__________________________________________________Revista Científica, FCV-LUZ / Vol.

XXIV, Nº 5, 408 - 413, 2014

EFFECT OF SUBCLINICAL MASTITIS ON THE PHYSICOCHEMICAL

QUALITY OF BOVINE MILK
Efecto de la mastitis subclínica sobre la calidad físico-química de la leche bovina

Alfonso Calderón-Rangel 1,4*, Margarita Arteaga-Márquez 2, Virginia Rodríguez-Rodríguez 1,4,

Germán Arrieta-Bernate 1,4 y Oscar Vergara-Garay 3
1Instituto
de Investigaciones Biológicas del Trópico (IIBT), Facultad de Medicina Veterinaria y Zootecnia, Universidad de Córdoba.
2Grupo de Investigación en Procesos Agroindustriales, Facultad de Ingenierías, Universidad de Córdoba. 3Grupo de Investigación
en Producción Animal Tropical, Facultad de Medicina Veterinaria y Zootecnia, Universidad de Córdoba. 4Salud Pública y Auditoria
en Salud, Corporación Universitaria del Caribe, Sincelejo. *e-mail: [email protected]

RESUMEN leches con altos conteos de CS, los componentes químicos

disminuyeron significativamente (P£0,05) en comparación
La mastitis bovina puede ser clasificada como clínica y subclí- con las células de recuento bajo.
nica, de acuerdo a la presencia o ausencia de signos clínicos.
Palabras clave: Calidad de la leche, células somáticas, mas-
En ambos casos, hay un incremento de las células somáticas
titis subclínica.
(CS), siendo superior en la mastitis clínica. El propósito de
este estudio fue determinar el efecto de la mastitis subclínica
sobre la calidad físico-química de la leche en sistemas de ga- ABSTRACT
nado doble propósito (DP). Para este estudio se utilizó un
muestreo no probabilístico en seis empresas de ganado DP en The bovine mastitis can be classified into clinical and subclini-
el municipio de Montería, Córdoba (Colombia). Mediante el cal, according to presence or absence of clinical signs. In both
test de California para mastitis (TCM) fueron seleccionados los cases there is an increase of somatic cells (SC) being higher
cuartos evaluados como TCM 3 al tomar las muestras y cuar- for clinical mastitis. The purpose of this study was to deter-
tos evaluados como TCM 0, en la misma vaca como control. mine the effect of subclinical mastitis on physical and chemical
Las muestras fueron colectadas asépticamente y se guardaron milk components in dual purpose systems (DP). Using a non-
refrigeradas hasta su procesamiento. El análisis físico-químico probabilistic sampling in six DP livestock enterprises in Monte-
fue determinado mediante el equipo Biolac 60. La determina- ria, Cordoba (Colombia), a cross-sectional study was imple-
ción de caseína fue realizada por espectofotometría y el con- mented. By California mastitis test (CMT) were selected quar-
teo de CS mediante un contador de células óptico portátil. ters evaluated as CMT 3 to take samples, and quarters evalu-
Para la evaluación de las variables físico-químicas y el recuen- ated as CMT 0, in the same cow, for control. The samples
to de CS se agruparon dentro de cuatros fases (0-2 meses, were collected aseptically and were kept refrigerated until
2-4 meses, 4-6 meses y mayores a 6 meses de lactancia). La processing. The physicochemical analysis was determined by
leche, con un conteo de CS inferior a 250.000 fueron conside- Biolac 60 equipment. The determination of casein was done
radas sin mastitis subclínica, y con mastitis, las que presenta- by spectrophotometry, and SC count by an optical and port-
ron conteos iguales o superiores a 250.000 CS/mL. Los pro- able cell counter. The evaluation of the physicochemical vari-
medios para proteína total para leches con alto y bajo conteo ables and SC count were grouped into four phases (0-2
de células somáticas fueron 2,93 ± 0,13 y 3,12 ± 0,13, respec- months, 2-4 months, 4-6 months and more of 6 months of lac-
tivamente. Para el porcentaje de grasa, los promedios fueron tation). Milk with cell count less than 250,000 was defined as
3,36 ± 0,29 para leches con alto conteo de CS y 3,70 ± 0,46 without subclinical mastitis and with subclinical mastitis when
para leches con bajo conteo de CS. En términos generales, las cell count was greater than or equal to 250,000 SC/mL. The
averages for total protein for milk with high and low SC counts
were 2.93 ± 0.13 and 3.12 ± 0.13, respectively. For fat per-
centage, averages were 3.36 ± 0.29 for high count milks SC
Recibido: 03 / 09 / 2013 . Aceptado: 18 / 06 / 2014.

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and 3.70 ± 0.46 for milk with low count of SC. Overall, milk with Animals and type of management
high counts of SC, the chemicals components decreased sig- For this study, cows from crosses between Bos taurus x
nificantly (P£0.05) compared to the low count of cells. Bos indicus were used. The cows had between two and eight
calving. The animal feeding was based angleton (Dichantium
Key words: Quality milk, subclinical mastitis, somatic cells.
aristatum) pastures and were supplied mainly mineralized salt
and water ad libitum. Milking was done in the morning (at
INTRODUCTION around 5: am) and calf remained with the cows till noon, and
then is separated from the mother until the next day. The sam-
Mastitis is defined as any inflammation of the mammary plings were taken in the rain season.
gland in response to various infectious agents or non-infectious
etiology [34]. The mastitis by the presence or absence of clini- California Mastitis Test
cal signs can be classified into clinical and subclinical [36]. In
California Mastitis Test (CMT) was applied to all cows
both cases, there is an increase of somatic cell (SC) [5].
that on the day of the visit was in milking, according to the pro-
Invading pathogens activate the immune defense in the posed by Philpot and Nickerson [36]. In order to compare the
udder, is a complex biological process which involves not only SM effect, only were sampled quarters evaluated as CMT 3
resident immune cells and recruited but also mammary epithe- (maximum grade of SM and as control, quarters evaluated as
lial and endothelial cells. The result is the increased number of CMT 0 (WSM) in the same cow.
polymorphonuclear (PMN) by recruitment and epithelial
desquamation of lactiferous ducts and udder cistern [15]. Sampling
Somatic cell count (SCC) is used as indicator of udder The samples were taken aseptically, for which, each
health in the cow (Bos primigenius taurus y Bos primigenius in- teat was washed and dried with a disposable towel, subse-
dicus), sheep (Ovis aries) and goat (Capra hircus) [35, 36]. In quently the teat end was disinfected rubbing with cotton swabs
milk from quarters without subclinical mastitis (WSM), the cel- soaked with antiseptic alcohol 70% as often as necessary, un-
lularity is low, but in milk from quarters with subclinical (SM) or til the last swab keeps clean. Ten mL of milk were taken in
clinical mastitis (CM), the PMN increase according to the se- sterile glass screw-cap. A total of 86 samples of milk were col-
verity of inflammation [19]. lected, 43 cases (CMT SM 3) and 43 control samples. The
samples were kept refrigerated in an expanded polystyrene
Besides the decreased volume of milk produced as a result
cooler until processing at the Biological Research Institute of
of mastitis [14], the physical and chemical composition of milk
the Tropics (IIBT) of the University of Cordoba (Colombia).
changes, such as, the casein, major protein, decreases as a con-
sequence of infection and the whey proteins (lactalbumin and lac-
toglobulin) are increased by augmented vascular permeability, re- Physicochemical analysis of milk
duces the stability of the milk to heat by coagulation or floccula- Percentages of total protein, fat and non fat solid (NFS),
tion during pasteurization and ultrapasteurization processes, also mineral salts, lactose, cryoscopic point, and density were de-
there is a decreased calcium in milk; factors affecting milk yield in termined according to the method referenced by International
the production of cheese [12], potassium predominant mineral in Dairy Federation (IDF) 141 B [25], using an ultrasonic milk
milk, declines and the concentrations of sodium and chloride ions analyzer Lac 60 (Boeco, Germany). The samples were me-
rise and increases the electrical conductivity. The lactose content chanically stirred during five min and then processed at 20° C.
is reduced. Plasmin and other proteolytic enzymes, derived from The determination of casein was done by spectrophotometry,
SC, cause lysis of casein in the udder; proteolytic activity of plas- for which a standard curve made with casein 95% purity, using
min is increased more than two times during mastitis [26]. The the Biuret method [30, 42], scanning was performed between
deterioration of milk continues during the storage and may have 540 and 580 nm, showing a maximum absorption lamda peak
casein proteolysis due to presence of proteolytic enzymes [9]. at 560 nm [27].
The purpose of this study was to determine the effect of subclini-
cal mastitis on physical and chemicals components of milk in dual Somatic cells determination
purpose systems in the Colombian tropical low.
The somatic cells count (SCC) was performed with a op-
tical and portable SC counter (DCC, DeLaval International AB,
MATERIALS AND METHODS Sweden). The samples were mechanically stirred during five
min and with a device cassette-type 60 µL of milk were taken.
Type of study This device contains capillary impregnated with a fluorescent
Using a non-probabilistic sampling and convenience, in probe labeled with propidium iodide that binds specifically to
six Dual-Purpose (DP) cattle enterprises, located in Monteria cellular DNA. Then the device was placed in the reading cam-
Municipality, Cordoba (Colombia) a cross-sectional study was era, where it was exposed to the action of light, resulting in the
implemented [6]. production of fluorescent signals that were counted [18].

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Quality of bovine milk / Calderón-Rangel, A. et al. ___________________________________________________________________________

Statistical analysis RESULTS AND DISCUSSION

For the evaluation of all physicochemical variables and
SCC, the milk samples were distributed into four groups: phase In the TABLE I, the changes of the physicochemical
1, 0-2 (0 – 8 weeks) months of lactation; phase 2, of 2-4 (9-16 quality of milk with SM and WSM are presented, in each stage
weeks) months; phase 3, 4-6 (17 -24 weeks) months; and of lactation. The TABLE II, shows the differences of the phys-
phase 4, 6-8 (25 – 32 weeks) months. For this work was de- icochemical variables of milk with SM and WSM.
fined as SM free milk, when SCC was less than 250,000 A significant difference (P<0.05) was determined when
SC/mL, and subclinical mastitis milk with count greater than or compared all variables included in the study. In each lactation
equal to 250,000 SC/mL, the literature has used different stage, milk from udder with subclinical mastitis has a decrease
thresholds to differentiate healthy from unhealthy udders [29]. of chemical and physical compounds concentration compared
A value with minimal diagnostic error, 200,000 cells/mL was to milk from udder WSM (TABLE I). This decrease was due to
proposed by Schukken et al. [41], Pyörälä [37] defined that the rise in SC as a result of inflammation which reduces the
subclinical mastitis can be considered ³ 200,000 SC/mL with- synthesis of the different milk components and also due to in-
out growth in bacterial culture. Caraviello [13] said healthy creased vascular permeability, causing an abnormal increase
mammary glands have values < 200,000 CS/mL and higher in blood plasma containing enzymes such as proteases, lipase
counts are usually associated with an infection. Khan and and plasmin, that accelerate the breakdown of protein and
Khan [28] counts <100,000-150,000 CS/mL as no SM. Barlow milk fat [20, 26,29]. Vinhas et al. [46] concluded that a high
et al. [3], defined and identify cases of SM as milk with ³ SCC directly affects the quality of the milk The density of the
200,000 CS/mL. milk from udder with SM showed significant difference in rela-
Analysis of each sample were performed by triplicate tion to milk from udder WSM. Equally, when decrease the syn-
and obtained an average; arithmetic mean, standard deviation thesis of all chemical components of milk [16], the cryoscopy
and variance were obtained. For the SCC results were trans- point increases, which could result in a mistaken presumption
formed (log transformed) because the data did not show a nor- of impaired milk with addition of water [22]. The milk density
mal distribution. The dates were analyzed using the SAS sta- average with low SCC milk was 1,032 g/mL (TABLE II), value
tistical software [40]. previously reported for milk in Colombia [10, 11].
The value of protein percentage was statistically differ-
Ethical aspects ent (P<0.05) in milk from udder with SM compared with milk
The cows used in this experimentation were handling from udder WSM. Milk from cows with mastitis has a reduced
according to ethical standards established by law 84/1989 of level of casein, but lactalbumin and lactoglobulin levels in-
the Republic of Colombia [38]. The ethics committee of the crease [26]. Schukken et al. [41] observed that when lowered
IIBT reviewed, qualified and approved this work, as with low the SCC, the fat and lactose increased but this increase was
impact. lower for protein. In high SCC milks a decrease of protein be-

TABLE I
AVERAGE PHYSICOCHEMICAL QUALITY OF MILK WITH AND WITHOUT SUBCLINICAL MASTITIS IN EACH STAGES
OF LACTATION IN COWS DUAL PURPOSE IN MONTERIA, CORDOBA (COLOMBIA)

1 Phase lactation 2 Phase lactation 3 Phase lactation 4 Phase lactation

Properties ­ SCC ¯ SCC ­ SCC ¯ SCC ­ SCC ¯ SCC ­ SCC ¯ SCC
a b a b a b a
Total protein (%) 3.00 3.09 2.89 3.08 3.00 3.25 2.81 3.11b
a b a b a b a
Caseín (%) 2.21 2.41 2.27 2.44 2.23 2.57 2.11 2.46b
Fat (%) 3.46a 3.932b 3.40a 3.64a 3.35a 3.76b 3.24a 3.76b
Lactose (%) 4.29a 4.69b 4.13a 4.68b 4.24a 4.77b 4.12a 4.74b
Non fat solids (%) 7.65a 8.40b 7.62a 8.57b 7.54a 8.59b 7.27a 8.73b
a b a b a b a
Minerals (%) 0.742 0.700 0.694 0.696 0.740 0.692 0.760 0.687b
Totals solids (%) 11.11a 12.33b 11.01a 12.21b 10.88a 12.35b 10.51a 12.50b
Densityd (gr/mL) 1.028a 1.033b 1.029a 1.033b 1.029a 1.032b 1.029a 1.032b
Cryoscopic point 0.521a 0.548b 0.512a 0.540b 0.522a 0.552b 0.517a 0.550b
a b a b a b a
SCC (SC/mL) 474,061 79,818 56,1424 70,697 91,3545 37,048 2,411,182 39,812b
a
For the same stage of lactation different letters in the same row are statistically different (P<0.05).
¯ SCC: < 250,000 SC/mL; ­ SCC: ³ 250,000 SC/mL.

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TABLE II These significant differences (P<0.05) of the chemical

AVERAGE PHYSICOCHEMICAL QUALITY OF MILK WITH parameters of the milk as: fat percentage, lactose percentage,
AND WITHOUT SUBCLINICAL MASTITIS ACCORDING nonfat solids percentage, minerals percentage, total solid per-
IN COWS DUAL PURPOSE IN MONTERIA,
centage, may be due to an increase in SC as a result of in-
CORDOBA (COLOMBIA)
flammation which reduces the synthesis of the different com-
Properties ­ SCC ¯ SCC ponents of milk and increased vascular permeability. This
a causes an abnormal increase in blood plasma containing en-
Total protein (%) 2.93 ± 0.13 3.12 ± 0.13b
zymes such as proteases, lipase and plasmin enzymes that
Casein (%) 2.21 ± 0.13a 2.47 ± 0.12b accelerate the breakdown of protein and milk fat [20, 26, 29].
Fat (%) 3.36 ± 0.29a 3.70 ± 0.46b In this study, when compare the variations of SCC and pro-
tein, between the different stages of lactation, according to in-
Lactose (%) 4.19 ± 0.21a 4.76 ± 0.15b
creases of the phase, increases SCC and decreases protein
Minerals (%) 0.75 ± 0.02a 0.70 ± 0.02b percentage.
Totals solids (%) 10.88 ± 0.49a 12.32 ± 0.56b It was found that at each stage of lactation, the differ-
Density (gr/mL) 1.029 ± 0.001a 1.032 ± 0.001b ence between the concentration of lactose in milk with SM
- 0.52 ± 0.01 a - 0.55 ± 0.01b and milk WSM was statistically significant (P<0.05) (TABLE
Crioscopia point
I). Harmon [24] established that the mastitis reduce lactose
SCC (SC/mL) 1,090,053 ± 954,793a 54,756 ± 54,756b concentration between 5 and 20%. Bonfoh et al. [8] found
a
For the same stage of lactation different letters in the same row are that the concentration of lactose did not differ significantly
statistically different (P<0.05). between herds and cows but there was significant differ-
¯ SCC: < 250,000 SC/mL; ­ SCC: ³ 250,000 SC/mL.
ence in accordance with SCC. The rise in the SCC and the
changes in milk composition were more marked in the quar-
tween 6 to 8% was reported [21]. The degree of mastitis dimin- ter affected by major pathogens (Staphylococcus aureus,
ishes the values of protein in buffalo (Bubalus bubalis) milk Streptococcus agalactiae, other species of Streptococcus,
[45]. Phenomena of proteolysis and epithelial permeability in- and Escherichia coli) that minor pathogens (coagulase-
crease the levels of plasmin and other proteases from SC lead- negative Staphylococcus and Corynebacterium spp.), indi-
ing to degradation of casein [1]. Batavani et al. [4] found that cating that the severity of inflammation was associated with
the content of albumin in milk in SM milks was significantly the type of pathogen [1]. Sharif et al. [43] determined a de-
higher compared with milk from healthy quarters. Equally, An- crease in lactose content according to the SCC increase in
dreatta et al. [2] found significant differences (P<0.05) for pro- buffalo milk. Dangh and Anand [17] confirmed that high
tein in milk with high SCC. SCC is characteristic of an infection and this resulted in a
Comparing the percentage of casein between samples reduction in lactose. Sharif et al. [44] explained that as in-
analyzed it was found that the value was statistically differ- creases the severity of mastitis and SCC in buffalo milk, the
ent in milk with SM compared with milk WSM at each stage lactose content decreased significantly. Ogola et al. [33],
of lactation. This significant difference for mastitis free milk claim that a high prevalence of SM is a major constraint in
may be due to rise plasmin, proteolytic enzyme that lyses the production of quality milk. These decreases in the con-
the casein [26]. Haenlein et al. [23] concluded that when the centration of milk components are due to the reduction of
CCS was >500,000 SC/mL there was a decrease on casein synthetic activity of alveolar tissue [21, 32].
and that this was greater when >1,000,000 SCC. When comparing the physicochemical variables of milk
It was determined that the fat percentage has a differ- from high and low SCC, at all stages of lactation (TABLE II)
ence statistically significant (P<0.05) between milk with SM was determined that all the variables studied were statistically
and WSM, unlike of Roman et al. [39] in Venezuela, who found different (P<0.05).
no significant differences in the percentage of milk fat of
82,000 and 325,560 SC/mL. Bernal et al. [7], identified a highly CONCLUSIONS
significant correlation between total solids and fat (r = 0.7;
P<0.05). Bonfoh et al. [8], in Mali showed that the percentage In milk from SM was determined that the chemical com-
of fat was influenced by the supplement feeding, race, age, ponents of raw milk decreased significantly compared with no
breastfeeding and SM. Ullah et al. [45] determined that the se- SM milk, which affects its quality. Among the physical vari-
verity of mastitis decreases fat values from 5.01 ± 0.19%, ables, the cryoscopic point increased as a result of decreased
maximum content of buffalo milk negative for subclinical masti- synthesis of all the chemical components of milk and de-
tis, to 4.91 ± 0.17% and 4.39 ± 0.15% in SM. Leitner et al. [31] creased density, which could be misconstrued as an addition
showed that bacterial infection significantly affected the con- of water to milk. The SCC is an excellent tool for diagnosing
centration of fat and protein in milk. the health of the mammary glands.

411
Quality of bovine milk / Calderón-Rangel, A. et al. ___________________________________________________________________________

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