International Dairy Journal 47 (2015) 1e5

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International Dairy Journal

journal homepage: www.elsevier.com/locate/idairyj

Reproducibility and repeatability of milk coagulation properties

predicted by mid-infrared spectroscopy
M. Penasa*, M. De Marchi, S. Ton, L. Ancilotto, M. Cassandro

16, 35020, Legnaro, PD, Italy
Department of Agronomy, Food, Natural Resources, Animals and Environment, University of Padova, Viale dell'Universita

a r t i c l e i n f o a b s t r a c t

Article history: The objective of this study was to assess reproducibility and repeatability of milk coagulation properties
Received 18 November 2014 (MCP) predicted by mid-infrared spectroscopy (MIRS). Individual milk samples from a single dairy herd
Received in revised form were collected during 8 sampling dates, added with preservative (Bronopol) and analysed in two lab-
11 February 2015
oratories. Ten cows were randomly selected within each sampling date. Rennet coagulation time (RCT,
Accepted 13 February 2015
min) and curd rmness (a30, mm) were predicted in the two laboratories using MIRS. Besides predicting
Available online 3 March 2015
MCP through MIRS, RCT and a30 were measured by Formagraph. Reproducibilities of RCT and a30 pre-
dicted by MIRS were 67.3 and 71.9%, respectively. Repeatabilities of RCT and a30 predicted by MIRS and
determined by Formagraph were 92.8 and 95.8%, and 98.6 and 95.8%, respectively. Results indicated that
MIRS predictions of MCP are repeatable, but not highly reproducible. Further efforts are needed to
improve the standardisation among laboratories to enhance reproducibility.
2015 Elsevier Ltd. All rights reserved.

1. Introduction
The European Union manufactures approximately half the total
world's cheese production and it is the major supplier of the in-
ternational cheese trade. Moreover, the world import demand of
cheese will increase signicantly, by 20%, until 2022 (OECD-FAO,
2013). Under this scenario, milk coagulation properties (MCP),
which describe the ability of milk to coagulate after rennet addi-
tion, are very important for dairy industry. Milk coagulation
properties have been widely investigated in the past, both from the
phenotypic (De Marchi, Dal Zotto, Cassandro, & Bittante, 2007;
Malacarne et al., 2006, 2014) and genetic point of view
(Cassandro et al., 2008; Ikonen, Morri, Tyrisev
a, Ruottinen, & Ojala,
2004; Vallas et al., 2010).
As reviewed by O'Callaghan, O'Donnell, and Payne (2002), MCP
can be assessed by several devices; among them, the Formagraph
(Foss Electric A/S, Hillerd, Denmark) has been historically used to
provide measures of rennet coagulation time (RCT, min), curd-
rming time, and curd rmness (a30, mm). Moreover, this instru-
ment has been recently compared with other devices (Cipolat-
Gotet, Cecchinato, De Marchi, Penasa, & Bittante, 2012; Pretto
* Corresponding author. Tel.: 39 049 8272629.
E-mail address: mauro.penasa@unipd.it (M. Penasa).
et al., 2011) and has been chosen as the gold standard to develop
mid-infrared spectroscopy (MIRS) prediction models (De Marchi,
Penasa, Tiezzi, Toffanin, & Cassandro, 2012; De Marchi, Toffanin,
Cassandro, & Penasa, 2014). Mid-infrared spectroscopy is based
on the study of the interaction between matter and electromag-
netic radiation in the wavelength range between 2500 and
25,000 nm. When matter is crossed by electromagnetic radiation,
the bonds of the molecules make movements such as vibration and
rotation and this contributes a certain absorption of the provided
energy. On the basis of supplied energy and the amount absorbed
by the irradiated sample, it is possible to determine its chemical
composition (De Marchi et al., 2014).
The development of MIRS models for MCP started in the fall of
2011 in 2 laboratories of Veneto region, northeast Italy (De Marchi
et al., 2012) and currently, their implementation is rapidly moving
to other regions of the country. The use of MIRS equations for
routine prediction of MCP requires the periodical alignment be-
tween MCP models and gold standard, and between MCP models
installed in different laboratories. This can be achieved through ring
test. While indications about the accuracy of Formagraph measures
have been reported by Caroli, Bolla, Pagnacco, Rampilli, and Degano
(1990) and ASPA (1999), no information on reproducibility and
repeatability of MCP predicted by MIRS under eld conditions is
currently available. Therefore, the aim of this study was to estimate
reproducibility and repeatability of RCT and a30 predicted by MIRS.

http://dx.doi.org/10.1016/j.idairyj.2015.02.004
0958-6946/ 2015 Elsevier Ltd. All rights reserved.
2 M. Penasa et al. / International Dairy Journal 47 (2015) 1e5
2. Materials and methods
2.1. Sample collection
A ring test for MCP was carried out during 8 laboratory sessions
from April 2012 to June 2013. Ten lactating cows from a com-
mercial dairy herd of the northeast of Italy were randomly
selected within each session, and individual milk samples
(250 mL) were collected during evening milking. Immediately
after collection, each sample was divided into 3 subsamples that
were combined with preservative (Bronopol, Knoll Pharmaceuti-
cals, Nottingham, UK) at a concentration of 250 mL 50 mL1 milk,
refrigerated at 4  C, transferred to the milk quality laboratory of
the Breeders Association of Veneto region (Padova, Italy) (Lab 1),
and stored at 4  C. The day after collection, 1 subsample was
IAC 100 a30  meana30 =SDa30 *2:5  RCT  meanRCT =SDRCT *2:5
transported at 4  C to the milk quality laboratory of Veneto
Agricoltura (Thiene, Italy) (Lab 2).
2.2. Analysis of milk coagulation properties and quality traits
Reference analysis for MCP was carried out in Lab 1 using
Formagraph (Foss Electric A/S, Hillerd, Denmark). Two milk
samples at a time were removed from the refrigerator 1 h before
the beginning of the analysis and left at room temperature. After
1 h, samples were heated to 40  C in water bath and 10 mL of
milk were inserted in each measuring units of Formagraph, in 5
replicates for each milk sample. Measuring units were then
heated to 35  C for 15 min in a steel plate thermostat and added
with 200 mL of rennet (Naturen Plus 215 international milk
clotting units mL1, with 80% chymosin and 20% pepsin; Pacovis
Amrein AG, Bern, Switzerland) diluted 1.2% in distilled water
immediately before the start of analysis. Measurements of MCP
lasted 30 min after the addition of the clotting enzyme and
recorded traits were RCT, dened as the time interval, in minutes,
from the addition of rennet to the beginning of coagulation, and
a30, dened as the width, in millimeters, of the diagram at the
end of the analysis.
Besides measuring MCP through the reference method, RCT and
a30 were predicted by MIRS using a Milko-Scan FT6000 and Milko-
Scan FT (Foss Electric A/S) in Lab 1 and Lab 2, respectively. Sam-
ples were removed from the refrigerator, left at room temperature
for 1 h and heated to 40  C for 15 min using a water bath before
MIRS analysis. The number of replicates for each sample were 10
until January 2013 and 3 thereafter. Mid-infrared spectroscopy
models implemented for routine prediction of MCP showed satis-
factory accuracies with coefcients of determination in cross-
validation of 0.76 and 0.70 for RCT and a30, respectively. Full de-
tails on tting statistics of MIRS equations used to predict MCP can
be retrieved from De Marchi et al. (2012) and De Marchi, Toffanin,
Cassandro, and Penasa (2013).
Finally, milk samples were analysed in Lab 1 for fat content,
protein content, and casein content using a MilkoScan FT6000,
and for somatic cell count (SCC) using a Fossomatic 5000 (Foss
Electric A/S). Values of SCC were log-transformed to somatic cell
score (SCS) to achieve normality and homogeneity of variances
according to the following formula: SCS 3 log2 (SCC/
100,000).
2.3. Statistical analyses
2.3.1. Data
The nal dataset accounted for 1122 records (74 cows) of MCP
predicted by MIRS and 385 records (77 cows) measured by For-
magraph. The number of records was slightly lower than expected
(n 1180 for MIRS and 400 for Formagraph), and the difference was
due to accidental loss of subsamples from one cow during trans-
portation and to removal of non-coagulating records (n 29; 2.5%),
i.e., milks not forming a curd within the testing time of 30 min
(a30 0 mm).
Besides considering RCT and a30 as two separate traits, they
were also combined together to form an index of milk aptitude to
coagulate (IAC), standardised to mean 100 and SD 5. The formula to
calculate IAC was as follows:
(1)
The above index was calculated within MIRS and Formagraph,
and thus means and SD were those of 1122 and 385 records,
respectively.
2.3.2. Calculation of z-scores
To evaluate if MCP predicted by MIRS in Lab 1 and Lab 2 were in
agreement with MCP determined using the reference method
(Formagraph), z-scores (z) were calculated for RCT and a30 using
the following formula:
m  VALREF
z ; (2)
SD
where m is the average value of predicted RCT or a30 computed
within each laboratory and ring test session; VALREF is the reference
value (median) for RCT or a30 measured by Formagraph in each ring
test session; and SD is the standard deviation of measures of RCT or
a30 determined by Formagraph in each ring test session. The z-
scores were calculated to standardise the data and thus to enable
easier comparison between laboratories within each session or to
evaluate if they were reliable in performing a specic analysis.
According to Thompson, Ellison, and Wood (2006), the result of the
laboratory is satisfactory if jzj < 2, questionable if 2 < jzj < 3 and
unsatisfactory if jzj > 3.
2.3.3. Estimation of reproducibility and repeatability
A preliminary analysis showed that all studied variables were
normally distributed, with skewness and kurtosis that were always
smaller than 0.80 in absolute value. Pearson correlations between
RCT, a30, and IAC were estimated within MIRS and Formagraph
using the SAS software (SAS Inst. Inc., Cary, NC, USA). Variance
components for MCP predicted by MIRS and for IAC were estimated
with the VARCOMP procedure of SAS (SAS Inst. Inc.) through
restricted maximum likelihood (REML) method according to the
following linear model:


yijkl m cowi sessionj cow  labik session  labjk
ijkl ;
(3)
where yijkl is the observed trait (RCT, a30, or IAC); m is the overall
intercept of the model; cowi(sessionj) is the random effect of the ith
cow (i 1e74) nested within the jth laboratory session (j 1e8);
 M. Penasa et al. / International Dairy Journal 47 (2015) 1e5 3

(cow  lab)ik is the random interaction effect between the ith cow the absolute difference between 2 predictions of fat content,
and the kth laboratory (ik 74  2 148 levels); (session  lab)jk is protein content, casein content or SCS is expected to lie with a
the random interaction effect between the jth laboratory session probability of 95% (ISO, 1994a,b). The RT% was calculated using (8)
and the kth laboratory (jk 8  2 16 levels); and ijkl is the and it expresses the probability that two predictions of milk
random error term ~ N(0, s2 ). quality traits obtained on the same milk sample are repeatable.
The same model, without the inclusion of the random interac-
tion effects, was adopted to obtain variance components for mea-
3. Results and discussion
sures of MCP determined by Formagraph in Lab 1.
Reproducibility (RD) and repeatability (RT) of MCP and IAC were
3.1. Means, variation, and Pearson correlations
computed following the guidelines proposed by the International
Organisation for Standardisation (ISO, 1994a,b). In the present
Fat, protein, and casein contents averaged 4.06, 3.24, and 2.50%,
work, RD aimed at evaluating the agreement between predictions
respectively, and the mean value of SCS was 2.88. The CV ranged
of MCP obtained through MIRS in different laboratories, and it was
from 10 (protein content) to 66% (SCS), highlighting large differ-
dened as the value below which the absolute difference between
ences among traits (results not shown). Means for protein and
2 predictions of MCP obtained by MIRS on the same milk sample
casein contents, and SCS were lower and fat content was higher
under different conditions (different laboratories) is expected to lie
than ndings of Cassandro et al. (2008).
with a probability of 95% (ISO, 1994a,b). This parameter was
RCT predicted by MIRS averaged 16.69 min, which was lower
computed according to the following function of estimated vari-
than the mean value obtained using Formagraph (18.11 min;
ance components:
Table 1), and close to optimal RCT recommended by Annibaldi,
r
  Ferri, and Mora (1977) for renneting classication of milk. Curd
RD 2 2 s2cowxlab s2e ; (4) rmness predicted by MIRS averaged 31.83 mm, which was very
similar to the value measured by Formagraph (31.13 mm), and
lower than a30 proposed by Annibaldi et al. (1977) for milk ren-
where s2cowxlab is the variance of the interaction effect between cow
neting classication. Besides traditional MCP, the IAC was created
and laboratory, and s2e is the residual variance.
and introduced as a new standardised trait to summarise RCT and
Repeatability aimed at evaluating the agreement between pre-
a30, attributing the same importance (50%) to these traits in the
dictions of MCP obtained using MIRS and between measures of
index. The choice of giving the same relevance (50/50) to RCT and
MCP determined by Formagraph in the same laboratory, and it was
a30 was arbitrary in the context of the paper and the ratio can be
dened as the value below which the absolute difference between
changed according to different applications and/or cheese pro-
2 predictions or 2 measures of MCP obtained on the same milk
ductions. The IAC could be adopted by the dairy industry as an
sample in the same laboratory is expected to lie with a probability
overall measure of milk coagulation ability to reward or penalise
of 95% (ISO, 1994a,b). This parameter was computed as:
milk for clotting characteristics in payment systems. Moreover, the
q IAC could be regarded as phenotypic information recorded at in-
RT 2 2s2e : (5) dividual level to set up breeding strategies for genetic improvement
of MCP by selecting animals with high estimated breeding values
The coefcients of reproducibility (RD%) and repeatability (RT%)
for this new trait.
were also calculated. The RD% expresses the probability that 2
Coefcients of variation of MCP ranged from 30 to 54%, and were
predictions of MCP obtained by MIRS on the same milk sample are
greater for measured than predicted data (Table 1). A recent study
reproducible in different laboratories, and RT% is the probability
of Penasa, Tiezzi, Sturaro, Cassandro, and De Marchi (2014) on
that 2 predictions or 2 measures of MCP obtained on the same milk
predicted coagulation characteristics of milk from mixed-breed
sample are repeatable. These parameters were computed as
herds of Veneto region reported worse values of RCT and a30
compared with those of the present research.
s2cowsession
RD% *100; (6) To evaluate if RCT and a30 predicted by MIRS in Labs 1 and 2
s2cowsession s2cowxlab s2sessionxlab s2e were in agreement with reference values determined by the For-
magraph, z-scores were calculated within each ring test session. All
where s2cowsession is the variance of cow (sample) nested within
laboratory session and s2sessionxlab is the variance of the interaction
effect between laboratory session and laboratory, and
Table 1
Descriptive statistics for and Pearson correlations (P < 0.001) between rennet
s2cowsession s2cowxlab s2sessionxlab coagulation time (RCT) and curd rmness (a30) measured by Formagraph and pre-
RT% *100: (7) dicted by mid-infrared spectroscopy (MIRS).a
s2cowsession s2cowxlab s2sessionxlab s2e
Descriptor Formagraph (n 385) MIRS (n 1122)
Because measures of MCP by Formagraph were determined only
RCT (min) a30 (mm) IAC RCT (min) a30 (mm) IAC
in Lab 1, RT% of RCT, a30, and IAC determined using this device was
calculated as follows: Statistic
Mean 18.11 31.13 100 16.69 31.83 100
SD 5.61 16.86 4.79 4.98 11.39 4.75
s2cowsession Minimum 3.00 2.58 90.91 1.76 0.48 88.31
RT% *100: (8) Maximum 29.50 74.84 109.77 28.53 72.03 112.88
s2cowsession s2e
Trait Pearson correlation coefcients
RCT 0.84 0.96 0.81 0.95
Finally, RT was calculated for fat, protein, and casein contents, a30 0.96 0.95
and SCS using (5), according to the guidelines suggested by ISO a
Descriptive statistics for and Pearson correlations (P < 0.001) between the
(1994a,b). This parameter aimed at evaluating the agreement be- standardised index of milk aptitude to coagulate (IAC)a and milk coagulation
tween predictions of milk quality traits obtained by Milko- properties are also presented; IAC 100 a30  meana30 =SDa30 *2:5
ScanFT6000 in Lab 1, and it was dened as the value below which RCT  meanRCT =SDRCT *2:5, where SD is the standard deviation.
4 M. Penasa et al. / International Dairy Journal 47 (2015) 1e5

(A) 3.00

2.00

1.00

z-score
0.00

-1.00

-2.00

-3.00
Apr 2012 May 2012 Jun 2012 Dec 2012 Jan 2013 Mar 2013 May 2013 Jun 2013

Ring test session

(B) 3.00

2.00

1.00
z-score

0.00

-1.00

-2.00

-3.00
Apr 2012 May 2012 Jun 2012 Dec 2012 Jan 2013 Mar 2013 May 2013 Jun 2013

Ring test session

Fig. 1. Values of z-scores for (A) rennet coagulation time and (B) curd rmness predicted by mid-infrared spectroscopy in Lab 1 ( ) and Lab 2 ( ). Values have been calculated
within each ring test session.

z-scores for RCT and a30 were <2 in absolute value (Fig. 1), sug- 4.70 and RD% of 73.7% (Table 2). To our knowledge, no other es-
gesting that the result of the laboratories was satisfactory timates of reproducibility of MCP predicted by MIRS are currently
(Thompson et al., 2006). available in the literature and hence comparisons were made with
RCT exhibited a strong and negative relationship with a30 studies that dealt with MCP measured by mechanical instruments.
(Table 1), both when traits were predicted by MIRS (0.81;
P < 0.001) and measured by Formagraph (0.84; P < 0.001),
meaning that milk characterised by long RCT produced a weaker
Table 2
curd than milk characterised by short RCT. These estimates were
Estimates of repeatability (RT) and coefcient of repeatability (RT%) for rennet
comparable to ndings of Pretto et al. (2011), who reported coagulation time (RCT) and curd rmness (a30) measured by Formagraph and pre-
phenotypic correlation of 0.86 between RCT and a30 measured by dicted by mid-infrared spectroscopy, and reproducibility (RD) and coefcient of
Formagraph, and to correlations of 0.87, 0.76, and 0.75 esti- reproducibility (RD%) for the aforementioned traits predicted by mid-infrared
spectroscopy (MIRS).a
mated by Ikonen et al. (2004), Cassandro et al. (2008), and Dal
Zotto et al. (2008), respectively, using data of MCP determined Parameter Formagraph (n 385) MIRS (n 1122)
by computerised renneting meter (Polo Trade, Monselice, Italy). As RCT (min) a30 (mm) IAC RCT (min) a30 (mm) IAC
expected, the IAC was strongly related with RCT and a30: regard-
Repeatability
less of the method used to assess MCP (Formagraph or MIRS), RT 1.82 9.62 1.91 3.67 6.46 3.14
correlations were always greater than 0.95 in absolute value RT% 98.6 95.8 98.0 92.8 95.8 94.3
(P < 0.001; Table 1). Reproducibility
RD 5.22 12.46 4.70
RD% 67.3 71.9 73.7
3.2. Reproducibility and repeatability of milk coagulation properties a
Estimates of repeatability and reproducibility for the standardised index of milk
aptitude to coagulate (IAC) are also presented;
RD and RD% of RCT and a30 predicted by MIRS were 5.22 min IAC 100 a30  meana30 =SDa30 *2:5  RCT  meanRCT =SDRCT *2:5, where SD is
and 12.46 mm, and 67.3 and 71.9%, respectively, and IAC had RD of the standard deviation.
 M. Penasa et al. / International Dairy Journal 47 (2015) 1e5
The RD% of RCT from the present work (67.3%) was much lower
than ndings of ASPA (1999) and Dal Zotto et al. (2008), who re-
ported values of 91.0 and 93.5%, respectively, whereas RD% of a30
(71.9%) was much greater than that (8.0%) of ASPA (1999) and
comparable to the value (64.6%) of Dal Zotto et al. (2008). The
study of ASPA (1999) aimed at estimating reproducibility and
repeatability of MCP evaluated in 14 laboratories through lacto-
dynamographic analysis on powder milk samples, whereas
reproducibility in Dal Zotto et al. (2008) aimed at evaluating the
agreement between measures of MCP determined in the same
laboratory by computerised renneting meter considering samples
with and without Bronopol as preservative. RD% values from the
present study were not very high, and this might be mainly
related to laboratory conditions, especially in terms of milk
preparation before MIRS analysis. Milk preparation procedures
(e.g., heating, blending) are quite hard to standardise among lab-
oratories and this can affect MIRS predictions. This is particularly
true for not traditional traits like MCP. The second reason to
explain the quite low RD values for MCP might be related to
MilkoScan instruments. In the present study, the two laboratories
had two different versions of MilkoScan (FT6000 in Lab 1 and FT
in Lab 2). However, both FT6000 and FT are in the Central
Milking Testing (CMT) circuit of FOSS instruments and they are
equipped with the same MCP prediction models developed for
CMT devices. Based on our previous experience, these two in-
struments produce a spectrum with same spectra range even if
they have different cuvettes.
Repeatability and RT% of RCT and a30 predicted by MIRS were
3.67 min and 6.46 mm, and 92.8 and 95.8%, respectively, and IAC
had RT of 3.14 and RT% of 94.3% (Table 2). The RT% of RCT and a30
measured by Formagraph (98.6 and 95.8%, respectively), and IAC
(98.0%) were slightly greater than those obtained using predicted
traits (Table 2). To our knowledge, no other studies investigated
repeatability of MCP predicted by MIRS. Regardless the method
used to assess MCP (Formagraph or MIRS), RT% for RCT was very
similar to ndings of Caroli et al. (1990), ASPA (1999), and Dal Zotto
et al. (2008), who reported estimates of 96.4, 97.0, and 95.7%,
respectively, for MCP determined using mechanical instruments.
Concerning a30, estimates of RT% from the present work were
comparable to that (95.3%) of Caroli et al. (1990), but much greater
than values of 72.0 and 77.3% calculated by ASPA (1999) and Dal
Zotto et al. (2008), respectively.
Estimates of RT% for fat content, protein content, casein con-
tent, and SCS predicted in Lab 1 were always greater than 99%
(results not shown), suggesting that quality traits are more
repeatable than MCP. This result was expected as quality traits
are routinely monitored in milk quality laboratories through
reference samples periodically distributed by the National
Breeders Association. Currently, there are no ofcial ring tests for
MCP.
4. Conclusion
Milk coagulation properties predicted by MIRS were similarly
reproducible, with an average estimate of 70.0%. Coefcients of
repeatability for MCP predicted by MIRS were greater than 90.0%,
and they were slightly lower than those obtained for MCP
measured by Formagraph. More effort is needed to increase the
level of standardisation among laboratories and improve repro-
ducibility. Once standardisation is reached, MIRS models can be
adopted by milk quality laboratories at national level and per-
formance of prediction models for MCP can be easily monitored
through periodic prociency tests carried out by the National
Breeders Association using standard samples.
5
Acknowledgements
This research was supported by Regione Veneto with the project
CheeseBull, n. 2070868, Reg. CE 1698/2005, P.S.R. del Veneto -
DGR 1354 del 03/08/2011.
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