment
Salting creates conditions that are not optimal for survival or before cheese production, they will not be inactivated. They have all
growth due to the decline of the water activity. Depending on the caused a certain number of outbreaks linked to cheese and Sal-
time, temperature, pH, water activity and NaCl concentration, dry monella, L. monocytogenes, S. aureus and VTEC have been detected
matter content and the competing microbiota, growth or inacti- in cheeses. Salmonella, Campylobacter and VTEC can cause disease
vation of the pathogens present in the milk will occur during in low numbers (often a few cells) and for Salmonella and VTEC
ripening (Farrokh et al., 2013). Plastic coating used on certain there are growth possibilities during production and storage (sur-
cheeses prevents them from drying out and prevents contamina- vival for VTEC during storage). L. monocytogenes and S. aureus have
tion with pathogens and fungi from the environment. The coating to grow to cause disease, which is possible as can be seen from
may contain antifungal components such as natamycin. Vacuum Table 4.
packaging and paraffin are physical barriers and the vacuum Concerning butter, cream and buttermilk, there is less infor-
packaging will inhibit the development of fungi and strict aerobic mation available in the scientific literature. For butter made from
microorganisms. The presence of internal and external microbiota raw milk, the main microbiological hazards are L. monocytogenes,
during ripening provides competition with the pathogens. During VTEC and S. aureus because these pathogens have been detected in
the ripening period, the physical and chemical characteristics of the butter. However, the risk of infection after consumption of raw milk
cheese often change which can provide a better survival and even butter is estimated to be relatively lower in comparison with
enable growth. During ripening a post-contamination can occur. certain cheeses, especially due to the limited growth possibilities of
Especially soft and semi-soft cheeses as well as cheeses with a L. monocytogenes. For cream made from raw milk, the main
washed crust such as red smear cheeses, are more exposed to microbiological hazards are estimated to be L. monocytogenes,
surface contamination (Farrokh et al., 2013). Microorganisms will S. aureus and VTEC because L. monocytogenes and S. aureus have
behave differently on the surface or in the crust due to the different been detected in cream and VTEC was linked to a cream outbreak.
conditions such as the pH. With regard to buttermilk made from raw milk, there is no infor-
The results documented in specific studies on the survival, mation available in the scientific literature and the microbiological
growth and inactivation of pathogens in dairy products made from hazards related to the consumption of this product cannot be
raw milk are summarised in Table 3. Information was only available identified.
for cheeses and butter. Concerning cheese, a distinction was made There are some additional risks linked to the consumption of
between hard, semi-hard and soft cheeses based on the classifica- dairy products made from raw milk, especially when they are
tion made in the publications. When this classification was not produced on farms where animals are frequently infected with
clear, ‘non specified’ cheeses are mentioned. certain pathogens. This is the case for Brucella spp. Cattle can be
Table 3
Behaviour of human pathogenic microorganisms in different types of cheese made from raw milk during production and storage/ripening.
Production Storage and/or ripening References
Hard cheese
Inoculation of 4e6 log cfu mL1 of Campylobacter jejuni, One week after storage at 11e13 C for 90 d: no detection of any of Bachmann and Spahr
Escherichia coli, Listeria monocytogenes, Salmonella inoculated pathogens (1995)
Typhimurium, Staphylococcus aureus, Yersinia enterocolitica
in milk; 1 d after production: only low numbers of S. aureus
Inoculation of 4e5 log cfu mL1 of Mycobacterium avium subsp. Steady and slow decrease during ripening at 12 C for 10 d, 22 C for Spahr and Schafroth (2001)
paratuberculosis (MAP) in cow milk 60 d or 12 C for 50 d; viable cells detected at day 120
One of thirty-five cows shedding 2.3 log cfu mL1 of Salmonella One of two vats positive after storage at 5 C for 125 d Wood, Collins-Thompson,
Muenster in milk; 11 of 181 vats of curd positive; 2 of 11 vats Irvine, and Muhr (1984)
of cheese positive
Inoculation of 2 log cfu mL1 of E. coli K12 in milk; increase Decrease of 1.5e2 log during storage at 4 C for 120 d Amornkul and Henning
during production (2007)
Inoculation of 1e5 log cfu mL1 of E. coli O157:H7 in milk; 1
Storage at 7 C for 1 wk; decrease of less than 1 log cfu g at day 60; Schlesser et al. (2006)
increase during production decrease of less than 2 log cfu g1 at day 120
Inoculation of 1.3 log cfu mL1 of E. coli O157:H7 in milk; Storage at 9 C; 2.2 log cfu mL1 in cheese on day 1; decrease to D'Amico, Druart, and
1.3 log cfu mL1 in milk before coagulation, 1.6 log cfu g1 in 1.4 log cfu g1 on day 60; below 0.7 log cfu g1 after 108 d; Donnelly (2010)
curd after cutting; 1.3 log cfu mL1 in whey at draining; Detection after more than 270 d
2.4 log cfu g1 in curd before salting
Inoculation of 1.4 log cfu mL1 of E. coli O157:H7 in milk; Storage at 14 C for 5 wk, then at 9 C; 2.2 log cfu mL1 in cheese on D'Amico et al. (2010)
1.4 log cfu mL1 in milk before coagulation, 1.8 log cfu g1 in day 1; decrease to 0.7 log cfu g1 on day 60; below 0.7 log cfu g1
curd after cutting; 0.5 log cfu mL1 in whey removed; after 94 d; detection after more than 270 d
0.7 log cfu mL1 in whey plus wash water; 2.6 log cfu g1 in
curd before salting; 3.0 log cfu g1 in cheese before brining
Natural contamination of L. monocytogenes in cheese Never >1.3 log cfu g1; no detection after 5 months Dalmasso and Jordan
(2014)
Semi-hard cheese
Inoculation of 4e6 log cfu mL1 of C. jejuni, E. coli, After storage at 11e13 C for 90 d: only L. monocytogenes detected Bachmann and Spahr
L. monocytogenes, S. Typhimurium, S. aureus, Y. enterocolitica (1995)
in milk
Inoculation of 4e5 log cfu mL1 of MAP in cow milk Steady and slow decrease during ripening at 14e15 C for 120 d; Spahr and Schafroth (2001)
viable cells detected at day 120
Inoculation of 1 and 3 log cfu mL1 of E. coli (5 strains including Increase of 3.5 log cfu g1 at day 1 (concentration effect and Peng et al. (2013)
3 verocytotoxin-producing Escherichia coli (VTEC)) growth); slow and continuous decrease during ripening; generic
E. coli Survived at higher counts; 6 cheeses with low inoculum:
>1 log cfu g1 at end of ripening; after enrichment: VTEC detection
in almost all cheeses
Inoculation of 2.4 log cfu mL1 S. aureus in milk; 3.3 log cfu mL1 3.8 log cfu g1 in cheese at day 7; 0 cfu g1 in cheese at week 10 Jørgensen et al. (2005)
in gel of early coagulation; 2.3 log cfu mL1 in whey.
4.2 log cfu g1 in curd at pressing
Inoculation of 4 log cfu g1 of L. monocytogenes in sheep milk Decrease after 6 wk; log reduction at 4 C: 2.10 at day 91, 3.19 at day Valero et al. (2014)
101, presence at day 111, absent at day 114; log reduction at 12 C:
1.74 at day 77, 2.90 at day 91, presence at day 98, absent at day 104;
log reduction at 22 C: 1.76 at day 54, 2.45 at day 67, 4.02 at day 70,
presence at day 74, absent at day 77
Soft cheese
Inoculation of 4 log cfu mL1 of E. coli O157:H7 and Storage at 2 C for 75 d; E. coli O157:H7: highest count at day 10, Ramsaran, Chen, Brunke,
L. monocytogenes; growth of both pathogens during decrease after 10 d, count at day 75 higher than inoculum; Hill, and Griffiths (1998)
production L. monocytogenes: survival, count at day 75 higher than inoculum
Inoculation of 4 log cfu mL1 of E. coli O157:H7 and Storage at 2 C for 65 d; E. coli O157:H7: highest count after 24 h, Ramsaran et al. (1998)
L. monocytogenes; growth of both pathogens during decrease after 24 h, count at day 65 higher than inoculum;
production L. monocytogenes: survival, count at day 65 higher than inoculum
Inoculation of 3 log cfu mL1 of VTEC; increase of 1 Storage at 4 C; decrease during early stages of ripening Montet et al. (2009)
e2 log cfu g1 during production;
stabilisation during salting/drying
Inoculation of 3.6 log cfu mL1 of Brucella abortus in milk; Storage at 12 C; 3.0 log cfu g1 in cheese at day 5, 1.5 log cfu g1 in Plommet et al. (1988)
4.2 log cfu g1 in curd; 4.3 log cfu g1 in curd out of mould cheese at day 8, 1.3 log cfu g1 in cheese at day 12, 1.1 log cfu g1 in
cheese at day 15, 0.4 log cfu g1 in cheese at day 18, 0 cfu g1 in
cheese at day 22
Inoculation of 0.7 and 0.3 log cfu cm2 of L. monocytogenes Storage at 4 C; increase after day 28; increase to 2.96 log cfu g1 at D'Amico et al. (2008)
day 60 (low inoculum); increase to 4.55 log cfu g1 at day 60 (high
inoculum)
Natural contamination of 3.8 log cfu mL1 of L. monocytogenes in 2.3e2.8 log cfu g1 7 d after storage at 4 C for 7 d Schoder, Winter, Kareem,
sheep milk Baumgartner, and Wagner
(2003)
Mozzarella
Inoculation of 5 log cfu mL1 of E. coli O157:H7 in cow milk; Storage at 4 C for 7 d; no detection Spano et al. (2003)
curd stretching at 80 C for 5 min: loss of viability; curd
stretching at 70 C for 5 min: 1 log reduction
Inoculation of 7.1e8.7 log cfu g1 of VTEC O157 and O26 of curd; Trevisani, Mancusi, and
4D reduction during heating curd Valero (2014)
(continued on next page)
Production Storage and/or ripening References
Non specified cheese

Inoculation of E. coli O157:H7, O26:H11, O103:H2 and Decrease during 6 months of ripening; detectable at end of storage/ Miszczycha et al. (2013)
O145:H28 in cow, goat or sheep milk; during first 24 h of ripening
production: growth of 2e3 log cfu g1, no growth when acid
coagulation
Inoculation of E. coli O157:H7 and O26:H11 in cow milk; during Stable around 4 log cfu g1 during ripening and storage Miszczycha et al. (2014)
first 24 h of production: growth from 2 to 4 log cfu g1
Inoculation of 1.52 log cfu mL1 of E. coli O157:H7 in milk 1
Storage a 6 C; increase to 3.4 log cfu g at day 1; decrease during Maher, Jordan, Upton, and
ripening to <0 cfu g1 in rind at day 21; decrease during ripening to Coffey (2001)
<1 log cfu g1 in core at day 21; detection of viable cells at day 90
Inoculation of 3.56 log cfu g1 dry weight of L. monocytogenes in Storage at 13 C for 14 d and at 8 C for 14 d; increase of 2 log cfu g1 Schvartzman et al. (2011)
cow milk; no growth during production dry weight during first 4 d of ripening; survival/decrease until end
of ripening
Inoculation of 6 log cfu mL1 of E. coli, Listeria innocua and Storage at 8 C for 56 d; E. coli highest count at day 7, decrease after Masoud et al. (2012)
S. aureus in milk; during production; increase of E. coli, day 7; Listeria innocua and Staphylococcus aureus no growth
survival of L. innocua and S. aureus
Average counts of S. aureus: 1.26 log cfu mL1 in cow/goat milk, Average counts of S. aureus: 3.50 log cfu g1 in cheese (5e6 h), Jakobsen et al. (2011)
2.80 log cfu mL1 in curd 3.13 log cfu mL1 in cheese (24 h), 1.04 log cfu g1 in cheese (30 d)
Inoculation of 9.7 log cfu g1 of Brucella melitensis in goat milk; 3.0 log cfu mL1 during storage at 4 C for 13e30 d; 4 log cfu mL1 Mendez-Gonza
lez et al.
decrease during production; 6.3 log cfu mL1 in whey at curd during storage at 24 C for 6e15 d; no detection during storage at (2011)
cutting; 6 log cfu mL1 at draining 24 C for days 16e30
Butter
Inoculation of L. monocytogenes and L. innocua in cream No significant growth during storage at 4, 10 or 20 C for 4 wk De Reu and Herman (2004)
Natural contamination of 0.6 to 1.2 log cfu g1 of One log reduction during storage at 4 or 10 C for 4 or 5 wk De Reu and Herman (2004)
L. monocytogenes
infected with Brucella abortus and sheep can be infected with the main reservoirs of C. burnetii (Rahimi, Doosti, Ameri, Kabiri, &
Brucella melitensis in certain areas of Southern Europe. The same Sharifian, 2008). In general, people get infected by inhalation of
holds for M. bovis in regions where this pathogen is endemic, for contaminated dust and aerosols mainly formed during birth of
example among cattle. Goats can be parasitised by the tick Ixodes animals, via manure or via contact with infected animals (Sci Com,
ricinus that often carry the TBEV. The infection of goats is asymp- 2010a, 2010b). Infection via the food chain occurs less frequently
tomatic and the TBEV can enter the bloodstream through the tick (Berri et al., 2005). Infectious C. burnetii can persist for long periods
followed by an excretion in the milk during the viraemic phase. In in milk and milk products. From scientific literature, it appears that
risk areas in Eastern Europe the TBEV can be endemic and therefore dairy products made from unpasteurised milk may contain viable
this is also an important microbiological hazard linked to dairy C. burnetii. Concerning MAP, the information in the scientific liter-
products made from raw milk. ature is limited and up to now, there is uncertainty whether this
For some microorganisms, the foodborne potential is not known bacterium is zoonotic or to be considered as a human foodborne
or limited documentation is available. Cattle, goats and sheep are pathogen. Nevertheless, MAP and C. burnetii could be considered as
Table 4
Summary of information on microbiological hazards.
Organism Possibly Detected in dairy Reported human Worst case behaviour in raw milk cheese Score according to
present in products made from cases and outbreaks EFSA (2013)
Production Storage/ripening
raw milk raw milk (minimum in Europe, the
e maximum frequency US and Canada due
of occurrence in %) to cheese consumption
in Europe
Listeria monocytogenes Yes 0.0e41.9 (cheese, 8 Growth Growth 2

butter, cream) survivalb survivalb
Escherichia coli (human Yes 0.0e55.3 (cheese) 18a Growth Survival 3
pathogenic)
Staphylococcus aureus Yes 0.0e100.0 (cheese, butter) 4 Growth Growth 1
Salmonella Yes 0.0e4.3 (cheese) 22 Growth Growth 3
Campylobacter Yes 0.0 (cheese) 5 No survival No survival 3
Brucella Yes ec 7 Growth Survival 3
Bacillus cereus Yes 0.0e28.0 (cheese) 0 e e 1
Mycobacterium bovis Yes e 0 e e 3
Tick-borne encephalitis virus Yes e 1 e e 3
Coxiella burnetii Yes 0.0e57.0 (cheese, cream) 0 e e ed
Streptococcus Yes e 1 e e 3e
Mycobacterium avium subsp. Yes 0.0e20.0 (cheese) 0 Survival Survival ef
paratuberculosis
a
One due to cream consumption.
b
In butter.
c
A dash (e) indicates no information was available unless otherwise indicated.
d
Foodborne potential not known.
e
Pathogenic species not frequent.
f
Zoonotic potential not known.
a potential microbiological hazard present in dairy products made To limit the exposure to pathogens due to consumption of dairy
from raw milk. products made from raw milk several control measures can be
taken from farm to fork. At farm level, the pathogenic microor-
6. Discussion ganisms that contaminate the raw milk can come from the milk-
producing animal or from the environment. Mastitis or udder
The contamination levels of several pathogens such as infection is the most common disease in cattle (Halasa, Huijps,
L. monocytogenes and S. aureus usually encountered in raw milk are Osteras, & Hogeveen, 2007). The intramammary infection is
mostly lower than the level they have to reach to cause disease. It is mostly caused by bacteria that penetrate the udder through the teat
assumed (based on the authors' expert opinion) that numbers of canal. In the holistic approach of prevention and control of mastitis,
L. monocytogenes in raw cow milk are usually lower or at the level of it is of utmost importance to keep the infection pressure in the
ca. 1 log cfu mL1. In the case of a subclinical mastitis of the milk stable as low as possible by means of good hygiene management
producing animal, high initial numbers of L. monocytogenes or and optimal comfort of the cows to obtain a good udder health and
S. aureus could be encountered in the raw milk (Pintado et al., 2009; optimal milk quality (Barkema et al., 1998; Elbers et al., 1998; van
Sahebekhtiari et al., 2011). Although this is rare and such milk is Gastelen, Westerlaan, Houwers, & van Eerdenburg, 2011;
diluted in the normal industrial milk supply, it may occur, e.g., in a Schukken, Grommers, Vandegeer, Erb, & Brand, 1990). However,
short supply chain. For low initial numbers of these pathogens that contamination of the milk during milking cannot completely be
have to grow to produce disease, the growth possibilities during avoided, not even with elaborate cleaning and disinfection
cheese production and storage will influence the risk of infection. (Magnusson, Christiansson, Svensson, & Kolstrup, 2006). Between
When present in the raw milk, the growth of most pathogens is the milking and the processing of dairy products, time should be
restricted by storage at refrigerator temperatures although, restricted and temperatures kept as low as possible to prevent the
depending on the storage time and temperature, some pathogens pathogens that are possibly present from growing. During milk
such as L. monocytogenes could develop. processing, a quick fermentation with efficient starter cultures
From the scientific literature, it seems that prevalences or con- should be applied to restrict the growth of the pathogens. After the
centrations of certain pathogens such as VTEC, L. monocytogenes, production of cheese, a restriction of the shelf life and adherence to
S. aureus and C. burnetii are mostly lower in dairy products made the cold chain from retail to consumer is important to ensure the
from pasteurised or heat treated milk than in dairy products made safety of such products. The control of the procedures of cleaning
from raw milk (Civera et al., 2007; Eldin et al., 2013; Fach, Perelle, and disinfection of the material that is used during the production
Dilasser, & Grout, 2001; Greenwood, Roberts, & Burden, 1991; process is also important from the milking to the sales of the
Loncarevic, Danielsson-Tham, & Tham, 1995; Rosengren, Fab- products. Finally, both producers and consumers, in particular
n, & Lindqvist, 2010). Concerning outbreaks, it
ricius, Guss, Sylve persons belonging to the YOPI group, should be aware of the risks
seems that cheese outbreaks are more linked to cheese made from pertaining to dairy products made from raw milk.
unpasteurised milk than from cheese made from pasteurised milk There are some limitations linked to the analysis of the infor-
(Altekruse, Timbo, Mowbray, Bean, & Potter, 1998; De Buyser, mation collected in this work. The frequencies of occurrence of
Dufour, Maire, & Lafarge, 2001; Gould, Mungai, & Behravesh, pathogenic microorganisms in dairy products made from raw milk
2014). Moreover, the study of Gould et al. (2014) showed that raw originate from ad hoc convenience sampling and the modalities
milk cheese outbreaks were mostly related to contamination of the conditions of the sampling plan (number of samples taken, method
raw product or the ingredients by pathogens from animals or the of analysis and corresponding limit of detection) as well as the
environment, whereas pasteurised cheese outbreaks were more method of analysis and detection limit may vary among these
related to health and hygiene of the workers in contact with the surveys and consequently it was not always easy to compare the
cheese. outcome of these publications. Also, it is not known if the detected
Regarding the behaviour of the pathogens during production pathogens are able to cause disease. In particular, in the case of the
and storage of cheese, there are differences depending on the use detection of potential pathogenic E. coli serotypes, it is not known if
of raw milk or pasteurised milk. For example, L. monocytogenes all positive results actually refer to E. coli strains that carry virulence
showed in an inoculation experiment growth during the cheese genes. Concerning the outbreaks due to the consumption of dairy
production process when made from pasteurised milk whereas products made from raw milk, only reported outbreaks were
no growth was observed when made from raw milk, most included. There can be underreporting due to, e.g., a long incuba-
probably due to the presence of background flora. However, tion period. Regarding the behaviour of the pathogens during the
during cheese ripening, growth of this pathogen occurred in raw production process and the storage or ripening period of dairy
milk cheese, but inactivation occurred in pasteurised cheese due products made from raw milk, it is evident that there is a variety of
to the physicochemical conditions of the cheeses (Schvartzman cheeses with their proper production process, intrinsic physico-
et al., 2011). Another study found no difference in the growth chemical characteristics, indigenous microbiota and actual stor-
potential of L. monocytogenes inoculated on the surface of age conditions, which will impact on the growth potential of the
cheeses made from raw or pasteurised milk during storage pathogens.
(D'Amico, Druart, & Donnelly, 2008). In addition, the natural
microbiota can influence the behaviour of pathogens in cheese. 7. Conclusion
Delcenserie et al. (2014) found that cheese made from raw and
pasteurised milk had different microbiota in the crust of the Overall, the available information on some pathogens or dairy
cheeses. Overall, pasteurisation ensures the inactivation of products made from raw milk is limited, but if everything is taken
vegetative pathogenic microorganisms, which increases the into consideration the microbiological hazards and dairy products
safety of products made thereof in comparison with dairy made from raw milk of main concern are linked to raw milk cheeses
products made from raw milk. However, it should be noted that and L. monocytogenes, pathogenic VTEC, enterotoxin-producing
dairy products made from pasteurised milk could be susceptible S. aureus, Salmonella and C. jejuni/coli. Next, L. monocytogenes,
to post-contamination. Therefore, application of a good Hazard VTEC and S. aureus have been identified as microbiological hazards
Analysis and Critical Control Points (HACCP) system during pro- in raw milk butter and cream, albeit to a lesser extent because of a
duction is essential. reduced growth potential of these pathogens in the latter products
compared with cheese. In endemic areas, dairy products made from van Cauteren, D., Jourdan-da Silva, N., Weill, F. X., King, L., Brisabois, A.,
Delmas, G., et al. (2009). Outbreak of Salmonellaenterica serotype Muenster
raw milk may also be contaminated with Brucella spp., M. bovis or
infections associated with goat's cheese, France, March 2008. Euro-
the tick-borne encephalitis virus and need particular attention in surveillance, 14. Article 8.
monitoring and surveillance. Finally, C. burnetii and MAP are CDC. (1983). Group C streptococcal infections associated with eating homemade
identified as potential hazards. For C. burnetii the role of food (dairy cheese e New Mexico. Morbidity and Mortality Weekly Report, 32(510), 515e516.
CDC. (2000). Outbreak of Escherichia coli O157:H7 infection associated with eating
products made from raw milk) seems to be limited and for MAP no fresh cheese curds e Wisconsin, June 1998. Morbidity and Mortality Weekly
sufficient knowledge is available. Report, 49, 911e913.
Due to the possible exposure of the consumer to the above CDC. (2001). Outbreak of listeriosis associated with homemade Mexican-style
cheese e North Carolina, October 2000eJanuary 2001. Morbidity and Mortal-
mentioned pathogenic microorganisms in dairy products made ity Weekly Report, 50, 560e562.
from raw milk, appropriate risk communication on the consump- CDC. (2007). Salmonella Typhimurium infection associated with raw milk and
tion of these products in particular to a vulnerable population, is cheese consumption e Pennsylvania, 2007. Morbidity and Mortality Weekly
Report, 56, 1161e1164.
recommended. CDC. (2008). Outbreak of multidrug-resistant Salmonella enterica serotype Newport
infections associated with consumption of unpasteurized Mexican-style aged
cheese e Illinois, March 2006eApril 2007. Morbidity and Mortality Weekly
Acknowledgements Report, 57, 432e435.
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International Dairy Journal 50 (2015) 32e44

Contents lists available at ScienceDirect

International Dairy Journal

A review of the microbiological hazards of dairy products made from

Consumers' attitudes show a trend towards increased con-

Dairy product made Frequency of Number of Comments Country References

Verocytotoxin-producing Escherichia coli (VTEC)

Dairy product made Frequency of Number of Comments Country References

0.0 51 Spain Arrese and Arroyo-Izaga (2012)

Mycobacterium avium subsp. paratuberculosis

Production Storage and/or ripening References

Production Storage and/or ripening References

Non speciﬁed cheese

Listeria monocytogenes Yes 0.0e41.9 (cheese, 8 Growth Growth 2

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