ABSTRACT
This study aimed to assess the impact of incorporating Citrullus colocynthis fruit pulp (CCFP) into the diet of broiler chickens as a replacement for antibiotic growth promoters (AGPs) on growth performance, blood biochemistry, and intestinal microbial count. A total of 600 unsexed Ross-308 day-old broiler chicks were randomly assigned to 6 groups using a completely randomized design. Each group had 5 replicates, with 20 chicks per replicate. The study included a control group (T1) that did not receive any CCFP or AGP supplementation. The other experimental groups were as follows: T2 (0.15 g/kg AGP, 0 g/kg CCFP), T3 (0.11 g/kg AGP, 0.75 g/kg CCFP), T4 (0.075 g/kg AGP, 1.5 g/kg CCFP), T5 (0.037 g/kg AGP, 2.25 g/kg CCFP), and T6 (0 g/kg AGP, 3 g/kg CCFP). The results indicated a reduction in feed intake (p = 0.045) in group T3 compared to the control group (T1). Blood biochemical analysis showed that group T6 had higher levels of serum total protein (p = 0.050) and globulin (p = 0.044) compared to the control group (T1). The cecal microbial count revealed a lower total bacterial count (p = 0.01) in groups T2 and T3, and a reduced E. coli count (p = 0.050) in group T3 compared to the group T5. However, the ileal microbial count showed no significant differences between treatments. In conclusion, these findings suggest that a diet containing 0.75 g/kg CCFP combined with 0.11 g/kg AGP may improve the growth of broiler chickens while maintaining a healthy microbial balance.
Keywords: Citrullus colocynthis fruit pulp; antibiotics; blood biochemistry; microbial count
INTRODUCTION
Between 1961 and 2020, world poultry meat production increased from 9 to 133 million tonnes (FAO, 2020). During this period, most poultry feeds contained antibiotic growth promoters (AGPs) to enhance production efficiency. However, rising concerns over AGPs’ contribution to antibiotic resistance in humans prompted the European Union to enforce a complete ban on all AGPs in animal feed in January 2006 (Milanov et al., 2016). Other countries, including the USA, Canada, Mexico, Japan, Hong Kong, China, and India, have also imposed restrictions on antimicrobial use in animal feed. The USA in particular has focused on reducing antibiotic use in food animal production, and since 2017, FDA regulations have prohibited the use of antibiotics for growth promotion (Salim et al., 2018). In some countries, the regulations for obtaining veterinary prescriptions for administering antibiotics in food animals remain limited. The use of AGPs in poultry can alter the composition and function of gut microflora (Al-Dobaib & Mousa, 2009), and these changes can negatively impact nutrient absorption and gut health (Miyakawa et al., 2024). To address this issue, various alternatives to AGPs are being utilized, including vitamins, minerals, enzymes, amino acids, organic acids, phytobiotics, probiotics, prebiotics, and synbiotics (Ahmad et al., 2022; Yilmaz & Gul, 2023). Among these, phytobiotics such as Citrullus colocynthis (CC) are regarded as highly effective natural growth stimulants. Additionally, there is a growing consumer preference for chickens raised on fully natural diets (Nuriyasa et al., 2022).
The Cucurbitaceae family is highly valued for its medicinal properties and has been extensively researched, comprising over 800 species and 130 genera (Dhiman et al., 2012). Among these, Citrullus colocynthis is particularly notable for boosting immunity, promoting growth, and serving as an alternative to AGPs. Known for its bitter taste, dry texture, and spongy pulp, CC is prized for its therapeutic, pharmacological, and nutraceutical benefits (Gurudeeban et al., 2010). CC contains a variety of compounds such as carbohydrates, proteins, saponins, steroids, amino acids, tannins, phenolics, flavonoids, terpenoids, flavone glucosides, alkaloids, cucurbitacins, cardiac glycolipids, and microelements. These compounds contribute to its antimicrobial, anti-inflammatory, anticancer, antidiabetic, gastrointestinal protective, analgesic, and other medicinal effects (Al-Snafi, 2016). Additionally, CC has growth-promoting properties, and its dry pulp is traditionally used to treat gastrointestinal issues such as indigestion, gastroenteritis, and intestinal parasites. Both globally and in Pakistan, there is very limited data on the effects of Citrullus colocynthis fruit pulp (CCFP) on broiler performance. Kamran et al. (2021) conducted a study exploring the impact of Citrullus colocynthis fruit powder on broiler performance, but they only tested two levels of powder inclusion, leaving a gap in knowledge regarding the optimal CCFP level in broiler diets in Pakistan. It was hypothesized that adding CCFP to broiler diets could provide performance benefits similar to those of AGP-containing diets while being more cost-effective. Therefore, this study aimed to evaluate the effects of dietary CCFP supplementation on broiler growth performance, blood biochemistry, and intestinal microbial count.
MATERIALS AND METHODS
Animal welfare
The experiment was conducted in accordance with the approved guidelines established by the Ethical Review Committee of Cholistan University of Veterinary and Animal Sciences (CUVAS), Bahawalpur, Pakistan.
Experimental site, study design, and birds’ husbandry
The trial was conducted in an environmentally controlled house at the Islamia University of Bahawalpur, Pakistan. A total of 600 unsexed day-old Ross-308 broiler chicks were obtained from a hatchery and divided into 6 dietary groups, using a completely randomized design (CRD). Each group consisted of 5 replicates, with 20 chicks per replicate. The control group (T1) received no CCFP or AGP supplementation, while the other experimental groups were as follows: T2 (0.15 g/kg AGP, 0 g/kg CCFP), T3 (0.11 g/kg AGP, 0.75 g/kg CCFP), T4 (0.075 g/kg AGP, 1.5 g/kg CCFP), T5 (0.037 g/kg AGP, 2.25 g/kg CCFP), and T6 (0 g/kg AGP, 3 g/kg CCFP). The CC fruits and lincomycin (4.4%) used as AGP were procured from the local market. The CC fruits were sun-dried and ground into fine powder using a commercial grinder to make CCFP. The powder was then chemically analyzed in the Nutrition laboratory at CUVAS, following the methods of AOAC International (2005). The proximate composition of CC powder is given in Table 1. The chicks were housed in 30 floor pens with rice husk litter as bedding, maintaining a stocking density of 5 birds per 1 m2. Each pen (2 × 2 m2) was equipped with four round feeders and two nipple drinkers to provide feeding and clean drinking water ad libitum. The chicks were vaccinated against infectious bronchitis and Newcastle disease at the hatchery. During the first week after hatching, the brooding temperature and relative humidity were maintained at 34 ± 1.1°C and 62 ± 3%, respectively. The temperature was then gradually decreased by 3°C per week until it reached 24°C on day 21, with a relative humidity of 65%. Throughout the study, a lighting schedule of 23 hours of light and 1 hour of darkness was implemented. A corn-based basal diet was formulated for the starter (1 to 11 days), grower (12 to 21 days), and finisher (22 to 35 days) phases to meet the dietary requirements of commercial broilers (see Table 2). The diets were provided as crumbs in the starter phase and as pellets in the grower and finisher phases. All diets were iso-nitrogenous and iso-caloric.
DATA COLLECTION
Growth performance
Data on weekly feed intake and refusal, as well as weekly body weight measurements, were collected for the study. These data were then utilized to calculate the cumulative feed intake (CFI), weight gain (WG), and feed conversion ratio (FCR) using the method described by Khan et al. (2019).
Blood biochemistry
On day 35, 4ml blood samples were taken from 6 birds per experimental unit (30 birds per treatment) to assess the impact of CCFP on total serum protein (TP), albumin (AB), globulin (GB), and the albumin to globulin ratio (AB:GB). Prior to blood collection, the birds were carefully restrained in a lateral recumbent position, and the brachial vein was cleaned aseptically with a 70% isopropyl alcohol swab. A sterile disposable syringe with a 25-gauge needle was then used to puncture the vein at a 20° angle for blood collection (Kelly & Alworth, 2013). The syringe plunger was pulled slowly to avoid hematoma formation. Once the syringe contained 4ml of blood, it was removed and the blood was immediately placed in a clot activator vacutainer. The vacutainers were then centrifuged at 3000 rpm for 5 minutes, and the serum was extracted using a micropipette. The collected serum was stored in an Eppendorf tube at -20°C for further analysis. Subsequently, the serum was thawed at 4°C and analyzed for total serum protein, albumin, and globulin.
Intestinal microbial count
On day 35, ileal and cecal digesta were collected to assess the impact of CCFP on the total bacterial count (TBC), total coliform count (TCC), and E. coli count (EC). The birds were slaughtered using the Halal method to obtain intestinal samples. Using forceps and scissors, the ilea and ceca were separated from the rest of the intestine. In an aseptic environment, the ceca were opened and 1 g of cecal contents was collected. The samples were preserved in 1.5-mL Eppendorf tubes at -20°C for further analysis. Subsequently, the cecal and ileal contents were analyzed at the Microbiology laboratory of the Cholistan University of Veterinary and Animal Sciences (CUVAS), Bahawalpur. The Agars of Oxoid (Violet red bile lactose agar CM0107, Nutrient agar CM0003, and Eosin methylene blue agar CM0069) were purchased from the market. Violet red bile lactose agar, nutrient agar, and eosin methylene blue agar each weighed 38.75 g, 28.08 g, and 37.5 g, respectively, and were mixed separately with 1000 ml of distilled water. After properly mixing the agar with distilled water, the pH of each agar was adjusted using a Milwaukee pH meter (Mi 151). 1N hydrochloric acid and 10N sodium hydroxide were used for pH adjustment. A few drops of hydrochloric acid and sodium hydroxide were added to adjust the pH of nutrient agar (7.4), violet red lactose bile agar (7.6), and eosin methylene blue agar (6.8) to provide a suitable environment for culturing microbes. Conical flasks filled with agar, micropipette tips, and phosphate buffer saline were covered with aluminum foil and placed in an autoclave at 121°C and 15 bar pressure. They were then removed after 3 hours, once the pressure of the autoclave dropped below 40°C. To sterilize the glass spreader, the spreader was first dipped in 95% ethanol and then ignited using a spirit lamp. After cooling, the agars were poured into petri plates that had been labeled in the biosafety cabinet. Once the media had solidified, samples (Eppendorf tubes) were removed from the refrigerator and thawed at room temperature. Phosphate buffer saline (1 ml) was added to the Eppendorf tubes, and 100 µL of the samples were mixed in. Dilutions ranging from 10-1 to 10-7 were prepared. From each dilution, 100 µL was poured onto the media using a micropipette, spread with a glass spreader, and then incubated for 24 hours to analyze the bacterial population. After the 24-hour incubation period, the petri plates were taken out of the incubator. The bacterial colonies were counted using a colony counter (BC-504) by marking the petri plates into four quadrants. The results were calculated as log10 colony forming units per gram (CFU/g) of cecal contents. The same protocol was repeated for the ileal contents.
Statistical analysis
The data were analyzed through one-way ANOVA under CRD using the GLM procedure of SAS (SAS Institute Inc., Cary, NC, 2002-2003). Treatment means were separated through Tukey’s Honesty Significant Difference (Tukey’s HSD) test at a 5% probability level, considering each pen as an experimental unit. The statistical model used was:
Where, Yij, observation of dependent variable recorded on ith treatment; μ, Population mean; Ti, Effect of ith treatment; and Ԑij, Random error.
RESULTS AND DISCUSSION
Growth performance
The use of synthetic antibiotics, alongside rigorous biosecurity and hygiene measures, has undoubtedly contributed to the growth of the poultry industry by mitigating the negative impact of various diseases (Mohamed & Hassan, 2023). However, this has also resulted in a persistent issue that poses serious risks to human health (Bortolaia et al., 2016; Mehdi et al., 2018). Phytobiotics may provide an effective alternative to these challenges without compromising bird performance. This study aimed to assess the impact of CCFP on different growth parameters in broilers. Different levels of CCFP were added to broiler diets, replacing commercially available AGP. The findings indicated a significant decrease in CFI (p = 0.045) in group T3 compared to the control group (T1). However, no significant differences were observed in WG (p = 0.224) and FCR (p = 0.565) among the groups (Table 3). The exact reason for the reduction in feed intake in group T3 is not entirely clear, but may be linked to a synergistic effect between CCFP and lincomycin at a specific dosage. Additionally, the low feed intake might be attributed to the possibility of CCFP powder negatively impacting the feed’s palatability. These findings are consistent with previous studies conducted by Cross et al. (2007) and Ertas et al. (2005), who evaluated the effects of herbs (thyme, oregano, marjoram, rosemary, yarrow, clove, or anise) on performance, microbial population, and digestibility. Furthermore, the total bacterial count and E. coli also decreased, which might have contributed to the reduced feed intake and numerically improved FCR in group T3 compared to the other groups supplemented with phytobiotics. A decreased microbial population reduces the degradation of amino acids, resulting in a greater availability of these nutrients, which may explain the lower feed intake and numerically better FCR observed in group T3. Similar results were obtained by other researchers, who found that supplementing broiler chickens’ diet with a phytogenic product reduced feed intake (Hashemipour et al., 2013; Mandey & Sompie, 2021). However, Alzarah et al. (2021) found that supplementing broilers with CC seeds improved feed intake (P<0.05) compared to the non-supplemented group.
Furthermore, it was noted that the supplementation of CCFP at 1.5 g/kg (T4) and 2.25 g/kg (T5) led to a numerical increase in weight gain among the birds compared to the control group. This improvement in weight gain may be attributed to the growth-promoting factors and medicinal properties found in CCFP. These findings contradict the observations of Sawaya et al. (1986), who found that chickens grew normally with up to 15% processed whole CC seeds included in their diet. Additionally, these outcomes challenge the observations of Bolu et al. (2011), who reported that birds fed 10% Citrullus lanatus experienced the highest weight gain compared to other groups. The differences in findings may be due to the varying levels of supplemented CC and the distinct chemical profiles of the CC used. The dietary concentration of CC also varied significantly between this study and previous research, which accounts for the high variability in broiler growth performance results observed in the current study compared to earlier studies.
Blood biochemistry
Blood biochemical indicators revealed that group T6 exhibited higher levels of TP (p = 0.050) and GB (p = 0.044) compared to the control group (T1). However, there were no significant differences in AB levels alone (p = 0.516) or in the AB to GB ratio (p = 0.100) among the groups (Table 4). These findings are consistent with Ghazalah & Ali (2008), who found that supplementing broilers with phytobiotics (rosemary leaves) enhanced protein, albumin, and globulin levels. Najafi & Torki (2010) also support these findings, noting that the addition of phytobiotic supplements and toxin binders to aflatoxin-containing diets improved total serum protein in poultry. The enhanced serum protein profile observed in broilers fed a phytobiotic diet may partly result from increased body weight, which correlates with greater protein mass (Piotrowska et al., 2011). Moreover, phytobiotics may interact with the intestinal epithelium, enhancing nutrient absorption by boosting the secretion of digestive enzymes and improving nutrient digestibility, ultimately leading to higher total serum protein levels (Abudabos et al., 2016).
Albumin plays a crucial role in maintaining blood colloid osmotic pressure and transporting various molecules. Our findings are consistent with those of Toghyani et al. (2010), who noted a slight increase in albumin concentration when thyme powder was compared to antibiotics in broiler diets. While we did not find significant results, we observed higher albumin levels in the T4 group (supplemented with 75 g of CCFP) compared to both the other CCFP-supplemented groups and the control group. This increase may be attributed to the dose-dependent competitive interaction between phytobiotics and AGP, which reduces protein breakdown into nitrogen at the intestinal surface, thereby increasing the available surface area for nutrient absorption and subsequently elevating albumin concentration. Similarly, Amad et al. (2013) reported higher blood albumin and protein levels in broilers fed phytobiotics.
Globulin consists of enzymes, antibodies (immunoglobulins), and carrier proteins. Most globulins are produced by the liver, where they play an essential role in nutrient delivery and immune defense against infections. In our study, we observed that globulin levels increased in the T6 group compared to the other groups. This increase may be linked to the immune-stimulating properties of CCFP, primarily due to its alkaloids, polyphenols, sulfur compounds, terpenes, essential oils, saponins, and tannins. Supplementation of CCFP could enhance the concentration of immunoglobulin G (IgG) and boost the production of immune cells, such as macrophages. IgG, along with IgA, is vital for defending against pathogenic bacteria, particularly in the intestines, which may account for the elevated globulin levels. However, Abudabos et al. (2018) found no differences in globulin levels between the control and phytobiotic-treated groups, possibly due to variations in the nutritional and therapeutic profiles of the herbs used. Similarly, Ghazalah & Ali (2008) reported increased globulin, albumin, and protein levels in broilers when phytobiotics (0.5% rosemary leaves) were added to their diet, which is consistent with our findings. The rise in globulin levels indicates the immune-boosting effects of CCFP.
Microbial count
Intensive poultry farming exposes chickens to poor hygiene conditions, which increases their susceptibility to diseases from various sources, including feed, bedding, farm staff, water, and sick birds within the facility. To improve the health and efficiency of poultry production, several strategies are implemented. These strategies involve the use of growth promoters, altering the gastrointestinal microbiome composition, and enhancing metabolic and immune system functions. Incorporating phytobiotics into drinking water or feed aids digestion and metabolism, promotes the growth of beneficial microbiomes, restricts pathogen spread, and enhances the structure and function of enterocytes.
The cecal microbial count revealed a significant reduction in TBC (p = 0.01) in groups T2 and T3, as well as a lower E. coli count (p = 0.025) in group T3 compared to the other groups. However, no significant differences were observed in TCC (p = 0.284) among the groups (Table 5). Supporting these results, Kamran et al. (2021) reported that CCFP significantly affected the gut bacterial population, leading to positive changes in cecal bacterial colonies compared to the control group. Additionally, another study indicated that dietary supplementation with plant extracts as broiler feed additives significantly reduced intestinal pH. This suggests that the medium-chain fatty acids present in these phytobiotics can help decrease the presence of pathogenic microbes in the gut (Jamroz et al., 2003). However, Ren et al. (2019) noted that the supplementation of probiotics (Lactobacillus) and phytobiotics (eugenol, carvacrol, and cinnamaldehyde) did not influence the caecal microbiota.
Poultry is considered the most efficient source of high-quality protein for humans due to its low production costs and short life cycle (Radwan et al., 2022). However, the industry faces challenges from infectious diseases, which can lead to higher mortality rates, hindered growth, and a reliance on both curative and preventive chemotherapeutics (Daehre et al., 2018). Numerous bacteria, including E. coli, Salmonella spp., Proteus spp., Enterobacter spp., Pseudomonas spp., Klebsiella spp., Staphylococcus spp., and Streptococcus spp., are commonly found in diseased poultry (Ali et al., 2019; Abd El-Mawgoud et al., 2021). Gastrointestinal microbes play a crucial role in the metabolism, nutritional health, and overall well-being of poultry (Falcinelli et al., 2015). Conversely, an increased presence of pathogenic bacteria, such as E. coli, Clostridium, and Salmonella can disrupt the gut’s balanced environment, leading to impaired growth (Oz, 2017). E. coli is typically found in the intestinal tract but can become pathogenic by colonizing the intestinal mucosa (Raheel et al., 2022). This colonization can result in diarrhea and other intestinal diseases (Croxen et al., 2013; Tahir et al., 2021). The poultry intestine serves as a major reservoir for E. coli (Rodriguez-Siek et al., 2005), with continuous shedding of the bacteria (Ewers et al., 2005), which can lead to severe infections in birds (McPeake et al., 2005). When included as growth promoters in broiler diets, phytobiotics can inhibit the growth of pathogenic bacteria (Chang et al., 2016; Laptev et al., 2019). In our study, the total coliform count was not significantly different (p>0.05); however, the numerical value in group T3 was the lowest (5.81) compared to the other treatment groups, suggesting the antibacterial properties of CCFP against total coliforms. Murugesan et al. (2015) also found that dietary supplementation with phytobiotics and bacitracin in chickens significantly decreased Clostridium counts and total anaerobic bacteria, while phytobiotics alone reduced coliform counts. This supports our findings that phytobiotics (CCFP) can effectively lower coliform counts, as shown in our experimental study.
The problem of E. coli in chickens is multifaceted, resulting in both health and economic consequences for broiler farms. These repercussions include increased mortality rates, the need to cull sick birds, reduced weight gain, lower final weights, and inconsistencies in the size and weight of birds at various growth stages. The E. coli count in group T3 was significantly lower, which is consistent with the findings of Kamran et al. (2021), who noted a reduction in E. coli levels in broilers fed with Citrullus colocynthis fruit powder. Additionally, Marzouk et al. (2010) reported that extracts from CCFP effectively targeted E. coli populations. Similarly, Bnyan et al. (2013) demonstrated that ethanol extracts of CCFP inhibited E. coli and other harmful bacteria. This effect may be attributed to the antibacterial properties of flavonoids, glycosides, and alkaloids found in CC, which enhance intestinal health and overall performance. However, the ileal microbial count showed no significant impact of CCFP supplementation on TBC (p=0.873), TCC (p=0.827), or E. coli count (p=0.761) (Table 6).
CONCLUSION
Our results indicate that a diet containing 0.75 g/kg CCFP combined with 0.11 g/kg AGP may improve the growth of broiler chickens while maintaining a healthy microbial balance. However, further research on the dosage and effects of CCFP at an industrial level, as well as molecular studies, are highly recommended.
ACKNOWLEDGEMENTS
The authors would like to extend their sincere appreciation to the Researchers Supporting Project number (RSPD2024R694), King Saud University, Riyadh, Saudi Arabia and the administration of the Poultry Farm of the Islamia University of Bahawalpur, Pakistan for facilitating the trial.
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FUNDING
The authors would like to extend their sincere appreciation to the Researchers Supporting Project number (RSPD2024R694), King Saud University, Riyadh, Saudi Arabia.
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DATA AVAILABILITY STATEMENT
Data will be available upon request.
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DISCLAIMER/PUBLISHER’S NOTE
The published papers’ statements, opinions, and data are those of the individual author(s) and contributor(s). The editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions, or products referred to in the content.
Data availability
Data will be available upon request.
Publication Dates
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Publication in this collection
16 Dec 2024 -
Date of issue
2024
History
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Received
18 Apr 2024 -
Accepted
20 Oct 2024