Agrarian Academic Journal
doi: 10.32406/v6n5/2023/89-97/agrariacad
Clinical evaluation and digestibility of banana (Musa spp.) compared to the Coast Cross hay (Cynodon sp.) as food for sheep. Avaliação clínica e digestibilidade da banana (Musa spp.) comparada ao Coast Cross feno (Cynodon sp.) como alimento para ovelhas.
Bruno Leonardo Mendonça Ribeiro
1, Eduardo Carvalho Marques2, Mariane Ferreira Franco2, Lucas Alencar Fernandes Beserra2*, Gisela Gregoria Choque2, Lilian Gregory2
1- University Federal of Rondônia (UNIR). Rolim de Moura, RO, Brazil.
2*- University of São Paulo (USP). Av. Professor Orlando Marques de Paiva, 87, Cidade Universitária, São Paulo, SP, Brazil. E-mail: beserralfb@usp.br
Resumo
O objetivo deste trabalho foi realizar um ensaio alimentar para avaliar os aspectos nutricionais da parte aérea da banana em ovinos sadios. No primeiro ensaio, doze ovelhas foram utilizadas nos testes para determinar a digestibilidade da matéria seca da bananeira. No segundo foram utilizados seis ovinos com cânulas ruminais para avaliar o teor de matéria seca, proteína bruta, fibra em detergente neutro e ácido. Três tratamentos foram analisados: (A) talo mais folhas secas de bananeira, (B) talo seco de bananeira e (C) folhas secas de bananeira. As folhas e talos da bananeira mostrou-se como uma fonte alternativa para nutrição de ovinos, que em formulação adequada, não compromete a saúde animal.
Palavras-chave: Nutrição. Pequenos ruminantes. Sustentabilidade.
Abstract
The objective of this work was to carry out a feeding trial to evaluate the nutritional aspects of the aerial part of the banana in healthy sheep. In the first trial, twelve ewes were used in the tests to determine the digestibility of banana dry matter. In the second, six sheep were used with ruminal cannulas to evaluate the content of dry matter, crude protein, neutral and acid detergent fiber. Three treatments were analyzed: (A) stalk plus dried banana leaves, (B) dried banana stalk and (C) dried banana leaves. The leaves and stems of the banana tree proved to be an alternative source of nutrition for sheep, which, when properly formulated, does not compromise animal health.
Keywords: Nutrition. Small ruminants. Sustainability.
Introduction
The banana (Musa spp.) cultivation is among the expanding crops. It has been gaining prominence in the agricultural market, being that, the banana is one of the most produced and consumed fruits in the world (FAO, 2019). Casas et al. (2020) concluded that the use of banana residues, in cattle, did not affect ruminal and hepatic health, being able to provide these animals. Banana peel has the potential to be used in sheep feed. It is considerably rich in nutrients, phenols and tannins and its composition may be different, depending on the variety and its degree of ripening (RAMDANI et al., 2019).
The aerial parts of the banana plants could be utilized as forage food. In addition to the economic advantage of using these plants, they contain secondary compounds known to exhibit different degrees of anthelmintic activity, because of tannins presence in this plant, which is of particular interest of the sheep industry (FERRÃO, 2013). Although the banana leaves have a higher PB content than the pseudostem, its digestibilityis lower, probably due to its high lignin content. Due to the low crude protein content in the pseudostem, when it is used as single food, the ingestion, growth and the milk production will be depressed, as a result of low nitrogen availability for ruminal fermentation and low dry matter intake. Banana peel, leaves and pseudostem can be a good food source for ruminants, may contribute to increasing weight gain and milk production, provided it is subjected to appropriate treatment and with supplementation (RUSDY, 2019).
The addition of banana leaf hay and pseudostem can replace hay of Cynodon sp. without changing the intake, digestibility of nutrients and the ruminal concentration of short-chain fatty acids. The lowest dry matter digestibility and organic were observed in diets with levels of banana leaf hay when compared to the same proportion of the pseudostem hay, probably due to higher concentration of lignin (88,1g Kg-1) in the leaf hay, although the ingestion did not differ between treatments. In study, the inclusion of 400g Kg-1 of leaf hay, reduced digestibility of NDF in relation to treatments containing Cynodon spp. hay or of pseudostem. These results can be explained by the high percentage of ADF and high lignin content in this treatment. The pH ruminal was kept close to neutral in all treatments. However, it is important to highlight that the average pH 7.0±0.15 may have been affected by the time of collection of rumen fluid (CARMO et al., 2018).
The inclusion of banana residue in the diet of growing lambs, increases the economic viability of the activity. The treatment with 40% of banana leaf hay and 60% of concentrate presented the best economic indicators, based on the highest net revenue, at the highest rate of return and e in the highest profitability for marketing live or slaughtered animals (GERASSEV et al., 2013). The objective of the work was to conduct a feeding trial to evaluate the nutritional aspects of the aerial portion of the banana (Musa spp.) in healthy sheep fitted with rumenal cannulae.
Materials and methods
This work was approved by the Ethics Committee for Animal Experimentation at the University of Santo Amaro. Twelve castrated sheep Suffolk were used in the tests, aged between two and three years and weighing 55 kg on average. Six animals, two to three years of age, were cannulated. All animals were individually examined once a week according to the specific and general physical examination criteria published by Rosenberger (1979). Blood samples were collected before and after treatments.
The experiment was divided in two trials. In the first one, twelve animals (six fistulated and six not fistulated) were studied in a completely randomized design (GOMES, 1985) to determine the apparent digestibility of three treatments: 15, 25 and 35% dry matter from the banana plant (leaf + stalk) in a standard mixture of concentrated (40% soybean meal, 57% corn meal and 3% mineral salt) and hay coast-cross, which is a maintenance diet. The provided samples were minced, exposed to room temperature for a pre-drying and subsequently crushed and placed in an oven at 36° C for 48 hours.
The technical evaluation of digestibility was performed after total faeces samples were collected from twelve confined sheep for 5 consecutive days with the goal of determining the following parameters: dry matter, crude protein, crude fiber, ether extract and nitrogen free extract (NFE). All the procedures were performed according to AOAC (2000).
Hepatic and renal functions were analysed. Serum urea levels were quantified (mg / dL) according to the methodology described by Talke and Schubert (1965) using a Diasys® commercial kit (DiaSys. Europe). Serum creatinine levels were determined based on the method of Jaffe modified, according to the technique described by Lustgarten and Wenk (1972). Serum albumin levels were measured by the bromocresol green method in accordance with the technique recommended by Doumas and Bigges (1972). The enzymatic activity of serumaspartate aminotransferase was determined using the kinetic methodology recommended by the International Federation of Clinical Chemistry with a Biosystems® commercial kit. The enzymatic activity of serum gamma glutamyl was quantitated according to the kinetic methodology recommended by the International Federation of Clinical Chemistry using a Diasys® commercial kit. All the assays were performed on an automatic biochemical analyser (AMS®, model Liasys®) (Figure 1).
Figure 1 – Trail one.
In the second trial six fistulated animals were used. The in situ nylon bag technique was utilized (ORSKOV, 1982; LUCCI, 1997): five grams of sample (a) banana leaf, (b) dried banana stalk and (c) dried banana leaf) was placed in each bag, which was incubated in the rumen of the fistulated sheep for 0, 6, 12, 24, 48, 72 and 96 h. The feed consisted of coast-cross hay (roughage) and concentrate with 20% protein. All the animals (1-6) received three nylon bags with the respective treatment (A, B or C).
Ruminal fluid samples were executed at times 0, 1, 2, 3, 4, 6, 8 and 24 hours after feeding, for analysis of NH3 concentrations (crop 1 and 2 hours), and determination of pH (crop 0, 1 and 2 hours). The following degradability parameters were analysed: dry matter (DM), crude protein (AOAC, 2000), acid detergent fiber (ADF) and neutral detergent fiber (NDF) (VAN SOEST; WINE, 1968; UDÉN et al., 2005) (Figure 2 ).
Figure 2 – Trail two.
Statistical analysis
In situ digestibility analysis: the degradability data were adjusted using the Orskov et al. (1980) model, and the effective degradability (dge) was calculated based on the Orskov et al. (1980) equation with a passage rate of r = 0.2.
A statistical analysis was performed on the Latin square design (GOMES, 1985) with three treatments: (A) stalk plus dried banana leaf, (B) dried banana stalk and (C) dried banana leaf. The feed consisted of coast-cross hay (roughage) and concentrate with 20% protein. All the animals (1-6) received three nylon bags with the respective treatment (A, B or C). The effective degradability data for dry matter (DM), crude protein (CP), acid detergent fiber (ADF) and neutral detergent fiber (NDF) were subjected to statistical regression analyses, as proposed by Gomes (1985), with the regressions considered statistically significant when p ≤ 0.05. The variance of the treatments was split into linear regression (1 degree of freedom) and deviation from regression (1 degree of freedom).
Apparent digestibility factors and metabolism
Analytical methods: twelve animals were used in a completely randomized design as Gomes (1985), in order to study the apparent digestibility in three treatments: 15%, 25% e 35% of dry matter of banana leaves (stalk plus dried banana leaf) in a standard mixture of concentration and coast cross.
A) 15% of banana leave and 85% of standard mixture;
B) 25% of banana leave and 75% of standard mixture;
C) 35% of banana leave and 65% of standard mixture;
The statistical analysis was performed using SAS software. The significant differences that reached 5% probability were analysed by searching for linearity in the responses obtained with different treatments.
Results
Among the three treatments, dried banana stalk had the highest degradability of dry matter (56.73%). The degradability of dry leaf and dry stalk plus dry leaves was 28.67%, and 35.77%, respectively (Table 1). The NDF content (Table 1a) was significantly different between the treatments. Treatments A (1%) and C (0.96%) were equal, and treatment B exhibited the best digestibility (0,02%).
Table 1 – in situ digestibility of dry banana leaves fed to sheep.
TreatmentVariable |
(A)%
|
(B)% |
(C)% |
Dry Matter |
35.7 |
56.7 |
28.6 |
Crude Protein |
11.0 |
6.0 |
14.0 |
The ADF (Table 1a) differed between all treatments (P ≤ 0.05). The degradability of dry leaves (treatment C) was the best (0,030%), followed by treatment A (0,050%). Treatment B was the worst in terms of ADF degradation (0,047%). The apparent digestibility results are presented for all treatments in Table 2: 15, 25 and 35% of dry matter of the banana plant (leaf + stalk) added to a standard mixture of concentrate and coast-cross hay.
Table 1a – in situ digestibility of dry banana plants leaves fed to sheep.
Treatment |
(A)% |
(B)% |
(C)% |
NDF |
1.00 a |
0.02 b |
0.96 a |
ADF |
0.05 a |
0.047 b |
0.030 c |
There was no change in hepatic or renal function in the animals that received feed supplemented with banana leaves. All the values were within the normal limits. The pH measurements indicated severe ruminal alkalosis in the animals, with a pH between 7.5 and 9.0.
Table 2 – the apparent digestibility of dry banana leaves in sheep.
Leaf concentration (%) |
15%* |
25%** |
35%*** |
Dry matter |
61.70 a |
63.39 a |
41.05 b |
Crude protein |
67.55 a |
67.27 a |
53.99 b |
Crude fiber |
61.41 a |
56.59 a |
21.99 b |
NNE |
73.05 a |
72.52 a |
59.73 b |
The same lowercase letters in the same row represent data that are not significantly different, and different lowercase letters in the same row indicate significant differences (P ≤ 0.05).
*Treatment (A)/ ** Treatment (B)/ ***Treatment (C)
Discussion
Among the three treatments, dried banana stalk had the highest degradability of dry matter (56.73%). The degradability of dry leaf and dry stalk plus dry leaves was 28.67%, and 35.77%, respectively (Table 1). There are two possible explanations for these data: the leaves are covered with waxes and lipids; and a higher proportion of the fiber in the stems is hemicellulose, whereas the leaves are rich in cellulose. These hypotheses suggest the need to analyze the leaves and stems separately to determine the lipid components in the leaves and the cellulose and hemicellulose content of the stalk and leaf fibers. These data, together with the tannin concentrations in the stalks and leaves, would clarify the results of this experiment. The NDF content (Table 1a) was significantly different between the treatments. Treatments A (1%) and C (0.96%) were equal, and treatment B exhibited the best digestibility (0,02%).
The ADF (Table 1a) differed between all treatments (P ≤ 0.05). The degradability of dry leaves (treatment C) was the best (0,030%), followed by treatment A (0,050%). Treatment B was the worst in terms of ADF degradation (0,047%). Another explanation for the best NDF degradation of treatment B relates to the higher concentration of hemicellulose in the stalk. The good ADF degradation of treatments A and C may be due to the amounts of cellulose and lignin present in the leaves. The clinical evaluations of the animals showed no changes.
The apparent digestibility results are presented for all treatments in Table 2: 15, 25 and 35% of dry matter of the banana plant (leaf + stalk) added to a standard mixture of concentrate and coast-cross hay. As the quantity of leaves added to the standard feed increased, the total digestibility decreased to a greater degree, what was measured by rates of CP, CF, NFE and DM. There was a decrease in digestibility in the range of 25% to 35%, since in the range of 15% to 25% was not observed a significant difference, as showed in table 2. It was assumed that the greater tannin concentration in the leaves impaired digestibility (EGGUM; CHRISTENSEN, 1975; MEHANSHO et al., 1987).
Palatability was reduced with the dry banana leaf, which was not the case when the animals were fed with fresh leaves. According to Patra and Saxena (2010), high tannin concentrations adversely affect nutrition in grazing ruminants. Tannins have an astringent flavor, which alters the palatability of the diet and reduces feed intake. The dried leaves have a higher tannin concentration because of water loss during the drying process. Chung et al. (1998a) reported that tannins are also nutritionally undesirable compounds because of their ability to precipitate proteins, inhibit digestive enzymes and affect the utilization of vitamins and minerals. The ingestion of tannins on a large scale can result in adverse health effects. However, small quantities of banana (Musa spp.) leaves have a different effect than the findings reported by Chung et al. (1998a), since physical and clinical examinations did not uncover any deleterious effects of Musa spp (HOSTE; TORRES-ACOSTA, 2011).
Tannins form complexes that are insoluble and indigestible in the rumen and intestine; these complexes inhibit microbial enzymes involved in fiber degradation (SMITH; MACKIE, 2004; WALLER, 2006). Tannins are also responsible for decreased growth rate, food absorption, energy metabolism and protein digestibility. Eggum and Christensen (1975), Kumar et al. (2012), discovered that the addition of tannic acid to the diet of rats decreased the digestibility of protein and amino acids and the use of metabolic proteins. Mehansho et al. (1987) demonstrated that tannins can bind to epithelial cells and cause subsequent precipitation of proteins that penetrate the cells surface, causing damage to the liver. Furthermore, tannins reduce the amount of vitamin A in the liver and interfere with the use of vitamin B12 Chung et al. (1998b), Krishnan et al. (2014), they also form insoluble complexes with divalent iron, making it less absorbable. Interestingly, tannins have astringent properties, antidiarrheal activity, antimicrobial (SCALBERT, 1991), antifungal activity (HART; HILLIS, 1972) and antiseptic effects. They also have the ability to form waterproof layers over exposed skin and mucous membranes, and they are haemostatic (precipitate alkaloids).
There was no change in hepatic or renal function in the animals that received feed supplemented with banana leaves. All the values were within the normal limits. The pH measurements indicated severe ruminal alkalosis in the animals, with a pH between 7.5 and 9.0. However, these animals did not exhibit any clinical symptoms. It was not possible to perform ammonia tests due to reagent problems.
This project was the first to study banana plant leaves and stalks as an alternative feed source for sheep. Further studies should be performed to establish acceptable standards for the safe amounts of secondary compounds, such as tannins, and to standardize the methods for quantifying these secondary compounds.
Conclusion
Banana plant (Musa spp.) leaves and stalks can be used as an alternative source of nutrition for ruminants in a program that emphasizes sustainability, since these biomass residues are used judiciously. The indiscriminate use of banana leaves can result in low digestibility and consequently, economical losses to the farmer. However, in a proper nutritional formulation, banana leaves and stalks can substantially benefit the producers and will not impinge on animal health.
Conflicts of interest
The authors declare no conflicts of interest regarding the work presented here.
Authors’ contribution
Bruno Leonardo Mendonça Ribeiro – execution of the experiment; Mariane Ferreira Franco – writing and execution of the experiment; Eduardo Carvalho Marques – execution of the experiment; Lucas Alencar Fernandes Beserra – work corrections; Gisela Gregoria Choque – work corrections; Lilian Gregory – guidance, corrections and revision of the text.
Financial support
We are grateful to the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for their financial support – 11/17731-2.
Acknowledgements
We are grateful to the Faculty of Veterinary Medicine and Animal Science of the University of São Paulo for the support. These experiments comply with the current Brazilian law.
References
AOAC. Association of Official Analytical Chemists. Official Methods of the Analysis of AOAC International, 17th ed. Washington, DC, 2000.
CARMO, T. D.; BARBOSA, P. M.; GERASEEV, L. C.; COSTA, D. S.; SELES, G. M.; DUARTE, E. R. Intake and digestibility of lamb fed diets containing banana crop residues. Pesquisa Agropecuária Brasileira, v. 53, n. 2, p. 197-205, 2018. https://doi.org/10.1590/S0100-204X2018000200008
CASAS, B. A. D.; PHILIPPE, M. G.; BECKER, T.; RAMOS, B. H.; BORGES, V. E.; MARTINS, C. E. N.; SCHWEGLER, E.; PERIPOLLI, V. Use of residues from the northern region of the state of Santa Catarina in cattle feed on ruminal and hepatic health. Brazilian Journal of Development, v. 6, n. 4, p. 19357-19370, 2020. https://doi.org/10.34117/bjdv6n4-197
CHUNG, K. T.; WONG, T. Y.; WEI, C. I.; HUANG, Y. W.; LIN, Y. Tannins and human health: a review. Critical Reviews in Food Science and Nutrition, v. 38, n. 6, p. 421-464, 1998a. https://doi.org/10.1080/10408699891274273
CHUNG, K. T.; WEI, C. I.; JOHNSON, M. G. Are tannins a double-edged sword in biology and health? Trends in Food Science & Technology, v. 9, n. 4, p. 168-175, 1998b. https://doi.org/10.1016/S0924-2244(98)00028-4
DOUMAS, I. B. T.; BIGGES, H. G. Standard Methods of Clinical Chemistry, v. 7. Academic Press, New York, 1972, 333p.
EGGUM, B. O.; CHRISTENSEN, K. D. Breeding for Seed Protein Improvement Using Nuclear Techniques. International Atomic Energy Agency, Vienna, Austria, 1975.
FAO. Food and Agriculture Organization of the United Nations. 2018.
FERRÃO, J. E. M. Na linha dos descobrimentos dos séculos XV e XVI – Intercâmbio de plantas entre a África Ocidental e a América. Revista de Ciências Agrárias, v. 36, n. 2, p. 250-269, 2013. https://doi.org/10.19084/rca.16303
GERASSEV, L. C.; MOREIRA, S. J. M.; ALVES, D. D.; AGUIAR, A. C. R.; MONÇÃO, F. P.; SANTOS, A. C. R.; SANTANA, C. J. L.; VIEGAS, C. R. Viabilidade econômica da utilização dos resíduos da bananicultura na alimentação de cordeiros confinados. Revista Brasileira de Saúde e Produção Animal, v. 14, n. 4, p. 734-744, 2013. https://www.scielo.br/j/rbspa/a/lang=en
HART, J. H.; HILLIS, W. E. Inhibition of Wood-Rotting Fungi by Ellagitannins in the Heartwood of Quercus alba. Phytopathology, v. 62, p. 620-626, 1972. https://doi.org/10.1094/Phyto-62-620
HOSTE, H.; TORRES-ACOSTA, J. F. J. Non-Chemical control of helminths in ruminants: adapting solutions for changing worms in a changing world. Veterinary Parasitology, v. 180, n. 1-2, p. 144-154, 2011. https://doi.org/10.1016/j.vetpar.2011.05.035
KRISHNAN, S. S. C.; SUBRAMANIAN, I. P.; SUBRAMANIAN, S. P. Isolation, characterization of syringin, phenylpropanoid glycoside from Musa paradisiaca tepal extract and evaluation of its antidiabetic effect in streptozotocin-induced diabetic rats. Biomedicine and Prevention Nutrition, v. 4, n. 2, p. 105-111, 2014. https://doi.org/10.1016/j.bionut.2013.12.009
KUMAR, K. P. S.; BHOWMIK, D.; DURAIVEL, S.; UMADEVI, M. Traditional and medicinal uses of banana. Journal of Pharmacognosy and Phytochemistry, v. 1, n. 3, p. 51-63, 2012. https://www.phytojournal.com/archives/2012.v1.i3.22/traditional-and-medicinal-uses-of-banana
LUCCI, C. Nutrição e Manejo de Bovinos Leiteiros. Manole, São Paulo, Brazil, 1997.
LUSTGARTEN, J. A.; WENK, R. E. Simple, rapid, kinetic method for serum creatinine measurement. Clinical Chemistry, v. 18, n. 11, p. 1419-1422, 1972. https://doi.org/10.1093/clinchem/18.11.1419
MEHANSHO, H.; BUTLER, L. G.; CARLSON, D. M. Dietary tannins and salivary proline-rich proteins: interactions, inductions, and defense mechanisms. Annual Review of Nutrition, v. 7, p. 423-440, 1987. https://doi.org/10.1146/annurev.nu.07.070187.002231
ORSKOV, E. R. Protein Nutrition in Ruminants. San Diego: Academic Press, 1982, 160p.
ORSKOV, E. R.; HOVELL, F. D.; MOULD, F. The use of nylon bag technique for the evaluation of feedstuffs. Tropical Animal Production, v. 5, n. 3, p. 195-213, 1980. https://www.cipav.org.co/TAP/TAP/TAP53/53_1.pdf
PATRA, A. K.; SAXENA, J. A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen. Phytochemistry, v. 71, n. 11-12, p. 1198‑1222, 2010. https://doi.org/10.1016/j.phytochem.2010.05.010
RAMDANI, D.; HERNAMAN, I.; NURMEIDIANSYAH, A. A.; HERYADI, D.; NURACHMA, S. Potential Use of banana peels waste at different ripening stages for sheep feeding on chemical, tannin, and in vitro assessments. IOP Conference Series: Earth and Environmental Science, v. 334, 2019. https://doi.org/10.1088/1755-1315/334/1/012003
ROSENBERGER, G. Clinical Examination of Cattle. Verlag Paul Parey, Berlin and Hamburg, Germany, 1979.
RUSDY, M. Nutritional value of bananas (Musaceae) wastes for ruminants. CAB Reviews, v. 14, n. 44, 2019. https://doi.org/10.1079/PAVSNNR201914044
SCALBERT, A. Antimicrobial properties of tannins. Phytochemistry, v. 30, n. 12, p. 3875-3883, 1991. https://doi.org/10.1016/0031-9422(91)83426-L
SMITH, A. H.; MACKIE, R. I. Effect of condensed tannins on bacterial diversity and metabolic activity in the rat gastrointestinal tract. Applied and Environmental Microbiology, v. 70, n. 2, p. 1104‑1115, 2004. https://doi.org/10.1128/AEM.70.2.1104-1115.2004
TALKE, H.; SCHUBERT, G. E. Enzymatic urea determination in the blood and serum in the Warburg optical test. Klinische Wochenschrift, v. 43, p. 174-175, 1965. https://doi.org/10.1007/BF01484513
UDÉN, P.; ROBINSON, P. H.; WISEMAN, J. Use of detergent system terminology and criteria for submission of manuscripts on new, or revised, analytical methods as well as descriptive information on feed analysis and/or variability. Animal feed science and technology, v. 118, n. 3-4, p. 181-186, 2005. https://doi.org/10.1016/j.anifeedsci.2004.11.011
VAN SOEST, P. J.; WINE, R. H. Determination of lignin and cellulose in acid detergent fiber with permanganate. Journal of the Association of Official Analytical Chemists, v. 51, n. 4, p. 780-785, 1968. https://doi.org/10.1093/jaoac/51.4.780
WALLER, P. J. From discovery to development: current industry perspectives for the development of novel methods of helminth control in livestock. Veterinary Parasitology, v. 139, n. 1-3, p. 1-14, 2006. https://doi.org/10.1016/j.vetpar.2006.02.036
Received on Abril 11, 2023
Returned for adjustments on July 27, 2023
Received with adjustments on November 7, 2023
Accepted on November 13, 2023