Makoto Mitsumori, Institute of Livestock and Grassland Science, National Agriculture and Food Research Organization (NARO), Tsukuba, 305-0901 Ibaraki, Japan.

Email: [email protected]

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Rie Sawado,

Rie Sawado

orcid.org/0009-0005-7093-3548

Institute of Livestock and Grassland Science, NARO, Tsukuba, Japan

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Ryo Osawa,

Ryo Osawa

Agricultural Technology Research Center, Saitama, Japan

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Hideo Sobajima,

Hideo Sobajima

Swine and Poultry Research Department, Livestock Research Institute, Gifu, Japan

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Noboru Hayashi,

Noboru Hayashi

Central Livestock Hygiene Service Center, Gifu, Japan

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Itoko Nonaka,

Itoko Nonaka

Institute of Livestock and Grassland Science, NARO, Tsukuba, Japan

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Fuminori Terada,

Fuminori Terada

Meiji Feed Company Limited, Ibaraki, Japan

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Makoto Mitsumori,

Corresponding Author

Makoto Mitsumori

[email protected]

orcid.org/0000-0002-3722-1128

Institute of Livestock and Grassland Science, NARO, Tsukuba, Japan

Correspondence

Makoto Mitsumori, Institute of Livestock and Grassland Science, National Agriculture and Food Research Organization (NARO), Tsukuba, 305-0901 Ibaraki, Japan.

Email: [email protected]

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First published: 20 August 2024

https://doi.org/10.1111/asj.13988

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Abstract

Short-chain fatty acids (SCFAs) produced in the rumen are key factors affecting dairy cows' energy balance (EB). This study aimed to quantitatively evaluate the effects of SCFAs production on EB in dairy cows. Primiparous dairy cows were divided into high non-esterified fatty acid (NEFA; group H) and low NEFA (group L) groups based on their blood NEFA levels at week 3 postpartum, which served as an indicator of EB. The amounts of SCFAs produced in the rumen, including acetate, propionate, and butyrate (SCFAsP), were calculated using the predicted rumen volume. Because there were no differences between the groups in SCFAsP/dry matter intake, whereas 4% fat-corrected milk (FCM)/SCFAsP was significantly higher in group H, it was suggested that more body fat was mobilized for milk production in group H. However, group L, which showed better EB, had propionate dominant and lower FCM/SCFAsP and milk energy/SCFAs energy at 3 and 7 weeks postpartum, indicating that group L had a better energy supply for milk production. These results suggest that SCFAsP produced by rumen fermentation and the composition of SCFAs in the rumen affect milk production and EB.

1 INTRODUCTION

The energy balance (EB) of dairy cows has been used as an indicator of energy excess or deficiency, expressed as the energy intake minus the energy requirement. Understanding rumen fermentation is important because cows use short-chain fatty acids (SCFAs) produced as energy sources by the anaerobic digestion of feed by various anaerobic microorganisms living in the rumen. Although rumen SCFAs concentrations are often used to characterize the general properties of rumen fermentation activity status and patterns (Seymour et al., 2005), Sutton et al. (2003) reported that SCFAs' concentrations in the rumen do not necessarily reflect SCFAs production. Hall (2013) also indicated that other approaches are needed to improve evaluation and interpretation for rumen fermentation (Hall, 2013), and there were many factors (e.g., absorption rate of SCFAs, passage rate of SCFAs, rumen fluid volume, etc.) affecting SCFAs concentration (Hall et al., 2015). Therefore, we attempted to solve this problem by converting SCFAs concentrations to quantifiable values.

A noteworthy characteristic of ruminants is that they use SCFAs by rumen fermentation as an energy source to produce milk and meat (Kruger Ben Shabat et al., 2016). Thus, the EB should consider rumen fermentation conditions to improve feed management. Energy intake is usually determined from feed intake, and energy requirements are calculated from body weight (BW), DG, and milk yield (NARO, 2017). In many cases, SCFAs produced in the rumen are treated as SCFAs concentration data; however, they are not used as quantitative data in the EB. This study aimed to quantify the effects of SCFAs production on EB in dairy cows by linking factors related to feed intake, rumen fermentation, and milk yield.

2 MATERIALS AND METHODS

2.1 Data

No actual experimental research on animals nor sampling were performed in this study. The data in this study were a reanalysis of the data obtained from experiments previously reported by Hayashi et al. (2014), in which animal studies were conducted according to the basic guidelines for animal experiments of the Ministry of Agriculture, Forestry and Fisheries of Japan (MAFF), and are briefly described below.

The experimental studies were carried out in seven prefectural research institutes (Miyagi, Fukushima, Ibaraki, Saitama, Shizuoka, Gifu, and Kumamoto Prefectures) using primiparous Holstein dairy cows. The study was conducted twice, and 52 cows were tested from 6 weeks before parturition to 16 weeks postpartum. Cows were fed a total mixed ration (TMR) containing timothy hay, alfalfa hay cubes, and concentrate. During the first half of the prepartum, these cows were offered a diet consisting of 55% timothy hay, 25% alfalfa hay cubes, and 20% concentrate. During late prepartum, these cows were offered a diet consisting of 40% timothy hay, 25% hay cubes, and 35% concentrate. In both periods, forages were fed to meet 100% of the maintenance, 0.3 kg of daily gain, and total digestible nutrient (TDN) and crude protein (CP) requirements for pregnancy according to the Japanese Feeding Standard for Dairy Cattle (NARO, 2006). Post-parturition diets consisted of 24% timothy hay, 16% alfalfa hay cubes, and 60% concentrate and were fed ad libitum. The chemical compositions of the TMR fed post-parturition were 87.9 ± 0.19% (mean ± standard error) dry matter (DM), 16.1 ± 0.20% CP in DM, 3.5 ± 0.15% ether extract in DM, and 74.3 ± 0.27% TDN in DM.

Nutrient intake was calculated from the feed component values and the digestibility and non-digestibility rate in the Standard Tables of Feed Composition in Japan (Japan Livestock Industry Association, NARO, 2009). Milk yield was measured twice daily, and milk quality tests (fat, nonfat solids, and protein) were conducted weekly. Blood samples were collected from the jugular vein using heparinized tubes 1 week before, on the day of parturition, and at 13:00 at −1, 3, 7, and 16 weeks. The collected blood samples were immediately cooled and centrifuged (1500 × g, 10 min, 5°C), and plasma samples were stored below −30°C until general components analysis (plasma glucose, blood urea nitrogen, calcium, inorganic phosphorus, total cholesterol, total protein, albumin, aspartate aminotransferase, gamma-glutamyl transpeptidase, and non-esterified fatty acid; NEFA). Rumen fluid was collected at the same time as blood sampling. Collection was conducted via the mouth at 13:00 h. After pH measurement, the collected rumen fluid was filtered through a double layer of sterile gauze. Filtered rumen fluid was centrifuged (1500 × g, 15 min, 5°C) as samples for ammonia-form nitrogen (NH₃-N) and SCFAs measurements and the residual samples were then stored at −20°C until analysis. The NH₃-N was measured using the indophenol method. SCFAs were measured using gas chromatography (GC-14B; Shimadzu, Tokyo, Japan). The testing condition was as follows: packed column E-5476 (2.1 m long, 3.2 mm inner diameter; Shinwa-kako, Saitama, Japan), 250°C flame ionization detector, 250°C injector, and 115°C column temperatures. Helium and crotonic acid were used as the carrier gas and the inner standard, respectively.

2.2 Calculation for ruminal volume

Methane production (CH₄P mol/d) was estimated using the following equation for each short-chain fatty acid concentration (Williams et al., 2019):

{\mathrm{CH}}_4\mathrm{P}\ \left(\mathrm{mol}/\mathrm{d}\right)=\left\{\left[3.28\times \left({\mathrm{Ac}}^{\ast }+{\mathrm{Bu}}^{\ast}\right)/{\Pr}^{\ast}\right]+7.60\right\}/16.042\times \mathrm{DMI}\ \left(\mathrm{kg}/\mathrm{d}\right)

where * refers to mmol/L, Ac to acetate, Pr to propionate, Bu to butyrate, and DMI to dry matter intake. SCFAs consist of Ac, Pr, and Bu combined.

The methane concentration in the rumen (CH₄ mM) was calculated from the flow of metabolic hydrogen ([H]). This was estimated from [H] utilized (HU) and [H] produced (HP) in the rumen. HP and HU in SCFAs (HUS) and methane were obtained from the molar proportions of Ac, Pr, and Bu and the molar concentration of methane in the rumen using the following equations (Goel et al., 2009; Mitsumori et al., 2019; Ungerfeld, 2015):

\mathrm{HP}\ \left(\mathrm{mM}\right)=2\times \mathrm{Ac}+\Pr +4\times \mathrm{Bu}

\mathrm{HUS}\ \left(\mathrm{mM}\right)=2\times \Pr +2\times \mathrm{Bu}.

HU was calculated as HP × 0.9 (Demeyer, 1991; Moss et al., 2000). Thus, HU was calculated using [H] recovery in methane (HUM) according to Goel et al. (2009) as follows:

\mathrm{HU}\ \left(\mathrm{mM}\right)=\mathrm{HP}\times 0.9=\mathrm{HUS}+\mathrm{HUM}=\left(2\times \Pr +2\times \mathrm{Bu}\right)+\left(4\times {\mathrm{CH}}_4\right)

The equation used to calculate the CH₄ (mM) (Marty & Demeyer, 1973; Ungerfeld, 2015) was

{\mathrm{CH}}_4\ \left(\mathrm{mM}\right)=\left(\mathrm{HU}-\mathrm{HUS}\right)/4=\left[\left(0.9\times \mathrm{HP}\right)-\mathrm{HUS}\right]/4,

The predicted rumen volume (PRV, L/d) was calculated using the following equation (Mitsumori et al., 2019):

\mathrm{PRV}\ \left(\mathrm{L}/\mathrm{d}\right)={\mathrm{CH}}_4\mathrm{P}\kern0.35em \left(\mathrm{mol}/\mathrm{d}\right)/\left[{\mathrm{CH}}_4\kern0.35em \left(\mathrm{mM}\right)/1000\right]

SCFAs production, including acetate, propionate, and butyrate (SCFAsP mol/d), was estimated using ruminal concentrations of SCFAs and PRV as follows:

\mathrm{SCFAsP}\ \left(\mathrm{mol}/\mathrm{d}\right)=\mathrm{SCFAs}\ \left(\mathrm{mM}\right)\times \mathrm{PRV}\ \left(\mathrm{L}/\mathrm{d}\right).

The theoretical turnover rate (TTOR) of the rumen liquid fraction (Mitsumori et al., 2019) was estimated using the metabolic BW (MBW), which is BW^0.75 with the following equation as follows:

\mathrm{TTOR}\ \left(\left(\mathrm{L}/\mathrm{d}\right)/\mathrm{MBW}\right)=\mathrm{PRV}/\mathrm{MBW}.

The molar masses of HU, HUM, and HUS were calculated using the PRV (L/d) as follows:

\mathrm{HU}\ \left(\mathrm{mol}/\mathrm{d}\right)=\mathrm{HU}\ \left(\mathrm{mM}\right)\times \mathrm{PRV}\ \left(\mathrm{L}/\mathrm{d}\right)/1000

\mathrm{HUS}\ \left(\mathrm{mol}/\mathrm{d}\right)=\mathrm{HUS}\ \left(\mathrm{mM}\right)\times \mathrm{PRV}\ \left(\mathrm{L}/\mathrm{d}\right)/1000

\mathrm{HUM}\ \left(\mathrm{mol}/\mathrm{d}\right)=\mathrm{HUM}\ \left(\mathrm{mM}\right)\times \mathrm{PRV}\ \left(\mathrm{L}/\mathrm{d}\right)/1000.

The energy of each SCFA was calculated based on its molecular weight and caloric content. The molecular weight and calories of Ac were 60.05 g/mol and 3.5 kcal/g, respectively, those of Pr were 74.08 g/mol and 5 kcal/g, respectively, and those of Bu were 88.11 g/mol and 6 kcal/g, respectively (Akoh, 2017). The energy of fat-corrected milk (FCM) was calculated to be 750 kcal/kg (McDonald et al., 2002).

2.3 Statistical analysis

Statistical analyses were performed using JMP software (version 13.0; SAS Institute Inc., Cary, NC, USA) and R 4.1. Cluster analyses were conducted using ln NEFA values at week 3 after parturition using Ward's method. Two NEFA groups were classified: a low NEFA concentration group (group L) and a high NEFA concentration group (group H). When the value was more than three times the standard deviation from the mean, it was identified as an outlier and was displaced. There were no outliers. Figure 1 shows the results of the classification of the groups. We then analyzed the data using the following mixed model: the model included groups, weeks from parturition, and the interaction of groups × weeks as fixed effects and cow ID as a random effect. If an interaction was identified between groups or groups × weeks, contrast analyses were conducted as post hoc tests.

\mathrm{V}\ \mathrm{ijk}=\upmu +\mathrm{Gi}+\mathrm{Wj}+{\mathrm{Gi}}^{\ast }\ \mathrm{Wj}+\mathrm{Ck}+\mathrm{eijk}

where V is value, μ is least square means, G is groups, W is weeks; G * W is the interaction of groups and weeks, C is the cow ID (random effect), and e is error.

Details are in the caption following the image — **FIGURE 1**
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Box plots of two groups (Group L and Group H) clustered by the natural logarithm of the log-transformed NEFA concentration (ln NEFA) at 3 weeks after parturition. The means ± standard deviations of groups L and H were 5.46 ± 0.378 (n = 30) and 6.59 ± 0.294 (n = 22), respectively. Abbreviations: H, high NEFA group; L, low NEFA group; NEFA, non-esterified fatty acid.

3 RESULTS

The parameters related to DMI, BW, milk, blood composition, and rumen fermentation are shown in Table 1. There were no significant differences between groups in DMI (P = 0.13) or milk production (P = 0.62). Dry matter intake/BW^0.75 tended to interact with group and week (P = 0.051). After parturition, the DMI/BW^0.75 of group H was lower than that of group L but gradually recovered to the same level as that of group L. BW had a significant interaction with group and week (P < 0.01). The postpartum BW recovery in group H was lower than that in group L (P < 0.01; BW 1 week before parturition was 100). Milk production showed no significant differences, but FCM tended to be higher in group H (P < 0.1). The sufficiency rate of TDN of group H, calculated using the Japanese feed standard, was lower than that of group L at weeks 3 and 7 (P < 0.05 and P < 0.1, respectively). NEFA was significantly different for blood parameters between the groups (P < 0.01), and all concentrations in group H were significantly higher than those in group L. Glucose concentrations were not significantly different between the groups (P = 0.2). The rumen SCFAs concentrations in group H tended to be lower than those in group L at weeks −1, 3, and 7 (P < 0.1). Ac (mM) showed no significant difference between the groups. The Pr (mM) and Bu (mM) levels in group H were lower than those in group L (P < 0.05). Consistent with these results, group H's Ac/Pr ratio tended to be higher than group L's ratio (P < 0.1). Rumen pH did not differ between these groups. No difference in SCFAsP (mol/d) was observed between the two groups (Table 1).

TABLE 1. Physical, milk, blood, and rumen fermentation parameters (n = 52).

Parameter		Weeks postpartum
		−1 w			+3 w			+7 w			+16 w			P value
		LSM	±SE	P	LSM	±SE	P	LSM	±SE	P	LSM	±SE	P	Group	Week	G × W
Physical
DMI (kg)	L	10.3	0.38	n.s.	17.0	0.38	n.s.	19.7	0.38	n.s.	21.2	0.38	n.s.	0.13	<0.01	0.18
DMI (kg)	H	10.2	0.45	n.s.	15.6	0.44	n.s.	18.9	0.44	n.s.	20.8	0.46	n.s.
DMI/BW^0.75 (g)	L	83	3.2	n.s.	155	3.2	**	179	3.2	n.s.	183	3.2	n.s.	0.08	<0.01	0.05
DMI/BW^0.75 (g)	H	79	3.8	n.s.	140	3.8	**	171	3.8	n.s.	183	3.9	n.s.
BW (kg)	L	619	10.2	*	528	10.2	n.s.	533	10.2	n.s.	567	10.2	n.s.	0.57	<0.01	<0.01
BW (kg)	H	653	11.9	*	537	11.9	n.s.	533	11.9	n.s.	557	11.9	n.s.
BW change (%)	L	100	0.0	n.s.	85	0.8	*	86	0.8	**	92	0.8	**	<0.01	<0.01	<0.01
BW change (%)	H	100	0.0	n.s.	82	1.0	*	82	1.0	**	86	1.0	**
Milk production (kg)	L	-	-	-	29.1	0.9	n.s.	32.0	0.9	n.s.	31.7	0.9	n.s.	0.62	<0.01	0.40
Milk production (kg)	H	-	-	-	30.0	1.1	n.s.	33.2	1.1	n.s.	31.5	1.1	n.s.
FCM (kg/day)	L	-	-	-	30.2	1.1	*	31.4	1.1	n.s.	29.4	1.1	n.s.	0.08	0.02	0.38
FCM (kg/day)	H	-	-	-	33.9	1.2	*	33.3	1.2	n.s.	31.2	1.3	n.s.
Milk fat (%)	L	-	-	-	4.3	0.15	**	3.9	0.15	n.s.	3.5	0.15	^†	0.02	<0.01	0.19
Milk fat (%)	H	-	-	-	4.9	0.17	**	4.0	0.17	n.s.	4.0	0.18	^†
Milk protein (%)	L	-	-	-	3.1	0.04	n.s.	3.0	0.04	n.s.	3.1	0.04	n.s.	0.65	<0.01	0.18
Milk protein (%)	H	-	-	-	3.2	0.05	n.s.	3.0	0.05	n.s.	3.1	0.05	n.s.
SNF (%)	L	-	-	-	8.6	0.06	n.s.	8.6	0.06	n.s.	8.7	0.06	n.s.	0.82	<0.01	0.65
SNF (%)	H	-	-	-	8.6	0.07	n.s.	8.5	0.07	n.s.	8.6	0.07	n.s.
Sufficiency rate of TDN (%)	L	101.8	2.3	n.s.	83.0	2.3	**	92.7	2.3	*	101.5	2.3	n.s.	0.02	<0.01	0.10
Sufficiency rate of TDN (%)	H	98.0	2.7	n.s.	71.3	2.7	**	85.5	2.7	*	96.7	2.8	n.s.
Blood
Total protein (g/dL)	L	6.0	0.12	n.s.	7.3	0.12	n.s.	7.4	0.12	n.s.	7.4	0.12	n.s.	0.48	<0.01	0.81
Total protein (g/dL)	H	5.9	0.14	n.s.	7.2	0.14	n.s.	7.3	0.14	n.s.	7.4	0.14	n.s.
Albumin (g/dL)	L	3.5	0.06	n.s.	3.6	0.05	n.s.	3.7	0.05	n.s.	3.8	0.05	n.s.	0.24	<0.01	0.53
Albumin (g/dL)	H	3.5	0.06	n.s.	3.8	0.06	n.s.	3.8	0.06	n.s.	3.8	0.06	n.s.
BUN (g/dL)	L	13.2	0.63	n.s.	11.9	0.62	n.s.	15.0	0.62	n.s.	15.4	0.62	n.s.	0.73	<0.01	0.10
BUN (g/dL)	H	13.8	0.73	n.s.	12.4	0.73	n.s.	13.8	0.73	n.s.	14.4	0.73	n.s.
NEFA (μEq/L)	L	230.3	32.23	*	250.9	31.77	**	176.7	32.23	**	123.0	31.77	**	<0.01	<0.01	<0.01
NEFA (μEq/L)	H	333.6	37.10	*	763.9	37.10	**	358.1	37.10	**	265.3	37.10	**
Glucose (mg/dL)	L	72.0	1.40	n.s.	64.0	1.38	n.s.	67.3	1.38	n.s.	67.5	1.38	n.s.	0.20	<0.01	0.38
Glucose (mg/dL)	H	71.8	1.61	n.s.	59.8	1.61	n.s.	64.9	1.61	n.s.	66.0	1.61	n.s.
T-Cho (mg/dL)	L	70.6	8.07	n.s.	142.3	7.95	n.s.	209.7	7.95	*	257.9	7.95	n.s.	0.06	<0.01	0.50
T-Cho (mg/dL)	H	82.8	9.29	n.s.	155.3	9.29	n.s.	239.4	9.29	*	267.0	9.29	n.s.
AST (U/L)	L	44.8	5.42	n.s.	64.4	5.34	n.s.	68.0	5.34	n.s.	86.8	5.34	n.s.	0.40	<0.01	0.37
AST (U/L)	H	46.5	6.24	n.s.	79.1	6.24	n.s.	72.5	6.24	n.s.	84.6	6.24	n.s.
GGT (U/L)	L	25.5	2.25	n.s.	29.8	2.21	n.s.	31.2	2.21	n.s.	36.6	2.21	n.s.	0.39	<0.01	0.69
GGT (U/L)	H	25.5	2.59	n.s.	34.4	2.59	n.s.	33.6	2.59	n.s.	37.6	2.59	n.s.
Ca (mg/dL)	L	11.1	0.28	n.s.	11.3	0.27	n.s.	11.7	0.27	n.s.	11.8	0.27	n.s.	0.89	<0.01	0.30
Ca (mg/dL)	H	11.2	0.32	n.s.	11.4	0.32	n.s.	12.0	0.32	n.s.	11.6	0.32	n.s.
iP (mg/dL)	L	5.5	0.22	n.s.	5.4	0.22	n.s.	5.4	0.22	n.s.	5.8	0.22	n.s.	0.25	0.07	0.78
iP (mg/dL)	H	5.9	0.26	n.s.	5.5	0.26	n.s.	5.8	0.26	n.s.	6.1	0.26	n.s.
Rumen
SCFAs (mM)	L	83.8	4.07	^†	84.6	3.97	^†	87.4	3.97	^†	87.9	3.97	n.s.	0.06	0.03	0.86
SCFAs (mM)	H	71.7	4.71	^†	73.4	4.67	^†	76.9	4.64	^†	79.5	4.64	n.s.
Ac (mM)	L	56.6	2.54	n.s.	53.9	2.47	n.s.	56.2	2.49	n.s.	56.7	2.47	n.s.	0.13	0.17	0.89
Ac (mM)	H	50.1	2.94	n.s.	48.9	2.91	n.s.	50.9	2.89	n.s.	52.5	2.89	n.s.
Pr (mM)	L	17.2	1.17	*	19.7	1.14	*	21.2	1.15	*	21.0	1.14	^†	0.02	<0.01	0.80
Pr (mM)	H	13.5	1.36	*	15.5	1.35	*	17.0	1.34	*	17.8	1.34	^†
Bu (mM)	L	9.9	0.64	^†	11.1	0.62	*	10.8	0.63	^†	10.2	0.62	n.s.	0.05	0.04	0.58
Bu (mM)	H	8.0	0.74	^†	9.0	0.73	*	9.0	0.73	^†	9.1	0.73	n.s.
Ac (%)	L	68.4	0.69	n.s.	64.2	0.67	*	64.3	0.67	^†	65.0	0.67	n.s.	0.04	<0.01	0.58
Ac (%)	H	70.1	0.80	n.s.	66.5	0.79	*	66.3	0.78	^†	66.0	0.78	n.s.
Pr (%)	L	20.0	0.63	n.s.	22.9	0.61	^†	23.7	0.61	^†	23.6	0.61	n.s.	0.08	<0.01	0.89
Pr (%)	H	18.8	0.73	n.s.	21.3	0.72	^†	22.1	0.71	^†	22.5	0.71	n.s.
Bu (%)	L	11.5	0.33	n.s.	12.9	0.31	n.s.	12.0	0.31	n.s.	11.5	0.31	n.s.	0.29	<0.01	0.59
Bu (%)	H	11.1	0.37	n.s.	12.2	0.37	n.s.	11.7	0.36	n.s.	11.5	0.36	n.s.
Ac/Pr ratio	L	3.5	0.11	n.s.	2.9	0.10	^†	2.8	0.10	n.s.	2.8	0.10	n.s.	0.07	<0.01	0.85
Ac/Pr ratio	H	3.8	0.12	n.s.	3.2	0.12	^†	3.1	0.12	n.s.	3.0	0.12	n.s.
SCFAsP (mol/day)	L	44.6	1.78	n.s.	72.3	1.70	n.s.	83.7	1.71	n.s.	89.6	1.70	n.s.	0.24	<0.01	0.13
SCFAsP (mol/day)	H	45.3	2.05	n.s.	66.5	2.01	n.s.	80.5	1.98	n.s.	88.3	2.05	n.s.
Rumen (pH)	L	6.7	0.08	n.s.	6.5	0.07	n.s.	6.5	0.07	n.s.	6.5	0.07	n.s.	0.12	<0.01	0.36
Rumen (pH)	H	6.9	0.09	n.s.	6.7	0.09	n.s.	6.6	0.09	n.s.	6.6	0.09	n.s.
NH₃-N (mg/dL)	L	4.6	0.58	n.s.	5.5	0.55	n.s.	5.3	0.55	n.s.	5.9	0.55	*	0.04	0.31	0.75
NH₃-N (mg/dL)	H	3.6	0.66	n.s.	4.1	0.64	n.s.	4.0	0.64	n.s.	4.0	0.64	*

Abbreviations: Ac, acetate; AST, aspartate aminotransferase; Bu, butyrate; BUN, blood urea nitrogen; BW, body weight; Ca, calcium; DMI, dry matter; FCM, 4% fat corrected milk; GGT, gamma-glutamyl transpeptidase; H, high NEFA group; iP, inorganic phosphorus; L, low NEFA group; NEFA, non-esterified fatty acids; NH3-N, ammonia nitrogen; Pr, propionate; SCFA, short chain fatty acid; SCFAsP, SCFAs production; SNF, solids not fat; T-cho, total cholesterol; TDNI/FS, total digestive nutrients intake/feed standard.
^† Significant difference: P < 0.1.
* Significant difference: P < 0.05.
** Significant difference: P < 0.01.

Table 2 shows parameters relating to [H]. [HUS] production (mol/d) of group H was lower than that of group L at weeks 3 and 7 (P < 0.05), that of group H tended to be lower than that of group L at week 16 (P < 0.1). The HUM/HUS ratio of group H was higher than that of group L (P < 0.05). Estimated rumen CH₄ concentration (mM) and CH₄P (mol/d) showed no statistically significant differences between these groups (P = 0.19 and P = 0.96, Table 2). CH₄/DMI (mol/kg) of group H tended to be higher than that of group L (P < 0.1). PRV and TTOR showed no significant difference between these groups (Table 2).

TABLE 2. Parameters relating to metabolic hydrogen ([H]) flow.

		−1 w			+3 w			+7 w			+16 w			P value
		LSM	±SE	P	LSM	±SE	P	LSM	±SE	P	LSM	±SE	P	Group	Week	G × W
HU (mM)	L	153.0	7.50	^†	154.5	7.32	^†	159.0	7.36	^†	157.7	7.32	n.s.	0.07	0.14	0.81
HU (mM)	H	131.3	8.69	^†	134.2	8.62	^†	139.3	8.55	^†	143.5	8.55	n.s.
HUS (mM)	L	54.3	3.44	*	61.5	3.36	*	64.0	3.38	*	62.4	3.36	n.s.	0.02	<0.01	0.66
HUS (mM)	H	43.0	3.99	*	48.9	3.96	*	52.0	3.93	*	53.9	3.93	n.s.
HUM (mM)	L	98.7	4.52	n.s.	93.0	4.38	n.s.	95.0	4.41	n.s.	95.3	4.38	n.s.	0.19	0.4	0.87
HUM (mM)	H	88.3	5.22	n.s.	85.4	5.17	n.s.	87.3	5.12	n.s.	89.6	5.12	n.s.
HU (mol/day)	L	81.5	3.41	n.s.	132.2	3.25	n.s.	150.9	3.28	n.s.	160.9	3.25	n.s.	0.31	<0.01	0.14
HU (mol/day)	H	83.0	3.92	n.s.	124.4	3.85	n.s.	146.1	3.79	n.s.	159.3	3.92	n.s.
HUS (mol/day)	L	28.1	1.22	n.s.	51.4	1.15	**	59.3	1.16	**	62.3	1.15	^†	<0.01	<0.01	0.08
HUS (mol/day)	H	27.0	1.40	n.s.	44.7	1.37	**	54.2	1.34	**	58.9	1.40	^†
HUM (mol/day)	L	53.3	2.85	n.s.	80.8	2.73	n.s.	91.5	2.73	n.s.	98.5	2.73	n.s.	0.95	<0.01	0.39
HUM (mol/day)	H	55.9	3.28	n.s.	76.8	3.23	n.s.	91.9	3.19	n.s.	100.2	3.28	n.s.
HUM/HUS ratio (mol/mol)	L	1.95	0.06	n.s.	1.58	0.05	*	1.56	0.06	n.s.	1.59	0.05	n.s.	0.05	<0.01	0.75
HUM/HUS ratio (mol/mol)	H	2.08	0.07	n.s.	1.76	0.07	*	1.70	0.06	n.s.	1.68	0.06	n.s.
CH₄ (mM)	L	24.7	1.13	n.s.	23.2	1.10	n.s.	23.7	1.10	n.s.	23.8	1.10	n.s.	0.19	0.44	0.87
CH₄ (mM)	H	22.1	1.30	n.s.	21.3	1.29	n.s.	21.8	1.28	n.s.	22.4	1.28	n.s.
CH₄P (mol/day)	L	13.3	0.71	n.s.	20.2	0.68	n.s.	22.9	0.69	n.s.	24.6	0.68	n.s.	0.96	<0.01	0.38
CH₄P (mol/day)	H	14.0	0.82	n.s.	19.2	0.81	n.s.	23.0	0.80	n.s.	25.1	0.82	n.s.
CH₄P/DMI (mol/kg)	L	1.32	0.02	n.s.	1.18	0.02	^†	1.15	0.02	n.s.	1.15	0.02	n.s.	0.08	<0.01	0.96
CH₄P/DMI (mol/kg)	H	1.37	0.03	n.s.	1.25	0.03	^†	1.21	0.03	n.s.	1.20	0.03	n.s.
PRV (L/day)	L	572	56.1	n.s.	957	54.5	n.s.	1,033	54.9	n.s.	1,106	66.9	n.s.	0.55	<0.01	0.47
PRV (L/day)	H	667	64.9	n.s.	945	64.2	n.s.	1,083	63.7	n.s.	1,152	64.9	n.s.
TTOR	L	4.56	0.45	n.s.	8.60	0.44	n.s.	9.24	0.44	n.s.	9.45	0.44	n.s.	0.47	<0.01	0.50
TTOR	H	5.15	0.52	n.s.	8.48	0.51	n.s.	9.78	0.51	n.s.	10.11	0.52	n.s.

Abbreviations: CH4, methane concentration (mM); CH4P, methane production (mol/day); DMI, dry matter, PRV; predicted rumen volume; H, high NEFA group; HU, [H] utilized; HUM, [H] utilized in methane; HUS, [H] utilized in SCFAs; L, low NEFA group; LSM, least squares mean; P, P value; SE, standard error of the mean; TTOR, the turnover rates of the ruminal liquid fraction per unit MBW per day.
^† Significant difference: <0.1.
* Significant difference: <0.05.
** Significant difference: <0.01.

The relationships between DMI, SCFAsP, and FCM are shown in Figure 2. FCM/DMI (kg/kg; Figure 2a) was significantly different between the groups (P < 0.01) and was significantly higher in group H at week 3 (P < 0.01). SCFAsP/DMI (mol/kg; Figure 2b) did not differ significantly between groups. The FCM/SCFAsP (kg/mol; Figure 2c) was significantly higher in group H (P < 0.01) than in group L, especially at week 3 (P < 0.01).

Figure 3 shows a comparison of SCFAs production between groups. The Pr (mol/d) of group H was lower at weeks 3 and 7 than that of group L, and week 16 did not cause statistical differences in SCFAsP. The Bu (mol/d) in group H was lower than that in group L at week 3 (P < 0.01).

Gross energy intake (GEI) and energy of SCFAs (SCFAsE), FCM (milkE), and CH₄ (CH₄E) are shown in Table 3. There were no differences in the GEI between these groups. Energy of SCFAs levels tended to differ between these groups (P < 0.1) and were higher in group L at weeks 3 (P < 0.05) and 7 (P < 0.1). Energy of milk tended to differ between these groups (P < 0.1) and was significantly lower in group L at week 3 (P < 0.05). MilkE/GEI (Mcal/Mcal, feed efficiency) in group H at weeks 3 and 7 were higher than in group L (P < 0.01 and P < 0.1, respectively). SCFAsE/GEI (Mcal/Mcal) was not different between these groups. MilkE/SCFAsE (Mcal/Mcal) was significantly different between these groups, week, and interaction (P < 0.01). No differences were observed in the amount of energy lost concerning CH₄. CH₄E/GEI (Mcal/Mcal) tended to differ between these groups and that of group L at week 3 was lower than that of group H (P < 0.1).

TABLE 3. The amount of energy of DMI (GEI), SCFAs, FCM, and CH4 parameters in primiparous.

		−1 w			+3 w			+7 w			+16 w			P value
		LSM	±SE	P	LSM	±SE	P	LSM	±SE	P	LSM	±SE	P	Group	Week	G * W
GEI (Mcal/day)	L	46.1	1.70	n.s.	76.2	1.70	n.s.	88.7	1.70	n.s.	95.4	1.70	n.s.	0.13	<0.01	0.18
GEI (Mcal/day)	H	45.9	2.01	n.s.	70.0	1.98	n.s.	85.1	1.98	n.s.	93.4	2.05	n.s.
SCFAsE (Mcal/day)	L	12.5	0.48	n.s.	20.8	0.45	**	23.9	0.46	^†	25.4	0.45	n.s.	0.08	<0.01	0.09
SCFAsE (Mcal/day)	H	12.5	0.55	n.s.	18.8	0.54	**	22.8	0.53	^†	24.9	0.55	n.s.
MilkE (Mcal/day)	L	-	-	-	22.6	0.79	*	23.6	0.79	n.s.	22.1	0.79	n.s.	0.08	0.02	0.38
MilkE (Mcal/day)	H	-	-	-	25.4	0.92	*	25.0	0.92	n.s.	23.4	0.95	n.s.
MilkE/GEI	L	-	-	-	0.302	0.0108	**	0.267	0.0108	^†	0.231	0.0108	n.s.	<0.01	<0.01	<0.01
MilkE/GEI	H	-	-	-	0.373	0.0126	**	0.297	0.0126	^†	0.250	0.0130	n.s.
SCFAsE/GEI	L	0.272	0.0017	n.s.	0.273	0.0016	n.s.	0.269	0.0016	n.s.	0.267	0.0016	n.s.	0.43	<0.01	0.79
SCFAsE/GEI	H	0.272	0.0019	n.s.	0.270	0.0019	n.s.	0.267	0.0018	n.s.	0.266	0.0019	n.s.
milkE/SCFAsE	L	-	-	-	1.103	0.0396	**	0.992	0.0400	*	0.868	0.0396	n.s.	<0.01	<0.01	<0.01
milkE/SCFAsE	H	-	-	-	1.383	0.0470	**	1.116	0.0463	*	0.940	0.0478	n.s.
CH₄E (Mcal/day)	L	2.83	0.151	n.s.	4.28	0.145	n.s.	4.85	0.146	n.s.	5.22	0.145	n.s.	0.95	<0.01	0.39
CH₄E (Mcal/day)	H	2.97	0.174	n.s.	4.07	0.171	n.s.	4.87	0.169	n.s.	5.31	0.174	n.s.
CH₄E/GEI	L	0.062	0.0011	n.s.	0.056	0.0011	^†	0.054	0.0011	n.s.	0.054	0.0011	n.s.	0.08	<0.01	0.96
CH₄E/GEI	H	0.065	0.0013	n.s.	0.059	0.0013	^†	0.057	0.0013	n.s.	0.057	0.0013	n.s.

Abbreviation: CH4E, methane gas energy; DMI, dry matter intake; FCME, 4% fat corrected milk energy; GEI, gross energy intake; LSM, least squares mean; P, P value; SCFAsE, short chain fatty acids energy (Mcal); SE, standard error of the mean.
^† Significant difference: P < 0.1.
* Significant difference: P < 0.05.
** Significant difference: P < 0.01.

4 DISCUSSION

The total amount of SCFAs in the rumen, which are the products of rumen fermentation, is a key factor in milk production. The estimation of SCFAsP using isotopes is currently the most accurate method; however, according to Sutton et al. (2003), the method requires complicated processing to isolate the substance of interest from biological samples. However, methane is not readily dissolved into the rumen liquid fraction (Speight, 2017) and is rarely absorbed through the rumen wall. Therefore, methane could be used as a stable indicator of ruminal fermentation (Mitsumori et al., 2019). This study estimated SCFAsP using methane to determine rumen volume, and its relationship with EB was further examined. Hristov et al. (2013) and Mitsumori et al. (2019) estimated CH₄P using DMI as a variable. We used the estimation equation by Williams et al. (2019), which considers rumen fermentation patterns because the ratio of roughage to concentrate per DMI is expected to change owing to feed changes before and after parturition.

NEFA concentrations reflect the body fat released into the blood as long-chain fatty acids owing to energy deficiency. Therefore, NEFA concentrations are used as an indicator to determine short-term energy balance (van Knegsel et al., 2005). In general, the normal range of NEFA is 185 ± 77 μEq/L in the dry period, 225 ± 173 Eq/L in the early lactation period, and 135 ± 42 μEq/L or less in the mid-lactation period (Inokuma et al., 2017). This study showed that cows in group H showing negative energy balance (NEB) at week 3 continued to develop NEB until week 16. Primiparous cows distribute more energy for body growth than multiparous cows (Wathes, Cheng, et al., 2007); hence, they are less likely to develop NEB caused by milk production than multiparous cows are. Nevertheless, these are still primiparous cows categorized as NEB owing to high NEFA concentrations; therefore, this study examined the factors contributing to EB in primiparous cows. Fluctuations in glucose are more tightly controlled than those in NEFA (Wathes, Fenwick, et al., 2007) and decrease under severe low-energy conditions (van Knegsel et al., 2005). In this study, glucose decreased at week 3 regardless of group, but concentrations were within the normal range (group L: 64.0 mg/dL, group H: 59.8 mg/dL).

Lactating cows generally reach peak milk yield approximately 4–5 weeks after parturition, whereas DMI peaks approximately 8–10 weeks after. This discrepancy could be one reason for the NEB (NARO, 2017). During NEB, cows lose weight as body fat mobilization compensates for the energy required for milk production. Group H had higher NEFA levels and was 15% lower in BW at weeks 7 and 16 than at week −1. Body weight recovery in group H was slow, suggesting that NEB persisted for a long time. Group H produced more FCM despite having the same feed composition and low TDN sufficiency rates after parturition, suggesting that group H had a slower BW recovery and a longer NEB period than group L.

In general, changes in the ratio of roughage and concentrate in feed affect rumen fermentation (Janssen, 2010; Johnson & Johnson, 1995; Sutton et al., 2003). In this study, the composition of SCFAs differed among individuals despite having the same feed composition, indicating that rumen fermentation patterns varied among individuals, even without differences in feed composition. Furthermore, cows in group L, which tended to be propionate dominant, had milder NEB before and after parturition, even when fed the same feed.

The SCFAs concentration in the rumen is commonly measured to determine rumen fermentation parameters (Seymour et al., 2005). However, the SCFAs concentration in rumen fluid is not sufficient as an indicator of rumen microbial activity because of the difference between the rate of production by rumen microorganisms and the rates of absorption through the rumen wall and disappearance into the digestive tract (Dijkstra et al., 1993; Hall et al., 2015). In this study, SCFAsP was calculated from SCFAs concentrations and PRV. Results of SCFAsP ranged from 45.2 to 89.6 mol/d, which is close to the values reported by Sharp et al. (1982) and Dieho et al. (2016) (45 to 81.8 mol/d and 49 to 126 mol/d, respectively). Furthermore, the SCFAsP/DMI was calculated to be between 4.22 and 4.43 mol/kg. Previously reported SCFAsP/DMI ranged from 3.4 to 5.8 mol/kg (Whitelaw et al., 1970), and the values obtained in the present study fell within this range. Although the SCFAs concentrations in group L tended to be higher than those in group H, there were no significant differences in SCFAsP between these groups. Both groups produced the same amount of SCFAsP, suggesting that the SCFAs composition affects NEB.

Microorganisms rapidly remove [H] in the rumen. Methanogenesis is one of the main pathways of [H] removal. Acetate and butyrate production promotes methanogenesis because they release [H] during biosynthesis; however, propionate competes with CH₄ because it utilizes [H] (Ungerfeld, 2020). There was no difference in HUM (mol/d) and CH₄ (mol/d) between the two groups; however, HUS (mol/d) was higher in group L after parturition. This means that more [H] was used in the biosynthesis of propionate. Propionate production (mol/d) was significantly higher in group L after parturition, and the energy of SCFAs (Mcal/d, SCFAsE) was significantly higher in group L at 3 weeks postpartum and tended to be higher at 7 weeks. The better EB in group L may reflect the SCFAsE (Mcal/d) produced in the rumen.

The quantitative relationships between feed, rumen fermentation, and milk production were also analyzed using DMI, SCFAsP, and FCM. Regarding the relationship between DMI and FCM, the FCM was significantly higher in group H at week 3; however, no significant differences were observed at weeks 7 and 16. In contrast, the FCM/DMI was significantly higher in group H during the entire period. This indicated higher milk production per DMI, suggesting more body fat mobilization, leading to higher NEFA, that is, NEB status, in group H. Considering that there were no differences in SCFAsP/DMI (mol/kg) between the groups, the SCFAsP produced per DMI did not seem directly related to EB. Because FCM/SCFAsP and FCM/DMI were higher in group H at weeks 3 and 7, group H produced more milk relative to the amount of SCFAs produced in the rumen, which could be one of the reasons why more fat was mobilized for milk production. Hoedemaker et al. (2004) showed that feeding glucogenic nutrients decreased NEFA and BHBA concentrations in the blood. Increased utilization of glucogenic nutrients improves EB and reduces the risk of metabolic and reproductive disorders (van Knegsel et al., 2007). These reports indicated propionate, a glucogenic SCFA, is closely associated with energy sufficiency. The glucose required for milk production is mainly derived from feed intake and body fat mobilization. Although the proportion of glucose sources was unclear in this study, a significant difference in propionate production was observed between the groups. We also examined the relationship between feed, rumen fermentation, and milk production from an energy perspective. There were no significant differences in the SCFAsP levels between the groups. However, SCFAsE was higher in group L at weeks 3 and 7, presumably owing to significantly higher propionate and butyrate concentrations in group L, which may be one of the factors that had a positive effect on EB in group L. Interestingly, the ratio of SCFAs energy to feed energy (SCFAsE/GEI) was nearly the same for all observations, that is, 0.27 for any week, which approximated the value (0.315) obtained by Whitelaw et al. (1970).

In conclusion, the present study demonstrates that SCFAsP can be calculated using PRV. Because there were no differences between the groups in SCFAsP/DMI, and FCM/SCFAsP was significantly higher in group H, it is suggested that more body fat was mobilized for milk production in group H. However, the group with better EB (group L) had propionate dominant and showed lower FCM/SCFAsP, indicating a better energy supply for milk production. Further research is required to clarify the detailed mechanisms underlying EB and rumen fermentation.

ACKNOWLEDGMENTS

We express our deepest gratitude to the researchers at the prefectural research institutes (Miyagi, Fukushima, Ibaraki, Saitama, Shizuoka, Gifu, and Kumamoto Prefectures) for collecting the data used in this study. We thank Mr. Ishibashi, Stat Labo Co., Ltd., for their assistance with the statistical analysis. This study was supported by the Cabinet Office, Government of Japan, Moonshot Research and Development Program for Agriculture, Forestry and Fisheries (funding agency: Bio-oriented Technology Research Advancement Institution) (No. JPJ009237). The data used in this study were provided from studies conducted by Hayashi et al. (2014), which were carried out under the following project studies “Practical technology development project for promoting new agriculture, forestry and fisheries policies” and “Promotion of scientific and technical research in agriculture, forestry, fisheries and food industry” commissioned by the Ministry of Agriculture, Forestry and Fisheries (MAFF).

CONFLICT OF INTEREST STATEMENT

Authors declare no conflict of interests for this article.

REFERENCES

C. C. Akoh (Ed.). (2017). Food lipids: Chemistry, nutrition, and biotechnology, fourth edition ( 4th ed.). CRC Press. https://doi.org/10.1201/9781315151854
10.1201/9781315151854
Google Scholar
Demeyer, D. I. (1991). Quantitative aspects of microbial metabolism in the rumen and hindgut. In J. P. Jouany (Ed.), Rumen microbial metabolism and ruminant digestion (pp. 217–237). INRA Editions.
Google Scholar
Dieho, K., Dijkstra, J., Schonewille, J. T., & Bannink, A. (2016). Changes in ruminal volatile fatty acid production and absorption rate during the dry period and early lactation are affected by the rate of increase of concentrate allowance. Journal of Dairy Science, 99(7), 5370–5384. https://doi.org/10.3168/jds.2015-10819
10.3168/jds.2015-10819
CAS PubMed Google Scholar
Dijkstra, J., Boer, H., Van Bruchem, J., Bruining, M., & Tamminga, S. (1993). Absorption of volatile fatty acids from the rumen of lactating dairy cows as influenced by volatile fatty acid concentration, pH and rumen liquid volume. The British Journal of Nutrition, 69(2), 385–396. https://doi.org/10.1079/bjn19930041
10.1079/BJN19930041
CAS PubMed Google Scholar
Goel, G., Makkar, H. P. S., & Becker, K. (2009). Inhibition of methanogens by bromochloromethane: Effects on microbial communities and rumen fermentation using batch and continuous fermentations. The British Journal of Nutrition, 101(10), 1484–1492. https://doi.org/10.1017/S0007114508076198
10.1017/S0007114508076198
CAS PubMed Google Scholar
Hall, M. B. (2013). Dietary starch source and protein degradability in diets containing sucrose: Effects on ruminal measures and proposed mechanism for degradable protein effects. Journal of Dairy Science, 96(11), 7093–7109. https://doi.org/10.3168/jds.2012-5663
10.3168/jds.2012-5663
CAS PubMed Google Scholar
Hall, M. B., Nennich, T. D., Doane, P. H., & Brink, G. E. (2015). Total volatile fatty acid concentrations are unreliable estimators of treatment effects on ruminal fermentation in vivo. Journal of Dairy Science, 98(6), 3988–3999. https://doi.org/10.3168/jds.2014-8854
10.3168/jds.2014-8854
CAS PubMed Web of Science® Google Scholar
Hayashi, N., Hideo, S., Naoki, O., Hidetoshi, S., Hitoshi, I., Ryo, O., Sachie, K., Ryota, M., Akito, S., Itoko, N., Fuminori, T., Koji, H., Shiro, K., Makoto, H., & Osamu, E. (2014). Effect of non-fiber carbohydrate level in lactation diet on the blood and ruminal fluid properties, dairy and reproductive performance of primiparous Holstein cows. Japanese Journal of Embryo Transfer, 36, 157–167. [In Japanese]
Google Scholar
Hoedemaker, M., Prange, D., Zerbe, H., Frank, J., Daxenberger, A., & Meyer, H. H. D. (2004). Peripartal propylene glycol supplementation and metabolism, animal health, fertility, and production in dairy cows. Journal of Dairy Science, 87(7), 2136–2145. https://doi.org/10.3168/jds.S0022-0302(04)70033-8
10.3168/jds.S0022-0302(04)70033-8
CAS PubMed Web of Science® Google Scholar
Hristov, A. N., Oh, J., Firkins, J. L., Dijkstra, J., Kebreab, E., Waghorn, G., Makkar, H. P. S., Adesogan, A. T., Yang, W., Lee, C., Gerber, P. J., Henderson, B., & Tricarico, J. M. (2013). SPECIAL TOPICS—Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options. Journal of Animal Science, 91(11), 5045–5069. https://doi.org/10.2527/jas.2013-6583
10.2527/jas.2013-6583
CAS PubMed Web of Science® Google Scholar
I. Inokuma, H. Kitagawa, & Y. Naitou (Eds.). (2017). Large animals. In Japanese academy of veterinary internal medicine, textbook of veterinary internal medicine ( 2nd ed.). Buneido Publishing. [In Japanese]
Google Scholar
Janssen, P. H. (2010). Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics. Animal Feed Science and Technology, 160(1–2), 1–22. https://doi.org/10.1016/j.anifeedsci.2010.07.002
10.1016/j.anifeedsci.2010.07.002
CAS Web of Science® Google Scholar
Japan Livestock Industry Association, NARO. (2009). Standard tables of feed composition in Japan. National Agriculture and Food Research Organization. [In Japanese]
Google Scholar
Johnson, K. A., & Johnson, D. E. (1995). Methane emissions from cattle. Journal of Animal Science, 73(8), 2483–2492. https://doi.org/10.2527/1995.7382483x
10.2527/1995.7382483x
CAS PubMed Web of Science® Google Scholar
Kruger Ben Shabat, S., Sasson, G., Doron-Faigenboim, A., Durman, T., Yaacoby, S., Berg Miller, M. E., White, B. A., Shterzer, N., & Mizrahi, I. (2016). Specific microbiome-dependent mechanisms underlie the energy harvest efficiency of ruminants. The ISME Journal, 10(12), 2958–2972. https://doi.org/10.1038/ismej.2016.62
10.1038/ismej.2016.62
PubMed Google Scholar
Marty, R. J., & Demeyer, D. I. (1973). The effect of inhibitors of methane production of fermentation pattern and stoichiometry in vitro using rumen contents from sheep given molasses. The British Journal of Nutrition, 30(2), 369–376. https://doi.org/10.1079/bjn19730041
10.1079/BJN19730041
CAS PubMed Web of Science® Google Scholar
McDonald, P., Edwards, R. A., Greenhalgh, J. F. D., Morgan, C. A., Sinclair, L. A., & Wilkinson, R. G. (2002). Animal nutrition. Pearson Education India.
Google Scholar
Mitsumori, M., Hasunuma, T., Okimura, T., Shinkai, T., Kobayashi, Y., Hirako, M., & Kushibiki, S. (2019). Theoretical turnover rate of the rumen liquid fraction in dairy cows and its relationship to feed intake, rumen fermentation, and milk production. Animal Science Journal, 90(12), 1556–1566. https://doi.org/10.1111/asj.13305
10.1111/asj.13305
CAS PubMed Web of Science® Google Scholar
Moss, A. R., Jouany, J. P., & Newbold, J. (2000). Methane production by ruminants: Its contribution to global warming. Animal Research, 49(3), 231–253. https://doi.org/10.1051/animres:2000119
10.1051/animres:2000119
CAS Google Scholar
National Agriculture and Food Research Organization, NARO. (2006). Japanese feeding standard for dairy cattle. Japan Livestock Industry Association. [In Japanese]
Google Scholar
National Agriculture and Food Research Organization, NARO. (2017). Japanese feeding standard for dairy cattle. Japan Livestock Industry Association. [In Japanese]
Google Scholar
Seymour, W. M., Campbell, D. R., & Johnson, Z. B. (2005). Relationships between rumen volatile fatty acid concentrations and milk production in dairy cows: A literature study. Animal Feed Science and Technology, 119(1–2), 155–169. https://doi.org/10.1016/j.anifeedsci.2004.10.001
10.1016/j.anifeedsci.2004.10.001
CAS Google Scholar
Sharp, W. M., Johnson, R. R., & Owens, F. N. (1982). Ruminal VFA production with steers fed whole or ground corn grain. Journal of Animal Science, 55(6), 1505–1514. https://doi.org/10.2527/jas1982.5561505x
10.2527/jas1982.5561505x
CAS PubMed Google Scholar
J. G. Speight (Ed.). (2017). Lange's handbook of chemistry ( 17th ed.). McGraw-Hill Education. https://www.accessengineeringlibrary.com/content/book/9781259586095
Google Scholar
Sutton, J. D., Dhanoa, M. S., Morant, S. V., France, J., Napper, D. J., & Schuller, E. (2003). Rates of production of acetate, propionate, and butyrate in the rumen of lactating dairy cows given normal and low-roughage diets. Journal of Dairy Science, 86(11), 3620–3633. https://doi.org/10.3168/jds.S0022-0302(03)73968-X
10.3168/jds.S0022-0302(03)73968-X
CAS PubMed Web of Science® Google Scholar
Ungerfeld, E. M. (2015). Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: A meta-analysis. Frontiers in Microbiology, 6(FEB), 37. https://doi.org/10.3389/fmicb.2015.00037
10.3389/fmicb.2015.00037
PubMed Google Scholar
Ungerfeld, E. M. (2020). Metabolic hydrogen flows in rumen fermentation: Principles and possibilities of interventions. Frontiers in Microbiology, 11(April), 589. https://doi.org/10.3389/fmicb.2020.00589
10.3389/fmicb.2020.00589
PubMed Google Scholar
Van Knegsel, A. T. M., van den Brand, H., Dijkstra, J., Tamminga, S., & Kemp, B. (2005). Effect of dietary energy source on energy balance, production, metabolic disorders and reproduction in lactating dairy cattle. Reproduction, Nutrition, Development, 45(6), 665–688. https://doi.org/10.1051/rnd:2005059
10.1051/rnd:2005059
CAS PubMed Google Scholar
Van Knegsel, A. T. M., Van Den Brand, H., Dijkstra, J., Van Straalen, W. M., Jorritsma, R., Tamminga, S., & Kemp, B. (2007). Effect of glucogenic vs. lipogenic diets on energy balance, blood metabolites, and reproduction in primiparous and multiparous dairy cows in early lactation. Journal of Dairy Science, 90(7), 3397–3409. https://doi.org/10.3168/jds.2006-837
10.3168/jds.2006-837
CAS PubMed Google Scholar
Wathes, D. C., Cheng, Z., Bourne, N., Taylor, V. J., Coffey, M. P., & Brotherstone, S. (2007). Differences between primiparous and multiparous dairy cows in the inter-relationships between metabolic traits, milk yield and body condition score in the periparturient period. Domestic Animal Endocrinology, 33(2), 203–225. https://doi.org/10.1016/j.domaniend.2006.05.004
10.1016/j.domaniend.2006.05.004
CAS PubMed Web of Science® Google Scholar
Wathes, D. C., Fenwick, M., Cheng, Z., Bourne, N., Llewellyn, S., Morris, D. G., Kenny, D., Murphy, J., & Fitzpatrick, R. (2007). Influence of negative energy balance on cyclicity and fertility in the high producing dairy cow. Theriogenology, 68(SUPPL. 1), S232–S241. https://doi.org/10.1016/j.theriogenology.2007.04.006
10.1016/j.theriogenology.2007.04.006
CAS PubMed Web of Science® Google Scholar
Whitelaw, F. G., Hyldgaard-Jensen, J., Reid, R. S., & Kay, M. G. (1970). Volatile fatty acid production in the rumen of cattle given an all-concentrate diet. The British Journal of Nutrition, 24(1), 179–195. https://doi.org/10.1079/bjn19700019
10.1079/BJN19700019
CAS PubMed Google Scholar
Williams, S. R. O., Hannah, M. C., Jacobs, J. L., Wales, W. J., & Moate, P. J. (2019). Volatile fatty acids in ruminal fluid can be used to predict methane yield of dairy cows. Animals, 9(12), 1006. https://doi.org/10.3390/ani9121006
10.3390/ani9121006
PubMed Web of Science® Google Scholar

Volume95, Issue1

January/December 2024

e13988

This article also appears in:

Nutrition and feeding management of dairy cattle

Analysis of the relationship between energy balance and properties of rumen fermentation of primiparous dairy cows during the perinatal period

Abstract

1 INTRODUCTION