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Incidence, prevalence and impact of SARA in dairy herds
Animal Feed Science and Technology 172 (2012) 4–8
Contents lists available at SciVerse ScienceDirect
Animal Feed Science and Technology journal homepage: www.elsevier.com/locate/anifeedsci
Incidence, prevalence and impact of SARA in dairy herds夽 J.L. Kleen a,∗ , C. Cannizzo b a b
CowConsult, Hochfeldstr. 2, 26670 Uplengen, Germany Department of Veterinary Clinical Sciences, University of Padua, Viale dell’Università 16, I-35020, Legnaro (PD), Italy
a r t i c l e
Keywords: SARA Feed efficiency Metabolism Dairy cattle
i n f o
a b s t r a c t Whilst the exact definition of subacute ruminal acidosis (SARA) remains debatable, it is certain that SARA is present in a large number of dairy herds, affecting a limited proportion of animals. It is uncertain, however, what the exact consequences in the individual animal within a herd are. Based on the current knowledge, it appears fair to assume that not SARA in itself has negative consequences in the individual as well as in the herd, but that these are arising simultaneously with other pathologic alterations. The challenge for the future is to describe the impact of SARA on herd level. Detrimental effect on feed efficiency described seems to be the most important economic consequence. Furthermore, research may focus on the question whether SARA has to be understood as a signal differentiating optimal from suboptimal management in dairy herds. © 2011 Elsevier B.V. All rights reserved.
1. Introduction – definition of subacute ruminal acidosis Beginning in the 1990s, subacute ruminal acidosis (SARA) has been differentiated from acute or lactic acidosis (Garrett et al., 1999). SARA is usually differentiated from acute ruminal acidosis by its transient character and the limited pH drop down to pH values of around 5.5, thus not leading to massive growth of lactate-producing bacteria such as Streptococcus bovis (Kleen et al., 2003). However, SARA is characterized by a drop of ruminal pH to non-physiological levels. This is caused either by a lack of structural fibre or an excess of concentrates, generally rapidly fermentable carbohydrates, or both. This leads to an accumulation of volatile fatty acids (VFA) within the rumen. A narrow definition of SARA appears difficult: Firstly, it remains debatable what the threshold of a physiological ruminal pH would be. Various values between pH 5.5 and 6.0 have been advocated, often the pH values of 5.5 and 5.8 are used to define individuals or groups experiencing SARA or being at risk for SARA, respectively (Kleen et al., 2003; Plaizier et al., 2008). Secondly, there is uncertainty on how pH values have to be interpreted correctly in order to justify the diagnosis of SARA and whether they are indeed detrimental to the animal’s health (Plaizier et al., 2008; Zebeli et al., 2008). A study by Garrett et al. (1999) is so far the only one suggesting a scheme for SARA diagnosis on herd level. According to their study, SARA is present in a herd if three out of twelve cows would be found with a ruminal pH of 5.5 or less. It is important to understand, however, that in this study the pH threshold of 5.5 was chosen for statistical, not physiological reasons and it has to be measured by means of rumenocentesis (Duffield et al., 2004). As the reticulo-ruminal compartment is not maintaining a steady pH, the pH 5.5 is
Abbreviations: CLA, conjugated linoleic acid; DMI, dry matter intake; MFD, milk fat depression; NDF, neutral detergent fibre; NEB, negative energy balance; PUFA, polyunsaturated fatty acids; SARA, subacute ruminal acidosis; peNDF, physically effective neutral detergent fibre; TMR, total mixed ration; VFA, volatile fatty acids. 夽 This paper is part of the special issue entitled: Rumen Health: A 360◦ Analysis, Guest Edited by A. Van Vuuren, S. Calsamiglia and Editor for Animal Feed Science and Technology, P. Udén. ∗ Corresponding author at: Dip ECBHM, Hochfeldstr. 2, D-26670 Uplengen, Germany. Tel.: +49 0 4956 928056. E-mail address: [email protected] (J.L. Kleen). 0377-8401/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.anifeedsci.2011.12.003
J.L. Kleen, C. Cannizzo / Animal Feed Science and Technology 172 (2012) 4–8
5
to be understood as the lowest threshold of a functioning amylolytic biosystem. It is usually measured 2–8 h post feeding, depending on feeding technique. Below pH 5.5, lactate production will increase rapidly, microbial protein metabolism will be impaired and the microbial ability to ferment structural carbohydrates will decrease significantly (Kaufmann, 1976; Bach et al., 2005; Jouany, 2006). Its transient character differentiates SARA from acute acidosis; its dynamics have been described in models. Duffield et al. (2004) used 16 lactating dairy cows on a standard lactating cow ration for description of ruminal pH dynamics. Independently of SARA being prevalent, ruminal pH was found to be at or below 5.5 for 1 h per day on average, however, with a huge variation between 0 h and 6 h and a standard deviation of almost 2 h. Penner et al. (2009) showed variation in VFA uptake in sheep possibly explaining individual variation of pH-dynamics. Dohme et al. (2008) were able to show an increasing severity in terms of pH nadir and length of acidosis episodes over three subsequent periods with a challenge for SARA. Whilst the time with pH 5.5 or below increased to up to 6 h, the nadir of pH decreased down to 5.1 during the third of the SARA episodes. SARA is therefore likely to be present in just a small proportion of individuals in a herd at a time and may intensify. 2. Prevalence and incidence of SARA Diagnosis of SARA is difficult as clinical signs are subtle and proxy parameters like faecal pH or net-acid-base-excretion are not suitable for diagnosis (Enemark, 2008). A definite diagnosis therefore generally requires the sampling of ruminal fluid. Whilst rumen-fistulated cows are frequently used in clinical trials, the puncture of the rumen (rumenocentesis) is regularly used in field trials and is tolerated well by sampled animals (Kleen et al., 2004). The sampling of ruminal fluid by ways of this method gives however only a mere snapshot of the actual ruminal environment. Research has been done on the development of devices, measuring ruminal or, respectively, reticular pH continuously (Schneider et al., 2010). The use of these devices will allow a more precise determination of prevalence and incidence by showing pH fluctuations during the day and for a longer time. The prevalence describes what proportion of animals within a herd or a group are experiencing SARA at any given point of time. Determining prevalence therefore demands for a detection method and a valid definition of the condition. Few field studies have so far determined the prevalence of SARA on herd level and on dairy cows population level. In Europe, Morgante et al. (2007) investigated SARA in 10 Italian herds and found three herds having more than 33% of individuals with a pH of 5.5 or less. Kleen et al. (2009) found an overall prevalence of 13.8% in 18 Dutch dairy herds with stage of lactation having no detectable influence on SARA prevalence. O’Grady et al. (2008) described SARA in grazing Irish dairy cows and reported a prevalence of 11%. An Iranian study determined an overall prevalence of 27.6% in 10 dairy herds (Tajik et al., 2009). In these field studies generally the pH thresholds of 5.5 and 5.8 are used, whilst rumenocentesis is used as method for sampling of ruminal fluid. Although different risk periods in the course of lactation have been defined (Kleen et al., 2003), no study has so far shown an influence of stage of lactation on the prevalence of SARA. The studies show that animals with a pH of 5.5 or below can be found in very different production systems, independently from production level or stage of lactation. However, it has also been shown that in similar production systems the prevalence of SARA can vary among herds. Kleen et al. (2009), for example, found prevalences ranging from 0% and close to 40% in very similarly managed herds. Whilst the prevalence is related to a fixed point of time, incidence describes how many animals would enter a period of experiencing SARA within a given period of time, e.g. per day. The incidence of SARA is therefore difficult to determine, as it would require the use of a system that monitors ruminal pH continuously or at defined intervals. Studies reporting on the incidence are therefore all based on models in a limited number of animals and so far no field data are available. In a study conducted by Zebeli et al. (2008) it has been stated that the incidence of SARA could be minimized by maintaining a level of 300–330 g/kg DM of physically effective NDF (peNDF) in the ration fed. The question remains what the incidence of SARA within herds would be. As stated above, it appears likely that individual cows are experiencing SARA repeatedly and for a longer time rather than whole herds do for only a limited period of time. Therefore, in herds experiencing SARA its incidence will be low for a defined time, independently of its prevalence. The abovementioned system using internal probes will certainly aid in understanding the incidence of SARA and deliver sound data. In summary it has to be stated that general feeding management seems to be decisive in explaining SARA prevalence and possibly its incidence. As shown by Morgante et al. (2007), the influence of management seems to contribute significantly to the incidence of SARA, independently from chemical composition of the ration like peNDF or proportion of fermentable carbohydrates. Examples for factors contributing are severe NEB due to management mistakes in late lactation, time of mixing in a feeder wagon for TMR, ability of animals to sort against certain components, feeding space at the feed trough, frequency of feeding or social stress within groups. 3. Impact of SARA The potential consequences of SARA like laminitis, milk fat depression, poor body condition and others have been reviewed thoroughly (Kleen et al., 2003; Plaizier et al., 2008; Enemark, 2008). It has to be stated, however, that the evidence base for the frequently cited consequences of SARA is to a very large extent not supported by observations from the field or from experiments. Reasons for this are various: obviously consequences from SARA would arise with a certain delay from the initial insult and it is difficult to relate them to actual rumen status. Laminitis, for example, is regularly mentioned as resulting
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from acidosis as there is a correlation between ration type, ruminal fermentation and hoof lesions (Bergsten, 1994; Nocek, 1997). The pathology of this condition, however, is multifactorial and correlating it to SARA in herds would be both a practical and epidemiological challenge. This may have prevented any further evidence from the field so far. Another example is the connection between milk composition, especially milk fat depression (MFD), and ruminal acidosis. Although this is based on sound evidence (Khafipour et al., 2009b), an impact on milk production parameters has not been described in any of the abovementioned field studies: no correlation could not be found, even under such different conditions as investigated by Tajik et al. (2009) in a very intensive system or O’Grady et al. (2008) in a grazing system, respectively. Milk fat depression has not been observed in herds with SARA being prevalent, nor was it found in individuals experiencing the condition (Kleen et al., 2009). In an experimental study, Krause and Oetzel (2005) induced SARA in 13 animals by adding grain pellets to a TMR and monitored ruminal pH continuously. Although induced SARA depressed milk production for two days after the challenge by about 10%, no effect on milk composition could be determined. In a theory proposed by Bauman and Griinari (2003) MFD was related to changes in milk fatty acids profile due to alterations in rumen biohydrogenation of poly-unsaturated fatty acids (PUFA). This would result in production of fatty acids intermediates which are absorbed and elicit direct inhibitory effects on milk fat synthesis. It was demonstrated that the trans10, cis-12 isoform of conjugated linoleic acid (CLA), which increases during dietary induced MFD due to biohydrogenation of 18 carbon PUFA, is a potent inhibitor of milk fat synthesis and secretion (Peterson et al., 2003). Some years later other fatty acids intermediates were examined for their effect on MFD like trans C18:1, especially trans-10 18:1 which is an intermediate in the major pathways of rumen biohydrogenation. It was demonstrated that this fatty acid increases in milk during MFD. This may be considered as a sign but trans-10 18:1 has not direct effect on milk fat synthesis (Lock et al., 2007). However, these results come from experimental conditions and just demonstrate that MFD and SARA could be related because both arise from similar conditions: a diet poor in fibre and rich in concentrate. The question remains whether cows that experienced MFD were really experiencing SARA and in consequence MFD could indeed be considered as a sign of SARA. In order to identify the link between SARA and other disorders, various pathomechanisms have been discussed in the past and clinical trials have shed new light on the potential consequences of SARA. Gozho et al. (2005) were able to show a systemic inflammatory response after SARA was induced by feeding wheat–barley pellets. Similar experiments were able to show a negative influence on dry matter intake (DMI), milk yield and butterfat (Khafipour et al., 2009a). However, SARA induced by feeding alfalfa-pellets did not lead to a systemic inflammatory response, although lipopolysaccharides did increase intraruminally (Khafipour et al., 2009b). This interestingly corresponds to an Italian field study (Cannizzo, 2008). In this study, 12 intensively managed herds were tested for SARA prevalence by means of rumenocentesis. For labelling herds as SARA positive or negative, the earlier-mentioned scheme for calculating sample size was used (Garrett et al., 1999). In herds diagnosed with SARA, a tendency for higher white blood cell counts and higher total protein levels was observed, although within the physiological limits. However, no correlation was observed between SARA and systemic inflammatory response as represented by acute phase proteins, both in individuals and herds classified as having SARA or not. This would again point to the assumption that SARA is not necessarily per se leading to clinically detectable consequences but rather arises in situations of management related stress like mentioned above. These results confirm also that it is probably more accurate to consider SARA as being indicative of individual and herd health problems and not as a herd problem per se. In summary it has to be stated that there is a certain discrepancy between field studies and clinical trials, at least when it comes to clinically detectable consequences. Whilst reports from the field are based on ruminal pH values deriving from actual rations fed, clinical trials often use high proportions of concentrate to create acidotic challenges. It remains to be shown whether SARA as it is actually found in the field is indeed modelled accurately. Field studies show that SARA is not necessarily related to the expected clinical consequences nor does it necessarily evoke a systemic inflammatory response. The question research has to answer in the future is whether the supposed clinical problems are consequences or causes of SARA, or whether they are related to SARA because both conditions arise from the same problem in general management. Independently from inflammation, SARA will have a negative impact on the ruminal fermentation and, subsequently, metabolism. Low ruminal pH will lead to reduced fibre digestion (Ørskov, 1999; Allen, 2000), altered pattern of volatile fatty acids (Cannizzo, 2008; Gianesella, 2007), impaired microbial protein metabolism (Bach et al., 2005; Calsamiglia et al., 2008), altered ruminal microflora (Khafipour et al., 2009a), and consequently exacerbating of negative energy balance (NEB) by less efficient digestion (Jouany, 2006). This corresponds to the findings of Kleen et al. (2009): here, individual cows experiencing SARA showed a significant poorer body condition score and more severe body condition loss around calving. Depression of dry matter intake (DMI) is of importance when it comes to the complex of production diseases that are linked to NEB and ruminal fermentation (Mulligan and Doherty, 2008). SARA is usually reported to depress DMI and the possible mechanisms for this have been reviewed (Allen, 2000; Plaizier et al., 2008). The monitoring of DMI is part of the rumen health control scheme as used by Mulligan et al. (2006). Depression of DMI leads to imbalances in the ruminal metabolism by sorting for concentrates in the ration and insufficient uptake of any nutrient. Effects of SARA on metabolism could therefore be increased in the form of a vicious cycle. As reviewed by Enemark (2008), the economic consequences of SARA are estimated with more than 1 US$ per day and animal. Considering the difficulty to diagnose SARA and associate it with pathological alterations, however, any estimate has to remain speculation. Instead of focusing on diseases of which the pathological pathways are not fully understood, it appears promising to focus on the influence that SARA might have on feed conversion efficiency, DMI, and NEB: a wellfunctioning rumen and consequently a well-functioning metabolism are fundamental to any animal’s health and production.
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The metabolism of the dairy cow is especially delicate and difficult to control; NEB puts any dairy cow at risk in early lactation and the balance between energy use and input is difficult to meet throughout. SARA appears to be an important aspect of this complex and needs to be understood better. 4. Conclusions Based on the current evidence, SARA is best described as a depression of ruminal pH to ≤5.5 if tested by means of rumenocentesis and intensifying to lower pH values, lasting several hours and occurring several times per day, depending on the type and management of feeding. It is certain that SARA is present in a large number of dairy herds, affecting a limited proportion of animals. The prevalence of SARA within and among herds is independent of stage of lactation, production level or management system. It is uncertain, however, what the exact consequences in the individual animal are. SARA will in itself have negative consequences in the individual, especially in terms of feed conversion efficiency; the mutual reinforcing effects it will have with other, simultaneous conditions need a better understanding. The task remains to describe the occurrence of SARA on a herd level: the development of a commercially available system that monitors reticulo-ruminal pH continuously will certainly aid in describing prevalence and incidence more exactly. It may also help in understanding the consequences of SARA better, as the uncertainty regarding its impact on health and economy remains. The detrimental effect on feed efficiency seems to be the most important economic consequence and certainly deserves more attention. Furthermore, research may focus on the question whether SARA has to be understood as a signal differentiating optimal from suboptimal management in dairy herds. Conflict of interest None. References Allen, M.S., 2000. Effects of diet on short-term regulation of feed intake by lactating dairy cattle. J. Dairy Sci. 83, 1598–1624. Bach, A., Calsamiglia, S., Stern, M.D., 2005. Nitrogen metabolism in the rumen. J. Dairy Sci. 88 (Suppl. 1), E9–E21. Bauman, D.E., Griinari, J.M., 2003. Nutritional regulation of milk fat synthesis. Annu. Rev. Nutr. 23, 203–227. Bergsten, C., 1994. Haemorrhages of the sole horn of dairy cows as a retrospective indicator of laminitis. An epidemiological study. Acta Vet. Scand. 35, 55–66. Calsamiglia, S., Cardozo, P.W., Ferret, A., Bach, A., 2008. Changes in rumen microbial fermentation are due to a combined effect of diet and pH. J. Anim. Sci. 86, 702–711. Cannizzo, C., 2008. Fermentative disturbances in the dairy cow: subacute ruminal acidosis in field conditions and metabolic-inflammatory effects observed. PhD Thesis, Padova. Dohme, F., DeVries, T.J., Beauchemin, K.A., 2008. Repeated ruminal acidosis challenges in lactating dairy cows at high and low risk for developing acidosis: ruminal pH. J. Dairy Sci. 93, 3554–3567. Duffield, T., Plaizier, J.C., Fairfield, A., Bagg, R., Vessle, G., Dick, P., Wilson, J., Aramini, J., McBride, B., 2004. Comparison of techniques for measurement for rumen pH in lactating dairy cows. J. Dairy Sci. 87, 59–66. Enemark, J.M., 2008. The monitoring, prevention and treatment of sub-acute ruminal acidosis (SARA): a review. Vet. J. 176, 32–43. Garrett, E.F., Pereira, M.N., Nordlund, K.V., Armentano, L.E., Goodger, W.J., Oetzel, G.R., 1999. Diagnostic methods for the detection of subacute ruminal acidosis in dairy cows. J. Dairy Sci. 82, 1170–1178. Gianesella, M., 2007. Subacute rumen acidosis in Italian dairy herds: occurrence and diagnostic tools. PhD Thesis, Padova. Gozho, G.N., Plaizier, J.C., Krause, D.O., Kennedy, A.D., Wittenberg, K.M., 2005. Subacute ruminal acidosis induces ruminal lipopolysaccharide endotoxin release and triggers an inflammatory response. J. Dairy Sci. 88, 1399–1403. Jouany, J.P., 2006. Optimizing rumen functions in the close-up transition period and early lactation to drive dry matter intake and energy balance in cows. Anim. Reprod. Sci. 96, 250–264. Kaufmann, W., 1976. Influence of the composition of the ration and the feeding frequency on pH-regulation in the rumen and on feed-intake in ruminants. Livest. Prod. Sci. 3, 103–114. Khafipour, E., Li, S., Plaizier, J.C., Krause, D.O., 2009a. Rumen microbiome composition determined using two nutritional models of subacute ruminal acidosis. Appl. Environ. Microbiol. 75, 7115–7124. Khafipour, E., Krause, D.O., Plaizier, J.C., 2009b. Alfalfa pellet-induced subacute ruminal acidosis in dairy cows increases bacterial endotoxin in the rumen without causing inflammation. J. Dairy Sci. 92, 1712–1724. Kleen, J.L., Hooijer, G.A., Rehage, J., Noordhuizen, J.P., 2003. Subacute ruminal acidosis (SARA): a review. J. Vet. Med. A Physiol. Pathol. Clin. Med. 50, 406–414. Kleen, J.L., Hooijer, G.A., Rehage, J., Noordhuizen, J.P., 2004. Rumenocentesis (rumen puncture) a viable instrument in herd health diagnosis. Dtsch Tierarztl Wochenschr 111, 458–462. Kleen, J.L., Hooijer, G.A., Rehage, J., Noordhuizen, J.P., 2009. Subacute ruminal acidosis in Dutch dairy herds. Vet. Rec. 164, 681–683. Krause, K.M., Oetzel, G.R., 2005. Inducing subacute ruminal acidosis in lactating dairy cows. J. Dairy Sci. 88, 3633–3639. Lock, A.L., Tyburczy, C., Dwyer, D.A., Harvatine, K.J., Destaillats, F., Mouloungui, Z., Candy, L., Bauman, D.E., 2007. Trans-10 octadecenoic acid does not reduce milk fat synthesis in dairy cows. J. Nutr. 137, 71–76. Morgante, M., Stelletta, C., Berzaghi, P., Gianesella, M., Andrighetto, I., 2007. Subacute rumen acidosis in lactating cows: an investigation in intensive Italian dairy herds. J. Anim. Physiol. Anim. Nutr. (Berl). 91, 226–234. Mulligan, F.J., Doherty, M., 2008. Production diseases of the dairy cow. Vet. J. 176, 3–9. Mulligan, F.J., O’Grady, L., Rice, D.A., Doherty, M.L., 2006. A herd health approach to dairy cow nutrition and production diseases of the transition cow. Anim. Reprod. Sci. 96, 331–353. Nocek, J.E., 1997. Bovine acidosis: implications. J. Dairy Sci. 80, 1005–1028. O’Grady, L., Doherty, M.L., Mulligan, F.J., 2008. Subacute ruminal acidosis (SARA) in grazing Irish dairy cows. Vet. J. 176, 44–49. Ørskov, E.R., 1999. Supplement strategies for ruminants and management of feeding to maximize utilization of roughages. Prev. Vet. Med. 38, 179–185. Penner, G.B., Aschenbach, J.R., Gäbel, G., Rackwitz, R., Oba, M., 2009. Epithelial capacity for apical uptake of short chain fatty acids is a key determinant for intraruminal pH and the susceptibility to subacute ruminal acidosis in sheep. J. Nutr. 139, 1714–1720. Peterson, D.G., Matitashvili, E.A., Bauman, D.E., 2003. Diet-induced milk fat depression in dairy cows results in increased trans-10, cis-12 CLA in milk fat and coordinate suppression of mRNA abundance for mammary enzymes involved in milk fat synthesis. J. Nutr. 133, 3098–3102.
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Plaizier, J.C, Krause, D.O., Gozho, G.N., McBride, B.W., 2008. Subacute ruminal acidosis in dairy cows: the physiological causes, incidence and consequences. Vet. J. 176, 21–31. Schneider, K., Gasteiner, J., Guggenberger, T., Urdl, M., Steiner, S., Neidl, A., Linhart, N., Baumgartner, W., 2010. Comparative measurements on ruminal pH-value in cattle. Berl Munch Tierarztl Wochenschr 123 (September–October (9–10)), 406–412. Tajik, J., Nadalian, M.G., Raoofi, A., Mohammadi, G.R., Bahonar, A.R., 2009. Prevalence of subacute ruminal acidosis in some dairy herds of Khorasan Razavi province, northeast of Iran. Iranian J. Vet. Res. 10, 28–32. Zebeli, Q., Dijkstra, J., Tafaj, M., Steingass, H., Ametaj, B.N., Drochner, W., 2008. Modeling the adequacy of dietary fibre in dairy cows based on the responses of ruminal pH and milk fat production to composition of the diet. J. Dairy Sci. 91, 2046–2066.
Contents lists available at SciVerse ScienceDirect
Animal Feed Science and Technology journal homepage: www.elsevier.com/locate/anifeedsci
Incidence, prevalence and impact of SARA in dairy herds夽 J.L. Kleen a,∗ , C. Cannizzo b a b
CowConsult, Hochfeldstr. 2, 26670 Uplengen, Germany Department of Veterinary Clinical Sciences, University of Padua, Viale dell’Università 16, I-35020, Legnaro (PD), Italy
a r t i c l e
Keywords: SARA Feed efficiency Metabolism Dairy cattle
i n f o
a b s t r a c t Whilst the exact definition of subacute ruminal acidosis (SARA) remains debatable, it is certain that SARA is present in a large number of dairy herds, affecting a limited proportion of animals. It is uncertain, however, what the exact consequences in the individual animal within a herd are. Based on the current knowledge, it appears fair to assume that not SARA in itself has negative consequences in the individual as well as in the herd, but that these are arising simultaneously with other pathologic alterations. The challenge for the future is to describe the impact of SARA on herd level. Detrimental effect on feed efficiency described seems to be the most important economic consequence. Furthermore, research may focus on the question whether SARA has to be understood as a signal differentiating optimal from suboptimal management in dairy herds. © 2011 Elsevier B.V. All rights reserved.
1. Introduction – definition of subacute ruminal acidosis Beginning in the 1990s, subacute ruminal acidosis (SARA) has been differentiated from acute or lactic acidosis (Garrett et al., 1999). SARA is usually differentiated from acute ruminal acidosis by its transient character and the limited pH drop down to pH values of around 5.5, thus not leading to massive growth of lactate-producing bacteria such as Streptococcus bovis (Kleen et al., 2003). However, SARA is characterized by a drop of ruminal pH to non-physiological levels. This is caused either by a lack of structural fibre or an excess of concentrates, generally rapidly fermentable carbohydrates, or both. This leads to an accumulation of volatile fatty acids (VFA) within the rumen. A narrow definition of SARA appears difficult: Firstly, it remains debatable what the threshold of a physiological ruminal pH would be. Various values between pH 5.5 and 6.0 have been advocated, often the pH values of 5.5 and 5.8 are used to define individuals or groups experiencing SARA or being at risk for SARA, respectively (Kleen et al., 2003; Plaizier et al., 2008). Secondly, there is uncertainty on how pH values have to be interpreted correctly in order to justify the diagnosis of SARA and whether they are indeed detrimental to the animal’s health (Plaizier et al., 2008; Zebeli et al., 2008). A study by Garrett et al. (1999) is so far the only one suggesting a scheme for SARA diagnosis on herd level. According to their study, SARA is present in a herd if three out of twelve cows would be found with a ruminal pH of 5.5 or less. It is important to understand, however, that in this study the pH threshold of 5.5 was chosen for statistical, not physiological reasons and it has to be measured by means of rumenocentesis (Duffield et al., 2004). As the reticulo-ruminal compartment is not maintaining a steady pH, the pH 5.5 is
Abbreviations: CLA, conjugated linoleic acid; DMI, dry matter intake; MFD, milk fat depression; NDF, neutral detergent fibre; NEB, negative energy balance; PUFA, polyunsaturated fatty acids; SARA, subacute ruminal acidosis; peNDF, physically effective neutral detergent fibre; TMR, total mixed ration; VFA, volatile fatty acids. 夽 This paper is part of the special issue entitled: Rumen Health: A 360◦ Analysis, Guest Edited by A. Van Vuuren, S. Calsamiglia and Editor for Animal Feed Science and Technology, P. Udén. ∗ Corresponding author at: Dip ECBHM, Hochfeldstr. 2, D-26670 Uplengen, Germany. Tel.: +49 0 4956 928056. E-mail address: [email protected] (J.L. Kleen). 0377-8401/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.anifeedsci.2011.12.003
J.L. Kleen, C. Cannizzo / Animal Feed Science and Technology 172 (2012) 4–8
5
to be understood as the lowest threshold of a functioning amylolytic biosystem. It is usually measured 2–8 h post feeding, depending on feeding technique. Below pH 5.5, lactate production will increase rapidly, microbial protein metabolism will be impaired and the microbial ability to ferment structural carbohydrates will decrease significantly (Kaufmann, 1976; Bach et al., 2005; Jouany, 2006). Its transient character differentiates SARA from acute acidosis; its dynamics have been described in models. Duffield et al. (2004) used 16 lactating dairy cows on a standard lactating cow ration for description of ruminal pH dynamics. Independently of SARA being prevalent, ruminal pH was found to be at or below 5.5 for 1 h per day on average, however, with a huge variation between 0 h and 6 h and a standard deviation of almost 2 h. Penner et al. (2009) showed variation in VFA uptake in sheep possibly explaining individual variation of pH-dynamics. Dohme et al. (2008) were able to show an increasing severity in terms of pH nadir and length of acidosis episodes over three subsequent periods with a challenge for SARA. Whilst the time with pH 5.5 or below increased to up to 6 h, the nadir of pH decreased down to 5.1 during the third of the SARA episodes. SARA is therefore likely to be present in just a small proportion of individuals in a herd at a time and may intensify. 2. Prevalence and incidence of SARA Diagnosis of SARA is difficult as clinical signs are subtle and proxy parameters like faecal pH or net-acid-base-excretion are not suitable for diagnosis (Enemark, 2008). A definite diagnosis therefore generally requires the sampling of ruminal fluid. Whilst rumen-fistulated cows are frequently used in clinical trials, the puncture of the rumen (rumenocentesis) is regularly used in field trials and is tolerated well by sampled animals (Kleen et al., 2004). The sampling of ruminal fluid by ways of this method gives however only a mere snapshot of the actual ruminal environment. Research has been done on the development of devices, measuring ruminal or, respectively, reticular pH continuously (Schneider et al., 2010). The use of these devices will allow a more precise determination of prevalence and incidence by showing pH fluctuations during the day and for a longer time. The prevalence describes what proportion of animals within a herd or a group are experiencing SARA at any given point of time. Determining prevalence therefore demands for a detection method and a valid definition of the condition. Few field studies have so far determined the prevalence of SARA on herd level and on dairy cows population level. In Europe, Morgante et al. (2007) investigated SARA in 10 Italian herds and found three herds having more than 33% of individuals with a pH of 5.5 or less. Kleen et al. (2009) found an overall prevalence of 13.8% in 18 Dutch dairy herds with stage of lactation having no detectable influence on SARA prevalence. O’Grady et al. (2008) described SARA in grazing Irish dairy cows and reported a prevalence of 11%. An Iranian study determined an overall prevalence of 27.6% in 10 dairy herds (Tajik et al., 2009). In these field studies generally the pH thresholds of 5.5 and 5.8 are used, whilst rumenocentesis is used as method for sampling of ruminal fluid. Although different risk periods in the course of lactation have been defined (Kleen et al., 2003), no study has so far shown an influence of stage of lactation on the prevalence of SARA. The studies show that animals with a pH of 5.5 or below can be found in very different production systems, independently from production level or stage of lactation. However, it has also been shown that in similar production systems the prevalence of SARA can vary among herds. Kleen et al. (2009), for example, found prevalences ranging from 0% and close to 40% in very similarly managed herds. Whilst the prevalence is related to a fixed point of time, incidence describes how many animals would enter a period of experiencing SARA within a given period of time, e.g. per day. The incidence of SARA is therefore difficult to determine, as it would require the use of a system that monitors ruminal pH continuously or at defined intervals. Studies reporting on the incidence are therefore all based on models in a limited number of animals and so far no field data are available. In a study conducted by Zebeli et al. (2008) it has been stated that the incidence of SARA could be minimized by maintaining a level of 300–330 g/kg DM of physically effective NDF (peNDF) in the ration fed. The question remains what the incidence of SARA within herds would be. As stated above, it appears likely that individual cows are experiencing SARA repeatedly and for a longer time rather than whole herds do for only a limited period of time. Therefore, in herds experiencing SARA its incidence will be low for a defined time, independently of its prevalence. The abovementioned system using internal probes will certainly aid in understanding the incidence of SARA and deliver sound data. In summary it has to be stated that general feeding management seems to be decisive in explaining SARA prevalence and possibly its incidence. As shown by Morgante et al. (2007), the influence of management seems to contribute significantly to the incidence of SARA, independently from chemical composition of the ration like peNDF or proportion of fermentable carbohydrates. Examples for factors contributing are severe NEB due to management mistakes in late lactation, time of mixing in a feeder wagon for TMR, ability of animals to sort against certain components, feeding space at the feed trough, frequency of feeding or social stress within groups. 3. Impact of SARA The potential consequences of SARA like laminitis, milk fat depression, poor body condition and others have been reviewed thoroughly (Kleen et al., 2003; Plaizier et al., 2008; Enemark, 2008). It has to be stated, however, that the evidence base for the frequently cited consequences of SARA is to a very large extent not supported by observations from the field or from experiments. Reasons for this are various: obviously consequences from SARA would arise with a certain delay from the initial insult and it is difficult to relate them to actual rumen status. Laminitis, for example, is regularly mentioned as resulting
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from acidosis as there is a correlation between ration type, ruminal fermentation and hoof lesions (Bergsten, 1994; Nocek, 1997). The pathology of this condition, however, is multifactorial and correlating it to SARA in herds would be both a practical and epidemiological challenge. This may have prevented any further evidence from the field so far. Another example is the connection between milk composition, especially milk fat depression (MFD), and ruminal acidosis. Although this is based on sound evidence (Khafipour et al., 2009b), an impact on milk production parameters has not been described in any of the abovementioned field studies: no correlation could not be found, even under such different conditions as investigated by Tajik et al. (2009) in a very intensive system or O’Grady et al. (2008) in a grazing system, respectively. Milk fat depression has not been observed in herds with SARA being prevalent, nor was it found in individuals experiencing the condition (Kleen et al., 2009). In an experimental study, Krause and Oetzel (2005) induced SARA in 13 animals by adding grain pellets to a TMR and monitored ruminal pH continuously. Although induced SARA depressed milk production for two days after the challenge by about 10%, no effect on milk composition could be determined. In a theory proposed by Bauman and Griinari (2003) MFD was related to changes in milk fatty acids profile due to alterations in rumen biohydrogenation of poly-unsaturated fatty acids (PUFA). This would result in production of fatty acids intermediates which are absorbed and elicit direct inhibitory effects on milk fat synthesis. It was demonstrated that the trans10, cis-12 isoform of conjugated linoleic acid (CLA), which increases during dietary induced MFD due to biohydrogenation of 18 carbon PUFA, is a potent inhibitor of milk fat synthesis and secretion (Peterson et al., 2003). Some years later other fatty acids intermediates were examined for their effect on MFD like trans C18:1, especially trans-10 18:1 which is an intermediate in the major pathways of rumen biohydrogenation. It was demonstrated that this fatty acid increases in milk during MFD. This may be considered as a sign but trans-10 18:1 has not direct effect on milk fat synthesis (Lock et al., 2007). However, these results come from experimental conditions and just demonstrate that MFD and SARA could be related because both arise from similar conditions: a diet poor in fibre and rich in concentrate. The question remains whether cows that experienced MFD were really experiencing SARA and in consequence MFD could indeed be considered as a sign of SARA. In order to identify the link between SARA and other disorders, various pathomechanisms have been discussed in the past and clinical trials have shed new light on the potential consequences of SARA. Gozho et al. (2005) were able to show a systemic inflammatory response after SARA was induced by feeding wheat–barley pellets. Similar experiments were able to show a negative influence on dry matter intake (DMI), milk yield and butterfat (Khafipour et al., 2009a). However, SARA induced by feeding alfalfa-pellets did not lead to a systemic inflammatory response, although lipopolysaccharides did increase intraruminally (Khafipour et al., 2009b). This interestingly corresponds to an Italian field study (Cannizzo, 2008). In this study, 12 intensively managed herds were tested for SARA prevalence by means of rumenocentesis. For labelling herds as SARA positive or negative, the earlier-mentioned scheme for calculating sample size was used (Garrett et al., 1999). In herds diagnosed with SARA, a tendency for higher white blood cell counts and higher total protein levels was observed, although within the physiological limits. However, no correlation was observed between SARA and systemic inflammatory response as represented by acute phase proteins, both in individuals and herds classified as having SARA or not. This would again point to the assumption that SARA is not necessarily per se leading to clinically detectable consequences but rather arises in situations of management related stress like mentioned above. These results confirm also that it is probably more accurate to consider SARA as being indicative of individual and herd health problems and not as a herd problem per se. In summary it has to be stated that there is a certain discrepancy between field studies and clinical trials, at least when it comes to clinically detectable consequences. Whilst reports from the field are based on ruminal pH values deriving from actual rations fed, clinical trials often use high proportions of concentrate to create acidotic challenges. It remains to be shown whether SARA as it is actually found in the field is indeed modelled accurately. Field studies show that SARA is not necessarily related to the expected clinical consequences nor does it necessarily evoke a systemic inflammatory response. The question research has to answer in the future is whether the supposed clinical problems are consequences or causes of SARA, or whether they are related to SARA because both conditions arise from the same problem in general management. Independently from inflammation, SARA will have a negative impact on the ruminal fermentation and, subsequently, metabolism. Low ruminal pH will lead to reduced fibre digestion (Ørskov, 1999; Allen, 2000), altered pattern of volatile fatty acids (Cannizzo, 2008; Gianesella, 2007), impaired microbial protein metabolism (Bach et al., 2005; Calsamiglia et al., 2008), altered ruminal microflora (Khafipour et al., 2009a), and consequently exacerbating of negative energy balance (NEB) by less efficient digestion (Jouany, 2006). This corresponds to the findings of Kleen et al. (2009): here, individual cows experiencing SARA showed a significant poorer body condition score and more severe body condition loss around calving. Depression of dry matter intake (DMI) is of importance when it comes to the complex of production diseases that are linked to NEB and ruminal fermentation (Mulligan and Doherty, 2008). SARA is usually reported to depress DMI and the possible mechanisms for this have been reviewed (Allen, 2000; Plaizier et al., 2008). The monitoring of DMI is part of the rumen health control scheme as used by Mulligan et al. (2006). Depression of DMI leads to imbalances in the ruminal metabolism by sorting for concentrates in the ration and insufficient uptake of any nutrient. Effects of SARA on metabolism could therefore be increased in the form of a vicious cycle. As reviewed by Enemark (2008), the economic consequences of SARA are estimated with more than 1 US$ per day and animal. Considering the difficulty to diagnose SARA and associate it with pathological alterations, however, any estimate has to remain speculation. Instead of focusing on diseases of which the pathological pathways are not fully understood, it appears promising to focus on the influence that SARA might have on feed conversion efficiency, DMI, and NEB: a wellfunctioning rumen and consequently a well-functioning metabolism are fundamental to any animal’s health and production.
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The metabolism of the dairy cow is especially delicate and difficult to control; NEB puts any dairy cow at risk in early lactation and the balance between energy use and input is difficult to meet throughout. SARA appears to be an important aspect of this complex and needs to be understood better. 4. Conclusions Based on the current evidence, SARA is best described as a depression of ruminal pH to ≤5.5 if tested by means of rumenocentesis and intensifying to lower pH values, lasting several hours and occurring several times per day, depending on the type and management of feeding. It is certain that SARA is present in a large number of dairy herds, affecting a limited proportion of animals. The prevalence of SARA within and among herds is independent of stage of lactation, production level or management system. It is uncertain, however, what the exact consequences in the individual animal are. SARA will in itself have negative consequences in the individual, especially in terms of feed conversion efficiency; the mutual reinforcing effects it will have with other, simultaneous conditions need a better understanding. The task remains to describe the occurrence of SARA on a herd level: the development of a commercially available system that monitors reticulo-ruminal pH continuously will certainly aid in describing prevalence and incidence more exactly. It may also help in understanding the consequences of SARA better, as the uncertainty regarding its impact on health and economy remains. The detrimental effect on feed efficiency seems to be the most important economic consequence and certainly deserves more attention. Furthermore, research may focus on the question whether SARA has to be understood as a signal differentiating optimal from suboptimal management in dairy herds. Conflict of interest None. References Allen, M.S., 2000. 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