Influence of body condition score on the metabolic and reproductive status of adult female Kacang goats

ABSTRACT

This study aimed to determine the influence of body condition score (BCS) on the metabolic and reproductive status of adult female Kacang goats (Capra hircus). Twenty-three local doe goats aged 3–6 years, which were not pregnant and had BCS ranging from 1–3 on a scale of 1–5, were studied. Blood samples were collected before slaughtering for biochemical analyses. After the goats were killed, the ovaries were collected for follicle and corpus luteum (CL) examination. Ovarian follicular fluid was aspirated for biochemical analyses. Most blood biochemistry parameters of the goats with BCS 1–3 did not show significant differences (P>0.05). The ovaries with BCS 1 were acyclic; whereas the ovaries with BCSs 2 and 3 were cyclic. The ovarian follicular fluid concentrations of glucose, Ca, and Mg in the goats with BCS 1 were significantly lower than those of the goats with BCSs 2 and 3. The levels of TP, ALB, and cholesterol in the ovarian follicular fluid were significantly correlated with the blood results (P<0.05). In conclusion, Kacang goats with poor body conditions showed ovarian dysfunction. The levels of TP, ALB, and cholesterol in follicular fluid were related to the blood metabolite levels.

KEYWORDS:

• Biochemistry
• blood
• body condition score
• follicle
• Kacang goat
• ovary

Introduction

A goat is a type of Bovidae which has a good capacity to acclimate or adapt to seasonal changes and whose meat is ingested by humans (Đuričić et al. 2012). In Indonesia, goats comprise 34.14% of the total ruminants and play a strategic role as an animal protein source (Nurdiman et al. 2019). However, metabolic and nutritional disorders remain an obstacle to improving productivity. Malnutrition is one of the factors which cause animals to become sick, die, and have a decreased productive and reproductive performance, causing an economic loss for farmers. Reproductive performance is closely related to the body condition score (BCS). A number of studies have shown that either poor BCS or a significant weight loss are factors which greatly influence reproductive performance, such as the duration of the anoestrous phase, probability of conception at first mating, birth interval, and conception rate (Chapa et al. 2001; Buckley et al. 2003; Gossen et al. 2006; Roche et al. 2007). It was reported that animals with optimum BCS at pre-calving are known to have better reproduction performance than animals with poor BCS (Patton et al. 2007; Patel et al. 2018). A study on cows and buffaloes showed that animals with BCS 3.75 (on a scale of 1–5) have a higher probability of becoming pregnant after their first insemination, fewer services per conception, and shorter postpartum oestrous period (Samarütel et al. 2006; Patel et al. 2018). Another study showed that significant weight loss during the dry period was reported to be closely associated with the incidence of metabolic disorders and impaired reproductive performance in the postnatal period (Kim and Suh 2003). Moreover, knowledge of the metabolite profile is very useful for predicting, diagnosing, and preventing various nutritional, pathological, and metabolic disorders/problems before adverse conditions occur (Sahlu et al. 1992; Žubčić 2001; Tambuwal et al. 2002; Daramola et al. 2005; Opara et al. 2010; Piccione et al. 2010; Elitok 2012; Onasanya et al. 2015; Silveira 2015). To date, the information on the relationship between BCS and nutritional, metabolic, and reproductive disorders of Indonesian Kacang goats is still limited. This study was designed to evaluate the effects of body condition on metabolic profile and ovarian function in doe Kacang goats.

Materials and methods

The research was approved by the Ethics Committee of Ethical Clearance for Pre-Clinical Research, Integrated Research and Testing Laboratory, Universitas Gadjah Mada, Yogyakarta, Indonesia under licence number 00030/04/LPPT/IV/ 2018.

This study used female Kacang goats aged 3–6 years. The goats did not have any physical defects, had given birth before, were not pregnant, and had body condition scores ranging from poor to good (BCS 1–3 on a scale of 1–5). They were intensively kept in staged pens and offered free access to kangkong (Ipomoea reptans Poir) and Gliricidia (Gliricidia sepium) (approximately 1.5–2 kg/day/animal) and drinking water. The proximate composition of the kangkong was 86.52% dry matter, 5.59% crude protein, 33.68% fibre, 14.73% ash, 1.35% crude fat, 3.03% Ca, and 0.29% P, whereas the proximate composition of the Gliricidia was 90.29% dry matter, 16.80% crude protein, 20.91% fibre, 11.00% ash, 2.58% crude fat, 2.80% Ca, and 0.20% P. The BCS of the animals were assessed according to the criteria described by Koyuncu and Altınçekiç (2013) and Villaquiran et al. (2018). The goats were divided into three groups according to BCS: BCS 1, BCS 2, and BCS 3. Blood samples were collected in the morning before slaughter. The female genital organs were collected immediately and transported to the laboratory for ovary examination, including follicles and corpus luteum (CL), and follicular fluid collection. Follicular fluid aspiration from ovaries was performed using an insulin syringe, and samples were collected regardless of follicle size. Serum samples and the supernatants of follicular fluid were separated by centrifugation at 3000 rpm for 15 min and immediately stored at −20°C until biochemistry analyses were carried out. The status of genital activity was then determined as cyclic or acyclic according to Azawi et al. (2008). Analysis of the biochemical parameters of serum and follicular fluid, that is total protein (TP), albumin (ALB), aspartate transaminase (AST), alanine transaminase (ALT), creatine phosphokinase (CK), blood urea nitrogen (BUN), creatinine, total cholesterol, low-density lipoprotein (LDL), high-density lipoprotein (HDL), triglycerides, total bilirubin, glucose, sodium (Na), potassium (K), chloride (Cl), phosphorus (P), calcium (Ca), magnesium (Mg), and iron (Fe) were carried out using a Cobas® 6000 analyser (Roche Diagnostics). Differences were assessed using a general linear model (GLM), followed by Duncan’s multiple range test (DMRT) for mean comparisons. Calculation of Pearson correlation coefficients between follicular fluid and serum levels of the same parameter (TP, glucose, cholesterol, Ca, P, and Mg) was performed. Statistical significance was set at P<0.05. All analyses were performed using SAS® software version 9.1.3. (SAS Institute Inc., 2002–2003).

Results and discussion

A recent study on metabolic and reproductive status in Kacang goats focused on animals with BCS of 1–3, based on the opinion of Jackson and Cockroft (2002) and Sharma et al. (2018) that the ideal BCS for fertility and reproduction performance is 2.5–3.5. The results of studies in cows showed that BCS is closely correlated to ovarian cycles (Grimard et al. 1992). Therefore, the aim of this study was to observe reproductive and metabolic status in animals with poor to ideal body conditions (BCS varying from 1 to 3). The study was conducted on 23 healthy doe goats. The results of the blood biochemistry analyses in all three animal groups are presented in Table 1.

Table 1. Blood biochemistry parameters of adult female Kacang goats with different levels of BCS.

Parameter	BCS 1 (n=8)	BCS 2 (n=7)	BCS 3 (n=8)
TP (g/dL)	7.74 ± 0.37^a	7.75 ± 1.10^a	7.23 ± 0.34^a
Albumin (g/dL)	3.57 ± 0.35^a	3.37 ± 0.36^a	3.58 ± 0.43^a
AST (U/L)	79.00 ± 11.63^a	78.83 ± 12.45^a	70.83 ± 17.10^a
ALT (U/L)	21.4 ± 4.89^a	17.00 ± 6.23^a	20.63 ± 7.95^a
CK (U/L)	153.00 ± 44.85^a	142.60 ± 25.47^a	177.40 ± 30.11^a
BUN (mg/dL)	19.16 ± 3.90^a	21.17 ± 5.62^a	21.37 ± 5.77^a
Creatinine (mg/dL)	0.87 ± 0.17^a	0.86 ± 0.17^a	1.02 ± 0.34^a
Cholesterol (mg/dL)	99.71 ± 17.02^a	99.67 ± 35.88^a	98.63 ± 17.49^a
LDL (mg/dL)	39.00 ± 7.62^a	46.17 ± 29.44^a	36.88 ± 7.40^a
HDL (mg/dL)	60.14 ± 10.40^a	56.67 ± 14.72^a	59.50 ± 12.39^a
Triglycerides (mg/dL)	27.71 ± 15.06^a	13.33 ± 3.44^b	23.25 ± 9.65^ab
Total bilirubin (mg/dL)	0.16 ± 0.07^a	0.18 ± 0.07^a	0.13 ± 0.04^a
Glucose (mg/dL)	54.00 ± 12.73^a	46.33 ± 11.55^a	48.71 ± 9.74^a
Na (mmol/L)	147.29 ± 2.14^a	145.33 ± 1.75^a	147.88 ± 3.04^a
K (mmol/L)	4.83 ± 0.31^a	4.51 ± 0.17^a	4.52 ± 0.57^a
Cl (mmol/L)	101.27 ± 2.59^a	101.65 ± 3.35^a	102.61 ± 4.16^a
P (mg/dL)	4.73 ± 1.15^a	4.65 ± 1.15^a	5.59 ± 1.53^a
Ca (mmol/L)	2.31 ± 0.12^a	2.32 ± 0.10^a	2.34 ± 0.12^a
Mg (mg/dL)	2.45 ± 0.19^a	2.42 ± 0.17^a	2.57 ± 0.18^a
Fe (ug/dL)	88.17 ± 19.55^a	87.40 ± 34.05^a	134.71 ± 25.89^b

^a,b Values with different superscripts in the same row indicate statistical differences (P<0.05).

Results of blood biochemistry analysis (Table 1) showed that the mean serum total protein and albumin concentrations of animals with BCS 1–2 were 7.74–7.75 mg/dL and 3.37–3.57 mg/dL, respectively. These values were not significantly different from those of animals with BCS 3, namely 7.23 and 3.58 mg/dL (P>0.05). Similarly, BUN and creatinine values of goats with BCS 1–2 were comparable to those of goats with BCS 3 (P>0.05). BUN is an indicator of protein metabolism (Roche et al. 2013) and is associated with protein intake or ureagenesis by hepatocytes (Strang et al. 1998; Macrae et al. 2006). The fact that no difference occurred in serum protein and BUN levels between the three BCS groups may indicate that protein intake and liver function did not differ significantly between groups. Furthermore, the serum levels of TP, ALB, creatinine, and BUN of animals in all groups in this study were also comparable to the reference values for these related parameters in goats (Stevens et al. 1994; Kraft and Dürr 1999) as well as the serum TP and ALB concentrations of healthy Boer and Saanen goats (Djuricic et al. 2011). These data also indicate that protein metabolism of Kacang goats in all BCS groups were within the normal physiological limit. According to Kraft and Dürr (1999), the parameters of BUN and creatinine in serum were related to renal function and rumen microbial digestion. Therefore, in this study, we found that the goats had normal renal and rumen digestion functions.

The enzyme activities of AST, ALT, and CK in Kacang goats with BCS 1–2 did not differ from Kacang goats with BCS 3 (P> 0.05). This indicated that the liver and muscle function of the animals in the BCS 1–2 groups were comparable to those of animals in the BCS 3 group. The serum levels of AST were lower, whereas CK levels of Kacang goats were comparable to those of healthy Boer and Saanen goats (Đuričić et al. 2008; Djuricic et al. 2011). Moreover, AST activity and BUN were equivalent to the related reference values for goats (Stevens et al. 1994; Kraft and Dürr 1999), possibly indicating the absence of abnormal liver function (Bobe et al. 2004) as well as degenerative changes in the muscles (Kraft and Dürr 1999; Carbone et al. 2012). BUN levels increase as protein intake or protein degradation is increased (Lee et al. 1978; Garcia-Bojalil et al. 1992; Watford 2003).

Serum lipids (total cholesterol, HDL, LDL, and triglycerides) and total bilirubin in goats with BCS 1–2 were not significantly different from the serum levels of goats with BCS 3 (P>0.05). This is in accordance with the findings in Boer and Alpine, where the total blood cholesterol or HDL levels of thin (BCS<2.75) and medium (BCS 2.75 – <3.50) animals were not significantly different (Barbosa et al. 2009; Đuričić et al. 2017). The total cholesterol levels of the goats in this study, which ranged from 98.63−99.71 mg/dL, were proportional to the physiological value for goats, that is 77–130 mg/dL (Kraft and Dürr 1999) and to the serum cholesterol level of Native Hair goats, 88.81 ± 5.25 mg/dL; Honamli goats, 90.51 ± 6.51 mg/dL (Devrim et al. 2015); Boer goats with medium body condition, 88.93 ± 16.24 mg/dL(Đuričić et al. 2017); and Alpine goats with medium body condition, 106.08 ± 5.9 mg/dL (Barbosa et al. 2009). Serum levels of triglycerides (13.33–27.71 mg/dL) were all comparable to the serum triglyceride levels of Native Hair goats, 19.86 ± 2.40 mg/dL, and Honamli goats, 26.01 ± 2.08 mg/dL (Devrim et al. 2015) as well as to the serum triglyceride levels of other ruminants (sheep), that is, 3–50 mg/dL (Kraft and Dürr 1999). Moreover, total bilirubin levels in the whole group of goats in a recent study were still in the physiological range of values for healthy goats, that is, up to 0.4 mg/dL (Kraft and Dürr 1999) and Mountain goats (Oreamnos americanus) (Rice and Hall 2007) or comparable to the total bilirubin level of clinically healthy adult female Saanen goats (Elitok 2012). These three biochemical blood parameters (cholesterol, triglycerides, and total bilirubin), which were in the physiological range, might indicate that these animals did not have bile duct disorders, metabolic disorders such as hypothyroidism, or hepatosteatosis (Kraft and Dürr 1999).

The mean levels of serum glucose in this study ranged from 46.33–54.00 mg/dL, showed no significant differences between the groups (P>0.05), and were in the physiologically healthy range for goats as stated in the literature (Stevens et al. 1994; Kraft and Dürr 1999). This finding agrees with the results of previous studies in Boer and Alpine goats with varying body condition scores from thin to obese (BCS 1-5) (Barbosa et al. 2009; Đuričić et al. 2017). Considering the results of studies on sheep, which showed that hypoglycaemia could suppress LH secretion (Clarke et al. 1990), and the results of studies on goats, which also confirmed that blood glucose levels are closely related to the regulation of GnRH release (Ohkura et al. 2004), Kacang goats with BCSs 1 and 2 may still have the ability to maintain GnRH regulator pulse activity. However, in comparison with the blood glucose levels of female Kacang goats (non-pregnant and non-lactating which were given adequate feed) reported previously, i.e. 73.88 ± 13.56 mg/dL (Widiyono et al. 2016), the Kacang goats’ blood glucose levels in the recent study were relatively low and needed intervention to attain optimum levels for regulation of GnRH release and the reproductive cycle.

The electrolytes (Na, K, Cl) and macrominerals (P, Ca, Mg) levels in the serum of Kacang goats with BCS 1–2 were in the normal physiological range of values for clinically healthy goats (Stevens et al. 1994; Kraft and Dürr 1999; Lérias et al. 2015) and also did not show significant differences from those goats with BCS 3 (P>0.05). These findings are consistent with those of Lérias et al. (2015), who studied electrolyte concentrations under different feeding and metabolic statuses in Majorera and Palmera goats. Meanwhile, serum iron levels of goats with BCS 1 and 2 ranged from 87.40–88.17 g/dL and were significantly lower than those of goats with BCS 3, which were 137.71 g/dL (P<0.05). However, compared with the reference value, all animals in this study had lower serum iron levels than the physiological value for small ruminants, which is approximately 200 µg/dL (Stevens et al. 1994; Bostedt and Dedie 1996). This could emphasise an existing subclinical iron deficiency in all groups of these Kacang goats. The significantly lower serum levels of iron in the BCS 1 and BCS 2 groups in this study highlight the likelihood of iron being a factor that may cause poor body condition in both groups of animals. According to Kumar et al. (2011), iron deficiency can lead to anaemia and decreased appetite and BCS, which in turn will result in a decrease in reproductive performance. Repeat breeding, an increased number of inseminations per conception, and abortion can be found in iron-deficient animals.

The results of the examination of Kacang goat ovaries are presented in Table 2. The numbers of small, medium and large follicles in the three animal groups did not differ significantly (P>0.05), but the numbers of small, medium and large follicles in the BCS 1 group tended to be lower than in the other groups with better body condition (BCSs 2 and 3). The tendency toward an increase in the number and development of ovarian follicles in animals with BCS 2 and BCS 3 might indicate an increase in follicular growth. Bindari et al. (2013) emphasised that follicular growth is often followed by increased production of reproductive hormones, and as a result, it can strengthen reproductive performance.

Table 2. Ovaries of Kacang goats with different BCS levels.

Parameter	BCS 1 (n=8)	BCS 2 (n=7)	BCS 3 (n=8)
Total small follicles(<2 mm)	4.29 ± 3.86^a	6.17 ± 4.58^a	12.38 ± 14.20^a
Total medium follicles(2–4 mm)	9.43 ± 4.89^a	9.67 ± 4.03^a	12.75 ± 4.47^a
Total large follicles (>4 mm)	1.43 ± 1.13^a	3.17 ± 1.94^a	2.14 ± 0.35^a
Total corpus luteum	0.00^a	1.67 ± 0.52^b	2.14 ± 0.35^b
Cyclic status	Acyclic (100%)	Cyclic (100%)	Cyclic (100%)

^{a b} Values with different superscripts in the same row indicate statistical differences (P<0.05).

The results of ovary examinations in the BCS 1 group showed that there was no CL or small CL in the ovary. Meanwhile, in the BCS 2 and 3 groups, CL was found, which tended to increase with increased body condition, i.e. 1.67 ± 0.52 and 2.14 ± 0.35, respectively. The number of CL could depict the number of ovulations that had occurred. These findings are in line with the results of a previous study of cattle, which showed that animals with a high energy balance spontaneously release multiple oocytes (two or more), whereas animals with a lower energy balance release one oocyte or may not even ovulate at all (Lucy et al. 1991). It is also in line with the results of a study on buffalo, which showed that reduced feed intake level (50% of NRC recommendations) resulted in decreased ovarian follicular development and ovulation (Hussein and Abdel-Raheem 2013). Moreover, animals with BCS 1 did not exhibit cyclicity (100% acyclic), whereas animals with BCSs 2 and 3 were cyclic. This finding was in accordance with the results of research in cattle, which emphasised that postpartum cyclicity was influenced by animal body condition. The percentage of cyclicity in animals with low BCS was lower than that in animals with higher BCS (Grimard et al. 1992). Furthermore, a study on lactating Holstein dairy cows has shown that BCS loss is a determining factor for delayed ovulation (Kafi and Mirzaei 2010).

The results of the chemical analyses of the ovarian follicular fluids of the three body condition groups are presented in Table 3. The mean glucose concentration in ovarian follicular fluid of the goats with BCSs 2 and 3 was 22.00 ± 9.14 mg/dL and 20.83 ± 7.29 mg/dL, respectively. It is comparable to the value found in sheep, 25.58 ± 3.60 mg/dL (Nandi et al. 2008), in Iraqi goats, 40.17 ± 24.07 mg/dL (Al-Hamedawi et al. 2017), as well as in cross-bred Malabari goats, 27.13 ± 9.25 mg/dL (Mohanan et al. 2019). Furthermore, the Ca and Mg concentrations of Kacang goats with BCS 3 (2.39 ± 0.05 mmol/L and 3.66 ± 0.37 mg/dL) were similar to the ovarian follicular levels in Iraqi goats, i.e. 2.61 ± 0.36 mmol/L and 2.77-5.32 mg/dL (Al-Hamedawi et al. 2017). Compared to Kacang goats with BCS 3, the animals with poor body condition (BCS 1) had significantly lower glucose, Ca, and Mg concentrations in their ovarian follicular fluid (3.25 ± 1.50 mg/dL, 2.10 ± 0.38 mmol/L, and 3.08 ± 0.61 mg/dL), respectively (P<0.05). The lower glucose concentration in ovarian follicular fluid of the animals with BCS 1 might be related to the findings that there were acyclic ovaries and no CL in the ovarium, or due to there being a dominating proportion of smaller and medium follicles in the poor BCS group. A previous study in sheep showed that acyclic sheep (ovaries without cycles) had lower glucose levels in their follicular fluid (Rufai et al. 2013). Moreover, Shabankareh et al. (2013) studied the chemical composition of follicular fluid of ovaries without CL and found that glucose concentrations in follicular fluid collected from small and medium follicles were significantly lower than those in follicular fluid collected from large follicles. Al-Hamedawi et al. (2017) suggested that glucose is an essential energy source for the ovaries, and therefore, low levels of glucose in the follicular fluid may indicate the absence of intensive glucose breakdown by the follicle. Furthermore, the lower glucose, Ca, and Mg levels in the BCS 1 group could also indicate a limited availability of energy sources and the lower metabolic process activity related to follicular development and steroid synthesis in this BCS 1 group. Nandi et al. (2007) studied the chemical composition of ovarian follicular fluids in relation to follicle size in sheep and found that Ca levels in the follicles are related to follicular development. It is suggested that Ca plays an important role in the regulation of ovarian steroidogenesis and ovulation. Al-Hamedawi et al. (2017) also reported the results of studies on Iraqi goats, which showed that in follicular fluids with high Ca and Mg concentrations, there were also high levels of oestrogen and progesterone, and vice versa. Dunlop and Malbert (2004) confirmed that Ca and Mg play an important role in regulating cell function and stimulating various biological responses.

Table 3. Ovarian follicular fluid biochemistry of Kacang goats with different BCS levels.

Parameters	BCS 1 (n=8)	BCS 2 (n=7)	BCS 3 (n=8)
Glucose (mg/dL)	3.25 ± 1.50^a	22.00 ± 9.14^b	20.83 ± 7.29^b
Ca (mmol/L)	2.10 ± 0.38^a	2.26 ± 0.10^ab	2.39 ± 0.05^b
Mg (mg/dL)	3.08 ± 0.61^a	3.30 ± 0.23^ab	3.66 ± 0.37^b
P (mg/dL)	10.02 ± 2.85^a	8.95 ± 1.32^a	12.04 ± 3.28^a
TP (g/dL)	5.78 ± 1.04^a	6.32 ± 1.08^a	6.04 ± 0.37^a
Albumin (g/dL)	2.68 ± 0.71^a	2.94 ± 0.42^a	3.00 ± 0.35^a
Cholesterol (mg/dL)	42.00 ± 8.28^a	49.83 ± 11.34^a	48.63 ± 8.70^a

^a,b Values with different superscripts in the same row indicate statistical differences (P<0.05).

The protein and cholesterol in the ovarian follicular fluids had average levels of 5.78-6.32 g/dL and 42.00-49.83 mg/dL, respectively. The ovarian follicular protein concentrations of the Kacang goats were higher than those of Black Bengal goats (4.24 ± 0.31 g/dL), but similar to those of sheep (6.17 ± 0.03 g/dL) and cross-bred Malabari goats (5.48 ± 0.62 g/dL) reported in previous studies (Mishra et al. 2003; Nandi et al. 2007; Mohanan et al. 2019). The albumin in the ovarian follicular fluids of Kacang goats had average levels of 2.68-3.00 g/dL. It is in accordance with the findings in cross-bred Malabari goats, 2.72 ± 0.76 g/dL (Mohanan et al. 2019). Meanwhile, the ovarian follicular cholesterol concentrations of the Kacang goats were lower than those of Black Bengal goats (95.57 ± 15.00 g/dL) (Mishra et al. 2003). The cholesterol concentrations in the ovarian follicular fluid were at a lower level than those in serum, i.e. 98.63-99.71 mg/dL (Table 1). Statistical analyses showed that there was a significant correlation between follicular fluid and blood total protein, albumin, and cholesterol levels (P<0.01, Table 4) in Kacang goats. This could imply that a substantial part of protein and cholesterol content in ovarian follicular fluid originates from the serum. The findings of a recent study in Kacang goats were similar to the findings of previous studies in cattle (Shabankareh et al. 2013). Furthermore, there were no significant differences in the mean levels of the ovarian follicular protein and cholesterol concentrations between the BCS groups of Kacang goats (P>0.05), although there was a tendency for animals with BCS 1 to have lower values. The lack of difference in cholesterol levels between body condition groups in these animals could illustrate the ability of goats to maintain steroid synthesis activity in follicles under unfavourable conditions. Wehrman et al. (1991) and Ryan et al. (1992) reported that the cholesterol content in the follicle plays a role in maintaining the activity of steroid synthesis. However, it is important to note that the cholesterol level in the follicular fluid of this Indonesian local goat (42.0.48.9 mg/dL) was lower than the previously reported sheep’s follicular fluid cholesterol level of 75.78 ± 11.21 mg/dL (Nandi et al. 2007), thereby possibly indicating insufficient fat intake in these Kacang goats. It is therefore interesting to consider that the performance of the reproductive organs (ovary) of Kacang goats can be improved through a higher-fat feeding approach. Wehrman et al. (1991) reported that administration of high-fat feed resulted in an increase in the number of medium follicles and the activity of steroid synthesis.

Table 4. Results of correlation analyses between serum and ovarian follicular fluid biochemistry parameters of Kacang goats with BCS 1–3 (n=23).

Parameter	Correlation Coefficient	Significance
Total protein	0.61048	0.0055
Albumin	0.69223	0.0010
Cholesterol	0.74651	0.0002
Glucose	−0.06047	0.8240
Mg	0.42947	0.0665
P	0.39288	0.0961
Ca	0.02186	0.9292

Conclusion

Based on the results of this study, the following conclusions can be drawn: the first, the blood metabolite profiles of Kacang goat were not significantly different regardless of the BCS level. However, the iron level of goats with poor BCS was significantly lower. Second, Kacang goats with poor body conditions showed ovarian dysfunction (inactive or acyclic) and low cholesterol, glucose, Ca, and Mg levels in ovarian follicular fluid, and third, the levels of TP, ALB, and cholesterol in follicular fluid were closely related to the level of blood metabolites.

Acknowledgements

The authors thank all staff at Department of Internal Medicine and Department of Physiology Faculty of Veterinary Medicine Universitas Gadjah Mada, who helped collected data for research.

Disclosure statement

No potential conflict of interest was reported by the author(s).

ORCID

Irkham Widiyono http://orcid.org/0000-0001-8082-9350

Sarmin Sarmin http://orcid.org/0000-0002-9116-4734

Yanuartono Yanuartono http://orcid.org/0000-0002-7090-8220

Additional information

Funding

This research was financially supported by the Ministry of Research,Technology, andHigher Education, Republic of Indonesia (Number 1823/UN1/ DITLIT/DIT-LIT/LT/2018).