ARTICLES

 

Effects of orégano essential oil and capsicum extract on fattening, serum constituents, and rumen fermentation of lambs

 

 

H .B. Ünlü^I; H.H. ipçak^II; Ç. Kandemir^I; M. Özdogan^{III, #}; Ö. Canbolat^IV

^IDepartment of Animal Science, Faculty of Agriculture, Ege University, izmir, Turkey
^IIDicle University, Agriculture Faculty, Department of Animal Science, 21280, Diyarbekir, Turkey
^IIIAdnan Menderes University, Agriculture Faculty, Department of Animal Science, 09010, Aydin, Turkey
^IVUludag University, Agriculture Faculty, Department of Animal Science, 16059, Bursa, Turkey

 

 

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ABSTRACT

This study investigated dietary supplementation of weaned lambs with Origanum vulgare essential oil and Capsicum oleoresin (chilli pepper) extract. Thirty-six eight-week-old male and female Menemen lambs were used in this study. Three dietary treatment groups consisted of T1, an unsupplemented control group; T2, a group supplemented with 300 mg/kg oregano essential oil, and T3, a group supplemented with 300 mg/kg Capsicum oleoresin. Feed and fresh water were available to the lambs ad libitum during the 56-day experiment. No significant effects of treatment were detected on growth rate, feed intake and feed conversion. In addition, serum urea, creatine, total protein, albumin, amylase, aspartate amino transferase (AST), alanine amino transferase (ALT), and gamma glutamyl transferase (GGT) levels did not differ among treatments on day 56 of the study. When oregano oil and capsicum extract were added to the feed, total volatile fatty acids (TVFA), acetate (AA), propionate (PA), butyrate (BA), isobutyrate (IBA), valerate (VA), and AA to PA ratio in the rumen were decreased significantly in comparison with the control group at two hours after feeding, with the effect of T2 being greater than that of T3. Female lambs had lower levels of TVFA than male lambs. Thus, although neither additive affected fattening performance and serum constituents of the lambs, both altered the rumen fatty acid profile.

Keywords: capsicum, lamb, oregano oil, performance, rumen parameters

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Introduction

High concentrate diets are generally used in intensive systems of fattening ruminant livestock. Within this framework, natural feed additives are crucial to maintaining animal health. The antagonistic interactions of amino acids and hexoses in the rumen pose threats to the health of animals (Busquet et al., 2006; Calsamiglia et al., 2007). The use of various feed additives has proved to improve efficiency, and decrease the production of methane and ammonia nitrogen through manipulation of the rumen microbiome (McGuffey et al., 2001). These additives include milled aromatic plants and their extracts. They have been reported to have physiological consequences for certain serum constituents, pancreatic hormones, digestive enzymes and rumen microflora (Babu & Srinivasan, 1997; Chaiyasit et al., 2009; Oh et al., 2017; Seirafy & Sobhanirad, 2017).

In vitro studies have shown that aromatic vegetable oils have antimicrobial and antibacterial effects (Adaszek et al., 2019; Maksimova et al., 2014; Burt, 2004), particularly oregano and chilli pepper extract. Whereas oregano oil is a phenolic compound (Veldhuizen et al., 2006), capsaicinoids (especially capsaicin, dihydrocapsaicin, nordihydrocapsaicin, homodihydrocapsaicin and homocapsaicin) are the main constituents of chilli pepper extract (Reyes-Escogido et al., 2011; Koffi-Nevry et al., 2012). In concentrate-based feeding programmes, chilli pepper extract has been shown to be effective in regulating rumen pH (Cardozo et al., 2005; Rodríguez-Prado et al., 2012). In vivo studies found that oregano and chilli pepper oils increase the performance and quality of animal products (Cardozo et al., 2006; Sanati et al., 2018). In addition, oregano and chilli pepper extracts and their secondary metabolites might act as modifiers of rumen fermentation in beef production systems (Cardozo et al., 2005; Cardozo et al., 2006; Castillejos et al., 2006; Calsamiglia et al., 2007; Foskolos et al., 2020). However, these additives have rarely been shown to modify serum constituents. It was thought that there was a need to evaluate further the consequences of using dietary oregano oil and chilli pepper extract on the performance, serum constituents and rumen fermentation parameters of fattening lambs.

 

Materials and Methods

This study was approved by Ege University Animal Care and Use Committee No. 2014-091. A total of 36 Menemen (Ile de France x Kivircik) male and female lambs, aged eight weeks, were used for the study. At the beginning of the experiment, the mean bodyweights (BWs) of male and female lambs for the three treatments were 19.15 ± 0.79 and 19.21 ± 0.79 kg, respectively. After being weighed, the animals were stratified by live weight and randomly allocated to T1, an unsupplemented control group, T2, a group supplemented with 300 mg/kg oregano essential oil, and T3, a group supplemented with 300 mg/kg chilli pepper extract. A total of 12 lambs (six males and six females) were assigned to each group. They were housed in individual pens (2 m²/lamb) for the duration of the experiment.

Oregano essential oil was obtained by steam distillation from selected Oregano onites ssp. growing wild in Turkey. The carvacrol and thymol contents, which are the most active compounds of oregano essential oil, were 85.87% and 7.81%, respectively. Chilli pepper extract, which contains 99% Capsicum oíeoresin, was obtained by steam distillation from selected Capsicum annuum L. The basal diet met the nutrient requirements (NRC, 1985) of animals for roughage and concentrate feed (Table 1). The diets and drinking water were offered ad libitum. The study was conducted over a feeding period of 56 days. Live weights (LW) and dry matter intake (DMI) were recorded at 14-day intervals, and daily weight gain (DWG) and FCR were calculated. The lambs were slaughtered at a commercial slaughterhouse at the end of the experiment.

Nutrient contents of the dietary ingredients and concentrate that were fed to the lambs were analysed according to the AOAC (1997), namely dry matter (DM) (method 934.01), ash (method 942.05), crude protein (CP) (method 990.03), ether extract (EE) (method 920.39), and crude fibre (CF) (method 962.09). The sugar content of the materials was determined by the Luff-Scroll method and their starch by the polarimetric method (AOAC, 1997). Neutral detergent fibre (NDF) and acid detergent fibre (ADF) contents were determined following Van Soest et al. (1991). Phosphorus (P) contents of the materials were read by spectrophotometer (Double Beam UV-V15, Perkin Elmer, Waltham, Massachusetts, USA) by calorimetric methods. Atomic absorption spectroscopy (Ultrospec 2100 Pro UV-visible spectrophotometer, Biochrom US, Holliston, Massachusetts, USA) was used to determine calcium (Ca) concentration. Metabolizable energy (ME, kcal/kg) content of the diet was predicted in kcal/kg^-1 of DM from its CP, CF, and EE contents (TSI, 1991):

At the beginning and end of the experiment, 10 ml of blood was drawn from the jugular vein of each animal at 10:00. The blood samples were brought to the laboratory at 4 °C. In the laboratory, the serum was harvested and urea, creatine, protein, albumin, amylase, AST, ALT and GGT contents were measured using a filtered photometric method on the Biotecnica BT-2000 Plus device (Biotecnica Instruments, Rome, Italy).

At the end of the experiment, two hours after feeding, 50 ml of rumen fluid was drawn from each animal with a rumen probe to measure pH, TVFA, AA, PA BA, IBA, VA, and IVA to assess rumen fermentation. The pH of the rumen fluid was measured in the digital pH meter. Then these samples were filtered, 0.5 ml 1 M hydrochloric acid was added, and stored at -20 °C until the VFAs were determined (Erwin et al., 1961). For the analysis of VFA in the rumen fluid, 5-7 ml rumen fluid was centrifuged at 4 °C (6000 rpm, 10 minutes). Then 5 ml rumen liquid was decanted into a new centrifuge tube to which 1 mL of metaphosphoric acid was added and held for 30 minutes. After this process, the tubes were centrifuged again (3000 rpm) and the supernatant was separated and put into Eppendorf tubes. The VFA contents of the samples were measured with a gas chromatography device (Agilent Technologies, Anaheim, California, USA). The detector temperature was programmed at 260 °C, injection temperature was 250 °C, oven temperature is programmed from 45 °C to 250 °C with gradual 2 °C increases, and hydrogen gas transition rate was 30 ml/min. Each sample was analysed twice (Erwin et al. 1961).

The data were subjected to analysis of variance using the general linear model procedure of SPSS (version 25, IBM Inc., Chicago, Illinois, USA). Effect of treatment and sex was determined from a two-way analysis of variance with interaction. Differences among treatment were determined using Duncan's multiple range test. Differences were considered significant based at the 0.05 level of probability.

 

Results and Discussion

The treatment by sex interaction was not significant for any of the traits (P >0.05). Oregano oil and capsicum extract supplementation had no effect on final BW, DWG, DMI and FCR. However, male lambs grew faster than female lambs and were heavier at the end of the experiment (P <0.01). The effects of oregano oil and capsicum extract supplementation on fattening performance, FI and FCR of lambs are given in Table 2.

The effects of oregano oil and capsicum extract supplementation on the serum constituents of the lambs are given in Table 3. Oregano oil and capsicum extract supplementation had no significant effect on the serum constituents. Nor did the interaction of treatment and sex. However, serum urea concentration was higher in female lambs than in male lambs (P <0.05).

Oregano oil supplementation decreased the TVFA, AA, PA, BA, IVA, VA, and AA/PA contents of the rumen fluid and increased its pH. Conversely, capsicum extract supplementation decreased the total VFA, AA, PA, and IBA concentrations and pH. The treatment by sex interaction affected TVFA and PA concentrations and pH (P <0.05). The effects of oregano oil and capsicum extract supplementation on serum parameters of lambs are given in Table 4.

Whereas oregano leads in the increasing demand for aromatic plants in the world, chilli pepper extract is preferred because of its unique aroma and secondary metabolites, which are effective in rumen fermentation. In this study, the diets did not detectably affect LW, DWG, DMI and FCR. However, male lambs grew faster than females and were therefore heavier at the end of the study, a finding that was consistent with previous studies (Kashan et al., 2005; Ozdogan et al., 2011; Mohammed et al., 2017). The sexes responded to the dietary supplements in a similar manner. Canbolat et al. (2018) reported that DWG of lambs decreased (P <0.05) linearly with increasing amounts (0, 400, 800, 1200 mg/kg DM) of oregano oil in their diets. These effects were coincident with numerically negative changes in LW, DMI and FCR. Chen et al. (2019) found that lambs that consumed 0, 86 and 172 mg/day of a mixture of Capsicum oíeoresin and sweetener decreased their DMI linearly (P = 0.06) with increasing concentrations of the Capsicum oíeoresin and sweetener, although DWG and FCR were not affected.

No differences were seen between the treatments in the constituents of the serum profile (urea, creatine, total protein, albumin, amylase, AST, ALT and GGT). Effects of gender and the interaction of treatment with gender were not detected. Previously, increased levels of dietary oregano oil have resulted in decreased serum glucose, urea, TVFA, and triglyceride levels (Canbolat et al., 2018). However, these effects were consistent across studies because serum cholesterol, triglyceride, high-density lipoprotein, and low-density lipoprotein of lambs were not affected by the addition of 250 and 500 ppm oregano essential oil (Unal & Kocabagli, 2014). Further, only serum insulin was found to be affected by diets containing 0, 86 and 172 mg/day Capsicum oíeoresin and sweetener from among the group of serum constituents that were analysed, including beta-hydroxybutyrate, non-esterified fatty acids, insulin, glucose, and cortisol (Chen et al., 2019).

Additional studies evaluated the changes in rumen function and its microbial population resulting from dietary inclusion of oregano oil and hot pepper extracts (Klevenhusen et al., 2012; Cobellis et al., 2015; Oh et al., 2015; Oh et al., 2016). Secondary effects were said to alter intestinal physiology, increasing mucosal blood flow rate and animal health (Cardozo et al., 2006; Sordillo & Aitken, 2009; Weiss & Wardrop, 2010; Holzer, 2011; Hashemzadeh-Cigari et al., 2014; Alford et al., 2016; Adaszek et al., 2019). In the current study, the TVFA, AA, PA, BA, IBA, VA, and the AA/PA values were significantly lower in the rumen of lambs fed diets containing oregano oil or Capsicum oíeoresin extract than in the the control group two hours after feeding, with oregano oil having greater effects than Capsicum oíeoresin. This result was believed to have been caused by suppression of the microorganism population in the rumen. However, changes in TVFA, AA, PA, AA to PA ratio, and rumen pH, although negative, were not significant in response to supplementation with 12% or 4.21% oil from oregano (Oh et al., 2015; Olijhoek et al., 2019). It has been claimed that supplying oregano essential oil could enhance the growth of certain rumen microbial populations, but the shifts were influenced by the amount of oil that was provided, with a low amount being favourable for rumen microbial populations, and higher amounts being detrimental to those populations (Zhou et al., 2019). Selenomonas are known to be more sensitive to oregano oil than Streptococcus bovis and thus the lactate produced by S. bovis cannot be metabolized rapidly by Selenomonas (Calsamiglia et al., 2007), resulting in an accumulation of lactic acid.

Adding 300 mg oregano oil or Capsicum oíeoresin extract to the diet was insufficient to alter the rumen pH of the lambs in the current study. However, the additions of 300 mg oregano oil and Capsicum oíeoresin extract produced a numerically greater rumen pH than in the control group. Previously, supplementation with oregano oil decreased the pH of rumen fluid (Castillejos et al., 2008). However, supplementation with 500 mg/day capsicum extract did not produce detectable effects on rumen pH, PA, AA, and AA to PA ratio, TVFA, and AA to butyrate ratio (Fandiño et al., 2008).

Female lambs had lower levels of rumen VFAs than male lambs in this study. This might be the result of differences in the rumen microbial populations, because Li et al. (2019) observed that heifers had significantly greater numbers of bacteria and fewer arachea than bulls.

 

Conclusions

Diets containing oregano oil or Capsicum oíeoresin extract had neglible effects on the fattening performance and serum constituents of weaned lambs. However, total VFA, AA, PA, BA, IBA, IVA, VA and the AA/PA ratio in the rumen were lower at two hours after feeding in control lambs than those supplemented with oregano oil and Capsicum oíeoresin extract. Dietary supplementation with oregano oil had a greater effect on the rumen VFA than Capsicum oíeoresin extract. Thus, while these additives did not impinge on the fattening performance or serum constituents of the lambs, they had positive effects on rumen physiology.

 

Acknowledgements

This study was supported by Ege University Scientific Research Projects Directorate under Grant 2016-ZRF-070.

 

Authors' Contributions

HBÜ and HI designed the study. HBÜ and ÇK executed the study. HBÜ, MÖ and ÖC implemented the study and analysed the samples. HBÜ, Hi and ÇK drafted the manuscript.

 

Conflict of Interest Declaration

There is no conflict of interest.

 

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Received 22 November 2020
Accepted 31 December 2020
Published 25 February 2021

 

 

# Corresponding author: ozdoganmursel@gmail.com