Correlation between ruminal pH and body condition score in cows with subacute ruminal acidosis

Ural Ph.D, Deniz Alıç; Ural Ph.D, Kerem; Örtlek M.Sc, Onur; Ural Ph.D, Deniz Alıç; Ural Ph.D, Kerem; Örtlek M.Sc, Onur

doi:10.21897/rmvz.1127

Services on Demand

Journal

Article

Indicators

Cited by SciELO
Access statistics

Revista MVZ Córdoba

Print version ISSN 0122-0268

Rev.MVZ Cordoba vol.22 no.3 Córdoba Sep./Dec. 2017

https://doi.org/10.21897/rmvz.1127

Originales

Correlation between ruminal pH and body condition score in cows with subacute ruminal acidosis

Correlación entre el pH ruminal y el índice de condición corporal en vacas con acidosis ruminal subaguda

Deniz Alıç Ural Ph.D¹^*

Kerem Ural Ph.D²

Onur Örtlek M.Sc²

^¹University of Adnan Menderes, Faculty Farm, Aydin, Turkey

^²University of Adnan Menderes, Faculty of Veterinary, Department of Internal Medicine, Aydin, Turkey

ABSTRACT

Objective.

The purposes of this field study were to a) confirm the presence of subacute ruminal acidosis (SARA) in Turkish dairy herds in Aydin region, b) record its regional distribution and c) to determine whether there is a relationship between body condition scoring, ruminal contractions and ruminal pH.

Materials and methods.

Ruminal fluid samples, via rumenocentesis, were withdrawn from a total of 120 Holstein dairy cows, from 5 herds (n=24 cows per herd). Rumen pH was analyzed on-site with a portable pH-meter for a precise SARA diagnosis. Classical body condition scoring systems (USBCS method) were utilized within 1-5 scale with 0.25 intervals.

Results.

Out of 120 cows enrolled 13 were (10.83%) classified as affected with SARA (pH<or=5.5), 6.6% were marginal (pH 5.6-5.8) and 82.5% were normal (pH>5.8). There was a significant difference (p<0.01) among farm V and other farms regarding mean ruminal pH. The overall means of BCS were found as 3.45±0.037, 3.43±0.122 and 4.30±0.075 in healthy animals, SARA suspected cows and cows with SARA, respectively with increased BCS in cows with SARA (p<0.01). Inter group comparison of ruminal contractions showed statistical significance (p<0.01). There were correlations among ruminal pH and ruminal contraction (r=0.622, p<0.01), ruminal pH and health status (r=-0.770, p<0.01), rumen contraction and health status (r=0.546, p<0.01).

Conclusions.

In the present study BCS and ruminal contractions data were used as indicators, in which correlations were found among ruminal pH and ruminal contraction and ruminal pH and BCS, favoring the usage or those parameters as probable biomarkers in cows with SARA.

Keywords: condition score; dairy cattle; subacute rumen acidosis (Source: CAB)

RESUMEN

Objetivo.

Los objetivos de este estudio de campo fueron a) confirmar la presencia de acidosis ruminal subaguda (SARA) en los rebaños de vacas lecheras turcas en la región de Aydin, b) registrar su distribución regional y c) determinar si existe una relación entre las puntuaciones del estado corporal, ruminal Contracciones y pH ruminal.

Materiales y métodos.

Se extrajeron muestras de líquido ruminal, a través de rumenocentesis, de un total de 120 vacas lecheras Holstein, de 5 hatos (n = 24 vacas por rebaño). El pH del rumen se analizó en el sitio con un pH-metro portátil para un diagnóstico preciso de SARA. Los sistemas clásicos de clasificación de estado corporal (método USBCS) se utilizaron en escala 1-5 con intervalos de 0,25.

Resultados.

De las 120 vacas inscritas, 13 fueron (10.83%) clasificadas como SARA (pH =5.5), 6.6% marginales (pH 5.6-5.8) y 82,5% normales (pH>5.8). Hubo una diferencia significativa (p<0.01) entre la finca V y otras fincas con respecto al pH ruminal medio. El promedio global de BCS fue de 3.45±0.037, 3.43±0.122 y 4.30±0.075 en animales sanos, SARA sospechosos de vacas y vacas con SARA, respectivamente con aumento de BCS en vacas con SARA (p<0.01). La comparación intergrupal de contracciones ruminales mostró significación estadística (p<0.01). Hubo correlaciones entre el pH ruminal y la contracción ruminal (r=0.622, p<0.01), pH ruminal y estado de salud (r =-0.770, p<0.01), contracción ruminal y estado de salud (r=0.546, p<0.01).

Conclusiones.

En el presente estudio se utilizaron indicadores BCS y contracciones ruminal como indicadores, en los que se encontraron correlaciones entre pH ruminal y contracción ruminal y pH ruminal y BCS, favoreciendo el uso o esos parámetros como biomarcadores probables en vacas con SARA.

Palabras clave: Condición de la condición corporal; ganado lechero; acidosis ruminal subaguda (Fuente: CAB)

INTRODUCTION

Subacute ruminal acidosis (SARA), a well known digestive disorder, has been characterized by repeated bouts of low ruminal pH ¹^-³. SARA generally results from diets low in digestible fiber or rich in simply fermentable carbohydrates ⁴^,⁵. Cows with SARA exhibited decreased rumen motility, loss of body condition score (BCS), diarrhea, depression,reduced milk production and laminitis ⁶^,⁷. Ruminal pH values detected between 5.5 and 6.0 were denoted for cows experiencing SARA or being at risk for SARA ⁷^,⁸.

The prevalence and the clinical consequences of (SARA) in dairy cows are still poorly understood. Given previous literature connecting SARA to health problems i.e. metabolic diseases of dairy cattle ⁹, the evidenced proof is relatively weak. SARA has previously been linked to cause systemic inflammation ⁷ and to participate in BCS loss of affected cows prone to be in poorer condition post calving ¹⁰^,¹¹. On the other hand regarding SARA detection of pathophysiological route remains difficult because of a) database from field conditions remains insufficient, b)less is known about real consequences, incidence and regional distribution of SARA on the field ¹¹. Furthermore experimental modelling for conceiving SARA in trial animals differ considerably from conditions detected in natural dairy herds. Therefore warranted research regarding the field, is necessary to better understand SARA¹¹. In the present study the purposes were to a) confirm the presence of SARA in Turkish dairy herds in Aydin region, b) record its regional distribution and c) determine whether there is a relationship between among condition scoring, ruminal contractions and ruminal pH.

MATERIALS AND METHODS

Farm data. The data from 5 dairy farms in Aydin municipality Eagean Region of Turkey, were collected. In an attempt to organize for the dairy herd health management program, one MS Agriculture Engineer [D.A.U. who is the director of Faculty Farm, Faculty of Veterinary, Adnan Menderes University and is specialized (author of many scientific reports on this subject) on BCS] and two Veterinary Surgeons (K.U. and O.Ö.) (from animal hospital, Faculty of Veterinary, Department of Internal Medicine, Adnan Menderes University), visited these farms regularly. During the visits, health status and reproductive performance were checked, at least once a month. The details of feeding management on these farms were similar to a previous study ¹². All farms included fed cows on total mixed ration (TMR). In the present study TMR was composed of forages, whole cottonseed, grains, protein, vitamin and mineral supplements mixed together to for a balanced ration

Cow data. A total of 120 cows (n=24 in each farm) with one lactation per cow, were included in the study. The cow data with lactation number, birth date, calving date and general health status were detected and noticed on farm visit. All included cows were examined for physiological reproductive function via rectal palpation 30 days following calving. There was no evidence of postpartum disorders (such as endometritis, displacement of abomasum, ketosis, as beacuse farmers or owners were routinely calling responsible farm veterinarian for examination, diagnosis if necessary).Two groups of 12 cows ¹³, were selected randomly in each herd. First group consisted of early lactation cows (0-70 days in milk) whereas other relevant composed of mid-lactation cows (70-140 days in milk).

Rumenocentesis and ruminal pH detection. Ruminal fluid collection was carried out via rumenocentesis by experienced researchers (K.U. and O.Ö) 4-8 hours after morning TMR feeding, from 264 selected cows through a period of January to September 2016. Ruminal fluid pH was determined immediately with a portable pH-meter (Edge pH meter, HANNA, Spain) able to detect pH changes from 0 to 14. All cows were checked for number of rumen contraction at the same time.

Body condition scoring. A previously described United States BCS (USBCS) system ¹⁴ through visual estimation composed of a 1-5 scale with 0.25 intervals, as was also adopted by some researchers ¹⁵^,¹⁶. After morning milking in farm, BCS data were collected and assessed by one of the present researchers (D.A.U), who is experienced, having MS and PhD degrees in Department of Animal Science, Agricultural Faculty. The latter author assessed BCS on visual observing flowcharts developed and used previously ¹⁴ and recently described in a very updated study ¹⁵.

Statistical analysis. In an attempt to perform analysis, determination of the effects of the factors on ruminal pH in the models were carried out using a General Linear Model (GLM) procedure of the SPSS Release 18.0. According to evaluation predicated on 5 traits (farm, lactation period, health status, BCS and ruminal contraction), it was stated that those characters had effect on ruminal pH. The model of this purpose was shown below. The differences between subclass means were determined by Duncan’s multiple range test ¹⁷. The statistical model used for the analysis is as follows:

Where; Yijkl: i. farm, j. lactation period, k. health status, l. body condition score, m. cow’s 305-day lactation milk yield,

μ :population mean,

s_i: i. farm’s effect (i: 1, 2, 2, 4, 5),

lp_j: j. lactation period’s effect (j: 1, 2),

hs_k: k. health status’s effect (k: 1, 2, 3),

VKP_l: l. body condition score’s effect (l: 1, 2, 3)

X_ijklm: i. farm, j. lactation period, k. health status, l. body condition score , m. cow’s ruminal contraction,

b_yx: partial regression coefficient with regard to ruminal contraction of ruminal pH,

e_ijklm: residual error.

The relations between traits and ruminal pH were investigated by Pearson Correlation Test (SPSS, 2009).

RESULTS

Lactation data. In each herd 2 groups of 12 cows were enrolled randomly in each herd. To those of an overall 120 animals included 13 were (10.83 %) classified as affected with SARA (pH< or=5.5) whereas 8 other cows (6.6%) were marginal (pH=5.6-5.8). To those of cows with SARA were detected in 1 out of 5 farms, in farm V. Out of those 13 cows, 7 were in early lactation and 6 were in midlactation period.

Ruminal contractions. Regarding health status (SARA, SARA suspected or healthy controls) of animals, group comparison showed statistical significance (p<0.01) for ruminal contractions.

Ruminal pH analysis. It was possible to draw a ruminal fluid from all initially selected 120 animals (60 in early lactation and 60 in midlactation period). Overall, 13 cows (10.83%) had a ruminal pH≤5.5 at the time of rumenocentesis. In farm V mean (st. dev) ruminal pH was 5.55±0.087, presenting statistical significance in contrast to other 4 farms without SARA positive animals. The minimum and maximum pH values were found to be 5.06 and 6.79, respectively. On the other side on farm V, marginal pH values, between 5.6 and 5.8, were found in 8 cows (6.6%) out of all cows, 4 (12%) early lactation and 4 (23.9%) mid-lactation cows.

BCS anaysis. In healthy animals mean (st. error) BCS were detected as 3.45±0.037, whereas in SARA suspected cows and in cows with SARA were deemed 3.43±0.122 and 4.30±0.075, respectively with a statistically significance (p<0.01). Overall interpretation revealed increased BCS in cows with SARA (Table 1).

Table 1 The means of BCS and Ruminal Contraction regarding Health Status of Cows

Groups	BCS
Groups	N		Min	Max
Healthy	99	3.45^a± 0.037	2.75	4.25
SARA Suspected	8	3.43^a± 0.122	2.75	3.75
SARA	13	4.30^b± 0.075	4.00	4.75
	Ruminal Contraction
Healthy	99	9.48^a± 0.123	7	12
SARA Suspected	8	8.63^a± 0.324	7	10
SARA	13	6.85^b± 0.154	6	8
a, b, c, d: Least square means on the same columnwithin each factor, followed by the different letter are significantly (p<0.01), ** p<0.01. NS: Nonsignificant, BCS: Body condition score

Descriptive statistics. The descriptive statistics of all type traits according to lactation number for farms were calculated and were shown in Table 2. The effects of farms on ruminal pH were found statistically significant (p<0.01). The means of ruminal pH were found similarly at lactation period and the effects of lactation period were found non-significant (p>0.05). The mean values of ruminal pH were found 5.26, 5.68 and 6.57 according to health status (respectively, SARA, SARA suspected and healthy) (Table 2). Finally, the means for BCS were ranged from 5.90 to 6.55 (Table 2). The effects of health status and BCS on ruminal pH were found significant (p<0.01). The effects of ruminal contraction on ruminal pH were found significant (p<0.05).

Table 2 The mean values of Rumen pH of cows

Factors	N	Ruminal pH	Min	Max
Factors	N		Min	Max
Farms	**
I	24	6.51^ab ± 0.079	5.69	7.13
II	24	6.75^c ± 0.085	6.27	7.67
III	24	6.35^a ± 0.066	5.72	6.77
IV	24	6.71^bc ± 0.069	5.96	7.21
V	24	5.55^d ± 0.087	5.06	6.79
Lactation period	NS
0-70. day	60	6.36 ± 0.067	5.40	7.67
70-140. day	60	6.38 ± 0.629	5.06	7.21
Health status	**
Healthy	99	6.57^a ± 0.039	5.69	7.67
SARA suspected	8	5.68^b ± 0.088	5.52	5.80
SARA	13	5.26^c ± 0.143	5.06	5.47
BCS	**
2<BCS<3	22	6.32^a ± 0.084	5.69	7.02
3<BCS<4	73	6.55^a ± 0.053	5.52	7.67
4≤BCS	25	5.90^b ± 0.743	5.06	7.13
a, b, c, d: Least square means on the same columnwithin each factor, followed by the different letter are significantly (p<0.01), ** p<0.01, NS: Nonsignificant, BCS: Body condition score

The correlations between factors and ruminal pH were presented in Table 3. The highest correlations among ruminal pH and ruminal contraction were found (0.622) and statistically significant (p<0.01). The lowest and negative correlations were found between ruminal pH and health status (r=-0.770) and was found significant (p<0.01). Also, correlations between rumen contraction and health status were found positive (r=0.546) and significant (p<0.01).

Table 3 The correlations between factors and ruminal pH

Factors	Ruminal pH	Health Status	BCS	Rumen Contraction
Ruminal Ph	1
Health Status	-0.770^**	1
BCS	0.622^**	-0.582^**	1
Rumen contraction	-0.226	0.546^**	-0.175	1
** p<0.01

DISCUSSION

Altough there has been several literature regarding SARA, an uncertainty is still evident for interpretation of ruminal pH values truly to diagnose SARA ⁷^,¹⁸. In practice by ruminocentesis manipulation, ruminal pH analysis was recommended for evaluation of SARA incidence in dairy farms ¹⁰. In the present study all 5 farms participated were employed within 24 cows per each. For the herd level, analysis of ruminal pH in a sample of 5-19 cows per herd might be of beneficial specifically at the postpartum period ¹⁰^,¹⁹. Most Turkish dairy cows are raised in small-medium sized farms [herd size ranges from 25 to 100 milking cows].All forages, protein supplements, minerals, vitamins and grains are thoroughly mixed in TMR, in which the cows were fed in the present study.

In the present study as was also aformentioned above at the time of rumenocentesis, 7 early lactation cows in and 6 other relevant mid-lactation cows in farm V were found to be experiencing SARA (cows with a ruminal pH ≤5.5). Similarly on that farm 4 early lactation cows and 4 other relevant mid-lactation cows were marginally acidotic.Interestingly out of 5 different farms enrolled, solely the farm V were composed of 21 (out of 24) SARA positive or SARA risk animals. At herd level if 1/3 or more of the cow population present rumen pH between 5.6-5.8, the animals were detected as marginally acidotic ¹³. Both SARA positive and SARA risk animals were located on the same farm, in which whole animals were fed TMR ration, similar to other farms (I to IV) involved where all cows were healthy. The difference might be briefly explained with either errors in ration formulation or inappropriate TMR particle size ²⁰. Similar findings were previously reported by Morgante et al. ¹⁹ detected that feeds chopped extremely fine were in association with SARA, in which could be the key factor in our study. The farm ration was formulized by the owner who has no sicentific education.Ration formulation and mixing errors were reported as foremost risk factors related to existence of SARA ²¹. Lastly regular interpretation of both ration formulation and feed particle size has growing interest ²⁰.

BCS possess significance during different lactation stages (fresh cows, early lactation, mid-lactation, late lactation and dry period). BCS frequently exists as 3 (5-point scale) in mid-lactation stage. If cows present over-form throughout mid-lactation, BCS varies from 3.5 to 4.0 (5-point scale) ²². In a very recent study a total of 50 head Holstein-Friesian cows in mid-lactation (at 1st-4rd parity), located in Aydin, Turkey were scored comperatively by use of the primary systems utilized within the US (1-5 scale with 0.25 intervals) and to those of Bayer Health Care Animal Health’s BCS Cowdition Smartphone App. In the latter study overall mean values of BCS were found as 3.37±0.068 and 3.45±0.060 for BCS Cowdition and USBCS, respectively. There was a positive correlation (r=0.81, p=0.01) among BCS Cowdition and USBCS systems with a positive linear relationship (r=0.66, p=0.001) ¹⁵.

Ruminal pH was detected lower in cows with extensive loss in BCS after calving. The reason for the poor BCS in low ruminal pH cows might be similar to a dairy cow study ¹⁰ in which metabolic acidosis resulted with elevated protein catabolism accompanied by growth impairment. In general during the postpartum period a cow loses BCS because of negative energy balance in an attempt to achieve a peak milk production ²³. In the present study mean BCS were detected as 3.45±0.037, whereas in SARA suspected cows and in cows with SARA were deemed 3.43±0.122 and 4.30±0.075, respectively with a statistically significance (p<0.01). Overall interpretation revealed increased BCS in cows with SARA. In addition there was a significant (p<0.01) correlation (r=0.622) between BCS and ruminal pH, observed in this study. The alterations of BCS could be related to several reasons i.e. appropriate level of nutrition and a well designed ration could affect body weight of cows along with conversion of tissues for increased productivity ²⁴^-²⁶.

Decreased number of ruminal contractions were previously denoted as a clinical finding in relation with SARA ²⁷. In a prior study in Iran, there were no significant differences between cows experiencing SARA and other cows in number of rumen contractions (in 2 min, p=0.592). Furthermore no significant difference was either detected between animals with SARA and those with marginal pH values and the rest of the cows regarding number of ruminal contractions (in 2 min, p=0.455) ¹³. In the present study taking into account health status (SARA, SARA suspected or healthy controls) of animals, group comparison showed statistical significance (p<0.01) for ruminal contractions.

The correlation between factors and ruminal pH were investigated in the present study. The highest correlations was found between ruminal pH and ruminal contraction (0.622) with a statistical significance (p<0.01). The lowest correlation was evident between ruminal pH and health status (r=-0.770, p<0.01). Between rumen contraction and health status a positive (r=0.546, p<0.01) correlation was detected.

In conclusion in the present study an attempt is made to establish the regional distribution of SARA in selected dairy herds in Aydin mucipality of Eagean Region based on the ruminal pH determination. Consequences of SARA on individual health, production level and metabolic status for both individual and herd level were established. Therefore BCS and ruminal contractions data were used as indicators, in which correlations were found among ruminal pH and ruminal contraction and ruminal pH and BCS, favoring the usage or those parameters as probable biomarkers in cows with SARA.

In a small to middle sized farms, the problem solely in 1 cow might affect the farmer’s income. Hence at the cow level, quick determination of ruminal pH in early lactation may have helped prevention and reduce economic loss ²⁸. Given the current and different feeding management conditions in Turkish dairy farms, and the association between ruminal pH and the incidence of postpartum disorders remains unclear, the interpretation of ruminal pH might provide useful and applicable information to improve the health and milk production of dairy cows²⁸. Furthermore this study and previous one ²⁹ also demonstrated the presence of SARA in this region, which may be taken into account with possible preventative measurements.

REFERENCES

1. Enemark JMD. The monitoring, prevention and treatment of sub-acute ruminal acidosis (SARA): A review. Vet J 2008; 176(1):32-43. [ Links ]

2. Enemark JMD, Jørgensen RJ, Kristensen NB. An evaluation of parameters for the detection of subclinical rumen acidosis in dairy herds. Vet Res Commun 2004; 28(8):687-709. [ Links ]

3. Plaizier JC, Krause DO, Gozho GN, McBride BW. Subacute ruminal acidosis in dairy cows: the physiological causes, incidence and consequences. Vet J 2009; 176(1):21-31. [ Links ]

4. Bramley E, Lean IJ, Fulkerson WJ, Stevenson MA, Rabiee AR, Costa ND. The definition of acidosis in dairy herds predominantly fed on pasture and concentrates. J Dairy Sci 2008; 91(1):308-321. [ Links ]

5. Aschenbach JR, Penner GB, Stumpff F, Gabel G. Ruminant nutrition symposium: role of fermentation acid and absorption in the regulation of ruminal pH. J Anim Sci 2011; 89(4):1092-1107. [ Links ]

6. Krause KM, Oetzel GR. Understanding and preventing subacute ruminal acidosis in dairy herds: a review. (Special Issue: Feed and animal health.). Anim Feed Sci Technol 2006; 126(3/4):215-236. [ Links ]

7. Gozho DN,, Plaizier JC, Krause DO,Kennedy AD, Wittenberg KM. Subacute ruminal acidosis induces ruminal lipopolysaccharide endotoxin release and triggers an inflammatory response. J Dairy Sci 2005; 88(4):1399-403. [ Links ]

8. Kleen JL, Hooijer GA, Rehage J, Noordhuizen JP. Subacute ruminal acidosis (SARA): A Review. J Vet Med Sci 2003; 50(8):406-414. [ Links ]

9. Mulligan F, Doherty M. Production diseases of the dairy cow. Vet J 2008; 176(1):3-9. [ Links ]

10. Kleen JL, Hooijer GA, Rehage J, Noordhuizen JPTM. Subacute ruminal acidosis in Dutch dairy herds. Vet Rec 2009; 164(22):681-683. [ Links ]

11. Kleen JL , Upgang L, Rehage J. Prevalence and consequences of subacute ruminal acidosis in German dairy herds. Acta Vet Scand 2013; 55(1):48. [ Links ]

12. Alic Ural D, Cengiz O, Ural K, Ozaydin S. Dietary Clinoptilolite Addition as a Factor for the Improvement of Milk Yield in Dairy Cows. J Anim Vet Adv 2013; 12(1):85-87. [ Links ]

13. Tajik J. Prevalence of subacute ruminal acidosis in some dairy herds of Khorasan Razavi province, northeast of Iran. Iran J Vet Res 2009; 10(1):28-32. [ Links ]

14. Edmonson AJ, Lean IJ, Weaver LD, Farver T, Webster G. A body condition scoring chart for Holstein dairy cows. J Dairy Sci 1989; 72(1):68-78. [ Links ]

15. Alic Ural D. The use of new practices for assessment of body condition score Rev MVZ Córdoba 2016; 21(1):5154-5162. [ Links ]

16. Bewley JM, Boyce RE, Roberts DJ, Coffey MP, Schutz MM. Comparison of two methods of assessing dairy cow body condition score. J Dairy Sci 2010; 77(1):95-98. [ Links ]

17. Steel RDG, Torrie JH. Principles and procedures of statistics. Mc-Graw Hill Book Co. Inc. 1984; New York, USA. [ Links ]

18. Zebeli Q, Dijkstra J, Tafaj M, Steingass H, Ametaj BN, Drochner W. Modeling the adequacy of dietary fiber in dairy cows based on the responses of ruminal pH and milk fat production to composition of the diet. J Dairy Sci 2008; 91(5):2046-66. [ Links ]

19. Morgante, M, Stelletta C, Berzaghi P, Gianesella M, Andrighetto I. Subacute rumen acidosis in lactating cows: an investigation in intensive Italian dairy herds. J Anim Physio Anim Nut 2007; 91(5-6):226-234. [ Links ]

20. Kitkas, G.C., Valergakis, G.E, Karatzias H, Panousis N. Subacute ruminal acidosis: prevalence and risk factors in Greek dairy herds. Iran J Vet Res 2013; 14(3):183-189 [ Links ]

21. Dohme F, DeVries TJ, Beauchemin KA. Repeated ruminal acidosis challenges in lactating dairy cows at high and low risk for developing acidosis: ruminal pH. J Dairy Sci 2008; 91(9):3554-3567. [ Links ]

22. Mishra, S., Kumari, K., Dubey, A. Body Condition Scoring of Dairy Cattle: A Review. RRJVS 2016; 2(1):58-65. [ Links ]

23. Rukkwamsuk T. Effect of nutrition on reproductive performance of postparturientdairy cows in the tropics: a review. Thai J Vet Med 2011; 41(suppl.):103-107. [ Links ]

24. Alic Ural D. A Study on body condition score of Holstein-Friesian cows raised at Bozdogan. Kocatepe Vet J 2012; 5(2):9-15. [ Links ]

25. Grubić G, Novaković Ž, Aleksić S, Sretenović LJ, Pantelić V, Ostojić-Andrić D. Evaluation of the body condition of high yielding cows. Biotech Anim Husb 2009; 25(1-2):81-91. [ Links ]

26. Vasseur E, Gibbons J, Rushen J and de Passillé AM. Development and implementation of a training program to ensure high repeatability of body condition scoring of dairy cows. J Dairy Sci 2013; 96(7):4725-4737. [ Links ]

27. Enemark JMD, Jørgensen RJ, Enemark PS. Rumen acidosis with special emphasis on diagnostic aspects of subclinical rumen acidosis: a review. Vet ir Zootech 2002;20:16-29. [ Links ]

28. Chaidate I, Somchai C, Jos N, Henk H. A cow-level association of ruminal pH on body condition score, serum beta-hydroxybutyrate and postpartum disorders in Thai dairy cattle. Anim Sci J 2014; 85(9):861-817. [ Links ]

29. Akin I, Aliç Ural D, Gültekin M, Ural K Subclinical Laminitis and Its Association with Po2 and Faecal Alterations: Isikli, Aydin Experience. Rev MVZ Cordoba 2015; 20(2):4534-4543. [ Links ]

Received: January 2017; Accepted: May 2017

^* Correspondence: alicdeniz@gmail.com

This is an open-access article distributed under the terms of the Creative Commons Attribution License