Effects of Fungal Fermented Feeds on Broiler Chicken Growth Performance, Gut Morphology, and Gastrointestinal Tract Microecology: A Review

Farah Ahmad, Uzma Rafi*, and Imran Afzal

Department of Biology, Lahore Garrison University, Lahore, Pakistan

ABSTRACT

Due to the shortage of poultry feed ingredients and the resultant continuous increase in their prices, researchers have been looking for their alternatives. Agricultural wastes and by-products (such as wheat bran, rice husk, sour cherry kernel, palm kernel, cassava pulp, rapeseed meal, and corn meal) are among such alternatives, although they cannot be used directly due to their high crude fiber content. Fermentation is an evolving process that converts complex substrates into simpler molecules using bacteria, fungi, and other microorganisms. It improves the nutrient content of feed ingredients. It is also used to ferment agricultural waste materials in order to improve their nutritional value, so they can be utilized as broiler feed. Moreover, it can provide an inexpensive feed source to poultry industry and convert waste materials into a useable product. Different bacterial and fungal strains are employed for fermentation. This review focuses on the use of fungal fermented agricultural waste-based feed and its effects on broiler chicken growth performance, gut morphology, and gastrointestinal tract microecology.

Keywords: agricultural waste, broiler chicken, fungal fermented feed, poultry industry

1. INTRODUCTION

The production of principal poultry products (eggs and meat) is increasing rapidly all over the world. This represents consumption driven by the consumer choice for high-quality products at a low price due to production efficiency [1]. The key goals of poultry industry include higher output, illness control, quality of product, and reasonable cost of production [2]. The poultry sector in Pakistan is a key and developing agricultural sector that contributes significantly to the GDP of the country (1.26% of GDP). Chicken farming at commercial level began in Pakistan in the 1960s and the public has been dependent on it to fulfil a significant portion of their daily protein requirement since then. The industry has profited from government incentives throughout the course of its development, although it has also encountered challenges such as disease breakouts and retail price changes. In Pakistan, the poultry sector is essential to fill the gap between protein supply and protein demand. Poultry production is one of the most vibrant and well organized industries of the country, providing for 26.8% of the total meat output, 5.76% of the agricultural sector, and 1.26% of the country's overall GDP. The poultry sector of Pakistan has experienced rapid expansion in recent years, providing employment to more than 1.5 million people. Despite showing remarkable potential and progress over the previous years, currently it is facing many challenges, such as disease outbreaks, low animal feed intake, poor quality, and high-priced feed [3].

Grain crops have been exploited to produce biomass energy in recent years due to the energy crisis, resulting in higher prices for the key materials used in animal feed. Alternative crops or agricultural by-products can be used to address feed shortage as unconventional feedstuffs [4]. Agricultural by-products are affordable as compared to main grain crops, although they are mostly useless as feed for monogastric animals due to their high fiber content. The principal by-product of wheat flour processing is wheat bran (WB). It includes a significant amount of total dietary fiber (451 g/kg) [5]. However, it is widely understood that increasing fiber content has a negative relationship with animal feed intake and digestibility, thus decreasing the growth and production performance of the poultry industry. As a result, the use of wheat bran in animal feed has been generally limited  [6,7]. Fermentation increases the nutritional value of feed materials, while lowering crude fiber content and harmful compounds [8]. Through fermentation, scientists have recently begun to employ fungal inoculum to increase the nutritional value of agricultural by-products [9]. Fermented feed ingredients show resistance to contamination by pathogens before they are fed to chickens [10]. The addition of fermented products into broiler feed can reduce the number of harmful microbes and support the growth of good microflora in the gut of broiler chicken [11]. Recently, several studies have been conducted regarding the addition of fermented feed into broiler diet to observe its effect on growth performance and gut health [12-14].

This review describes the use of fungal fermented agricultural waste-based feed and its effect on broiler chicken growth performance, gut morphology, and gastrointestinal tract microecology.

2. FUNGAL SPECIES EMPLOYED TO FERMENT SUBSTRATE

Scientists have recently begun to employ fungal inoculum to increase the nutritional value of agricultural by-products through fermentation. Filamentous fungi, such as Trichoderma species, are very well known cellulase producers [9]. The majority of commercial cellulase is produced from Trichoderma species. Filamentous fungi have a higher penetrating power into the insoluble substrates, making them better suited for the fermentation of lignocellulosic material. Researchers have found numerous strains of Trichoderma spp. as the most consistent and safe fungi for the synthesis of cellulase and hemicellulases. Fungi have a highly effective enzymatic system that allows them to breakdown lignocellulosic materials [13]. With solid-state fermentation, Aspergillus niger can create numerous enzymes, such as amylase, protease, tannase, cellulase, and lipase. These enzymes improve poultry growth and meat quality, while lowering the antinutritional components in the leaves of Ginkgo biloba, cottonseed meal, and olive leaves [14]. Filamentous fungi including Aspergillus niger, Pleorotus ostreatus, and Trichoderma spp. are typically  employed for solid-state fermentation to increase the substrate's feed value. These fungi are presumably able to grow not only on the surface of substrate particles but are also assumed to penetrate them [15]. Table 1 shows the some examples of fungal strains used to ferment substrates added to broiler diets.

Table 1.  Examples of fungal strains used to ferment substrates added to broiler diets.

3. FERMENTATION METHODS

Fermentation is an evolving process that converts complex substrates into simpler molecules and involves microbes, substrates, and ambient conditions [10]. Solid state fermentation (SSF) and submerged fermentation (SmF) are the two main types of fermentation processes, depending on the type of substrate [29]. These techniques are used to ferment agricultural waste materials to supplement broiler feed. SSF uses solid substrates – for example wheat bran, rice, grains, and rice bran (without free-flowing liquid). It is commonly used to make fermented dried up feed that could be crushed or powdered and added to basic diet mixtures, such as whole grain. Due to the lower moisture level, only a few microorganisms can perform the SSF method. Primarily, these include fungi such as Rhizopus spp. and Aspergillus spp., though bacterial species such as Lactobacillus species can also be utilized.. Still, SSF has attracted greater attention since it produces better yields and products with improved quality than SmF. Furthermore, the greater moisture content in SmF's fermented feeds may make poultry production difficult in the context of actual feeding and litter quality [30]. SSF has been proved to be a promising tool for recycling the agricultural and industrial wastes used in animal diets[31]. It enhances the digestibility of nutrients, increases the number of good bacteria (lactobacilli) in the large intestine of broilers, improves the morphology of their small intestine, and reduces the cost of poultry farming [22]. Aside from efficient feed storage, the fermentation technique can enhance the nutritional value of animal feed ingredients [13]. It improves the quality of feedstuffs by producing enzymes, eliminating harmful chemicals, and by improving the aroma [15].

Fermentation technique has been used to improve the quality of several feed ingredients, for instance, wheat bran [12,18,27] , cassava peel [16,26,28], palm kernel meal [15], rapeseed meal [22], copra meal [21], and sour cherry kernel [14].

4. UNCONVENTIONAL FEEDS

The poultry sector is currently experiencing swings in feed pricing as a result of the rising prices of conventional feedstuffs. Consequently, chicken nutritionists are looking for new feed supplements [16]. Wastes and by-products of various industries, such as palm kernel meal of palm oil industry [15] and cassava pulp of tapioca industry [16] can be used as unconventional feed sources in boiler diets. Such use, however, is limited due to their high fiber and low protein content, though fermentation can improve their nutritional value and decrease their crude fiber content [8]. The use of fungi to ferment a low quality feedstuff can improve its quality [15].

5. EFFECT ON GROWTH PERFORMANCE

Fermentation improves the nutritional value of feed ingredients but decreases the crude fiber content and toxic compounds [8], which can affect the growth of broiler chicks. The parameters used to measure their growth are body weight, weight gain, feed consumption, and feed to gain ratio [31]. According to a study, 10% fermented wheat bran group of broiler chickens had a reduced feed consumption and a higher feed to gain ratio than control group, which resulted in their improved growth [12]. Likewise, when comparing the average live weight of birds fed with fermented wheat bran (1640 g) to control group 1 (1147.7 g) and control group 2 (1363.5 g), the statistical analysis revealed a significant increase in the average live weight of birds fed with fermented wheat bran, while feed conversion ratio (FCR) was also the best of the group fed with fermented wheat bran [13]. Furthermore, the Acremonium charticola fermented Cassava pulp (AC-FCP) and AC-FCP + Antibiotic Growth Promotors birds had reduced feed costs per kg and live weight gain than that of the control and control + Antibiotic Growth Promotors birds [16]. 

Moreover, increased growth and FCR were observed in broilers fed on fermented wheat bran by bacillus and saccharomyces spp [25]. Likewise, broilers fed on wheat bran fermented by Cunninghamella spp. showed improved meat quality and health indicators [19]. According to [18], in comparison to the control group, the groups supplemented with the enzyme powder of Trichoderma pseudokoningii showed that body weight gain and FCR improved during the starting phase (1–21 day). The findings of [17] suggested that wheat bran is a good dietary supplement as it did not affect the growth of broilers.

Other than wheat bran, sour cherry kernel fermented by Aspergillus niger can also be added to broiler diet up to 2%, without having any negative effects on their growth [14]. Broilers fed on rapeseed meal fermented by Bacillus subtilis, Lactobacillus fermentum, and Enterococcus faecium showed improved FCR and weight gain [22]. Birds fed on unfermented palm kernel meal consumed less feed than other experimental groups [15]. Table 2 shows some examples of fermented agricultural waste-based feeds and their studied effects on broiler growth.

Table 2. Examples of Fermented Agricultural Waste-Based Feeds and their Effects on the Growth Performance of Broilers

6. EFFECTS ON BROILER CHICKEN GUT MORPHOLOGY

An increase in villus height results in a large surface area, which leads to an increase in the absorption of nutrients and also improves the health of gut tract [32]. Furthermore, it's possible to think of the crypt as a villus assembly line; indeed, a large crypt indicates faster tissue renewal and a higher energy demand during tissue development [33]. The low depth of crypt is considered good to save energy for animal growth [34]. To measure the absorption capacity of the small intestine, the ratio of villus height to crypt depth (VH:CD) is an important parameter [22]. A study reported the effects on the gut morphology of broiler chicken when 10% of basal diet was replaced with Trichoderma pseudokoningii fermented wheat bran. A significant increase was detected in the VH:CD ratio in the ileum, although no significant difference was observed in the jejunum [12]. Another study demonstrated an increase in the height of the villus and the VH:CD ratio in the ileum and the jejunum of broiler chickens fed with the fermented rapeseed meal during the starter phase [22]. Another study reported the effects on broiler chickens fed with Trichoderma longibrachiatum (SF1) fermented wheat bran. Normal villus height and histological structures were observed [13]. Table 3 shows some examples of agricultural waste-based fermented feed ingredients and their studied effects on the gut morphology of broiler chickens.

Table 3. Fermented Feeds and their Studied Effects on the Gut Morphology of Broiler Chickens

7. EFFECTS ON THE MICROECOLOGY OF GASTROINTESTINAL TRACT

The microflora of gut tract has a significant role in gut morphology, physiology, microbiology, immunology, and nutrition. Fermented feeds enhanced gut microbial ecosystems in pigs by reducing the number of enteric bacteria, such as coliform bacteria and salmonella [35]. The host's intestinal microflora is the first line of defense against diseases induced by pathogen colonization in the gastrointestinal tract [36]. Bacteria, such as lactobacilli, are capable of inhibiting the growth of pathogenic bacteria [22]. The use of fermented feeds, which has the potential to affect gut bacterial ecology, is receiving more scholarly attention. The effects of fermented feeds on gut ecology are mostly apparent in the flora and metabolites of the gastrointestinal tract. Due to its unique properties, SSF feeds cause the acidification of the upper part of the gastrointestinal tract and provides ideal circumstances for the development of bacteria that are beneficial to animals [36]. Short-chain fatty acids are produced by the beneficial microbial population, which lowers gut pH. This also serves as a natural protective barrier against infectious diseases and pathogenic microorganisms. Fermented feeds have a large quantity of lactic acid bacteria and a high quantity of lactic acid [10]. Fermented diets, because of essential features such as low pH, large number of lactobacillus species, high quantity of acetic and lactic acid, and a low number of enterobacteria, might also be helpful to maintain healthy gut microecology in broiler chickens [30]. According to a study, the number of lactic acid bacteria was higher in the colon of broiler chickens fed with diet 10% of which was replaced by solid state fermented rapeseed meal than control group broilers, which led to a reduced number of pathogenic microbes in gut [22]. Similarly, broiler chickens fed on fermented wheat bran showed a significant increase in good microflora (lactic acid bacteria) count in the gut [18,25]. The number of coliform bacteria was reduced in the gastrointestinal tract of broilers fed on fermented feeds [12,13,24]. Table 4 shows some examples of fermented feeds and their effects on gastrointestinal tract microecology.

Table 4. Fermented Feeds and their Studied Effects on Gut Microecology

 CONCLUSION

Fermentation is a low-cost technique that can improve the nutritive value of feed ingredients obtained through unconventional feedstuffs. It is evident by the literature that such fungal fermented feed ingredients obtained from agricultural waste materials and by-products can improve the broiler chicken growth performance, gastrointestinal tract morphology, and microecology without having any deleterious effects. Further study is needed to evaluate the effects of fungal fermented feeds on broiler chicken growth and gut health; however, this process can provide a cheap feed source to poultry which may eventually contribute to the potential growth of poultry industry in developing countries. Moreover, it may also provide a way to convert agricultural waste materials into a useful product.

REFERENCES

1. Scanes CG. The global importance of poultry. Poult Sci. 2007;86(6):1057–1058.
2. Hafez HM, Attia YA. Challenges to the poultry industry: Current perspectives and strategic future after the COVID-19 outbreak. Front Vet Sci. 2020;7:e516. https://doi.org/10. 3389/fvets.2020.00516
3. Hussain J, Rabbani I, Aslam S, Ahmad HA. An overview of poultry industry in Pakistan. World's Poult Sci J. 2015;71(4):689–700. https://doi.org/ 10.1017/S0043933915002366
4. Oguri M, Okano K, Ieki H, et al. Feed intake, digestibility, nitrogen utilization, ruminal condition and blood metabolites in wethers fed ground bamboo pellets cultured with white‐rot fungus (C eriporiopsis subvermispora) and mixed with soybean curd residue and soy sauce cake. Animal Sci J. 2013;84(9):650–655. https://doi.org/10.1111/asj.12054
5. Ravichandran S, Vimala R. Solid state and submerged fermentation for the production of bioactive substances: a comparative study. Int J Sci Nat. 2012;3(3):480–486.
6. Slominski BA, Boros D, Campbell LD, Guenter W, Jones O. Wheat by-products in poultry nutrition. Part I. Chemical and nutritive composition of wheat screenings, bakery by-products and wheat mill run. Canad J Animal Sci. 2004;84(3):421–428. https://doi. org/10.4141/A03-112
7. Nortey TN, Patience JF, Sands JS, Zijlstra RT. Xylanase supplementation improves energy digestibility of wheat by-products in grower pigs. Lives Sci. 2007;109(1-3):96–99. https://doi.org /10.1016/j.livsci.2007.01.092
8. Khempaka S, Molee W, Guillaume M. Dried cassava pulp as an alternative feedstuff for broilers: Effect on growth performance, carcass traits, digestive organs, and nutrient digestibility. Journal of Applied Poultry Research. 2009;18(3):487–493. https://doi.org /10.3382/japr.2008-00124
9. Sharma RK, Arora DS. Solid state degradation of paddy straw by Phlebia floridensis in the presence of different supplements for improving its nutritive status. Int Biodeterior. Biodegrad. 2011;65(7):990–996. https://doi.org /10.1016/j.ibiod.2011.07.007
10. Niba AT, Beal JD, Kudi AC, Brooks PH. Potential of bacterial fermentation as a biosafe method of improving feeds for pigs and poultry. Afr. J. Biotechnol. 2009;8(9).
11. Chuang WY, Lin WC, Hsieh YC, Huang CM, Chang SC, Lee TT. Evaluation of the combined use of Saccharomyces cerevisiae and Aspergillus oryzae with phytase fermentation products on growth, inflammatory, and intestinal morphology in broilers. Animals. 2019;9(12):e1051. https://doi.org/ 10.3390/ani9121051
12. Chu YT, Lo CT, Chang SC, Lee TT. Effects of Trichoderma fermented wheat bran on growth performance, intestinal morphology and histological findings in broiler chickens. Ital J Anim Sci. 2017;16(1):82–92. https:// doi.org/10.1080/1828051X.2016.1241133
13. Belal E. Assessment of the performance of chicks fed with wheat bran solid fermented by Trichoderma longibrachiatum (SF1). J SustainAgric Sci. 2017;43(2):115–126. https://dx.doi.org/10.21608/ jsas.2017.1162.1008
14. Gungor E, Erener G. Effect of dietary raw and fermented sour cherry kernel (Prunus cerasus L.) on digestibility, intestinal morphology and caecal microflora in broiler chickens. Poult Sci. 2020;99(1):471–478. https://doi. org/10.3382/ps/pez538
15. Sundu B, Adjis A, Sarjuni S, Mozin S, Hatta U. Fermented palm kernel meal by different fungi in broiler diets. InIOP Conference Series: Earth Environ Sci. 2021;788(1):e012041.
16. Sugiharto S, Yudiarti T, Isroli I, Widiastuti E, Putra FD. Effects of feeding cassava pulp fermented with Acremonium charticola on growth performance, nutrient digestibility and meat quality of broiler chicks. South Afr J Animal Sci. 2017;47(2):130–138. https://hdl.handle.net/10520/EJC-5673ba149
17. Zhang AR, Wei M, Yan L, Zhou GL, Li Y, Wang HM, Yang YY, Yin W, Guo JQ, Cai XH, Li JX. Effects of feeding solid-state fermented wheat bran on growth performance and nutrient digestibility in broiler chickens. Poult Sci. 2022;101(1):e101402. https://doi.org /10.1016/j.psj.2021.101402
18. Lin WC, Lee MT, Lo CT, Chang SC, Lee TT. Effects of dietary supplementation of Trichoderma pseudokoningii fermented enzyme powder on growth performance, intestinal morphology, microflora and serum antioxidantive status in broiler chickens. ItalJAnim Sci.  2018;17(1):153–164. https://doi.org /10.1080/1828051X.2017.1355273
19. Semjon B, Bartkovský M, Marcinčáková D, Klempová T, Bujňák L, Hudák M, Jaďuttová I, Čertík M, Marcinčák S. Effect of solid-state fermented wheat bran supplemented with agrimony extract on growth performance, fatty acid profile, and meat quality of broiler chickens. Animals. 2020;10(6):e942. https://doi. org/10.3390/ani10060942
20. Yasar S, Yegen MK. Yeast fermented additive enhances broiler growth. Rev Bras de Zootec. 2017;46:814–820. https://doi.org/10.1590/S1806-92902017001000004
21. Hatta U, Sjofjan O, Subagiyo I, Sundu B. Effects of fermentation by Trichoderma viride on nutritive value of copra meal, cellulase activity and performance of broiler chickens. Livest Res Rural Dev.2014;26(1).
22. Chiang G, Lu WQ, Piao XS, Hu JK, Gong LM, Thacker PA. Effects of feeding solid-state fermented rapeseed meal on performance, nutrient digestibility, intestinal ecology and intestinal morphology of broiler chickens. Asian-Australas J Anim Sci. 2009;23(2):263–271. https://doi.org /10.5713/ajas.2010.90145
23. Marcinčák S, Klempová T, Bartkovský M, et al. Effect of fungal solid-state fermented product in broiler chicken nutrition on quality and safety of produced breast meat. Biomed ResInt. 2018;2018:e2609548. https://doi.org /10.1155/2018/2609548
24. Lin WC, Lee TT. Laetiporus sulphureus–fermented wheat bran enhanced the broiler growth performance by improving the intestinal microflora and inflammation status. Poult Sci. 2020;99(7):3606–3616. https://doi.org/10.1016/j. psj.2020.04.011
25. Teng PY, Chang CL, Huang CM, Chang SC, Lee TT. Effects of solid-state fermented wheat bran by Bacillus amyloliquefaciens and Saccharomyces cerevisiae on growth performance and intestinal microbiota in broiler chickens. Ital JAnimSci. 2017;16(4):552–562. https://doi.org/ 10.1080/1828051X.2017.1299597
26. Okpako CE, Ntui VO, Osuagwu AN, Obasi FI. Proximate composition and cyanide content of cassava peels fermented with Aspergillus niger and Lactobacillus rhamnosus.
    J Food Agric Environ. 2008;6(2):251–255.
27. Wang CC, Lin LJ, Chao YP, Chiang CJ, Lee MT, Chang SC, Yu B, Lee TT. Antioxidant molecular targets of wheat bran fermented by white rot fungi and its potential modulation of antioxidative status in broiler chickens. Br.Poult Sci. 2017;58(3):262–271. https://doi.org/10.1080/00071668.2017.1280772
28. Oboh G. Nutrient enrichment of cassava peels using a mixed culture of Saccharomyces cerevisae and Lactobacillus spp solid media fermentation techniques. Electronic J Biotechnol. 2006;9(1). https://doi.org /10.2225/vol9-issue1-fulltext-1
29. Subramaniyam R, Vimala R. Solid state and submerged fermentation for the production of bioactive substances: a comparative study. Int J Sci Nat. 2012;3(3):480–486.
30. Sugiharto S, Ranjitkar S. Recent advances in fermented feeds towards improved broiler chicken performance, gastrointestinal tract microecology and immune responses: A review. Anim Nutr. 2019;5(1):1–10. https://doi.org /10.1016/j.aninu.2018.11.001
31. Alshelmani MI, Loh TC, Foo HL, Sazili AQ, Lau WH. Effect of feeding different levels of palm kernel cake fermented by Paenibacillus polymyxa ATCC 842 on nutrient digestibility, intestinal morphology, and gut microflora in broiler chickens. Anim Feed Sci Technol. 2016;216:216–224. https://doi.org/10.1016/j.anifeedsci.2016.03.019
32. Baurhoo B, Phillip L, Ruiz-Feria CA. Effects of purified lignin and mannan oligosaccharides on intestinal integrity and microbial populations in the ceca and litter of broiler chickens. Poult Science. 2007;86(6):1070–1078. https://doi.org/10.1093/ps/86.6.1070
33. Awad WA, Ghareeb K, Abdel-Raheem S, Böhm J. Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult Sci. 2009;88(1):49–56. https://doi.org/10.3382/ps.2008-00244
34. Parsaie S, Shariatmadari F, Zamiri MJ, Khajeh K. Influence of wheat-based diets supplemented with xylanase, bile acid and antibiotics on performance, digestive tract measurements and gut morphology of broilers compared with a maize-based diet. Br. Poult Sci. 2007;48(5):594–600. https://doi.org /10.1080/00071660701615788
35. Olukomaiya O, Fernando C, Mereddy R, Li X, Sultanbawa Y. Solid-state fermented plant protein sources in the diets of broiler chickens: A review. Anim Nutr. 2019;5(4):319–330. https://doi.org/10.1016/j.aninu.2019.05.005
36. Yang L, Zeng X, Qiao S. Advances in research on solid-state fermented feed and its utilization: The pioneer of private customization for intestinal microorganisms. Anim Nutr. 2021;7(4):905–916. https://doi.org /10.1016/j.aninu.2021.06.002

* Corresponding Author: uzmazeeshan@lgu.edu.pk