Fermented liquid feed for pigs

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Feb 25, 2008 - Keywords: Pig, Pig feeding, Wet feeding, Fermentation, Liquid diets. Review Methodology: The databases CAB Direct and Web of Science ...
CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2008 3, No. 073

Review

Fermented liquid feed for pigs Peter H. Brooks* Address: School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK. *Correspondence: Email: [email protected] 25 February 2008 4 September 2008

Received: Accepted:

doi: 10.1079/PAVSNNR20083073 The electronic version of this article is the definitive one. It is located here: http://www.cababstractsplus.org/cabreviews g

CAB International 2008 (Online ISSN 1749-8848)

Abstract Liquid feeding systems develop a microflora that usually becomes dominated by lactic acid bacteria (LAB), and this can be beneficial to the health of the pigs. When levels greater than 100 mM lactic acid are generated in liquid feed (LF), this can significantly reduce the numbers of enteropathogens and reduce the incidence of Salmonella. Using fermented co-products from the human food industry or deliberately fermenting LF has the potential to improve gut health and nutrient utilization. The evidence indicates that spontaneous fermentation of LF is unreliable and fails to yield consistently good results. Maintaining a continuous fermentation by retaining a proportion of the feed each day can result in the development of a resident microflora dominated by yeasts. This may compromise both palatability and health and reduce the nutritional value of the feed. Batch fermentation of the cereal portion of the diet using inoculants selected to generate high concentrations of lactic acid has the potential to produce more consistent results. This approach may enable the combination of the preservative and probiotic effects of LAB, while also improving the availability of nutrients in the feed and reducing levels of anti-nutrients and mycotoxins. Accurate assessment of these changes will enable nutritionists to modify raw material specifications and constraints to take advantage of these improvements, and in so doing, improve pig performance and reduce environmental impact. Keywords: Pig, Pig feeding, Wet feeding, Fermentation, Liquid diets Review Methodology: The databases CAB Direct and Web of Science were searched using combinations of search terms. The search was broadened using the ‘related records’ facility in the databases and by tracking citations. Electronic journal collections (Blackwell Synergy; Science Direct) were cross-checked using a variety of search terms, as were industry Web sites that publish technical reports.

Introduction Historically, liquid feeding systems developed in areas where liquid co-products from the human food industry, such as skim milk and whey, were abundant and cheap (e.g. the milk-producing regions of Denmark, The Netherlands, United Kingdom and New Zealand). Until the 1970s, the intrinsic variability of many liquid feed (LF) components and the relatively crude delivery systems often resulted in variable growth rate and carcass composition. Profitability resulted from the low cost of diets rather than from the intrinsic efficiency of the system, or the production of a high-value carcass.

The availability of inexpensive computing and processing capability revolutionized the liquid feeding sector. The development of linear programmes enabled rapid reformulation of diets to take account of variations in the composition of liquid components. At the same time, computer control of liquid feeding systems enabled producers both to maintain nutrient supply by changing diet formulations to reflect differences in nutrient intake and to ration diets with a high level of accuracy, thereby controlling carcass composition. Increasing feed costs, the reduction/removal of antimicrobial growth promoters and the development of quality assurance programmes aimed at reducing the

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Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources

pH

Log10 (CFU/ml)

2

Time

Figure 1 Phases in the fermentation of FLF

incidence of Salmonella in pig meat, are compelling reasons why producers should consider using liquid feeding. This review focuses on developments in the use of fermented LF (FLF) for pigs and on the contribution that this approach can make to increasing nutrient utilization and improving gut health. In this review, LF is defined as a complete, nutritionally balanced diet, prepared from a combination of dry, moist and liquid feed ingredients and/or water, typically containing less than 300 g/kg dry matter per litre [1]. Typically, the feed is prepared centrally on the unit and delivered to the pigs through a system of pipelines and valves. Two main feeding systems are in common use. In the first, feed is delivered in discrete meals and provided in long troughs enabling all the pigs in the pen to eat at the same time. Troughs are usually cleared within 20–30 min of feeding and feed residues are normally flushed from the pipeline between meals. The second (sensor feeding) system uses short troughs, from which only a proportion of the pigs in the pen can eat at any one time and aims to feed pigs as close to ad libitum as possible [2]. The feed delivery lines are continuously charged with feed and deliveries to the troughs are determined automatically by liquid sensors in the troughs. The sensors may be overridden for short periods in the day (and more often at night) to encourage pigs to clear all the feed from the trough and rinse cycles can be programmed to clean the delivery lines. Feeding systems in which food and water are delivered separately to the point of contact with the pigs (e.g. wet-dry feeder systems) are not considered in this review.

LF that has been mixed and delivered to pigs immediately, with very limited opportunity for fermentation, is referred to as non-FLF (NFLF). Feed that, unintentionally or intentionally, has been allowed to ferment for a period of time before feeding, through the action of the indigenous microflora, is referred to as spontaneously FLF (SFLF). Fermentation resulting from the inoculation of LF with selected lactic acid bacteria (LAB) is referred to as inoculated FLF (IFLF).

Microbiology of Liquid Feeding Systems Liquid feeding systems can have a resident microflora of 106–107 cfu/ml [3]. The microflora is derived predominantly from the feed materials used and develops in the system over time. Fermentation of cereal grains, or complete pig feeds, characteristically progresses through three phases. Feed materials mixed with water normally have a pH >6 and, in Phase 1, this permits a rapid proliferation of coliform bacteria [4–8] (Figure 1). Subsequently, fermentation by LAB inhibits pathogenic and spoilage organisms by the production of organic acids (particularly lactic acid), hydrogen peroxide and bacteriocins, as well as by lowering the pH and oxidation–reduction potential [9]. As pH is reduced to ca. pH 4, proliferation of Enterobacteriaceae is prevented and as the acid concentration increases further, such bacteria are excluded (Phase 2) [4, 6, 10, 11]. Subsequently, the LAB population and pH stabilizes, but over time, the yeast concentration of the feed can continue to increase (Phase 3) [6, 12, 13]. Depending on the

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circumstances in the individual system, the pig may receive feed that has reached any point along the continuum. In the preparation of fermented human foods, a portion of a previous successful fermentation is often retained and used as an inoculum for the next batch. This process is referred to as ‘backslopping’ [14]. A similar process occurs (often unintentionally) in liquid feeding systems when residues of previous feeds remain in the system. In sensor feeding systems, the pipelines contain feed for long periods of time (or continuously) and hence the delivery system acts as a fermentation vessel. The ‘backslopping’ process allows for the gradual selection of LAB and results in accelerated fermentation [15]. In pipeline feeding systems, the continual removal and replenishment of feed can result in the development of a stable ecosystem [13–16]. Normally, LAB dominate this flora, especially lactobacilli and leuconostocs [6, 10, 13, 17], limiting any negative effects of the resident microflora. Over a 3-month period, backslopping 10–15% of the feed resulted in an increase in the concentration of lactic acid (7.78–9.00 cfu/ml), proteolytic (2.00–5.98 cfu/ml) and lipolytic bacteria (5.15–7.38 cfu/ml) [13]. A recent study using rRNA gene sequencing of isolates [18] has demonstrated that over time, with backslopping, the species composition in fermented pig feed may vary considerably, even if viable cell counts indicate stable microbial populations. The dominant species and diversity were significantly affected by the raw materials used in the diets. Where problems have been encountered on commercial units, cleaning and disinfection of feeding systems has decreased bacterial counts by 2–3 log units. However, this effect is usually short-lived and bacterial counts often return to the pre-cleaning level within a week [19, 20]. After cleaning there is often an initial ‘bloom’ of coliforms in the feed before the system repopulates with LAB. This can perturb the gastrointestinal flora of pigs consuming the diets, resulting in diarrhoea [7].

FLF and Health If a feeding system frequently reverts to, or stabilizes in Phase 1, the feed can become a vehicle for the transmission of pathogens [20–23]. In a survey of 145 Danish units [24], it was found that the incidence of diarrhoea in both grower and finisher pigs was greater when the feed was at pH 4.6–6.5 than when it was at pH 3.5–4.5. If a system utilizes feed ingredients containing large number of yeasts (e.g. whey or brewery co-products), or stabilizes at late Phase 3 and becomes dominated by yeasts, this may have an adverse effect on pig health and performance [19, 25–29]. Yeast fermentations convert carbohydrate to alcohol, producing carbon dioxide as a byproduct [28]. This reduces the energy value of the feed. In some cases, feeding liquid diets has been implicated in the development of a disease complex that includes haemorrhagic bowel syndrome (HBS), gastrointestinal tympany

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and gastric torsion (volvulus) [19, 25–27]; however, there is disagreement on whether HBS and volvulus are the same condition [30]. Yeasts may impart ‘off-flavours’ to feed. In preference studies, eliminating yeast from fermentations by the addition of 2 g/kg potassium sorbate increased the selection and intake of fermented feed [10]. Pigs fed on large quantities of whey may die from a condition known as ‘whey-bloat’. It was reported [31, 32] that mean intra-gastric pressure of 6 pigs that died from ‘whey bloat’ was 40.83+4.4 mmHg, as compared with 3.5+1.5 mmHg in pigs from other units that had died from unrelated causes. An intra-abdominal pressure of 30 mmHg results in life-threatening multi-organ dysfunction. In Thompson’s study [31–32], death from ‘wheybloat’ did not involve torsion. Notwithstanding the commentary above, liquid feeding generally confers health benefits rather than causing problems. In some studies, the incidence of diarrhoea was reduced significantly when pigs were fed LF or FLF [24, 33], but in others, there was no effect [34]. In two studies [35, 36] diets including whey fermented with LAB did not reduce the incidence of post-weaning diarrhoea. A recent study [37] has shown that feeding IFLF (fermented with Lactobacillus plantarum LQ80) to weaner pigs for 28 days reduced the proportion of chlortetracyclineresistant Escherichia coli from 88.9 to 22.2%. Importantly, this effect was caused by a change in the levels of resistance genes, suggesting that IFLF can control antibioticresistance genes based on an interaction between the LAB and E. coli. A number of surveillance studies reported that the incidence of Salmonella was lower when pigs were fed liquid diets than when they were fed dry meal and, most particularly, dry pelleted diets [23, 38–48]. A study of 359 pig units across Europe found that pigs given whey had 2.6 times lower odds of testing seropositive for Salmonella than pigs not receiving whey [46]. Similarly, in a study of 317 finishing pig herds in the Netherlands [23], automated liquid feeding of food industry co-products was associated with a statistically significant decreased risk of Salmonella infection. A survey in Canada found Salmonella incidence was 6 and 0.8% in herds using dry and liquid feeding, respectively [49]. In addition to these surveillance studies, a large controlled feeding trial [50] found that, compared with dry pellet feeding, LF significantly reduced the percentage of pigs that tested positive for Salmonella at slaughter (meat juice ELISA 16 versus 35%; caecal presence 23 versus 39%; P < 0.05). It is worth noting that the European Food Safety Authority Scientific Panel on Biological Hazards has recognized the contribution that fermented feed can make to the mitigation of risk of Salmonella in pig production [51]. There are also indications that liquid feeding may reduce colonization of the gut with Lawsonia intercellularis [52] and may reduce infection with Brachyspira hyodysenteriae through an effect on the supply of fermentable carbohydrate in the gut [53, 54].

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Table 1 Lactic and acetic acid content of some liquid co-products used for feeding pigs Dry matter (g/kg) Liquid wheat starch Potato steam peelings Cheese whey Wet wheat-distillers grains High moisture corn (maize) Corn distillers solubles

225 139 70 95 750 300

Lactic acid (mM)

Acetic (mM)

NFLF

SFLF

NFLF

SFLF

References

176 64 75 15

189 207 165 84 18 278 IFLF 444 484

83 15 5 1.5

113 36 9 17 19 108

[61] [61] [61] [62] [63] [64]

111

Ensiled fish offal Ensiled chicken offal

LF usually contains ingredients with small particle size, often associated with the development of oesophagogastric ulcers [55]. However, reports on the influence of LF on the incidence of ulceration are contradictory. Incidence was reported to be slightly higher when pigs were fed LF more than three times a day or ad libitum [56], but other authors reported either no effect [57, 58], or a lower prevalence in pigs fed LF [45, 59, 60].

Effect of Fermentation on Microbial ‘Quality’ of LF A number of food industry co-products have been subject to fermentation by LAB and as a result have a low pH and contain significant quantities of lactic acid (Table 1). Lactic acid, and to a lesser extent acetic, generated by LAB fermentations, have been shown to be the key elements in the inhibition of food-borne pathogens [66–71]. The concentration of lactic and acetic acid was demonstrated to be responsible for the reduction of Salmonella in fermented pig feed [72]. At a lactic acid concentration of 200 mM there was a dose-dependent reduction in Salmonella typhimurium as acetic acid concentration increased from 10 to 30 mM. It was suggested that in order to reduce/eliminate Salmonella from feed it was necessary to have a concentration of 150 mM lactic acid or 80 mM acetic acid; with an appropriate pH (below 4.5). Salmonella reduction/exclusion from FLF appears to be the result of fermentation acids rather than bacteriocins produced by LAB [67, 72, 73]. In addition to Salmonella spp., FLF is also effective in excluding a wide range of potentially pathogenic coliform bacteria from FLF [74–76]. The rate of exclusion of enteropathogens from LF is temperature-dependent. At higher temperatures, LAB produces more acid [5, 10, 77, 78]. However, higher temperatures also increase the metabolism of pathogens and, counter-intuitively, increase their death rate. Acidresistant S. typhimurium DT104 : 30 was rapidly excluded from sterile feed fermented for >48 h with Pediococcus pentosaceus; however, the death rate was temperaturedependent. S. typhimurium DT104 : 30 died up to five times faster in feed maintained at 30 C (Dvalue=34–45 min) than in feed maintained at 20 C (Dvalue=137–250 min) [77].

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[65] [65]

This may also explain the observed reduction in diarrhoea reported on commercial units maintaining feed at a higher temperature (24 C) [79]. The death rate of Salmonella in acid feed is also affected by the mineral content. In LF acidified with 150 mM lactic acid, the presence of 50 ppm copper (Cu2+) resulted in a 10-fold increase in the death rate [80]. The effect of added copper varies in different organic matrices. Low inclusion levels of copper (2.5 ppm) had a far greater effect on the death rate of S. typhimurium DT104 : 30 in skim milk than in liquid pig feed [81]. The presence of both copper and zinc ions increased the death rate of Salmonella; but Salmonella survived three times longer in the presence of iron (Fe2+). This effect of Fe2+ may be the result of iron uptake being involved in acid tolerance in Salmonellae [82]. An important practical consideration is the rate at which potential enteropathogens are excluded at the start of the fermentation process. When LF was co-inoculated with S. typhimurium DT104 : 30 and P. pentosaceus the decimal reduction time of Salmonella was significantly greater at 30 C (Dvalue=34–45 min) than at 20 C (Dvalue=137– 250 min) [77]. It was found that a lactic acid concentration of 70 mM was bacteriostatic, but higher levels (>100 mM/ kg) were needed in order to be bactericidal [77].

Effects of FLF on the Gastrointestinal Tract (GIT) The potential benefits of feeding young pigs on LF and FLF were reviewed in 2001 [83]. Young pigs have an insufficiency of gastric acid, which is the first line of defence against bacterial invasion [84, 85]. When pigs are fed dry diets, the use of coarser, non-pelleted meals and/or the addition of organic acids to the feed increases the barrier function of the stomach against pathogens [86–95]. In a number of studies, feeding FLF reduced gastric pH and the number of coliforms in the stomach [10, 95–98]. This is not only because of the concentration of acid but also because of its high concentration in an undissociated form [95, 99]. The relative proportions of organic acids in the feed are reflected in the stomach [87, 89, 95, 98, 100], but generally are not necessarily reflected in the proportions

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in the remainder of the GIT. However, lactic, acetic and propionic acid concentrations in the ileal digesta were significantly higher when feed had been fermented [101]. Post-weaning anorexia can have a significant adverse effect on the villous architecture of the pig. In a number of studies, providing NFLF or FLF has helped to maintain gut architecture [10, 98, 102–107]. This may result from a combination of factors including, improved intake with NFLF or FLF, and reduced viscosity of feed and digesta, alterations to the nutrient supply for the lower gut microbiota and the probiotic or immunostimulatory properties of the LAB present in the FLF. In addition, fermentation has been shown to reduce ANF’s present in soybean meal (SBM) increasing villus height in the duodenum from 416 to 449 mm (P < 0.05) and the villus height:crypt depth ratio from 1.18 to 1.44 (P < 0.05) [108]. It has been demonstrated that increasing digesta viscosity predisposes pigs to coliform proliferation [109, 110]. NFLF and particularly FLF have reduced viscosity [111, 112] and reduce the dry matter content of the digesta [97, 112]. These physico-chemical differences may contribute to the observed changes in the ecophysiology of the pig’s GIT. Generally, feeding FLF does not produce any significant increase in the number of LAB present in the GIT (after the stomach) but it does dramatically reduce the number of coliforms in the lower small intestine, caecum and colon [5, 10, 97, 113, 114]. The ratio of LAB to coliforms in the lower gut of pigs weaned onto NFLF was very similar to that of pigs that continued to suckle the sow. However, when the pigs were weaned onto dry diets there was a significant shift in the ratio towards the coliform bacteria. Conversely, when pigs were weaned onto SFLF the number of coliforms was reduced and the ratio shifted in favour of the LAB [10]. A longitudinal study to measure the effect on gastrointestinal bacterial ecology of SFLF, in particular of its components lactic acid and L . plantarum, showed that fermented feed reduced the Enterobacteriaceae population in the faeces of pigs [113]. The effect on LAB:coliform ratio of grow–finish pigs was influenced by the organism used to ferment the diet [115]. Feeding sows NFLF but more notably IFLF during late gestation and lactation had no effect on the number of LAB in sows’ faeces, but feeding IFLF significantly reduced the number of coliforms shed [116]. Furthermore, the faeces of piglets that suckled sows coliforms (7.5 versus 8.1 log10 cfu/g) than the faeces of piglets suckling sows fed dry feed. The colostrum of sows fed IFLF had increased immunoglobulin activity and increased the mitogenic activity of lymphocytes and enterocytes [116, 117]. A detailed discussion of the reported immunomodulatory effects of LAB is beyond the scope of this review and raises important issues about the legal classification of LAB used to produce IFLF. However, it is clear that the immunomodulatory effects, of LAB depend both on the organism used and the dose [118, 119], and generally

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require continued ingestion. Dose levels required to produce an immunomodulatory effect appear to be of the order 109 cfu. This level is consistent with the daily dose of LAB that would be consumed in FLF.

Limitations of Spontaneous Fermentations Virtually any combination of feed ingredients will ferment if left to steep in water. Almost all raw materials have a natural flora, which includes potentially beneficial LAB and yeasts. Many also have an undesirable microflora, which can include coliforms, salmonellas and moulds. Spontaneous lactic fermentation has been extensively used, and studied, in the production and preservation of a range of fermented human food products [120–123]. The microflora present and the outcome of fermentation varies with the cereal being fermented. The spontaneous fermentation of complete diets has often produced very acceptable results in controlled experiments (Table 2). However, SFLF produced on commercial farms is inconsistent and often fails to generate sufficient lactic acid. We analysed SFLF from 15 Danish units (see [127]) and found the average lactic acid concentration was 62+ 39 mM with only 1 of 15 units exceeding the 100 mM needed to exclude pathogens. Fermentation (24 h at 30 C) of 100 wheat and barley samples from across the UK, produced lactic acid concentrations ranging from 0.14–134.9 mM (mean 59.6+40.0). Only 3% (9 of 300) of fermentations conducted produced more than 75 mM after 24 h fermentation [128]. In other studies, spontaneous fermentation of a mixture of barley and wheat yielded only 40 mM lactic and 13 mM acetic acid (pH 5.0) [126]. Spontaneous fermentation of sorghum produced 47 mM lactic, 51 mM acetic acid and, unusually, 38 mM succinic acid [129]. Thus spontaneous fermentations, which rely on the indigenous flora present on grains, cannot be relied upon to produce bactericidal levels of lactic acid. A number of studies have been undertaken using continuous fermentation (‘backslopping’) of complete diets [4, 5, 12, 13, 24, 34, 73, 98, 125, 130–132]. Although some of these gave good results, it is difficult to obtain a reliable and consistent fermentation. The outcome is also influenced by the substrates used: specifically, their resident microflora and their buffering capacity. For example, a recent study [78] demonstrated that fermenting a cereal mixture with either cheese whey, wet wheat-distillers grains (WWDG), or water, produced diets of a similar pH (4 or less). The fermented end products differed greatly in their acid composition. Despite having the highest concentration of lactic acid (151+2 mM), the whey-based diet contained 106 cfu/g Enterobacteriaceae, whereas in the other diets they were below the limit of detection. The cereal fermented with WWDG had the lowest concentration of lactic acid (24 mM) but contained 117 mM acetic acid and 33 mM succinic acid. This would

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[98] [95]

[114] [126]

Control +4.8 g Boliflor1 /kg +2.0 g formic acid/kg Diets based on fermented wheat

[34]

73 25 24 5 4 22 < 8.8 70 23 n.d. 69 20

36 32 14

28 days 10 weeks

2.2 : 1 2.0 : 1

4 n.d. In vitro

2.75 : 1 2.75 : 1

20 16.1 2.0 : 1

9.3 4.2

6–12 weeks

10.8 8.9

127 110 36 2.5 : 1 2.5 : 1 2.7 : 1 2.7 : 1 25–55 55–120 6–12 weeks 6–12 weeks

3:1 25–90 kg

300 261

122 153b 153 131 213 156 186 111 241 116 0.03 0.22

Lactic Water : feed Age/wt. of pigs

[125]

[124]

SFLF fed at 24 h; SFLFb fed at 84 h SFLF prepared with grain that was fermented 0.31 0.45b 50 41 4 23 38 25 42 5

a

Notes Acetic Lactic Acetic

Lactic

Acetic

SFLF NFLF Dry feed

be likely to have an adverse effect on palatability as acetic acid concentrations above 30 mM have been found to reduce feed intake, particularly in young pigs (Moran and Brooks, unpublished data). Once a poor quality fermentation has developed, it is hard to rectify it. It was not possible to improve SFLF of sub-optimal quality (deliberately produced by backslopping only 5% of the feed and inoculating with E. coli) by daily addition of either a LAB inoculant or a formicacid-containing product [133]. Neither treatment was effective in eliminating the Enterobacteriaceae. Lactic acid concentration was not increased by adding a LAB inoculant to a 5% feed residue of SFLF and was significantly lower (79+16 mM) than when 50% SFLF was retained (backslopped) each day (160+16 mM). When a good quality fermentation had been established, increasing the backslop proportion from 0.2 to 0.33 or 0.42 did not improve the antibacterial properties of the feed [134] and in all cases coliform bacteria were excluded only when the pH remained below 4.0 for a minimum of 24 h. A further issue with ‘backslopping’ is that the acid concentration in the feed fluctuates [5] and when the feed mixture is replenished there is often a period of time during which the acid concentration drops below bacteriostatic levels, allowing Enterobacteriaceae to proliferate until the acid concentration is restored [135] (Figure 2). In some studies, synthetic amino acids added to the diet have been degraded during the fermentation process [34, 136, 137], but in others, no loss was reported [136]. Protein-bound lysine does not appear to be affected [34, 138]. In a large feeding trial [139] there was no loss of synthetic lysine when pigs were fed either SFLF or IFLF (prepared using Pediococcus acidilactici; BactocellTM ). The loss of synthetic lysine is almost certainly a result of the action of the lysine decarboxylase possessed by Salmonella spp. and E. coli [140, 141]. This is supported by the observation that biogenic amines, produced by decarboxylation, increase in some fermented feed [34, 125]. There is some evidence [138] that the coliform bloom that occurs in Stage 1 of the fermentation may be responsible. Rapid acidification of the diet, fermenting only the cereal component of the diet and delaying the addition of synthetic amino acids until the feed has acidified, can overcome this problem [138]. Although the addition of 2.0 g formic acid or 4.8 g Boliflor1 FA 2300S per kg pig LF impeded the blooming of Enterobacteriaceae during the first hours of fermentation [142] did not prevent the loss of synthetic amino acids. The differences between studies may be a reflection of the indigenous LAB microflora present. In a study of potential LAB inoculants for fish silage, it was found that 17% of 77 LAB isolated from fermented fish produced one or more biogenic amines [143]. Most of these were obligatory heterofermentative lactobacilli belonging to the species Lactobacillus sakei and Lactobacillus curvatus. LAB that produce biogenic amines have also been isolated from cider [144]. Therefore, the

AQ4

Table 2 Lactic and acetic acid concentrations (mM) reported in some studies of SFLF

a

References

Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources

a

6

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Peter H. Brooks

AQ6

7

Figure 2 Effect of percentage of FLF retained each day on the lactic acid concentration in continuously FLF (after Niven et al. [129])

selection of potential inoculant LAB should take this into account. IFLF More predictable fermentation can be achieved by inoculating LF with LAB that produce lactic acid rapidly and have a high terminal lactic acid concentration. The prime objective when selecting organisms with which to inoculate LF is that they are capable of producing rapidly high concentrations of lactic acid (>150 mM) with low concentrations of acetic acid (< 30 mM). A high concentration of lactic acid is needed to exclude the Enterobacteriacae from LF and a low level of acetic acid is desirable to maintain palatability, particularly in diets for young pigs. A number of LAB species capable of producing 180–240 mM lactic acid in 24 h with < 30 mM acetic acid have been identified [10, 111, 145]. However, the concentration of acid produced in a given time is dependent upon the availability of soluble carbohydrate, temperature and the buffering capacity of the substrate [5, 77, 111]. Inoculation of a diet with L. plantarum REB1-RifR to give concentration of ca. 108 cfu/ml in the feed resulted in the immediate reduction in the numbers of Enterobacteriaceae and yeasts and they were detected only occasionally through a 70-day trial [12]. However, the addition of an inoculant does not necessarily increase lactic acid production if even a small amount of SFLF is present [142] or if a significant and active indigenous population of LAB have developed previously, e.g. in the case of stored highAQ1 moisture corn [63] (Table 3). An additional benefit would be if the organisms used as inoculants would survive passage through the stomach and duodenum (i.e. were tolerant of low acid concentrations and bile salts) and had beneficial effects on the gut ecosystem. LAB may be selected that restrict the growth of important pathogens either by competition for attachment

sites, by aggregation or by the production of bacteriocins. The ability of the LAB isolates of porcine origin to prevent Salmonella invasion of intestinal epithelial HT-29 cells has been investigated [147] and reductions of between 30% (Lactobacillus pentosus) and 80% (Lactobacillus murinus spp.) observed. Aggregating LAB may have an important defensive role within the gut [148, 149]. Demecˇkova´ [146] isolated 12 strains of aggregating LAB, some of which had the ability to bind to porcine mucin and collagen IV and to adhere to CaCo-2 and IPEC-I cells [150]. These organisms were capable of producing 220+8 mM lactic acid with only 19+3 mM acetic acid in LF. One Lactobacillus salivarius also had an immunomodulatory effect, increasing Ig concentration in sow colostrum and increasing mitogenic activity of lymphocytes and enterocytes [116, 117]. In these and other studies it has been demonstrated that there is vertical transmission of organisms used to ferment feed and/or as probiotics from the feed to the sow and subsequently to her piglets [117, 146, 151–153]. This approach may have significant effects on the initial colonization for the neonatal GIT and the future ecophysiology of the gut. It is beyond the scope of this review to discuss the legal status of inoculants used in LFds, but it should be noted that there are regulatory issues, with some countries affording them Generally Recognized as Safe (GRAS) status, while others require inoculants to complete Zootechnical Product registration (see [154] for a detailed discussion). The situation is particularly confused if claims made for an inoculant might be construed as changing its status from a ‘preservative’ or ‘technical aid’ to ‘probiotic’.

Performance Benefits from FLF In the absence of antibiotic growth promoters, diet acidification is the preferred method of maintaining gut health and biological performance. There is a large body

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Table 3 diets

Examples of organisms used to produce IFLF and the lactic and acetic acid concentrations (mM) produced in

Organism

Lactic

Acetic

Notes

References

Spontaneous Lactobacillus plantarum (PC-81-11-06) and Pediococcus pentosaceus (SHCM-02)1 Spontaneous L. plantarum (PC-81-11-06) and P. pentosaceus (SHCM-02) Spontaneous L. plantarum 342

356 316

57a 103b

Liquid wheat fermented for 24 h

[10]

600 619

80a 110b

Liquid wheat fermented for 48 h

[10]

52 56

76 71

Fermented sorghum and barley (succinic acid was 28 and 68 mmol, respectively)

[129]

90 84 98

22 36 27

Fermented cereal Complete LF Complete LF made with fermented cereal

[139]

Spontaneous P. acidilactici3 P. acidilactici310 Adjulact1

127 142 151 150

43 49 47 31

Spontaneous Bacillus subtilis and/or Lactobacillus acidophilus Lactobacillus salivarius

160 146–179

50 50

Diet based on high moisture corn

[64]

220

39

Lactating sow diet

[146]

Pediococcus acidilactici3 Spontaneous P. acidilactici3

AQ5

[145]

a,b

Means in same study differ at P < 0.05 or more. Alltech Inc., Kentucky, USA. 2 Australian Starter Culture Research Centre Ltd. 3 Bactocell1 Lallemand SA. 1

of literature that demonstrates the production benefits of acidifying pig diets (see reviews [155, 156]). Fermentation with LAB can be viewed as a cost-effective mechanism for generating organic acids in situ rather than adding them to liquid diets. A number of studies (reviewed by Jensen and Mikkelsen [5]) have been conducted comparing pig performance on dry feed, NFLF and SFLF. Results were variable but generally performance was improved when pigs were fed NFLF and improved again when they were fed SFLF. More recent studies continue to produce very variable results. Fermentation generally improves dry matter and protein digestibility by 3–8% [101, 157]. In a Danish study [125] feeding fermented grain in the diet of heavy pigs increased the production value by 11%. The increased productivity was the result of a higher daily gain (33 g/day) and of an improved feed conversion (0.15 FUp/kg gain) and increased profit by DKK56 per place unit/year. Conversely, in a recent UK study, using a fermented barley/wheat mixture in grow–finish diets reduced growth rate from 844 to 818 g/d and increased cost of production from 93.6 to 113.8 p/kg deadweight [139]. The apparent differences are easily explained. Generally, studies have been designed to look for improvements in biological performance rather than to assess potential reductions in cost of production (although that value may have been presented). If NFLF is nutritionally balanced initially, fermentation will improve performance only if it increases feed intake or improves gut health.

If intake is unaffected, it is likely that the biochemical changes produced by fermentation will produce a diet that is less well balanced. Apparent improvements in nutritional value can be counterproductive unless the specification of the fermented diet is adjusted to take these improvements into consideration. For example, in ‘onfarm’ situations we have observed that: 1. An increase in protein digestibility can distort the energy to digestible protein ratio, making the fermented diet less well balanced. In newly weaned pigs, the increase in protein digestibility has been sufficient to produce protein-induced diarrhoea. 2. An increase in available phosphorus (through the action of phytase enzymes) can widen the Ca:P ratio sufficiently to produce a reduction in feed intake (Brooks, unpublished observations). Therefore, it is essential to assess the true nutritional value of fermented components and modify formulation accordingly. For example, attributing the correct available phosphorus and digestible protein values to fermented wheat or fermented soybean, will not necessarily produce any increase in performance, but can significantly reduce cost per kg gain. Pre-treatment of Diet Components Liquid feeding provides an opportunity to modify raw materials prior to feeding. Steeping materials in water for

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Peter H. Brooks

Table 4.

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Some effects of fermentation on the physico-chemical properties of feed ingredients and feeds

Parameter

Effect

References

Protein

Increased proteolysis due to increase in the number of proteolytic bacteria and reduction in pH Crude protein digestibility increased ca. 6% Increased lysine availability through action of LAB and through genetically modified LAB Fermentation increased total protease and trypsin concentrations at the duodenum (8.4 and 52%, respectively) and jejunum (15 and 53%)

[13, 158]

Lysine Trypsin inhibitor Improved DE Fibre Viscosity

A-galactosidases Phosphorus Iron Zinc B-group vitamins

Crude fibre and NDF digestibility increased ca. 6% Reduced by the action of LAB on NSP and particularly the reduction in b-glucans Increased feed intake (17–25%) as a result of steeping and the addition of xylanase Reduced to undetectable levels after 96 h fermentation with LAB Degradation of phytate by natural phytase present (predominantly in cereal grains) and LAB Increased by up to 100%

a period can activate naturally occurring enzymes and these together with the enzymes produced by fermenting organisms can change the nutritional and physicochemical properties of the feed. Some of the reported changes are summarized in Table 4. Cereals and SBM are a major component of pig diets worldwide and there are particular and different opportunities to improve the value of these commodities by fermentation.

Cereals There are a number of biological and practical advantages in fermenting only the cereal fraction of the diet rather than fermenting complete diets [103, 134, 138]. Specifically: 1. pH may reduce more rapidly as cereals have a lower buffering capacity than compound feed. 2. There is less risk of synthetic amino acid loss and of producing undesirable protein breakdown products, such as ammonia and biogenic amines. 3. Cereals have a more constant composition than compound feed, which makes it simpler to optimize the inoculant and develop standard operating procedures for the fermentation system. 4. Fermented cereal can be included as a component in all the diets used on a pig farm unit, meaning that only one fermentation system is required. However, if only the cereal component is fermented, a higher concentration of acid must be generated (in order to compensate for dilution and buffering effects when the complete diet is produced) and this can only be achieved

[101] [159, 160] [108] [161, 162] [101] [112] [163] [63, 164–172] [170]

using selected LAB as inoculants to stabilize the process. The use of fermented grain (usually wheat) as a component of FLF has been reported in a number of studies [17, 98, 125, 126, 134, 139, 173, 174]. Additionally, there is relevant information to be gained from the literature relating to the use of fermented cereals in human diets [123, 158, 170, 175]. Fermentation of grain can increase available lysine content by 250–675%, depending on the grain and the conditions [176]. Fermentation of dehulled maize grains with Lactobacillus brevis and Saccharomyces cerevisiae increased the concentration of lysine and methionine from 0.3 to 1.8 and from 0.05 to 0.42 mg/g, respectively [159]. Endogenous phytase is activated when wheat and barley are steeped and/or fermented with LAB [164, 177, 178]. In one study [164], 17 and 79% of total phytate was degraded within the first 8 h of soaking, the rate being temperature-dependent. In another study, 45% of phytate was degraded in 9 h at room temperature [179]. Maize contains less endogenous phytase and benefits from the addition of exogenous phytase [180]. Most of the phytase activity in cereals is concentrated in the aleurone layer, and materials containing large amounts of phytase (e.g. wheat middlings and bran) can act as phytase donors and release phosphorus and other minerals from materials containing little or no natural phytase [111]. Conversely, heat and solvent processing can deactivate endogenous phytase. Therefore, it is important to be aware of the provenance of raw materials. A topic that has not yet been investigated in depth is the opportunity for using IFLF as a means of reducing mycotoxin. Both yeast (S. cerevisiae) and LAB have potential as mycotoxin decontaminating agents (see review by Shetty and Jesperson [181]). LAB strains have been

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Table 5 Aflatoxin binding abilities of strains of LAB (181) Number of aflatoxin B1 binding strains Percentage of binding1 Isolates

< 15

15–39

40–59

>60

Lactobacillus plantarum Lactobacillus fermentum Lactonacillus spp. Paralactobacillus selangorensis Pediococcus acidilactici Weissela confuse

0 0 0 4 0 0

0 1 1 1 0 1

4 0 0 0 1 0

1 1 0 0 0 0

1

109 Cells incubated in 1 ml of PBS containing 5 mg of aflatoxin B1 for 72 h at 25 C.

identified that are capable of binding more than 60% of aflatoxin B1 (Table 5).

Soybean There are two main advantages to be obtained from fermentation of SBM, namely an increase in protein digestibility and reduction in antinutritional factors (ANFs). There is a long history of improving the nutritional value of soybean for human consumption by fermentation. The most common approach is to cook soybean and then ferment it with Rhizopus spp. (used to produce the traditional fermented food tempeh), or Bacillus spp. (used to produce natto (Japan), thua-nau (Thailand) and dawadawa (West Africa)) and less frequently Aspergillus spp. [182– 184]. Fermentation with these organisms results in an alkaline fermentation (pH>6). Fermentation of autoclaved soybean with Bacillus subtilis (B83) resulted in an almost complete breakdown of all three subunits of b-conglycinin and both polypeptides from glycinin [185]. As a consequence in vitro digestibility was increased from 29 to 33–43%. Fermentation of soybean reduces ANFs, improves villus architecture, reduces diarrhoea and improves the performance of young pigs [108, 186]. Villus height in the duodenum, jejunum and ileum was significantly increased when pigs were fed cooked SBM fermented with B. subtilis [108]. There were morphological differences in the villi with those from pigs fed fermented SBM having longer, rounder, and more tapering villi. Similar results were obtained with LAB fermentation of SBM [186]. These improvements in gut architecture may result from the reduction in ANFs, the improved availability of peptides and free amino acids or changes in fermentation patterns in the gut, e.g. increased butyrate production, which could support improved intestinal growth and cell proliferation. When pigs were fed diets in which 20% full-fat SBM was replaced with cooked soybeans fermented with Rhizopus microsporus or B. subtilis, there was, respectively, an increase in feed intake (13 and 12%), daily gain (18 and 21%) and feed efficiency (3 and 8%) [187]. There was some

evidence that the fermented soybean also reduced the incidence of diarrhoea. In the case of soybean fermented with Rhizopus spp., there is some evidence that resultant product inhibited the adhesion of enterotoxigenic E. coli (ETEC) [188] and increased the uptake of solutes in pigs infected with ETEC. Fermenting SBM with Aspergillus oryzae increased crude protein digestibility from 72 to 84% and this resulted in a significant (P < 0.05) improvement in daily gain and FCR. Fermentation with Aspergillus usamii was also found to reduce phytate to non-detectable levels, with no adverse effects on protein digestibility [172]. Legumes have also been fermented with LAB [165, 186]. Spontaneous LAB fermentation of beans (Phaseolus vulgaris L.) significantly reduced a-galactoside concentration. After 96 h, raffinose concentration was below the limits of detection and stachyose was reduced by more than 90% [165, 189]. Depending on bean variety, spontaneous fermentation reduced trypsin inhibitor activity by 52–82% increased protein digestibility by 15–35% [165, 190]. These results suggest that fermentation could significantly improve the value of legumes used in pig feeding and the process could be particularly beneficial when SBM is used as an ingredient in diets for newly weaned pigs.

Conclusions The review demonstrates that FLF has the potential to improve gut health and nutrient utilization. The evidence indicates that spontaneous fermentations are unreliable and fail to yield consistently good results. Controlling fermentation by using carefully selected inoculants for use in batch fermentation of specific diet components has great potential. Such an approach may enable the combination of both the preservative and the probiotic effects of LAB, while also improving the nutritional value of the components. Fermentation may also be an effective and efficient means of reducing levels of anti-nutrients and mycotoxins. However, the benefits of fermentation can only be achieved by accurate assessment of these changes. This will enable nutritionists to modify raw material

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Peter H. Brooks

specifications and formulation constraints to take advantage of these improvements. By doing this, FLF provides an opportunity to improve pig performance and reduce environmental impact.

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27. Johannsen U, Strijkstra G, Klarmann D, Janthur I. Investigations into enterohaemorrhagic syndrome in pigs. Der Praktische Tierarzt 2000;81(5):440.

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29. Hoofs AIJ, Scholten RHJ. Feeding liquid feed from Vario-mix or using a long trough to growing–finishing pigs. (Brijvoer via Vario-mix of lange trog bij vleesvarkens). Sterksel, Netherlands: Verkensproefbedrijf Zuid- en West-Nederland; 1998. 30. Straw B, Dewey C, Kober J, Henry SC. Factors associated with death due to hemorrhagic bowel syndrome in two large commercial swine farms. Journal of Swine Health and Production 2002;10(2):75–9. 31. Thomson J, Miller W, Wolfenden N, Thomson D. Pressure related abdominal changes in pigs with ‘whey bloat’ – a case report. In: European Society of Veterinary Pathology, 24th Meeting, Edinburgh, Scotland; 2006. p. 134. Available from: http://www.esvp.eu/ESVP_meetings/ Proceedings_2006.pdf 32. Thomson JR, Miller WG, Woolfenden NJ, Thomson D. Pressure-related abdominal changes in pigs with ‘whey bloat’ – a case report. Pig Journal 2007;59:152. 33. Pedersen C, Roos S, Jonsson H, Lindberg JE. Performance, feeding behaviour and microbial diversity in weaned piglets fed liquid diets based on water or wet wheat-distillers grain. Archives of Animal Nutrition 2005;59(3):165–79. 34. Pedersen AØ. Fermented liquid feed for weaners. Report No. 510. The National Committee for Pig Production, Danish Bacon and Meat Council; 2001. Available from: URL: http:// www.danishpigproduction.dk/Research/Research_report/ Nutrition_Weaners/index.aspx?id=b9528922-9453-4a07890a-06fde2c6ff11 35. Amezcua MD, Friendship R, Dewey C, Weese JS, de Lange C, Reid G. Effects on growth performance, feed efficiency, and health of weanling pigs fed fermented liquid whey inoculated with lactic acid bacteria that inhibit Escherichia coli in vitro. Journal of Swine Health and Production 2007;15(6):320–9. 36. Amezcua MD, Friendship R, Dewey C, Weese S, de Lange CF. The effect of feeding fermented liquid whey plus dextrose inoculated with specific lactic acid bacteria of pig origin to weanling pigs challenged with Escherichia coli O149:K91:F4. Veterinary Therapeutics 2007;8(3):209–22. 37. Kobashi Y, Ohmori H, Tajima K, Kawashima T, Uchiyama H. Reduction of chlortetracycline-resistant Escherichia coli in weaned piglets fed fermented liquid feed. Anaerobe AQ2 2008;doi:10.1016/j.anaerobe.2008.07.001. 38. von Altrock A, Schutte A, Hildebrandt G. Results of the German investigation in the EU-project Salmonella in pork (salinpork) – part 1: investigations in the farms. Berliner Und Munchener Tierarztliche Wochenschrift 2000;113(5):191–201. 39. United States Animal Health Association. Report of the committee on food safety. 1999 [updated 1999; cited 14 March 2003]; Available from: URL: http://www.usaha.org/ reports/reports99/r99feed.html

42. van der Wolf PJ, Wolbers WB, Elbers ARW, van der Heijden H, Koppen J, Hunneman WA, et al. Herd level husbandry factors associated with the serological Salmonella prevalence in finishing pig herds in The Netherlands. Veterinary Microbiology 2001;78(3):205–19. 43. van der Wolf PJ, Wong D, Wolbers WB, Elbers ARW, van der Heijden H, van Schie FW, et al. A longitudinal study of Salmonella enterica infections in high- and lowseroprevalence finishing swine herds in the Netherlands. The Veterinary Quarterly 2001;23(3):116–21. 44. Beloeil PA, Fravalo P, Fablet C, Jolly JP, Eveno E, Hascoet Y, et al. Risk factors for Salmonella enterica subsp. enterica shedding by market-age pigs in French farrow-to-finish herds. Preventive Veterinary Medicine 2004;63(1–2):103–20. 45. Hansen CF. Choice of dry feed influences gastric conditions, incidence of Salmonella and performance in growing-finishing pigs [PhD thesis]. The Royal Veterinary and Agricultural University, Copenhagen, Denmark; 2004. 46. Lo Fo Wong DMA, Dahl J, Stege H, van der Wolf PJ, Leontides L, von Altrock A, et al. Herd-level risk factors for subclinical Salmonella infection in European finishing-pig herds. Preventive Veterinary Medicine 2004;62:253–66. 47. Kranker S, Dahl J, Wingstrand A. Bacteriological and serological examination and risk factor analysis of Salmonella occurrence in sow herds, including risk factors for high Salmonella seroprevalence in receiver finishing herds. Berliner Und Munchener Tierarztliche Wochenschrift 2001;114(9–10):350–2. 48. Stege H, Dahl J, Christensen J, Baggesen DL, Nielsen JP, Willeberg P. Subclinical salmonella infection in Danish finishing herds: risk factors. In: Bech-Nielsen S, Nielsen JP, editors. Proceedings of the Second International Symposium on Epidemiology and Control of Salmonella in Pork. Federation of Danish Pig Producers and Slaughterhouses, Copenhagen, Denmark; 1997. p. 148–52. 49. Farzan A, Friendship RM, Dewey CE, Warriner K, Poppe C, Klotins K. Prevalence of Salmonella spp. on Canadian pig farms using liquid or dry-feeding. Preventive Veterinary Medicine 2006;73(4):241–54. 50. MLC. Finishing Pigs: Systems Research Production Trial 1. Dry Versus Liquid Feeding in Two Contrasting Finishing Systems (Fully Slatted Versus Straw Based Housing). Meat and Livestock Commission, Milton Keynes; 2004. Available from: URL: http://www.bpex.org/technical/publications/pdf/ FinishingPigsTrial_1_Report.pdf. 51. EFSA. Opinion of the Scientific Panel on Biological Hazards on Risk assessment and mitigation options of Salmonella in pig production. The EFSA Journal 2006;341:1–131. 52. Boesen HT, Jensen TK, Schmidt AS, Jensen BB, Jensen SM, Moller K. The influence of diet on Lawsonia intracellularis

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Peter H. Brooks colonization in pigs upon experimental challenge. Veterinary Microbiology 2004;103(1–2):35–45. 53. Leser TD, Lindecrona RH, Jensen TK, Jensen BB, Moller K. Changes in bacterial community structure in the colon of pigs fed different experimental diets and after infection with Brachyspira hyodysenteriae. Applied and Environmental Microbiology 2000;66(8):3290–6. 54. Thomsen LE, Knudsen KEB, Jensen TK, Christensen AS, Moller K, Roepstorff A. The effect of fermentable carbohydrates on experimental swine dysentery and whip worm infections in pigs. Veterinary Microbiology 2007;119(2–4):152–63. 55. Wondra KJ, Hancock JD, Behnke KC, Stark CR. Effects of mill type and particle-size uniformity on growth, performance, nutrient digestibility, and stomach morphology in finishing pigs. Journal of Animal Science 1995;73(9):2564–73. 56. Rautiainen E, Hautala M, Saranpa¨a¨ T, Virtala AM. A comparative study of feeder pig units using dry or liquid feeding in the western part of Finland. Part 1: the mortality rate, causes of death and the gastric ulceration. Soumen Ela¨inla¨a¨ka¨rilehti 1991;97:284–96. 57. Chae BJ, Han IK, Kim JH, Yang CJ, Ohh SJ, Rhee YC, et al. Effects of feed processing and feeding methods on growth and carcass traits for growing-finishing pigs. Asian-Aus Journal of Animal Science 1997;10(2):164–9. 58. Ehrensperger F, Jucker H, Pfirter HP, Pohlenz J, Schlatter C. Influence of feed characteristics on the occurrence of oesophagogastric ulcers and on fattening of pigs. (Einfluss der Futterbeschaffenheit auf das Auftreten oesophagogastrischer Geschwure und auf die Mastleistung beim Schwein). Zentralblatt fur Veterinarmedizin A 1976;23(4):265–76. 59. Robertson ID, Accioly JM, Moore KM, Driesen SJ, Pethick DW, Hampson DJ. Risk factors for gastric ulcers in Australian pigs at slaughter. Preventive Veterinary Medicine 2002;53(4):293–303. 60. Quemere P, Castaing J, Chastanet JP, Latimier P, Saulnier J, Willequet F, et al. Effect of the form of feed presentation in meat pigs. 1. Comparison of dry, liquid and pelleted meal. Results of an ITP-AGPM/ITCF-EDF-SEREP trial conducted by the GEAPORC group. (Influence de la forme de pre´sentation de l’aliment aux porcs charcutiers: 1. Comparaison farine se`che, soupe, granule´. Re´sultats d’un essai ITP- AGPM/ITCF-EDF-SEREP, concerte´ dans le cadre de GEAPORC). Journe´es de la Recherche Porcine en France 1988(20):351–60. 61. Scholten RHJ, Rijnen MMJA, Schrama JW, Boer H, den Hartog LA, van der Peet-Schering CMC, et al. Fermentation of liquid coproducts and liquid compound diets: Part 2. Effects on pH, acid-binding capacity, organic acids and ethanol during a 6-day storage period. Journal of Animal Physiology and Animal Nutrition 2001;85(5–6):124–34. 62. Pedersen C, Jonsson H, Lindberg JE, Roos S. Microbiological characterization of wet wheat distillers’ grain, with focus on isolation of lactobacilli with potential as probiotics. Applied and Environmental Microbiology 2004;70(3):1522–7. 63. Niven SJ, Zhu C, Columbus D, Pluske JR, de Lange CFM. Impact of controlled fermentation and steeping of high moisture corn on its nutritional value for pigs. Livestock Science 2007;109(1–3):166–9.

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64. de Lange CFM, Zhu CH, Niven SJ. Effective application of enzymes and microbes to enhance the nutritional value of pig feed ingredients: a case for liquid feeding. 2007 [updated 2007; cited June 27 2007]. Available from: URL: http:// www.engormix.com/e_articles_view.asp?art= 538&AREA=POR-141. 65. Lassen TM. Lactic-acid fermentation of fish offal and chicken by-product with different starter cultures. Agricultural Science in Finland 1995;4(1):19–26. 66. Adams MR, Hall CJ. Growth inhibition of food-borne pathogens by lactic and acetic acids and their mixtures. International Journal of Food Science and Technology 1988;23:287–92. 67. de Keersmaecker SCJ, Verhoeven TLA, Desair J, Marchal K, Vanderleyden J, Nagy I. Strong antimicrobial activity of Lactobacillus rhamnosus GG against Salmonella typhimurium is due to accumulation of lactic acid. FEMS Microbiology Letters 2006;259(1):89–96. 68. Rubin HE, Nerad T, Vaughan F. Lactate acid inhibition of Salmonella typhimurium in yogurt. Journal of Dairy Science 1982;65(2):197–203. 69. Rubin HE, Vaughan F. Elucidation of the inhibitory factors of yogurt against Salmonella typhimurium. Journal of Dairy Science 1979;62(12):1873–9. 70. Russell JB. Another explanation for the toxicity of fermentation acids at low pH – anion accumulation versus uncoupling. Journal of Applied Bacteriology. 1992;73(5):363–70. 71. Doores S. Organic acids. In: Davidson PM, Branan AL, editors. Antimicrobials in Foods. Macel Dekker, New York; 1993. p. 95–127. 72. van Winsen RL, Lipman LJA, Biesterveld S, Urlings BAP, Snijders JMA, van Knapen F. Mechanism of Salmonella reduction in fermented pig feed. Journal of the Science of Food and Agriculture 2001;81(3):342–6. 73. Geary TM, Brooks PH, Beal JD, Campbell A. Effect on weaner pig performance and diet microbiology of feeding a liquid diet acidified to pH 4 with either lactic acid or through fermentation with Pediococcus acidilactici. Journal of the Science of Food and Agriculture 1999;79(4):633–40. 74. Moran CA, Beal JD, Kuri V, Campbell A, Brooks PH. Survival of pathogenic E. coli in fermented liquid feed. In: XV Congreso – LatinoAmericano de Microbiologia y XXXI Congreso Nacional de Micobiologia at Merida, 9–13 April 2000, Yucatan, Mexico; 2000. 75. Beal JD, Moran C, Brooks PH. Fermented liquid feed: the potential of eliminating enteropathogens from feed. In: Leontides L, editor. Safe Pork The 5th International Symposium on the Epidemiology and Control of Foodbourne Pathogens in Pork, 1–4 October 2003, Hersonissos, Crete. School of Veterinary Medicine, University of Thessaly, Greece; 2003. p. 155–7. 76. Beal JD, Moran CA, Campbell A, Brooks PH. The survival of potentially pathogenic E. coli in fermented liquid feed. In: Lindberg JE, Ogle B, editors. Digestive Physiology of Pigs. CABI Publishing, Wallingford, Oxford; 2001. p. 351–3. 77. Beal JD, Niven SJ, Campbell A, Brooks PH. The effect of temperature on the growth and persistence of Salmonella in fermented liquid pig feed. International Journal of Food Microbiology 2002;79(1–2):99–104.

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78. Lyberg K, Olstorpe M, Passoth V, Schnu¨rer J, Lindberg JE. Biochemical and microbiological properties of a cereal mix fermented with whey, wet wheat distillers’ grain or water at different temperatures. Animal Feed Science and Technology 2008;144:137–48. 79. Pedersen AØ, Ibsen MS. Prevalence of diarrhoea in growers and finishers in relation to uncontrolled fermentation of liquid feed: Report No. 635. The National Committee for Pig Production, Danish Bacon and Meat Council, Copenhagen; 2003 [updated 2003; cited 2 June 2005]; Available from: URL: http://www.danishpigproduction.dk/Research/ Research_report/Nutrition_Finishers/Report_635.html. 80. Beal JD, Niven SJ, Campbell A, Brooks PH. The effect of copper on the death rate of Salmonella typhimurium DT 104 : 30 in food substrates acidified with organic acids. Letters in Applied Microbiology 2003;38:8–12. 81. Beal JD, Brooks PH, Baron F. The effect of copper, zinc and iron on the death rate of salmonella under acid conditions. In: Proceedings of the 6th International Symposium on the Epidemiology and Control of Foodborne Pathogens in Pork, DoubleTree Hotel, Rohnert Park, California, 6–9 September. Pork Service Center, P. O. Box 9114, Des Moines, IA; 2005. p. 154–6. 82. Foster JW. Low pH adaptation and the acid tolerance response of Salmonella typhimurium. Critical Reviews in Microbiology 1995;21(4):215–37. 83. Brooks PH, Moran CA, Beal JD, Demecˇkova´ V, Campbell A. Liquid feeding for the young piglet. In: Varley MA, Wiseman J, editors. The Weaner Pig: Nutrition and Management. CABI Publishing Wallingford, UK; 2001. p. 153–78. 84. Smith HW, Jones JET. Observations on the alimentary tract and its bacterial flora in healthy and diseased pigs. Journal of Pathological Bacteriology 1963;86:387–412. 85. Cranwell PD, Noakes DE, Hill KJ. Gastric secretion and fermentation in the suckling pig. The British Journal of Nutrition 1976;36:71–86. 86. Hansen CF, Kjærsgaard HD, Knudsen KEB, Jensen BB. Effect of meal feed, coarse grinding of pelleted feed and Bacona FormiVækst on Salmonella, gastro-intestinal health and productivity of finishers: Report No. 534. The National Committee for Pig Production, Danish Bacon and Meat Council, Copenhagen; 2001. [updated 2001; cited 2 June 2005]. Available from: URL: http://www. danishpigproduction.dk/Research/Research_report/ Nutrition_Finishers/Report_534.html. 87. Hansen CF, Riis AL, Bresson S, Hojbjerg O, Jensen BB. Feeding organic acids enhances the barrier function against pathogenic bacteria of the piglet stomach. Livestock Science 2007;108(1–3):206–9. 88. Mikkelsen LL, Hojberg O, Jensen BB. Coarse structured feed stimulates members of the genera Lactobacillus and Mitsuokella as well as propionate and butyrate producers in the pig stomach. Livestock Science 2007;109(1–3):153–6. 89. Mikkelsen LL, Jensen BB. The stomach as a barrier that reduces the occurrence of pathogenic bacteria in pigs. In: Ball RO, editor. Proceedings of the 9th International Symposium on the Digestive Physiology of the Pig, 14–17 May 2003, Banff, AB, Canada. University of Alberta, Edmonton; 2003. p. 66–8. 90. Mikkelsen LL, Naughton PJ, Hedemann MS, Jensen BB. Effects of physical properties of feed on microbial ecology and survival of Salmonella enterica Serovar Typhimurium in

the pig gastrointestinal tract. Applied and Environmental Microbiology 2004;70(6):3485–92. 91. Bosi P, Jung HJ, Han IK, Perini S, Cacciavillani JA, Casini L, et al. Effects of dietary buffering characteristics and protected or unprotected acids on piglet growth, digestibility and characteristics of gut content. Asian-Australasian Journal of Animal Sciences 1999;12(7):1104–10. 92. Canibe N, Hojberg O, Hojsgaard S, Jensen BB. Feed physical form and formic acid addition to the feed affect the gastrointestinal ecology and growth performance of growing pigs. Journal of Animal Science 2005;83(6):1287–302. 93. Canibe N, Steien SH, Overland M, Jensen BB. Effect of K-diformate in starter diets on acidity, microbiota, and the amount of organic acids in the digestive tract of piglets, and on gastric alterations. Journal of Animal Science 2001;79(8):2123–33. 94. Jørgensen L, Kjærsgaard HD, Wachmann H, Jensen BB, Bach Knudsen KE. Weaner feed that reduces Salmonella: the effects of the form of the feed and of addition of lactic acid on the prevalence of Salmonella, Lawsonia, gastro-intestinal health, and productivity. Report No. 543. The National Committee for Pig Production, Danish Bacon and Meat Council; 2002 [updated 2002; cited 16 July 2002]. Available from: URL: http://www.danskeslagterier.dk/ view.asp?ID=1477. 95. van Winsen RL, Urlings BAP, Lipman LJA, Snijders JMA, Keuzenkamp D, Verheijden JHM, et al. Effect of fermented feed on the microbial population of the gastrointestinal tracts of pigs. Applied and Environmental Microbiology 2001;67(7):3071–6. 96. Mikkelsen LL, Jensen BB. Effect of fermented liquid feed (FLF) on growth performance and microbial activity in the gastrointestinal tract of weaned piglets. In: Laplace J-P, Fevrier C, Barbeau A, editors. Digestive Physiology in Pigs. EAAP Publication No. 88, INRA, Paris; 1997. p. 639–42. 97. Canibe N, Jensen BB. Fermented and nonfermented liquid feed to growing pigs: effect on aspects of gastrointestinal ecology and growth performance. Journal of Animal Science 2003;81(8):2019–31. 98. Scholten RHJ, van der Peet-Schwering CMC, den Hartog LA, Balk M, Schrama JW, Verstegen MWA. Fermented wheat in liquid diets: effects on gastrointestinal characteristics in weanling piglets. Journal of Animal Science 2002;80(5):1179–86. 99. Russell JB, Diez-Gonzalez F. The effects of fermentation acids on bacterial growth. Advances in Microbial Physiology 1998;39:205–34. 100. Mikkelsen LL, Jensen BB. Performance and microbial activity in the gastrointestinal tract of piglets fed fermented liquid feed at weaning. Journal of Animal and Feed Sciences. 1998;7(Supplement 1):211–5. 101. Hong TTT, Lindberg JE. Effect of cooking and fermentation of a pig diet on gut environment and digestibility in growing pigs. Livestock Science 2007;109(1–3):135–7. 102. Deprez P, Deroose P, Van den Hende C, Muylle E, Oyaert W. Liquid versus dry feeding in weaned piglets: the influence on small intestinal morphology. Journal of Veterinary Medicine 1987;34:254–9. 103. Scholten RHJ, van der Peet-Schwering CMC, Verstegen MWA, den Hartog LA, Schrama JW, Vesseur PC. Fermented co-products and fermented compound diets for

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Peter H. Brooks pigs: a review. Animal Feed Science and Technology 1999;82(1–2):1–19. 104. da Silva CA, Kronka RN, Thomaz MC, Kronka SN, Soto WC, de Carvalho LE. Wet feeding and water and rations with sweetener for weaned 21-d old piglets and its effects on intestinal histology and enzymatic development. Revista Brasileira De Zootecnia-Brazilian Journal of Animal Science 2001;30(3):794–801. 105. Hurst D. The influence of liquid feeding on gastrointestinal adaptation, growth and performance in the growing pig [PhD thesis]. Imperial College at Wye, University of London, Ashford, Kent; 2002. 106. Hurst D, Lean IJ, Hall AD. The effects of liquid feed on the small intestine mucosa and performance of piglets at 28 days postweaning. In: Proceedings of the British Society of Animal Science 2001. British Society of Animal Science, Penicuik, Scotland; 2001. p. 162. Available from: URL: http:// www.bsas.org.uk/downloads/annlproc/Pdf2001/161.pdf 107. Hurst D, Lean IJ, Hall AD. The effects of liquid feed on the small intestine mucosa and performance of finishing pigs at different water to feed ratios. In: Proceedings of the British Society of Animal Science 2001. British Society of Animal Science, Penicuik, Scotland; 2001. p. 161. Available from: URL: http://www.bsas.org.uk/downloads/annlproc/Pdf2001/ 162.pdf

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Epidemiology and Control of Foodborne Pathogens in Pork, DoubleTree Hotel, Rohnert Park, California, 6–9 September 2005. Pork Service Center, P. O. Box 9114, Des Moines, IA; 2005. p. 149–52. 116. Demecˇkova´ V, Kelly D, Coutts AGP, Brooks PH, Campbell A. The effect of fermented liquid feeding on the faecal microbiology and colostrum quality of farrowing sows. International Journal of Food Microbiology 2002;79(1–2): 85–97. 117. Demecˇkova´ V, Tsourgiannis CA, Brooks PH. Feeding fermented liquid feed to the gestating sow can reduce pathogen challenge in the neonatal environment. In: Leontides L, editor. Safe Pork The 5th International Symposium on the Epidemiology and Control of Foodbourne Pathogens in Pork, 1–4 October 2003, Hersonissos, Crete. School of Veterinary Medicine, University of Thessaly, Greece; 2003. p. 140–2. 118. Donnet-Hughes A, Rochat F, Serrant P, Aeschlimann JM, Schiffrin EJ. Modulation of nonspecific mechanisms of defense by lactic acid bacteria: effective dose. Journal of Dairy Science 1999;82(5):863–9. 119. Gill HS, Rutherfurd KJ. Viability and dose-response studies on the effects of the immunoenhancing lactic acid bacterium Lactobacillus rhamnosus in mice. The British Journal of Nutrition 2001;86(2):285–9.

108. Feng J, Liu X, Xu ZR, Lu YP, Liu YY. Effect of fermented soybean meal on intestinal morphology and digestive enzyme activities in weaned piglets. Digestive Diseases and Sciences 2007;52(8):1845–50.

120. Caplice E, Fitzgerald GF. Food fermentations: role of microorganisms in food production and preservation. International Journal of Food Microbiology 1999; 50(1–2):131–49.

109. Hopwood DE, Pethick DW, Hampson DJ. Increasing the viscosity of the intestinal contents stimulates proliferation of enterotoxigenic Escherichia coli and Brachyspira pilosicoli in weaner pigs. The British Journal of Nutrition 2002;88(5):523–32.

121. Nout MJR. Fermented foods and food safety. Food Research International 1994;27(3):291–8.

110. McDonald DE, Pethick DW, Mullan BP, Hampson DJ. Increasing viscosity of the intestinal contents alters small intestinal structure and intestinal growth, and stimulates proliferation of enterotoxigenic Escherichia coli in newly-weaned pigs. The British Journal of Nutrition 2001;86(4):487–98. 111. Brooks PH, Beal JD, Niven SJ, Campbell A. Fermented liquid feed for pigs: potential for improving productivity and reducing environmental impact. DEFRA Project Number LS0812. University of Plymouth, Plymouth; 2002. 112. Christensen P, Glitso V, Pettersson D, Wischmann B. Fibre degrading enzymes and Lactobacillus plantarum influence liquid feed characteristics and the solubility of fibre components and dry matter in vitro. Livestock Science 2007;109(1–3):100–3. 113. van Winsen RL, Keuzenkamp D, Urlings BAP, Lipman LJA, Snijders JAM, Verheijden JHM, et al. Effect of fermented feed on shedding of Enterobacteriaceae by fattening pigs. Veterinary Microbiology 2002;87(3):267–76. 114. Hansen LL, Mikkelsen LL, Agerhem H, Laue A, Jensen MT, Jensen BB. Effect of fermented liquid food and zinc bacitracin on microbial metabolism in the gut and sensoric profile of M. longissimus dorsi from entire male and female pigs. Animal Science 2000;71:65–80. 115. Brooks PH, Sofronidou S, Beal JD. The effect on biological performance and faecal microbiology of feeding finishing pigs on liquid diets fermented with lactic acid bacteria. In: Proceedings of the 6th International Symposium on the

122. Hammes WP, Tichaczek PS. The potential of lactic-acid bacteria for the production of safe and wholesome food. Zeitschrift Fur Lebensmittel-Untersuchung Und-Forschung 1994;198(3):193–201. 123. Corsetti A, Settanni L. Lactobacilli in sourdough fermentation. Food Research International 2007;40(5):539–58. 124. Smith P. A comparison of dry, wet and soaked meal for fattening bacon pigs. Experimental Husbandry 1976;30:87–94. 125. Pedersen AØ, Maribo H, Aaslyng MD, Jensen BB, Hansen ID. Fermented grain in liquid feed for heavy pigs. Report No. 547. The National Committee for Pig Production, Danish Bacon and Meat Council, Copenhagen; 2002. Available from: URL: http://www.danishpigproduction.dk/Research/ Research_report/Nutrition_Finishers/index.aspx?id= e6af8aff-eb86-4ba7-8.92-40d176e51cb4 126. Canibe N, Jensen BB. Fermented liquid feed and fermented grain to piglets- effect on gastrointestinal ecology and growth performance. Livestock Science 2007;108(1–3):198–201. 127. Anon. Advantages of controlled feremented liquid feed. Pig Progress 2005:14–6. 128. Beal JD, Niven SJ, Brooks PH, Gill BP. Variation in short chain fatty acid and ethanol concentration resulting from the natural fermentation of wheat and barley for inclusion in liquid diets for pigs. Journal of the Science of Food and Agriculture 2005;85(3):433–40. 129. Swanson M. Optimisation of sorghum-based fermented liquid feed for grower-finisher pigs [MRurSci.]. University of New England, Armidale, Australia; 2005.

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130. Geary TM, Brooks PH, Morgan DT, Campbell A, Russell PJ. Performance of weaner pigs fed ad libitum with liquid feed at different dry matter concentrations. Journal of the Science of Food and Agriculture 1996;72(1):17–24. 131. Hansen LL, Mikkelsen LL, Agerhem H, Laue A, Jensen MT, Jensen BB. Effect of fermented liquid feed and zinc bacitracin on microbial metabolism in the gut and sensoric profile of m.longissimus dorsi from entire male and female pigs. In: Bonneau M, Lundstrom K, Malmfors B, editors. Boat Taint in Entir Male Pigs. EAAP Publication No. 92. Wageningen Pers, Wageningen, The Netherlands; 1997. p. 92–6. 132. Lawlor PG, Lynch PB, Gardiner GE, Caffrey PJ, O’Doherty JV. Effect of liquid feeding weaned pigs on growth performance to harvest. Journal of Animal Science 2002;80(7):1725–35. 133. Canibe N, Miettinen H, Jensen BB. Effect of adding Lactobacillus plantarum or a formic acid containing-product to fermented liquid feed on gastrointestinal ecology and growth AQ2 performance of piglets. Livestock Science 2007; in press. 134. Moran CA, Scholten RHJ, Tricarico JM, Brooks PH, Verstegen MWA. Fermentation of wheat: effects of backslopping different proportions of pre-fermented wheat on the microbialand chemical composition. Archives of Animal Nutrition 2006;60(2):158–69.

response of Salmonella typhimurium. Molecular Microbiology 1996;20(3):605–11. 142. Canibe N, Virtanen E, Jensen BB. Effect of acid addition to pig liquid feed on its microbial and nutritional characteristics. Livestock Science 2007;108(1–3):202–5. 143. Dapkevicius MLNE, Nout MJR, Rombouts FM, Houben JH, Wymenga W. Biogenic amine formation and degradation by potential fish silage starter microorganisms. International Journal of Food Microbiology 2000;57(1–2):107–14. 144. Garai G, Duenas MT, Irastorza A, Moreno-Arribas MV. Biogenic amine production by lactic acid bacteria isolated from cider. Letters in Applied Microbiology 2007;45(5):473–8. 145. Missotten JAM, Michiels J, Goris J, Herman L, Heyndrickx M, De Smet S, et al. Screening of two probiotic products for use in fermented liquid feed. Livestock Science 2007;108(1–3):232–5. 146. Demecˇkova´ V. Benefits of fermented liquid diets for sows and their piglets [PhD thesis]. University of Plymouth, Plymouth; 2003. 147. Casey PG, Casey GD, Gardiner GE, Tangney M, Stanton C, Ross RP, et al. Isolation and characterization of anti-Salmonella lactic acid bacteria from the porcine gastrointestinal tract. Letters in Applied Microbiology 2004. AQ3

135. Niven SJ, Beal JD, Campbell A, Brooks PH. Consequences of backslopping on lactic acid and acetic acid production in fermented liquid feed for pigs. In: Frontiers in Microbial Fermentation and Preservation; 9–11 January 2002 Society for Applied Microbiology; Wageningen, The Netherlands; 2002.

148. Kmet V, Callegari ML, Bottazzi V, Morelli L. Aggregationpromoting factor in pig intestinal Lactobacillus strains. Letters in Applied Microbiology 1995;21351–3.

136. Pedersen AØ, Maribo H, Canibe N, Hansen ID, Aaslyng MD. Fermented liquid feed for finishers – mixed on-farm with whey not containing formic acid. Report No. 566. The National Committee for Pig Production, Copenhagen, Denmark; 2002 [updated 25 July 2002]. Available from: URL: http:// www.danishpigproduction.dk/Research/Research_report/ Nutrition_Finishers/Report_566.html

150. Demecˇkova´ V, Beal J, Brooks P. Screening and selection of porcine lactic acid bacteria as potential GI tract colonisers. The 4th International Yakult Symposium: The Gut, Immune Modulation and Probiotics, 22–23 November 2007, Palazzo della Gran Guardia, Verona, Italy; 2007.

137. Pedersen AØ, Maribo H, Kranker S, Canibe N, Hansen ID, Aaslyng MD. Fermented liquid feed for finishers – pelleted feed. Report No. 567. The National Committee for Pig Production, Copenhagen, Denmark; 2002 [updated 25 July 2002]. Available from: URL: http://www. danishpigproduction.dk/Research/Research_report/ Nutrition_Finishers/Report_567.html 138. Niven SJ, Beal JD, Brooks PH. The effect of controlled fermentation on the fate of synthetic lysine in liquid diets for pigs. Animal Feed Science and Technology 2006;129(3–4):304–15. 139. MLC. Finishing Pigs: Systems Research Production Trial 3. Final Report. Controlled fermentation of liquid diets fed to pigs in two contrasting finishing systems (fully slatted versus straw based housing. Meat and Livestock Commission, Milton Keynes; 2005. Available from: URL: http:// www.bpex.org/technical/publications/pdf/ FinishingPigsTrial_3_Report.pdf

149. Kmet V, Lucchini F. Aggregation of sow lactobacilli with diarrhoeagenic Escherichia coli. Journal of Veterinary Medicine 1999;46:683–7.

151. Demecˇkova´ V, Tsourgiannis CA, Brooks PH. Beneficial changes of Lactobacilli, coliforms and E. coli numbers in the feces of farrowing primiparous sows, achieved by fermented liquid feed, positively affect subsequent neonatal colonisation. In: Ball RO, editor. Proceedings of the 9th International Symposium on the Digestive Physiology of the Pig. University of Alberta, Edmonton, Banff, AB, Canada; 2003. p. 84–6. 152. Demecˇkova´ V, Tsourgiannis CA, Brooks PH. Effect on average daily feed intake during lactation and piglet growth during the first 2 weeks of life of feeding sows fermented liquid feed, non-fermented liquid feed or dry feed. In: Proceedings of the British Society of Animal Science 2003. British Society of Animal Science, Penicuik, Scotland; 2003. p. 70. Available from: URL: http://www.bsas.org.uk/ downloads/annlproc/Pdf2003/070.pdf 153. Taras D, Vahjen W, Simon O. Probiotics in pigs – modulation of their intestinal distribution and of their impact on health and performance. Livestock Science 2007;108(1–3):229–31.

140. Meng SY, Bennett GN. Nucleotide sequence of the Escherichia coli cad operon – a system for neutralization of low extracellular pH. Journal of Bacteriology 1992;174(8):2659–69.

154. Brooks PH, Beal JD, Demecˇkova´ V, Niven SJ. Probiotics for pigs – and beyond. In: van Vuuren AM, Rochet B, editors. Role of Probiotics in Animal Nutrition and their Link to the Demands of European Consumers. ID-Lelystad Report 03/ 0002713, Lelystad, The Netherlands; 2003. p. 49–59.

141. Park YK, Bearson B, Bang SH, Bang IS, Foster JW. Internal pH crisis, lysine decarboxylase and the acid tolerance

155. Partanen K. Organic acids – their efficacy and modes of action in pigs. In: Piva A, Bach Knudsen KE, Lindberg JE,

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Peter H. Brooks editors. Gut Environment of the Pig. Nottingham University Press, Nottingham, UK; 2001. p. 201–17. 156. Partanen KH, Mroz Z. Organic acids for performance enhancement in pig diets. Nutrition Research Reviews 1999;12(1):117–45. 157. Dung NNX, Manh LH, Ogle B. Effects of fermented liquid feeds on the performance, digestibility, nitrogen retention and plasma urea nitrogen (PUN) of growing-finishing pigs. Livestock Research for Rural Development [serial on the Internet]. 2005; 17(9). Available from: URL: http:// www.cipav.org.co/lrrd/lrrd17/9/xdun17102.htm 158. Haard NF, Odunfa SA, Lee C-H, Quintero-Ramirez R, Lorence-Quin˜ones A, Wacher-Radarte C. Fermented Cereals: A Global Perspective. Food and Agriculture Organization of the United Nations, Rome; 1999. Available from: URL: http://www.fao.org/docrep/x2184e/ x2184e00.HTM 159. Teniola OD, Odunfa SA. The effects of processing methods on the levels of lysine, methionine and the general acceptability of ogi processed using starter cultures. International Journal of Food Microbiology 2001;63(1–2):1–9. 160. Cahyanto MN, Kawasaki H, Nagashio M, Fujiyama K, Seki T. Construction of Lactobacillus plantarum strain with enhanced L-lysine yield. Journal of Applied Microbiology 2007;102(3):674–9. 161. Choct M, Selby EAD, Cadogan DJ, Campbell RG. Effects of particle size, processing, and dry or liquid feeding on performance of piglets. Australian Journal of Agricultural Research 2004;52(2):237–45. 162. Barber J, Brooks PH, Carpenter JL. The effects of water to food ratio on the digestibility, digestible energy and nitrogen retention of a grower ration. Animal Production 1991;52 : 601 (Abstr.). 163. Choct M, Selby EAD, Cadogan DJ, Campbell RG. Effect of liquid to feed ratio, steeping time, and enzyme supplementation on the performance of weaner pigs. Australian Journal of Agricultural Research 2004;55(2):247–52. 164. Carlson D, Poulsen HD. Phytate degradation in soaked and fermented liquid feed – effect of diet, time of soaking, heat treatment, phytase activity, pH and temperature. Animal Feed Science and Technology 2003;103:141–54.

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170. Svanberg U, Lorri W. Fermentation and nutrient availability. Food Control 1997;8(5–6):319–27. 171. Valaja J, Plaami S, Siljander-Rasi H. Effect of microbial phytase on digestibility and utilisation of phosphorus and protein in pigs fed wet barley protein with fibre. Animal Feed Science and Technology 1998;72(3–4):221–33. 172. Matsui K. Relationship between mineral availabilities and dietary phytate in animals. Animal Science Journal 2002;73:21–8. 173. Skrede G, Herstad O, Sahlstrom S, Holck A, Slinde E, Skrede A. Effects of lactic acid fermentation on wheat and barley carbohydrate composition and production performance in the chicken. Animal Feed Science and Technology 2003;105(1–4):135–48. 174. Skrede G, Storebakken T, Skrede A, Sahlstrom S, Sorensen M, Shearer KD, et al. Lactic acid fermentation of wheat and barley whole meal flours improves digestibility of nutrients and energy in Atlantic salmon (Salmo salar L.) diets. Aquaculture. 2002;210(1–4):305–21. 175. Zotta T, Ricciardi A, Parente E. Enzymatic activities of lactic acid bacteria isolated from Cornetto di Matera sourdoughs. International Journal of Food Microbiology 2007;115(2): 165–72. 176. Hamad AM, Fields ML. Evaluation of the protein quality and available lysine of germinated and fermented cereals. Journal of Food Science. 1979;44(2):456–9. 177. Nasi JM, Helander EH, Partanen KH. Availability for growing pigs of minerals and protein of a high phytate barleyrapeseed meal diet treated with aspergillus-niger phytase or soaked with whey. Animal Feed Science and Technology 1995;56(1–2):83–98. 178. Nasi M, Helander E. Effects of microbial phytase supplementation and soaking of barley soybean-meal on availability of plant phosphorus for growing pigs. Acta Agricultural Scandinavica: Section A, Animal Science 1994;44(2):79–86. 179. Skoglund E, Larsen T, Sandberg AS. Comparison between steeping and pelleting a mixed diet at different calcium levels on phytate degradation in pigs. Canadian Journal of Animal Science 1997;77(3):471–7.

165. Shimelis EA, Rakshit SK. Influence of natural and controlled fermentations on a-galactosides, antinutrients and protein digestibility of beans (Phaseolus vulgaris L.). International Journal of Food Science and Technology 2008;43(4):658–65.

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186. Wang NF, Chen Q, Le GW, Shi YH, Sun J. Effect of lactic acid fermented soyabean meal on the growth performance, intestinal microflora and morphology of weaned piglets. Journal of Animal and Feed Sciences. 2007;16(1):75–85. 187. Kiers JL, Meijer JC, Nout MJR, Rombouts FM, Nabuurs MJA, van der Meulen J. Effect of fermented soya beans on diarrhoea and feed efficiency in weaned piglets. Journal of Applied Microbiology 2003;95(3):545–52. 188. Kiers JL, Nout MJR, Rombouts FM, Nabuurs MJA, van der Meulen J. Inhibition of adhesion of enterotoxigenic

Escherichia coli K88 by soya bean tempe. Letters in Applied Microbiology 2002;35(4):311–5. 189. Granito M, Champ M, Guerra M, Frias J. Effect of natural and controlled fermentation on flatus-producing compounds of beans (Phaseolus vulgaris). Journal of the Science of Food and Agriculture 2003;83(10):1004–9. 190. Refstie S, Sahlstrom S, Brathen E, Baeverfjord G, Krogedal P. Lactic acid fermentation eliminates indigestible carbohydrates and antinutritional factors in soybean meal for Atlantic salmon (Salmo salar). Aquaculture 2005; 246(1–4):331–45.

Author Queries: AQ1: AQ2: AQ3: AQ4: AQ5: AQ6:

Please Please Please Please Please Please

verify the citation of Table 3 here. update reference [37] and [133]. provide vol. no. and page nos. for ref [147]. specify what superscripts ‘a’, ‘b’ stands for in Table 2. verify/modify the occurrence of 310 in Table 3 verify the author name cited for [129] (i.e. Niven et al.)

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