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The Effect of Butterfly Pea Flower Extract on Broilers Raised in High-Density Environments (Impact on Performance, Blood Profile and Gut Microbes)

Widya Citra1, Nur Sjafani2, Yusri Sapsuha2,*
1Master of Agricultural Science, Graduate Program, Universitas Khairun, Ternate, North Maluku, Indonesia.
2Department of Animal Science, Faculty of Agriculture, Universitas Khairun, Ternate, North Maluku, Indonesia.

ABSTRACT

Background: High-density farming systems can lead to oxidative stress and negatively impact broiler performance. Antibiotic growth promoters (AGPs) were used to improve broiler performance under stress conditions. However, long-term use of AGPs can lead to antibiotic resistance in humans as consumers. Therefore, the use of AGPs is now banned in broiler production. This study aimed to evaluate the effects of butterfly pea flower extract on the performance, blood profile and gut microbes of broilers raised in high-density environments. 

Methods: After 15 days of rearing, 370 unsexed Lohmann broiler chicks were assigned to five treatments in a completely randomized design, consisting of CONT+, CONT-, BPE0.5, BPE1.0 and BPE1.5. Sampling was conducted on day 35.

Result: The results indicated that the inclusion of butterfly pea flower extract in the diet of broilers raised at a high density (16 birds/m²) significantly (p<0.05) improved performance, lowered the pH in the ileum and cecum, increased lactic acid bacteria and reduced coliform bacteria in both the ileum and cecum. There was no significant effect (p>0.05) on the blood profile of broilers. 

 

INTRODUCTION

Broiler farming in Indonesia is one of the key industries as it fulfills the community’s need for animal protein, particularly in the form of chicken meat, which is an affordable and accessible source of protein. The efficiency of broiler farming is crucial for achieving maximum production outcomes with minimal operational costs. Implementing high stocking density in broiler farming is one strategy to increase meat production per square meter, thereby maximizing profits. However, high-density farming systems can lead to oxidative stress and negatively impact broiler performance and health (Abudabos et al., 2013). Previously, antibiotic growth promoters (AGPs) were used to improve broiler performance under stress conditions (Haque et al., 2020). However, long-term use of AGPs can lead to antibiotic resistance in both livestock and humans as consumers. Therefore, the use of AGPs is now banned in broiler production worldwide, including in Indonesia. Without AGPs, broiler farming under high stocking density has been reported to result in performance issues (Altaf et al., 2019). For sustainable broiler production, it is crucial to find safe alternatives to AGPs. Efforts have been made to address performance and health issues in broilers reared under high-density conditions during the ban on antibiotic use (Magnuson et al., 2020, Sugiharto et al., 2022).
       
Modern knowledge suggests that plant extracts contain phenolic compounds that can function as antioxidants (Oso et al., 2021). Butterfly pea flower (Clitoria ternatea L.) is one such plant with a high antioxidant content, making it a potential source of natural antioxidants (Niranjan et al., 2020; Sapsuha et al., 2023). Butterfly Pea Flower belongs to the Papilionaceae or Fabaceae family (legumes). Previous research has shown that butterfly pea flowers contain bioactive compounds such as flavonoids, phenols and terpenoids, which can function as antibacterial, antifungal and antioxidant agents (Seftiono et al., 2021, Sapsuha et al., 2023). These compounds have the ability to fight free radicals in the body, which can cause cell damage and various diseases. Therefore, the use of butterfly pea flower extract is expected to replace the role of AGPs, which have been banned from use.
       
Our previous study showed an improvement in broiler performance when butterfly pea flower extract was included in feed mixtures (Sapsuha et al., 2023). The bioactive compounds and antioxidant capacity found in butterfly pea flowers can effectively improve physiological conditions, resulting in better broiler growth performance (Sapsuha et al., 2023). To our knowledge, there is no prior documentation on the use of butterfly pea flower extract in broilers under stress conditions. Therefore, we investigated the impact of butterfly pea flower extract on the performance, blood index and gut ecology of broilers reared under stress conditions caused by high stocking density. We hypothesize that butterfly pea flower extract can improve the performance, blood profile and gut microbes of broilers raised in high-density conditions.

MATERIALS AND METHODS

Preparation of butterfly pea flower extract
 
Butterfly pea flowers were obtained from gardens around the campus of Universitas Khairun in Ternate, North Maluku Province, Indonesia. Before use, the butterfly pea flowers were air-dried and ground into powder. One kilogram of butterfly pea flower powder was extracted using the maceration technique by soaking it in 4 liters of 96% ethanol solution for 3x24 hours. During the maceration process, stirring was done twice a day, in the morning and evening. The resulting filtrate was then filtered and evaporated using a rotary evaporator to obtain butterfly pea flower extract (Sapsuha et al., 2023).
 
In vivo experiment
 
The Animal Ethics Committee of the Faculty of Agriculture, Universitas Khairun (No. 15/KEPH/PH/2024) approved this study. The trial was carried out on May to June 2024 in the experimental cage Department of Animal Science, Faculty of Agriculture, Universitas Khairun. A total of 370 unsexed Lohmann broiler chickens were reared collectively with normal stocking density from day 0 to day 14. On day 14, the broilers (with a body weight of 425.65±2.63 g) were randomly assigned to five treatments, with each treatment replicated five times: CONT+ (positive control with normal stocking density of 10 birds/m²), CONT- (negative control with high stocking density of 16 birds/m²) and BPE0.5, BPE01.0 and BPE1.5 with high stocking density of 16 birds/m². The feed provided was in mash form and formulated (Table 1) as starter feed (days 1-21) and finisher feed (days 22-35). Butterfly pea flower extract was added to the feed starting on day 14 at 0.5, 1.0 and 1.5 ml/kg for BPE0.5, BPE01.0 and BPE1.5 respectively, while no butterfly pea flower extract was added to the feed in CONT+ and CONT- treatments. During the rearing period, the broilers were housed in ventilated broiler cages with sawdust as bedding.

Table 1: Feed compositions of broilers as starter (days 1-21) and finisher (days 22-35).


 
Data collection and analysis
 
Body weight gain, feed intake and feed conversion ratio (FCR) were recorded weekly. On day 35, blood samples were collected from male chicks representing the average body weight of each pen via the brachial vein in the wing. Blood samples were collected from each bird for every replicate (five birds per treatment). To avoid physiological differences related to sex and body weight, male chicks with body weight reflecting the average weight of each pen were used for blood sampling.
       
For practical reasons, the chickens from which blood samples had been previously taken were slaughtered and their internal organs were subsequently removed. The internal organs of the experimental chickens were collected and weighed using an analytical balance. To measure the gut bacterial population, digesta was taken from the ileum and cecum and placed in sterile sample containers. Digesta was also collected from the duodenum, jejunum, ileum and cecum to measure pH values (using an electronic pH meter; Thermo Fisher Scientific Inc.). The complete blood profile was determined using the Prima Fully-Auto Hematology Analyzer (PT Prima Alkesindo Nusantara, Jakarta, Indonesia) following the manufacturer’s protocol.
       
The study was conducted based on a completely randomized design. The obtained data were analyzed using ANOVA (SPSS version 16.0) and Duncan’s Multiple Range Test was employed to differentiate statistically significant means (p<0.05).

RESULTS AND DISCUSSION

Broiler performance
 
Table 2 presents the performance of broilers raised under high-density conditions and given butterfly pea flower extract. Broilers raised under normal stocking density (CONT+) had significantly higher body weight (p<0.05) compared to broilers raised under high-density conditions without butterfly pea flower extract (CONT-). Throughout the rearing period, higher body weight gain (p<0.05) was observed in the CONT+, BPE0.5, bpe1.0 and bpe1.5 groups compared to the negative control (CONT-), while no significant differences (p>0.05) were observed between the positive control (CONT+; normal stocking density of 10 birds/m²) and the butterfly pea flower extract treatments (BPE0.5 and BPE1.0).

Table 2: Performance of broilers chickens.


       
Our study showed that raising broilers in high-density conditions reduced final body weight, weight gain and feed intake. Several studies have shown that high stocking density is associated with impaired growth and reduced feed efficiency in broilers (Yin et al., 2017, Gholami et al., 2020). Other research has also demonstrated a significant reduction in weight gain with increasing stocking density (Son, 2013, Adeyemo et al., 2016, Esmaeili-Fard et al., 2022). The decline in broiler growth performance under high-density conditions can be attributed to several factors, including increased temperature and reduced air circulation, increased stress and restricted space in the pen, which limits growth and feed access, potentially leading to nutritional deficiencies (Shakery et al., 2014, Sugiharto, 2022).
       
The current study shows that butterfly pea flower extract can mitigate the negative impact of high stocking density on broiler growth performance. To date, no research has been available in the literature explaining the effects of butterfly pea flower extract on weight gain improvement in broilers raised under high-density conditions. However, the effectiveness of butterfly pea flower extract is likely attributable to the synergistic action of various phytochemicals present in the flower (Lijon et al., 2017, Sapsuha et al., 2023) which in turn may improve the physiological conditions of the chickens. These improved conditions enhance feed utilization and efficiency, leading to better growth performance in broilers. Phytochemicals such as flavonoids, phenols and saponins have been reported to promote higher growth rates and better feed efficiency in broilers due to their ability to scavenge/neutralize free radicals and maintain the integrity of the intestinal mucosa (Zhou et al,. 2019; Essien and Udoh, 2021, Chen et al., 2021). Additionally, previous studies have shown that butterfly pea flower extract has antibacterial properties (Nguyen et al., 2016, Sapsuha et al., 2023) that can stimulate the growth of beneficial bacteria, deactivate pathogenic bacteria and enhance nutrient metabolism and absorption in the digestive tract, ultimately improving broiler growth performance.
       
Regarding feed consumption, it was observed that the inclusion of butterfly pea flower extract resulted in higher feed intake (p<0.05) during the rearing period. The addition of butterfly pea flower extract led to a lower feed conversion ratio (p<0.05) compared to the negative control (CONT-). However, the inclusion of 0.5 ml/kg butterfly pea flower extract in the diet (BPE0.5) did not result in a significant difference in feed conversion ratio (p>0.05) compared to the negative control (CONT-).
       
In terms of feed intake, the administration of butterfly pea flower extract appears to increase feed consumption, which in turn can lead to weight gain. The inclusion of plant extracts has been reported to enhance the palatability and flavor of feed, thereby increasing feed intake and weight gain (Hussein et al., 2020; Tavangar et al., 2021). The improved feed conversion observed in broilers given butterfly pea flower extract provides evidence of better feed utilization. The use of plants as phytogenics in broiler feed can improve intestinal digestibility, ultimately promoting broiler growth (Mahanta et al., 2017, Huang et al., 2018).
 
Relative weight of broiler internal organs
 
The results showed that raising broilers under high-density conditions had no significant effect (p>0.05) on the weight of internal organs, abdominal fat and carcass traits of broilers (Table 3 and Table 4). Our study shows that the weight of internal organs and abdominal fat of broilers raised under high-density conditions is relatively similar to those raised under normal stocking density. This aligns with reports from several researchers indicating that stocking density does not have a significant impact on the weight of internal organs and abdominal fat in broilers (Yin et al., 2017, Sugiharto et al., 2022). Similarly, Toghyani et al. (2011) and Mareta
et al. (2020) found no effect of cinnamon, garlic and bilimbi on the relative weight of internal organs in broilers.

Table 3: Organs weight of broiler chicks fed treatment diets.



Table 4: Carcass traits of broiler chicks fed treatment diets.


 
Broiler blood profile
 
Table 5 presents the blood profile of broilers raised under high-density conditions. The results indicated that the administration of butterfly pea flower extract to broilers raised under high-density conditions had no significant effect (p>0.05) on the blood profile of broilers. Our study also shows that raising broilers under high-density conditions did not affect their blood profile. The exact reason for this condition is unknown, but raising broilers in high-density conditions from day 14 to 35 may have allowed them to adapt to the environment, thereby compensating and adjusting their physiological mechanisms to cope with the stress. Our previous research (Sapsuha et el., 2021) also showed no effect of nutmeg flesh extract on broilers raised under high-density conditions.

Table 5: Blood profile of broiler chickens.


 
pH values and gut bacterial count in broilers
 
Table 6 presents the pH values and gut microbiota of broilers raised under high-density conditions. The results show that the administration of butterfly pea flower extract to broilers raised in high-density conditions significantly (p<0.05) reduced the pH in the ileum and cecum, with no significant effect (p>0.05) on the pH of the duodenum and jejunum. The data in Table 6 also indicate that the administration of butterfly pea flower extract to broilers raised under high-density conditions significantly (p<0.05) increased lactic acid bacteria and significantly (p<0.05) reduced coliform bacteria in the ileum and cecum.

Table 6: pH and bacterial population of broiler chickens fed treatment diets.


       
Our study also shows that raising broilers under high-density conditions did not affect their blood profile. The exact reason for this condition is unknown, but raising broilers in high-density conditions from day 14 to 35 may have allowed them to adapt to the environment, thereby compensating and adjusting their physiological mechanisms to cope with the stress. Raising broilers under high-density conditions can increase the pH in the cecum. Similar results were reported by Jang et al., (2014) and Tsiouris et al., (2015), who observed an increase in cecal pH in broilers raised under high-density conditions. It was further suggested that the rise in cecal pH might result from reduced litter quality, which affects the gut microbiota. The administration of butterfly pea flower extract to broilers raised under high-density conditions can lower the pH in the ileum and cecum. The carbohydrate content, especially oligosaccharides found in nearly all plants, can serve as a good substrate for fermentation processes that support the growth of beneficial microbes (Blajman et al., 2015).
       
The acidic conditions in the digestive tract, particularly in the ileum and cecum, support the balance of gut microflora, where lactic acid bacteria populations increase and pathogenic bacteria populations decrease (Dittoe et al., 2018). Lactic acid bacteria produce lactic acid, which helps maintain the acidic pH of the broiler’s digestive tract. Additionally, the acidic environment in the digestive tract can enhance the effectiveness of nutrient absorption by the intestinal walls, ensuring nutritional needs are met, health status is maintained and productivity is increased (Blajman et al., 2015, Sjofjan et al., 2021). Regarding stocking density, raising broilers under high-density conditions can reduce lactic acid bacteria and increase coliform bacteria in the ileum and cecum. The effects of rearing broilers at high density can cause stress (Sugiharto et al., 2022), characterized by changes in behavior, biochemistry and physiology, all aimed at restoring homeostasis, which ultimately alters the composition of gut microbes.
       
The results of this study show that the administration of butterfly pea flower extract to broilers raised under high-density conditions can increase lactic acid bacteria and reduce coliform bacteria in the ileum and cecum. The reason why butterfly pea flower extract has a positive impact on gut microbes is that it contains active components that can act as antibacterial agents (Lijon et al., 2017, Sapsuha et al., 2023), thus supporting the growth of beneficial bacteria and inhibiting pathogenic bacteria (Nguyen et al., 2016; Sapsuha et al., 2023). Additionally, the carbohydrate content, particularly oligosaccharides found in nearly all plants, can serve as a good substrate for the growth of beneficial microbes.

CONCLUSION

The administration of butterfly pea flower extract up to 1.5 mL/kg of feed can improve performance, increase the total lactic acid bacteria and reduce the total coliforms without causing negative effects on the blood profile of broilers raised under high-density conditions.

ACKNOWLEDGEMENT

The present study was supported by Ministry of Education, Culture, Research and Technology, Republic of Indonesia, through “Penelitian Pascasarjana Tesis Magister (PTM)” scheme, year 2024 (Contract No. 055/E5/PG.02.00.PL/2024; 414/PEN-PKDN/PG.12/2024).

DISCLAIMERS

The views and conclusions expressed in this article are solely those of the authors and do not necessarily represent the views of their affiliated institutions. The authors are responsible for the accuracy and completeness of the information provided, but do not accept any liability for any direct or indirect losses resulting from the use of this content.

INFORMED CONSENT

All animal procedures for experiments were approved by the Committee of Experimental Animal care and handling techniques were approved by the Animal Ethics Committee of the Faculty of Agriculture, Universitas Khairun (No. 15/KEPH/PH/2024).

CONFLICT OF INTEREST

The authors declare that there are no conflicts of interest regarding the publication of this article. No funding or sponsorship influenced the design of the study, data collection, analysis, decision to publish, or preparation of the manuscript.

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