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Article

Effects of Dietary Inclusion of Avocado Seeds on Performance, Nutrient Digestibility, Plasma Biochemical Profile, and Carcass and Meat Traits of Growing Pigs

Department of Nutrition and Sustainable Animal Production, Estación Experimental del Zaidín, Spanish National Research Council, CSIC, Profesor Albareda, s/n, 18008 Granada, Spain
*
Author to whom correspondence should be addressed.
Animals 2025, 15(6), 780; https://doi.org/10.3390/ani15060780
Submission received: 4 February 2025 / Revised: 26 February 2025 / Accepted: 5 March 2025 / Published: 10 March 2025
(This article belongs to the Section Animal Nutrition)

Simple Summary

The sustainability of pig feeding chains can be enhanced by the inclusion of by-products from agroindustry, giving additional value to materials that are considered as waste. Avocado production has increased worldwide, and seeds are often discarded during fruit processing. We tested the inclusion of dried-milled avocado seeds in the diets of growing pigs (0, 100 and 200 g/kg). The inclusion of dried-milled seeds did not affect the voluntary feed intake of pigs. An energy value for the inclusion of dried avocado seeds in pig diets is provided (11.5 and 10.9 kJ/g dry matter of digestible and metabolizable energy, respectively). Up to 100 g/kg dried avocado seeds can be added to the practical diets of growing pigs with no deleterious effects on performance and nutrient digestibility, contributing to the value of this waste product.

Abstract

Avocado seeds (which are discarded during fruit processing) generate residue that could be utilized in pig feeding. The objective of this study was to test the effects of dietary inclusion of dried-milled avocado seeds (DAS) on pig performance, nutrient and energy digestibility, plasma biochemical parameters, and carcass and meat traits. Twenty-four Landrace × Large White barrows (24 kg body weight, BW) were randomly allocated to three experimental treatments: control diet (CO; 18% CP, 1.12% Lys, and 14 MJ ME/kg), and two diets in which 100 or 200 g DAS/kg partially replaced a CO diet (S10 and S20, respectively). Pigs were individually housed (22 ± 1 °C), and feed and water were provided ad libitum. Animals were weighed weekly and individual intake was monitored daily. The total tract apparent digestibility (TTAD) and nitrogen balance were determined. The experiment ended at 40 kg BW, when the animals were slaughtered for blood and tissue sampling. Voluntary feed intake was not affected by the addition of up to 200 g DAS/kg to the diet. However, growth, nutrient TTAD, and nitrogen retention were depressed at the highest DAS inclusion level. The nutritional characteristics of longissimus lumborum muscle were not affected by DAS ingestion. The inclusion of up to 100 g DAS/kg in the diets of growing pigs could be used to add value to this waste product.

1. Introduction

Growing public concern for the environment and animal welfare is driving the adoption of sustainable practices in animal production and the food industry. Horticultural and fruit waste—abundant in Spain and in other European countries—contain beneficial compounds that can be reused in livestock diets, promoting the circular economy [1]. By-products are non-primary products obtained from a specific process that can be used as raw materials for other processes, adding value to production chains. Traditionally, the industry has used food by-products as raw materials for animal feeds and as substrates for composting [2,3]. Avocado (Persea americana Mill.) is a tropical and subtropical fruit native to southern Mexico and other Mesoamerican regions [4], of which production has increased worldwide [5]. The commercial processing of the fruit results in approximately 30% of the total fruit weight being discarded as waste [6]. The avocado processing industry yields essential oils, and after processing, the pulp, seeds, peels, and exhausted pulp are discarded as waste, generating a large amount of solid residue, representing a problem for processing industries due to the significant ecological impact of their disposal in landfills [7]. In Spain, more than 115.000 t are produced annually [8], generating a considerable amount of waste. On the other hand, avocado by-products can be considered as an energy source for animals [9,10]. Avocado seeds inclusion in animal feeds has been explored, due to their potential as a source of nutrients and beneficial compounds [11]. Avocado seeds contain high fiber content, which can improve gastrointestinal health; moreover, they contain phenolic compounds and flavonoids [6], which are natural antioxidants with the potential to enhance immune health and reduce oxidative stress in animals [12]. In addition, Chia and Dykes (2020) [13] demonstrated the antimicrobial activity of ethanol extracts of avocado seeds against selected Gram-positive and Gram-negative bacteria, and Leite et al. (2009) [14] showed the antifungal activity of methanol and hexane extracts of avocado seeds, as well as larvicidal activity in vivo.
Pork consumption is estimated to increase by 105% from 2010 to 2050 due to the increase in the world population and in animal protein consumption [15]. The scientific community is currently aware of the environmental costs associated with pork production, which are mainly caused by the economic and environmental costs of producing and transporting feedstuffs, such as cereals and soybeans, which are primarily produced in North and South America [16,17]. The introduction of avocado seeds as an industrial by-product in the pork industry would facilitate progress in the circular economy and waste reduction. Despite scientific evidence on their beneficial effects, there are few studies evaluating the inclusion of avocado by-products in pig diets in terms of performance, nutrient digestibility, or carcass traits [9,18,19,20], and none specifically dealing with the inclusion of avocado seeds. Our hypothesis is that the inclusion of dried avocado seeds in the diet does not negatively affect performance and nutrient digestibility in growing pigs. The objective of the present study was to test the effects of dietary inclusion of dried avocado seeds on growing pig performance, nutrient digestibility, plasma metabolites, and carcass and meat traits. An energy value for avocado seed inclusion in pig diets will also be provided.

2. Materials and Methods

2.1. Animals, Diets, and Experimental Procedures

Twenty-four Landrace × Large White barrows with 23.8 ± 0.94 kg initial body weight (BW) and a similar age (78 ± 2 d), provided by Piensos Jiménez S. L. (Jaén, Spain), were randomly allocated to 3 experimental diets, and individually housed in 2 m2 pens in an environmentally controlled room (22 ± 1 °C). The experimental diets (8 pigs/treatment) were: control diet (CO; commercial diet based on barley, corn, and soybean meal) and two diets in which 100 or 200 g/kg of dried-milled avocado seeds from a local producer (Grupo La Caña, Motril, Granada, Spain) were added to partially replace (weight/weight) the CO diet (diets S10 and S20, respectively). The seeds were dried and milled before mixing with the rest of the dietary components. Diets were offered in pelleted form. The CO diet was a standard diet for growing pigs (Cereales MACOB S.L. Villanueva Mesía, Granada, Spain) covering all nutrient requirements [21]. Feed and water were freely available. The nutrient composition of experimental diets and dried-milled seeds appear in Table 1.
Pigs were weighed weekly, and individual intake was monitored daily by collecting the refused feed. Total tract apparent digestibility (TTAD) and nitrogen balance measurements were carried out after two weeks of adaptation to the experimental treatments and environmental conditions (33.8 ± 0.75 kg BW). Pigs were moved to individual metabolic cages in an environmentally controlled room (21 ± 1 °C) 2 days before starting the excreta collection. Whole feces and urine were daily collected for 3 days, weighed, and representative aliquots were stored at −20 °C until homogenization and analysis. Urine samples were collected on 50 mL 4.5M H2SO4. At the end of the experiments, samples of feces and urine were pooled per pig. Apparent energy digestibility, metabolizability, and nitrogen retention were determined as in the methods described in Palma-Granados et al. (2021) [22].
The experiment ended when pigs achieved approximately 40 kg BW, and the animals were slaughtered by exsanguination after electronarcosis. Blood samples were taken in EDTA-containing tubes, placed in an ice bath, and centrifuged at 1400× g at 4 °C for 20 min. Plasma was stored at −80 °C until analyses.
Measurements of midline backfat (first rib, last rib, minimum fat over the gluteus medius muscle) and leanness (gluteal thickness at the cranial end of the gluteus medius muscle) were performed in the left-half carcass. The weights and yields of primal cuts were determined 24 h postmortem, as described previously [23]. Muscle traits were determined in the right-half carcass, as described in Seiquer et al. (2019) [24]. Briefly, at 30 min post-mortem (p.m.), the pH values of longissimus (last rib level) were measured using a pH meter (HI 99163, Hanna Instruments, Cluj-Napoca, Romania) equipped with a penetration electrode (pH30min). Carcasses were placed at 4 °C for 24 h, and thereafter, pH was measured again (pH24h). Then, the longissimus muscle was dissected and separated from the carcasses. A 3 cm thick steak was then trimmed of visible fat and allowed to bloom for 15 min at 4 °C for color measurements, which were performed instrumentally using a Minolta CR-400 colorimeter (Konica Minolta Corp., Tokyo, Japan), in accordance with the CIE L*, a*, b* color system. Thereafter, samples were vacuum-packed and stored at −20 °C for chemical composition analysis. In addition, 1.5–2 cm steaks were cut from the longissimus muscle, trimmed of external fat and connective tissue, and used for drip loss determinations, as described in Seiquer et al. (2019) [24].

2.2. Sample Analyses

The chemical determinations of feeds, feces, and urine were as those described in Palma-Granados et al. (2021) [22]. Briefly, fecal samples were freeze-dried and ground before analysis. The dry matter and ash content were determined according to the Association of Official Analytical Chemists [25] in feeds and feces. The chemical determinations in muscle samples were as described in Seiquer et al. (2019) [24]. Nitrogen contents in feed, feces, muscle, and urine were analyzed using a LECO Truspec CN determinator (Leco Corporation, St. Joseph, MI, USA). Crude protein content was calculated using the factor of 6.25. Gross energy was analyzed in an isoperibolic bomb calorimeter (PARR 1356, Biometa, IL, USA). Urine samples were freeze-dried in a polyethylene sheet of known energy value, and their gross energy was obtained by difference. The lipid content of feeds was determined by ether extraction [25]. Amino acids in feeds were analyzed by HPLC (Alliance 2695 separation module; Waters Cromatrografía SA, Madrid, Spain) after protein hydrolysis with 6 N HCl at 110 °C for 24 h following the Waters Pico Tag method [26], as described in Palma-Granados et al. (2021) [22]. The acid detergent fiber in feeds was determined in an ANKOM220 Fiber Analyzer Unit (ANKOM Technology Corporation, Macedon, NY, USA), and were expressed inclusive of residual ash and lignin, determined by solubilization of cellulose with sulfuric acid, following Goering and van Soest (1970) [27]. The total extractable polyphenols in feeds was determined using the methodology described by Julkunen-Tiito (1985) [28]. Plasma metabolites (glucose, triglycerides, cholesterol, albumin, total proteins, ammonium, creatinine, lactate, urea, and uric acid), lactate dehydrogenase, alkaline phosphatase, alanine aminotransferase, aspartate aminotransferase, and γ-glutamyl enzymatic activities were determined in duplicate using a COBAS INTEGRA 400 analyzer (Roche Diagnostics GmbH, Mannheim, Germany).

2.3. Statistics

The statistical treatment of data was assessed by analysis of variance to check the effects of the addition of dried-milled avocado seeds to the basal diet on the parameters under study. An individual pig was the experimental unit. Mean differences were assessed by Tukey’s multiple-range test. The level of significance was set to 0.05 and a tendency of significance was considered for p-values between 0.05 and 0.10. Linear regressions using inclusion levels of dried-milled avocado seeds on the basal diet (0, 100, or 200 g/kg) as the independent variable and digestible or metabolizable energy content (kJ/g DM) as the dependent variable were carried out to calculate the energy value of dried avocado seeds for pigs. The statistical calculations were carried out using STATGRAPHICS Centurion XVI, version 16.1.18 (StatPoint Technologies Inc., Warrenton, VA, USA).

3. Results

In the following sections, animal performance, nutrient digestibility and nitrogen balance, carcass traits and meat quality determinations, and plasma biochemical parameters are shown.

3.1. Animal Performance

The main results regarding pig growth appear in Table 2. Pigs fed with a S20 diet had a lower BW at slaughter and average daily gain (ADG) than CO and S10 pigs (9.8 and 25% lower, respectively; p < 0.05). There were no differences in daily intake (p > 0.05). Feed efficiency, expressed either as gain/feed or gain/metabolizable energy intake (MEI), was depressed in S20 pigs (20 and 15%, respectively; p < 0.05).

3.2. Total Tract Apparent Nutrient Digestibility (TTAD), Nitrogen Balance, and Estimation of Energy Values for Dried Avocado Seeds

Results regarding the TTAD of nutrients and nitrogen balance are described in Table 3. Dry matter TTAD tended to decrease in S20 pigs (p = 0.071), and TTAD for organic matter and gross energy decreased in S20 pigs by 3 and 4%, respectively, compared to CO and S10 pigs (p < 0.05). Energy metabolizability was also lower in S20 pigs (p < 0.01), resulting in a decreased metabolizable energy intake in the S20 group (p < 0.01). Nitrogen TTAD and nitrogen retention were decreased in S20 pigs compared to the rest of the pigs (by 12 and 31%, respectively; p < 0.01). At the same time, the efficiency of retention of ingested nitrogen decreased by 16% in S20 pigs (p < 0.01), although no differences were detected for the efficiency of retention of digested nitrogen (p > 0.05).
To calculate the energy value of dried avocado seeds for pig diets, linear regressions using inclusion levels of dried avocado seeds on the basal diet (0, 100, or 200 g/kg) as the independent variable, and the digestible or metabolizable energy content of the whole diet (kJ/g DM) as the dependent variable, were performed. The following highly significant equations (p < 0.001) were obtained:
DE = 15.989 (±0.157) − 0.00452 (±0.00121) × S; n = 24; r2 = 64.9; s.e. = 0.45
ME = 15.421 (±0.154) − 0.00452 (±0.00117) × S; n = 24; r2 = 67.4; s.e. = 0.42
where DE, ME, and S are digestible energy (kJ/g DM), metabolizable energy (kJ/g DM), and inclusion level of dried-milled avocado seeds in the diet (g/kg), respectively. The intercept of these equations estimates the DE and ME content (kJ/g DM) of the basal diet (CO), the slope, and the decrease in energy value per g of increase in dried-milled avocado seeds in replacement of the CO diet (g/kg). When assuming S = 1000, the DE and ME contents of the dried avocado seeds used in the present trial are estimated as 11.5 and 10.9 kJ/g DM, respectively.

3.3. Body Components and Carcass Traits

The relative weight of body (g/100 g empty body weight) and carcass (g/100 g carcass) components of pigs are presented in Table 4. Many body components remained unaffected by the dietary addition of dried-milled avocado seeds. However, the relative weights of liver and small intestine increased in S20 pigs by 23% (p < 0.01) and 11% (p = 0.09). On the other hand, the relative weight of kidneys reduced in S10 compared to S20 pigs (14%; p < 0.05), spleen decreased in S20 compared to CO pigs (12%; p < 0.05), and stomach reduced in S20 vs. S10 pigs (13%; p < 0.05). Fat carcass components remained unchanged; meanwhile, some lean components decreased (sirloin by 13%; p < 0.01), or tended to decrease in S20 pigs (loin and muscle thickness, p = 0.09 for both).

3.4. Physical Quality Traits and Chemical Composition of Longissiumus Lumborum Muscle

The muscle pH at 30 min and 24 h postmortem (Figure 1a) and pH drop between the two measurements (Figure 1b) showed no differences between experimental groups (p > 0.05). No differences were found in the chemical components and energy content of longissimus lumborum samples between groups (p > 0.05, Table 5). Similarly, muscle instrumental color parameters, brightness (L*), redness (a*), yellowness (b*), chroma index (C*) and hue angle (h°), showed no differences between the three groups (p > 0.05, Table 5).
Nevertheless, muscle water losses 24 h post-mortem were lower in S10 and S20 compared to CO pigs (by 27–37%, p < 0.05; Figure 2) indicating a higher water retention capacity in pigs fed diets with dried-milled avocado seeds added.

3.5. Plasma Biochemical Parameters

Plasma metabolites showed no differences between treatments, apart from a greater creatinine concentration in S20 pigs (p < 0.01, Table 6), and a trend for higher total cholesterol and LDL cholesterol in S20 pigs compared to the other groups (0.05 ≤ p ≤ 0.10; Table 6). Enzyme activities were similar between the groups, except for a trend for lower alkaline phosphatase activity in pigs fed diets containing dried-milled avocado seeds (p = 0.079; Table 6).

4. Discussion

In EU countries, it has been estimated that the inclusion of food waste in pig diets could reduce the land used for pork production by 20% [29]. This issue is of particular interest for Mediterranean countries with large amounts of agroindustrial by-products, with a high potential for recycling in livestock diets and reducing food/feedstuff competition [30]. Spain has the largest pig herd in the EU [31], and is also the main European avocado producer. Therefore, there are opportunities for using avocado by-products generated during industrial processing in the national pork industry, contributing to waste reduction and the circular economy. We have evaluated the impact of inclusion of dried-milled avocado seeds in the diet on growth performance, nutrient digestibility, plasma metabolites, and carcass and meat traits in pigs, and provided an energy value for their inclusion in pig diets. Although scientific evidence highlights their potential benefits, there are few studies evaluating the incorporation of avocado by-products into pig diets regarding performance, nutrient digestibility, or carcass characteristics [9,18,19,20]. Moreover, no research has specifically focused on the inclusion of avocado seeds in diets for pigs.
In our study, the addition of dried-milled avocado seeds produced a slight reduction in crude protein and digestible energy (in S20 in particular) and an increase in acid detergent fiber, lignin, and total extractable polyphenol contents. The dried-milled seeds used in the present work showed similar crude protein, ash, and gross energy content, although a lower lipid content than in other reports (3.7 vs. 16%, ¸Talabi et al. 2016 [32]). Tugiyanti et al. (2019) [33] reported similar crude protein, total lipids and gross energy, and lower ash content than our study (2.7 vs. 5.2%). Other authors reported lower ash (1.34 vs. 5.2; [34]) or lipid content (1.1 vs. 3.7%; [35]). Differences in seed composition are probably related to local variations and seed processing.
Pig intake was not affected by the inclusion of up to 200 g dried-milled seed/kg diet, indicating good pig tolerance to seed addition in our study. Similarly, George et al. (2020) [11] reported no effect of dietary inclusion of avocado seeds on the feed intake of broilers, although inclusion levels were much lower than in the present case (0 to 1.5%). Fránquez et al. (2017) [18] reported decreased feed intake (by 30%) in pigs consuming diets containing 21% fresh whole avocado paste vs. control pigs (0% paste); however, diets were not isoenergetic, as the paste is rich in pulp with a high lipid and energy content, which probably satiated the pigs fed the paste-added diet earlier. In our study, despite similar feed intake, S20 pigs grew slower and showed reduced feed efficiency compared to the rest of pigs. The S10 group, in contrast, had similar growth and feed efficiency as CO pigs, with growth rates within the normal range for their BW [36]. Growing pigs fed isoenergetic diets including different proportions of avocado silage (0 to 5%) showed no differences in performance [37]; however, the physical–chemical characteristics of avocado silage (silage from paste after oil extraction) differed considerably from that of dried seed. In our work, apart from slower growth, the S20 group also presented reduced TTAD of nutrients, energy, and of nitrogen in particular, compared to the rest of pigs. The reduced nitrogen TTAD could be related to the higher polyphenol content of the S20 diet due to the higher seed proportion. The ingestion of polyphenolic compounds (such as tannins) can be beneficial due to their antimicrobial, antioxidant, and anti-inflammatory properties for the gut [38], although they can also negatively affect protein (amino acid) digestibility [39,40]. In this sense, phytochemical analyses of avocado seed extracts revealed the presence of saponins, oxalates, cyanogenic glycosides, and tannins, among others [41]. Grageola et al. (2019) [19] reported decreased fecal nutrient digestibility in growing pigs fed with diets supplemented with avocado paste (including pulp, seed, and peels), which was not observed with the addition of only avocado pulp [9], which might be related to the increased fiber and polyphenol contents in seeds and peels compared to the pulp.
On the other hand, the DE and ME values obtained for dried-milled avocado seeds in our trials (11.5 and 10.9 kJ/g DM, respectively) can be useful for the inclusion of this waste product in practical pig feeding, with both environmental and economic benefits, as mentioned above. However, it is desirable to extend the trials to other physiological phases such as gestating and lactating sows, in which even higher inclusion levels could be considered. As polyphenols in avocado seeds may negatively affect dietary nitrogen digestibility and nitrogen retention, further characterization of their biological effects is needed.
No major effects of dietary inclusion of dried-milled avocado seeds on the relative weights of body components were detected. However, lower proportions of lean carcass components in S20 pigs, together with increased creatinine plasma concentrations, could indicate higher muscle protein catabolism [42] in S20 pigs, despite unaltered urinary N excretion.
The chemical composition and physical and organoleptic properties of longissimus lumborum muscle were unchanged after dried avocado seed ingestion, which showed no detrimental effects on meat quality. Interestingly, a higher water retention capacity in pigs fed diets with dried avocado seeds added was detected, a trait that can be considered positive for the quality and organoleptic properties of the meat, as it is related to juiciness and tenderness [43]. Other authors found differences in longissimus chemical composition when 30% whole avocado paste was added to the diets of finishing pigs (higher protein and lower intramuscular fat, as well as differences in fatty acid composition [44]), possibly related to the higher lipid content of the whole avocado paste compared to that of the dried-milled seeds.

5. Conclusions

Under the conditions of our study, the voluntary feed intake of growing pigs was not affected by the addition up to 200 g dried-milled avocado seed/kg diet. Nevertheless, pig growth, nutrient and energy digestibility, and nitrogen retention were depressed with the highest level of inclusion of avocado seeds (200 g/kg diet). Polyphenols in seeds may have negative effects on nutrient digestibility, in particular on dietary nitrogen, and further characterization of their biological effects is needed. No deleterious effects on meat quality were detected; on the contrary, water holding capacity was enhanced with seed ingestion. An energy value of dried-milled avocado seed for inclusion in pig diets is provided (11.5 and 10.9 kJ/g DM, respectively), for which up to 100 g/kg could be safely added to practical diets for growing pigs, contributing to the value of this waste product.

Author Contributions

Conceptualization, R.N., M.L., I.S. and I.F.-F.; methodology, C.G.-C., A.H., I.S. and L.L.; software, L.L.; validation, C.G.-C., L.L. and R.N.; formal analysis, C.G.-C., A.H., M.L., L.L. and I.S.; investigation, C.G.-C. and R.N.; resources, R.N.; data curation, C.G.-C., A.H. and L.L.; writing—original draft preparation, C.G.-C. and R.N.; writing—review and editing, C.G.-C., A.H., M.L., I.S., L.L., I.F.-F. and R.N.; visualization, C.G.-C. and R.N.; supervision, R.N.; project administration, R.N.; funding acquisition, R.N. All authors have read and agreed to the published version of the manuscript.

Funding

Supported by the AGUACAVALUE Operational Group (20180020012499), the European Union, and the Spanish Ministry of Agriculture, Fisheries and Feeding.

Institutional Review Board Statement

Experimental procedures and animal care were in agreement with Spanish Ministry of Agriculture guidelines (RD53/2013). Procedures were approved by the Bioethical Committee of the Spanish National Research Council (CSIC, Spain) and the competent local authority (Junta de Andalucía, Spain, project reference 27/03/2020/045).

Informed Consent Statement

The pigs were owned by the Spanish Research Council purchased from the company Piensos Jiménez S.L. All procedures were supervised by the Ethical Committe or our Institution and approved by the Competent Authority.

Data Availability Statement

The datasets that support the findings of this study are available from the corresponding author upon request.

Acknowledgments

We gratefully acknowledge Miguel A. Liñán, Alfonso García, and Gloria González for their valuable and skillful work looking after the pigs and performing laboratory work.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

  1. Kasapidou, E.; Sossidou, E.; Mitlianga, P. Fruit and Vegetable Co-Products as Functional Feed Ingredients in Farm Animal Nutrition for Improved Product Quality. Agriculture 2015, 5, 1020–1034. [Google Scholar] [CrossRef]
  2. Kumar, A.; Roy, B.; Lakhani, G.P.; Jain, A. Evaluation of Dried Bread Waste as Feedstuff for Growing Crossbred Pigs. Vet. World 2014, 7, 698–701. [Google Scholar] [CrossRef]
  3. Westendorf, M.L.; Zirkle Pas, E.W.; Gordon, R. Feeding Food or Table Waste to Livestock 1. Prof. Anim. Sci. 1996, 12, 129–137. [Google Scholar] [CrossRef]
  4. Bergh, B. The Origin, Nature, and Genetic Improvement of the Avocado. In California Avocado Society; California Avocado Society: Ventura, CA, USA, 1992; Volume 76. [Google Scholar]
  5. OECD-FAO. Agricultural Outlook 2023–2032. Available online: https://www.oecd.org/en/publications/oecd-fao-agricultural-outlook-2023-2032_08801ab7-en.html (accessed on 3 February 2025).
  6. Rojas-García, A.; Fuentes, E.; Cádiz-Gurrea, M.d.l.L.; Rodriguez, L.; Villegas-Aguilar, M.D.C.; Palomo, I.; Arráez-Román, D.; Segura-Carretero, A. Biological Evaluation of Avocado Residues as a Potential Source of Bioactive Compounds. Antioxidants 2022, 11, 1049. [Google Scholar] [CrossRef]
  7. López-Cobo, A.; Gómez-Caravaca, A.M.; Pasini, F.; Caboni, M.F.; Segura-Carretero, A.; Fernández-Gutiérrez, A. HPLC-DAD-ESI-QTOF-MS and HPLC-FLD-MS as Valuable Tools for the Determination of Phenolic and Other Polar Compounds in the Edible Part and by-Products of Avocado. LWT 2016, 73, 505–513. [Google Scholar] [CrossRef]
  8. MAPA 2025. Available online: https://www.mapa.gob.es/es/estadistica/temas/publicaciones/anuario-de-estadistica/2023/default.aspx?parte=3&capitulo=07&grupo=9&seccion=15 (accessed on 3 February 2025).
  9. Grageola, F.; Sangines, L.; Díaz, C.; Gómez, A.; Cervantes, M.; Lemus, C.; Ly, J. The Effect of Breed and Dietary Level of Avocado Fat on the N and Energy Balance in Young Pigs. J. Anim. Feed Sci. 2010, 19, 37–48. [Google Scholar] [CrossRef]
  10. Van Ryssen, J.B.J.; Skenjana, A.; van Niekerk, W.A. Can Avocado Meal Replace Maize Meal in Broiler Diets? Appl. Anim. Husb. Rural. Dev. 2013, 6, 22–27. [Google Scholar]
  11. George, O.S.; Kingsley, C.; Ekine, O.A. Effects of Dietary Inclusion of Avocado Seed Meal (Persea americana) on the Carcass Yield and Haematological Profile of Broiler Chickens. Niger. J. Anim. Prod. 2020, 47, 82–88. [Google Scholar] [CrossRef]
  12. Bahru, T.B.; Tadele, Z.H.; Ajebe, E.G. A Review on Avocado Seed: Functionality, Composition, Antioxidant and Antimicrobial Properties. Chem. Sci. Int. J. 2019, 27, CSIJ.45609. [Google Scholar] [CrossRef]
  13. Raymond Chia, T.W.; Dykes, G.A. Antimicrobial Activity of Crude Epicarp and Seed Extracts from Mature Avocado Fruit (Persea americana) of Three Cultivars. Pharm. Biol. 2010, 48, 753–756. [Google Scholar] [CrossRef]
  14. Leite, J.J.G.; Brito, É.H.S.; Cordeiro, R.A.; Brilhante, R.S.N.; Sidrim, J.J.C.; Bertini, L.M.; Morais, S.M.d.; Rocha, M.F.G. Chemical Composition, Toxicity and Larvicidal and Antifungal Activities of Persea americana (Avocado) Seed Extracts. Rev. Da Soc. Bras. Med. Trop. 2009, 42, 110–113. [Google Scholar] [CrossRef] [PubMed]
  15. Lestingi, A. Alternative and Sustainable Protein Sources in Pig Diet: A Review. Animals 2024, 14, 310. [Google Scholar] [CrossRef] [PubMed]
  16. Manceron, S.; Ben-Ari, T.; Dumas, P. Feeding Proteins to Livestock: Global Land Use and Food vs. Feed Competition. OCL-Oilseeds Fats 2014, 21, 10. [Google Scholar] [CrossRef]
  17. Martins, C.F.; Pestana Assunção, J.; Ribeiro Santos, D.M.; Madeira, M.S.M.d.S.; Alfaia, C.M.R.P.M.; Lopes, P.A.A.B.; Coelho, D.F.M.; Cardoso Lemos, J.P.; de Almeida, A.M.; Mestre Prates, J.A.; et al. Effect of Dietary Inclusion of Spirulina on Production Performance, Nutrient Digestibility and Meat Quality Traits in Post-Weaning Piglets. J. Anim. Physiol. Anim. Nutr. 2021, 105, 247–259. [Google Scholar] [CrossRef]
  18. Fránquez, P.; Rodríguez, G.; Lemus, C.; Grageola, F.; Ly, J. Performance Traits and Indexes of the Intake Pattern of Fattened Pigs with Fresh Paste of Whole Avocado. Cuba. J. Agric. Sci. 2017, 51, 329–336. [Google Scholar]
  19. Grageola, F.; Lemus, C.; Rodríguez, C.; Ponce, J.L.; Ly, J. Digestibility Indices in Pigs Fattened Ad Libitum with Diets Based on Cereals and Fresh Paste of Discarded Entire Avocados. Cuba. J. Agric. Sci. 2019, 53, 387–393. [Google Scholar]
  20. Seshoka, M.L.; Fourie, P.J.; Kanengoni, A.T.; Malebana, I.M.M.; Thomas, R.S.; Nkosi, B.D. Dietary Inclusion of Ensiled Avocado Oil Cake Affects Growth, Nutrient Digestion, and Carcass Characteristics of Pigs. S. Afr. J. Anim. Sci. 2020, 50. [Google Scholar] [CrossRef]
  21. De Blas, C.; Gasa, J.; Mateos, G.G.; Madrid, U.P.; Barcelona, U.A. Necesidades Nutricionales Para Ganado Porcino Normas FEDNA, 2nd ed.; Fundación Española para el Desarrollo de la Nutrición Animal: Madrid, Spain, 2013. [Google Scholar]
  22. Palma-Granados, P.; Lara, L.; Seiquer, I.; Lachica, M.; Fernández-Fígares, I.; Haro, A.; Nieto, R. Protein Retention, Growth Performance and Carcass Traits of Individually Housed Immunocastrated Male-and Female-and Surgically Castrated Male Iberian Pigs Fed Diets of Increasing Amino Acid Concentration. Animal 2021, 15, 100187. [Google Scholar] [CrossRef]
  23. Nieto, R.; Lara, L.; Barea, R.; García-Valverde, R.; Conde-Aguilera, J.A.; Aguilera, J.F. Growth of Body Components and Carcass Composition of Iberian Pigs of 10 to 150 Kg Body Weight as Affected by the Level of Feeding and Dietary Protein Concentration. J. Anim. Sci. 2013, 91, 4197–4207. [Google Scholar] [CrossRef]
  24. Seiquer, I.; Palma-Granados, P.; Haro, A.; Lara, L.; Lachica, M.; Fernández-Fígares, I.; Nieto, R. Meat Quality Traits in Longissimus Lumborum and Gluteus Medius Muscles from Immunocastrated and Surgically Castrated Iberian Pigs. Meat Sci. 2019, 150, 77–84. [Google Scholar] [CrossRef]
  25. Association of Official Analytical Chemists (AOAC). Official Methods of Analysis of AOAC International; AOAC: Rockville, MD, USA, 2005; Volume 2. [Google Scholar]
  26. Cohen, S.A.; Meys, M.; Tarvin, T.L. The Pico-Tag Method: A Manual of Advanced Techniques for Amino Acid Analysis; Millipore Corporation: Temecula, CA, USA, 1989. [Google Scholar]
  27. Goering, H.K.; Van Soes, P.J. Forage Fiber Analyses (Apparatus, Reagents, Procedures, and Some Applications); US Agricultural Research Service: Washington, DC, USA, 1970.
  28. Julkunen-Tiitto, R. Phenolic Constituents in the Leaves of Northern Willows: Methods for the Analysis of Certain Phenolics. J. Agric. Food Chem. 1985, 33, 213–217. [Google Scholar] [CrossRef]
  29. zu Ermgassen, E.K.H.J.; Phalan, B.; Green, R.E.; Balmford, A. Reducing the Land Use of EU Pork Production: Where There’s Swill, There’s a Way. Food Policy 2016, 58, 35–48. [Google Scholar] [CrossRef]
  30. Georganas, A.; Kyriakaki, P.; Giamouri, E.; Mavrommatis, A.; Tsiplakou, E.; Pappas, A.C. Mediterranean Agro-Industrial by-Products and Food Waste in Pig and Chicken Diets: Which Way Forward? Livest. Sci. 2024, 289, 105584. [Google Scholar] [CrossRef]
  31. MAPA 2024. Available online: https://www.mapa.gob.es/es/ganaderia/temas/produccion-y-mercados-ganaderos/indicadoressectorporcino2023_tcm30-564427.pdf (accessed on 3 February 2025).
  32. Talabi, J.Y.; Osukoya, O.A.; Ajayi, O.O.; Adegoke, G.O. Nutritional and Antinutritional Compositions of Processed Avocado (Persea americana Mill) Seeds. Pelagia Res. Libr. Asian J. Plant Sci. Res. 2016, 6, 6–12. [Google Scholar]
  33. Tugiyanti, E.; Iriyanti, N.; Apriyanto, Y.S. The Effect of Avocado Seed Powder (Persea americana Mill.) on the Liver and Kidney Functions and Meat Quality of Culled Female Quail (Coturnix Coturnix Japonica). Vet. World 2019, 12, 1608. [Google Scholar] [CrossRef]
  34. Ly, J.; Fránquez, P.; Rodríguez, G.; Lemus, C.; Dominguez, I.A.; Grageola, F. Note on in Vitro Digestion of Avocado Products for Pigs. Arq. Bras. Psicol. 2021, 51, 138–141. [Google Scholar] [CrossRef]
  35. Takenaga, F.; Matsuyama, K.; Abe, S.; Torii, Y.; Itoh, S. Lipid and Fatty Acid Composition of Mesocarp and Seed of Avocado Fruits Harvested at Northern Range in Japan. J. Oleo Sci. 2008, 57, 591–597. [Google Scholar] [CrossRef]
  36. MAPA 2004. Available online: https://www.mapa.gob.es/es/ganaderia/temas/ganaderia-y-medio-ambiente/porcino_blanco_2024_21-3-24subidoaweb_tcm30-440945.pdf (accessed on 3 February 2025).
  37. Nkosi, B.D.; Seshoka, M.L.; Fourie, P.J.; Kanengoni, A.T.; Malebana, I.M.M.; Thomas, R.S. Dietary Enzyme Addition on the Growth Performance and Carcass Characteristics of Pigs Fed Diets Containing Avocado Oil Cake Silage. Trop. Anim. Health Prod. 2020, 52, 2945–2953. [Google Scholar] [CrossRef]
  38. Caprarulo, V.; Giromini, C.; Rossi, L. Chestnut and Quebracho Tannins in Pig Nutrition: The Effects on Performance and Intestinal Health. Animal 2021, 15, 100064. [Google Scholar] [CrossRef]
  39. Mariscal-Landín, G.; Avellaneda, J.H.; de Souza, T.C.R.; Aguilera, A.; Borbolla, G.A.; Mar, B. Effect of Tannins in Sorghum on Amino Acid Ileal Digestibility and on Trypsin (EC 2.4. 21.4) and Chymotrypsin (EC 2.4. 21.1) Activity of Growing Pigs. Anim. Feed Sci. Technol. 2004, 117, 245–264. [Google Scholar] [CrossRef]
  40. Mariscal-Landın, G.; Lebreton, Y.; Sève, B. Apparent and Standardised True Ileal Digestibility of Protein and Amino Acids from Faba Bean, Lupin and Pea, Provided as Whole Seeds, Dehulled or Extruded in Pig Diets. Anim. Feed Sci. Technol. 2002, 97, 183–198. [Google Scholar] [CrossRef]
  41. Nwaogu, L.A.; Alisi, C.S.; Ojiako, O.A. Studies on the Nutritional and Phytochemical Properties of Persea americana Seed. Bio-Res. 2008, 6, 320–322. [Google Scholar] [CrossRef]
  42. Fernández-Fígares, I.; Lachica, M.; Nieto, R.; Rivera-Ferre, M.G.; Aguilera, J.F. Serum Profile of Metabolites and Hormones in Obese (Iberian) and Lean (Landrace) Growing Gilts Fed Balanced or Lysine Deficient Diets. Livest. Sci. 2007, 110, 73–81. [Google Scholar] [CrossRef]
  43. Font-i-Furnols, M.; Čandek-Potokar, M.; Maltin, C.; Prevolnik Povše, M. A Handbook of Reference Methods for Meat Quality Assessment; European Cooperation in Science and Technology (COST): Brussels, Belgium, 2015. [Google Scholar]
  44. Hernández-López, S.H.; Rodríguez-Carpena, J.G.; Lemus-Flores, C.; Grageola-Nuñez, F.; Estévez, M. Avocado Waste for Finishing Pigs: Impact on Muscle Composition and Oxidative Stability during Chilled Storage. Meat Sci. 2016, 116, 186–192. [Google Scholar] [CrossRef] [PubMed]
Figure 1. The pH at 30 min and 24 h post-mortem (a) and the corresponding pH fall (b) in longissimus lumborum muscle of growing pigs fed either a basal (control) diet or the control diet with 100 (S10) or 200 (S20) g of dried-milled avocado seed/kg added, respectively (eight pigs/treatment).
Figure 1. The pH at 30 min and 24 h post-mortem (a) and the corresponding pH fall (b) in longissimus lumborum muscle of growing pigs fed either a basal (control) diet or the control diet with 100 (S10) or 200 (S20) g of dried-milled avocado seed/kg added, respectively (eight pigs/treatment).
Animals 15 00780 g001
Figure 2. Water losses at 24 h post-mortem in longissimus lumborum muscle of growing pigs fed either a basal (control) diet or the control diet with 100 (S10) or 200 (S20) g of dried-milled avocado seed/kg added, respectively. Bars with different superscript differ (p < 0.05; eight pigs/treatment).
Figure 2. Water losses at 24 h post-mortem in longissimus lumborum muscle of growing pigs fed either a basal (control) diet or the control diet with 100 (S10) or 200 (S20) g of dried-milled avocado seed/kg added, respectively. Bars with different superscript differ (p < 0.05; eight pigs/treatment).
Animals 15 00780 g002
Table 1. Analyzed chemical composition of experimental diets and dried avocado seed, g/kg as fed 1.
Table 1. Analyzed chemical composition of experimental diets and dried avocado seed, g/kg as fed 1.
COS10S20Dried Seed
Dry matter893896894890
Crude protein18918817377.8
Lysine11.210.811.03.7
Threonine9.39.48.23.3
Methionine4.13.83.91.2
Valine9.99.69.44.6
Isoleucine8.27.57.63.4
Total ashes50.754.350.751.9
Lipids47.644.946.237.1
Acid detergent fiber51.264.060.096.1
Acid detergent lignin5.316.318.656.8
Total extractable polyphenols2.65.17.950
Gross energy (MJ/kg)17.317.217.216.7
Digestible energy (MJ/kg) 214.114.013.510.2
1 CO: basal diet (g/kg: barley, 397; maize, 321; soybean meal, 226; lard, 25; NaCl, 5.0; CaHPO4, 8.0; CaCO3, 6.3; vitamins and minerals, 4.0; L-Lys (98.5%), 3.9; L-Thr (98%), 2.0; DL-Met (99%), 1.4). S10 and S20: 100 or 200 g/kg of dried-milled avocado seeds added to partially replace (weight/weight) the CO diet, respectively. 2 Determined in present trials.
Table 2. Performance data of growing pigs fed either a basal (CO) diet or the CO diet added with 100 (S10) or 200 (S20) g of dried-milled avocado seeds/kg, respectively (eight pigs/treatment).
Table 2. Performance data of growing pigs fed either a basal (CO) diet or the CO diet added with 100 (S10) or 200 (S20) g of dried-milled avocado seeds/kg, respectively (eight pigs/treatment).
Treatments
COS10S20SEMp-Value 1
Initial BW, kg23.723.823.80.940.993
Final BW, kg41.2 b40.8 b37.0 a1.080.023
Intake, g DM/d15991583148160.00.324
ADG 2, g500 b482 b368 a22.10.001
Gain/feed0.313 b0.304 b0.248 a0.0090.001
Gain/MEI 3, g/MJ20.4 b20.2 b17.2 a0.6180.002
1 Within a row, mean values showing different superscript differ (p < 0.05). 2 Average daily gain. 3 Metabolizable energy intake.
Table 3. Total tract apparent digestibility (TTAD) and nitrogen balance of growing pigs fed either a basal (CO) diet or the CO diet added with 100 (S10) or 200 (S20) g of dried-milled avocado seed/kg, respectively (eight pigs/treatment).
Table 3. Total tract apparent digestibility (TTAD) and nitrogen balance of growing pigs fed either a basal (CO) diet or the CO diet added with 100 (S10) or 200 (S20) g of dried-milled avocado seed/kg, respectively (eight pigs/treatment).
Treatments
COS10S20SEMp-Value 1
Mean BW, kg37.9 b36.2 b32.7 a0.970.003
Dry matter TTAD0.8330.8340.8100.0080.071
Organic matter TTAD0.845 b0.845 b0.821 a0.0080.047
Gross energy TTAD0.816 b0.814 b0.784 a0.0090.025
Energy metabolizability0.791 b0.788 b0.752 a0.0090.007
ME intake, MJ/day20.4 b19.2 b16.8 a0.5130.001
ME intake, kJ/kg0.75.day1336 b1302 b1225 a23.60.008
ME, kJ/g DM15.3 b15.1 b14.4 a0.170.003
N intake, g/day45.0 b42.8 b36.1 a1.070.001
Nitrogen TTAD0.819 b0.783 b0.701 a0.0120.001
N retention, g/day26.9 b24.4 b17.7 a0.950.001
N retention, g/kg0.75.day1.76 b1.65 b1.30 a0.060.001
Retained N/ingested N0.597 b0.569 b0.489 a0.0170.001
Retained N/digested N0.7310.7270.6960.0200.378
1 Within a row, mean values showing different superscript differ (p < 0.05).
Table 4. Body components (g/100 g empty body weight), carcass components (g/100 g carcass), and carcass linear measurements of growing pigs fed either a basal (CO) diet or a CO diet added with 100 (S10) or 200 (S20) g of dried-milled avocado seed/kg, respectively (eight pigs per treatment).
Table 4. Body components (g/100 g empty body weight), carcass components (g/100 g carcass), and carcass linear measurements of growing pigs fed either a basal (CO) diet or a CO diet added with 100 (S10) or 200 (S20) g of dried-milled avocado seed/kg, respectively (eight pigs per treatment).
Treatments
COS10S20SEMp-Value 1
Body components
Blood4.914.995.290.1280.445
Carcass71.471.069.50.3240.061
Total viscera13.814.114.80.2080.186
Heart0.610.600.560.0140.405
Liver2.37 a2.50 a3.00 b0.0610.001
Lungs2.162.232.040.0750.585
Kidneys0.54 ab0.49 a0.57 b0.0100.031
Spleen0.26 b0.24 ab0.23 a0.0050.028
Digestive tract6.686.727.080.1240.374
Stomach1.05 ab1.08 b0.94 a0.0210.027
Small intestine3.363.373.750.0780.091
Large intestine2.272.272.40.0450.418
Mesenteric fat1.211.291.290.0320.499
Carcass components
Sirloin1.51 b1.41 b1.27 a0.1850.003
Loin7.407.686.900.1380.093
Butt lean4.21 b3.46 a3.54 ab0.1190.035
Backfat2.211.811.710.0980.113
Ribs11.411.111.40.2510.851
Ham32.232.933.10.3670.573
Shoulder24.024.024.70.2140.365
Belly12.012.611.50.2420.155
Spine5.144.965.970.2690.287
Backfat thickness, mm
At gluteus medius muscle6.57.66.40.3640.343
At last rib9.59.48.30.6630.691
At first rib15.916.916.00.7010.819
Carcass length, cm64.163.661.60.4990.121
Muscle thickness 2, mm45.444.140.10.9570.088
1 Within a row, mean values showing different superscript differ (p < 0.05). 2 At gluteus medius muscle.
Table 5. Nutritional composition and color parameters of longissimus lumborum muscle of growing pigs fed either a basal (CO) diet or the CO diet with 100 (S10) or 200 (S20) g of dried-milled avocado seed/kg added, respectively (eight pigs/treatment).
Table 5. Nutritional composition and color parameters of longissimus lumborum muscle of growing pigs fed either a basal (CO) diet or the CO diet with 100 (S10) or 200 (S20) g of dried-milled avocado seed/kg added, respectively (eight pigs/treatment).
Treatments
COS10S20SEMp-Value
Nutritional composition
Protein, g/100 g19.719.920.30.2410.288
Intramuscular fat, g/100 g3.102.622.760.1940.226
Total ash, g/100 g1.281.271.260.0250.953
Energy kJ/100 g54453454710.40.666
Water, g/100 g77.177.476.70.3320.329
Color, CieLAB
L*38.938.937.20.3480.272
a*5.906.115.440.3680.438
b*4.234.564.110.3580.680
C*7.347.646.840.4760.500
36.236.836.11.540.940
Table 6. Plasma biochemical parameters of growing pigs fed either a basal (CO) diet or the CO diet with 100 (S10) or 200 (S20) g of dried-milled avocado seed/kg added, respectively (eight pigs/treatment).
Table 6. Plasma biochemical parameters of growing pigs fed either a basal (CO) diet or the CO diet with 100 (S10) or 200 (S20) g of dried-milled avocado seed/kg added, respectively (eight pigs/treatment).
Treatments
COS10S20SEMp-Value 1
Glucose, mg/100 mL18216916211.40.450
Triglycerides, mg/100 mL42.634.342.14.000.285
Ammonia, µM/L29431134330.90.531
Lactate, mg/100 mL15916817123.70.937
Albumin, g/L36.637.536.01.640.798
Total proteins, g/L85.186.186.82.980.922
Total cholesterol, mg/100 mL1191201345.550.101
HDL cholesterol, mg/100 mL50.947.949.52.090.599
LDL cholesterol, mg/100 mL47.751.158.02.960.063
Creatinine, mg/100 mL1.05 a1.11 a1.26 b0.040.002
Urea N, mg/100 mL16.319.015.61.690.340
Uric acid, mg/100 mL0.2890.2110.2830.0320.193
Alkaline phosphatase, U/L19612214722.10.079
Alanine transaminase, U/L59.254.455.43.920.667
Aspartate aminotransferase, U/L94.488.995.514.80.945
γ-Glutamyl transferase, U/L15011194.920.10.159
Lactate dehydrogenase, U/L2329218820301270.273
1 Within a row, mean values showing different superscript differ (p < 0.05).
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García-Contreras, C.; Haro, A.; Lachica, M.; Seiquer, I.; Lara, L.; Fernández-Fígares, I.; Nieto, R. Effects of Dietary Inclusion of Avocado Seeds on Performance, Nutrient Digestibility, Plasma Biochemical Profile, and Carcass and Meat Traits of Growing Pigs. Animals 2025, 15, 780. https://doi.org/10.3390/ani15060780

AMA Style

García-Contreras C, Haro A, Lachica M, Seiquer I, Lara L, Fernández-Fígares I, Nieto R. Effects of Dietary Inclusion of Avocado Seeds on Performance, Nutrient Digestibility, Plasma Biochemical Profile, and Carcass and Meat Traits of Growing Pigs. Animals. 2025; 15(6):780. https://doi.org/10.3390/ani15060780

Chicago/Turabian Style

García-Contreras, Consolación, Ana Haro, Manuel Lachica, Isabel Seiquer, Luis Lara, Ignacio Fernández-Fígares, and Rosa Nieto. 2025. "Effects of Dietary Inclusion of Avocado Seeds on Performance, Nutrient Digestibility, Plasma Biochemical Profile, and Carcass and Meat Traits of Growing Pigs" Animals 15, no. 6: 780. https://doi.org/10.3390/ani15060780

APA Style

García-Contreras, C., Haro, A., Lachica, M., Seiquer, I., Lara, L., Fernández-Fígares, I., & Nieto, R. (2025). Effects of Dietary Inclusion of Avocado Seeds on Performance, Nutrient Digestibility, Plasma Biochemical Profile, and Carcass and Meat Traits of Growing Pigs. Animals, 15(6), 780. https://doi.org/10.3390/ani15060780

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