Next Article in Journal
Comparison of a Commercial Enzyme-Linked Immunosorbent Assay (ELISA) with the Modified Agglutination Test (MAT) for the Detection of Antibodies against Toxoplasma gondii in a Cohort of Hunting Dogs
Next Article in Special Issue
Effects of Glyceryl Monolaurate on Production Performance, Egg Quality, Oviduct Cytokines and Intestinal Microflora of 66 Weeks Old Laying Hens
Previous Article in Journal
The Importance of Nest Box Placement for Barn Owls (Tyto alba)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Animals
Volume 12
Issue 20
10.3390/ani12202816
animals-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Effect of Dietary Blue-Green Microalgae Inclusion as a Replacement to Soybean Meal on Laying Hens’ Performance, Egg Quality, Plasma Metabolites, and Hematology

by
Ahmed O. Abbas
1,2,*,
Abdulaziz A. Alaqil
1,
Gamal M. K. Mehaisen
2 and
Nancy N. Kamel
3
1
Department of Animal and Fish Production, College of Agricultural and Food Sciences, King Faisal University, P.O. Box 420, Al-Ahsa 31982, Saudi Arabia
2
Department of Animal Production, Faculty of Agriculture, Cairo University, 7 Gamma St., Giza 12613, Egypt
3
Department of Animal Production, National Research Centre, El Buhouth St., Dokki, Giza 12622, Egypt
*
Author to whom correspondence should be addressed.
Animals 2022, 12(20), 2816; https://doi.org/10.3390/ani12202816
Submission received: 8 September 2022 / Revised: 8 October 2022 / Accepted: 15 October 2022 / Published: 18 October 2022
(This article belongs to the Special Issue Feed Additives in Poultry Nutrition)
Versions Notes

Abstract

:

Simple Summary

In recent years, a variety of natural products and medicinal plants have been widely implemented as alternative nutritional strategies for poultry production. This study aimed to investigate the possible impact of different dietary levels of spirulina microalgae on the productive performance, egg traits, blood metabolites, and hematological parameters of laying hens. Based on the findings, the spirulina could be contained within the layer diets as an alternative source of protein, with positive impacts on the laying hens’ production and physiological performance.

Abstract

Spirulina platensisis (SP) is a blue-green microalgae with a high value for animal and poultry nutrition. The study employed 250 40-week-old, HY-Line W-36 commercial laying hens. The layers received one of five experimental diet substitutes in five groups for 10 consecutive weeks (five replicates of 10 hens each group); a soybean-corn basal diet formulation without SP (Control group) or the soybean partially substituted with 3% SP, 6% SP, 9% SP, and 12% SP (for the remaining four groups). The results showed that dietary SP treatment significantly (p < 0.05) improved the productive performance, egg quality, blood metabolites, and hematological parameters of laying hens. In addition, there were linear and quadratic effects for increasing the levels of SP inclusion into the layer diets; however, the highest values of most parameters were observed when using 9% SP (90 g/kg of the layer diets). Furthermore, the results showed that 4.7% of the soybean meal ingredient in the layer diet could be replaced by 1% of SP. In conclusion, the partial replacement of soybean meal by SP into layer diets could be used as a promising nutritional approach to optimize the performance of laying hens.

1. Introduction

SP is a blue-green microalgae which grows naturally in brackish water and lakes in several countries [1]. It gained prominence since it was used as a source of food during long-term space missions [2]. SP has abundant contents of the macro- and micronutrients, and therefore, it is used to produce safe nutritional and medicinal compounds [3,4]. It could be simply harvested and commercially processed into appropriate forms to be used as human and animal nutrition [5,6,7,8,9]. SP comprises high levels of protein (50–70%), carbohydrates (15–20%), lipids (5–7%), minerals (6–9%), and vitamins (1–4%) [1,10]. SP provides most of the essential amino acids, fatty acids, carotenoids, and other phytopigments [1]. It is a unique source of vitamin B12, γ-linolenic fatty acid, β-carotene, calcium, and iron [10].
The nutritional value of SP has attracted many researchers to study the effectiveness and the functional mechanism of the spirulina on animal species. It has been reported that SP enhances the productive performance and improves the general health of different animals [11,12,13,14]. In addition, it has been displayed that SP has favorable biological properties such as immunomodulation [15,16], tumor resistance [17], anti-inflammation [18], lowering-cholesterol [19], and antioxidant activation [20].
In particular, dietary supplementation with spirulina has positive results in poultry species. It was demonstrated that traditional protein sources of broiler diets could be substituted with up to 15% SP without negatively affecting the meat quality and production [21,22,23]. Additionally, it was reported that inclusion of 0.25–1.0% SP into broiler diets improved the growth efficiency, the nutrients digestibility, the antioxidant enzyme activity, the anti-inflammatory response, and the cecal microflora population [14,24,25]. In addition, Feshanghchi et al. [26] found that supplementing SP at 1% to broiler diets can effectively mitigate the negative effects of aflatoxins on the broiler performance, immunological function, and blood biochemical characteristics. In recent studies, it was found that adding 0.5–2% SP to broiler and quail diets can relieve the deleterious results of heat stress on the growth, carcass, redox, and physiological characteristics [12,27,28,29]. In contrast, feeding 2% SP to laying hens enhanced their egg yolk color and shell thickness and strength, and improved their liver functions, egg lipid profile, and antioxidant status [30,31]. Other studies [13,32,33] displayed that supplementing SP at 0.2–2.5% into the laying hen rations enhanced only the egg yolk color without exhibiting any effect on the other egg parameters.
According to our knowledge, most of the works of the literature investigating the dietary SP supplementation in laying hens applied no more than 5% SP as a feed additive into their basal diets [34,35]. In addition, there is a lack of sufficient studies discussing the possible effect of SP administration as a main diet ingredient replacing the traditional sources of protein into layer diets. The goal of this study was to highlight the potential impact of inserting various doses of SP as a replacement to soybean meal into laying hens’ diets on their performance, eggs traits, metabolites, and hematology profile.

2. Materials and Methods

2.1. Birds and SP Treatments

Two hundred and fifty 40-week-old, HY-Line W-36 commercial laying hens were placed individually in 40 × 40 × 50 cm cages maintained in an open housing system. The hens were kept in standard environmental and hygienic conditions. The hens were provided with a daily lighting system (16L/8D), ad libitum feed, and unlimited access to water. The hens were randomly allocated into five equal groups (5 replicates × 10 hens each, per group) and fed on one of five experimental diets for 10 consecutive weeks (40–50 weeks of age). The diets were formulated as mash to meet the nutritional recommendations for HY-Line W-36 layers (Table 1). The first group received a soybean–corn basal diet formulation without SP supplementation (Control group). The other four groups received a basal soybean–corn formulation diet substituted with 3%, 6%, 9%, and 12% Spirulina platensis microalgae (3% SP, 6% SP, 9% SP, and 12% SP groups, respectively). The SP microalgae was obtained as a freeze-dried powder form (Inner Mongolia Rejuve Biotech. Co., Ltd., Ordos, China) and mixed daily into the diet of the laying hens. The rest of the feed was sieved to check the percentage of the residual SP as an indicator for consuming SP by the birds without separation from the diet. The minimum requirements for poultry nutrition [36] were considered to figure out the nutrients of the experimental diets. The minerals and amino acid profile of soybean meal (SBM) and SP are presented in Table 1, according to the pamphlet of the commercial supplier. The nutritional analysis of the SP and the experimental diets were carried out using the guidelines of the Association of Official Analysis Chemists [37], and are included in Table 1 and Table 2, respectively.

2.2. Productive Performance

The hens were weighed at 40 and 50 wk of age to determine the initial and final body weights (IBW and FBW, respectively). Eggs were collected and weighed daily to assess the average hen daily egg production (EP%) and egg weight (EW) throughout the experiment. The feed intake (FI) was recorded daily. Feed conversion ratio (FCR) was then calculated based on the total FI per egg mass produced per hen.

2.3. Egg Quality

At the 50th week of age, 6 eggs per replicate in each treatment group (n = 30) were randomly selected to evaluate egg-quality traits. First, eggs were weighed (W), and then they were broken on a flat plate to obtain the internal parts (yolks and albumens). The heights of the albumens (AH) and the yolks (YH) were measured using a tripod micrometer (Baxlo Instrumentos de Medida y Precisión, SL, Barcelona, Spain). The diameters of the albumens (AD) and the yolks (YD) were also measured by a standard caliper (Total Tools, South Melbourne, Australia). The albumen index (AI) and yolk index (YI) were assessed by using the following formulas: AH/AD % and YH/YD %, respectively. The Haugh units (HU) were obtained by the following formula: 100 log (AH—1.7 W0.37 + 7.6). The yolk color (YC) score was physically determined using DSM-YC Fan (ORKA Food Technology, LLC, West Bountiful, UT, USA). The shells of the broken eggs were gently washed, air-dried, and then weighed to calculate the shell weight (SW) percent of the egg weight. The shell thickness (ST) was obtained via an eggshell thickness gauge (0–10 mm range, 0.01 mm sensitivity, Baxlo Instrumentos de Medida y Precisión, SL, Barcelona, Spain), based on the average measurements of 3 points on the equatorial regions and the blunt part of the egg. The shell strength (SS) was also measured by applying an assisted system pressure to the egg blunt (Egg Force Reader, ORKA Food Technology LLC, UT, USA).

2.4. Metabolites Assay

Immediately after the end of the treatments (50 weeks of age), two blood samples per replicate (n = 10) were collected from the brachial vein and transferred into heparinized tubes. The samples were centrifuged at 2000× g for 10 min under cooling temperature (4 °C) to separate plasma which was stored at −20 °C for further biochemical analysis. The total protein (TP), albumin (ALB), globulin (GLB), calcium (CA), phosphorus (PP), creatinine (CRT), and uric acid (UA) concentrations in the plasma as well as the activities of aspartate transferase (AST) and alanine transferase (ALT) enzymes were measured using an automated scanning spectrophotometer (CE1010, Cecil Instruments Limited, Cambridge, UK) and commercial colorimetric kits (BioDiagnostic, Giza, Egypt). The full protocol description for each analysis is presented in the Supplementary Materials (File S1).

2.5. Hematological Parameters

At the conclusion of the trial (50 weeks of age), blood samples were gathered from the brachial vein of 2 birds per replicate (n = 10) and relocated into heparinized tubes to figure out the hematological parameters. Two drops (10 µL) of each sample were diluted with either 490 µL of brilliant cresyl blue stain or 1.990 mL of physiological saline. A drop of each of these two dilutions was mounted on a Bright-Line™ hemocytometer slide (American Optical, Buffalo, NY, USA) to count the total white blood cells (WBC) and red blood cells (RBC), respectively, by using a light microscope at 200× magnification. The hemoglobin (HB) concentration was measured using a colorimetric kit (BioDiagnostic, Giza, Egypt) according to the cyanomethemoglobin method cited in a previous study [38]. The hematocrit (HT) values were determined by reading the packed cell volume on the graduated scale after centrifugation of the blood samples in Wintrobe hematocrit tubes (2000× g, 20 min, 4 °C). The mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), and MCH concentration (MCHC) were then calculated using the following equations:
MCV [fL] = (HT [%]/RBC [106/µL]) × 10,
MCH [pg/cell] = HB [g/dL]/RBC [106/µL] × 10,
MCHC [g/dL] = HB [g/dL]/HT [%] × 100,

2.6. Statistical Analysis

The SPSS software package (version 22.0; IBM Corp., Armonk, NY, USA, 2013) was used to analyze the data. Multivariate tests of the general linear model (GLM) analysis were carried out with respect to the SP inclusion levels into the layer diets as independent variables. Orthogonal polynomial contrasts were performed to test the linear and quadratic trends of the increasing SP levels applied in the present study on all parameters of the productive performance, egg quality, blood metabolites, and hematology. Five replicates of 10 birds per group were statistically analyzed for the productive performance data (n = 50), while 6 eggs per replicate were randomly selected in each group for analyzing egg quality data (n = 30), and 2 birds per replicate were randomly selected per group to analyze the plasma metabolites and hematological parameters (n = 10). Results of the means in addition to the pooled standard error of means (SEM) were presented. A pairwise comparison was used to separate the means considering the level of statistical significance at p < 0.05.

3. Results

3.1. Productive Performance

The effect of SP treatment on the productive performance of laying hens during 40–50 weeks of age is presented in Table 3. The FBW was linearly increased (p < 0.05), as the level of the SP increased to 12% into layer diets. The SP treatment linearly and quadratically (p < 0.05) increased the EP, EW, and FI, and decreased the FCR. The best values in EP, EW, and FCR were obtained when SP was included into layer diets at 9%, while the best values of FI were observed when using 12% of SP.

3.2. Egg Quality

The effect of SP treatment on the egg quality parameters is displayed in Table 4. Results showed that the SP treatment linearly and quadratically increased (p < 0.05) the egg AI and HU. Linear increasing trends were obtained in the YI and YC as a response to the increased levels of the dietary SP treatment, and a quadratic effect was also observed in the YC (p < 0.05). There was a quadratic increase in the SW and a linear increase in the ST as the dietary SP level increased (p < 0.05). In addition, the SP treatment linearly and quadratically (p < 0.05) increased the SS, obtaining the highest SS value with 9% SP.

3.3. Blood Metabolites

The effect of SP treatments on the plasma metabolites of laying hens is presented in Table 5. The TP, ALB, and GLB were linearly (p < 0.05) increased by the SP treatment, showing the highest values at 9% SP level. In addition, there was a quadratic effect (p < 0.05) for the increasing levels of the SP on the TP and GLB. The SP treatments linearly (p < 0.05) increased the plasma CA and PP levels, and a quadratic increase was found in the CA as the dietary SP level increased. On the other hand, the SP treatment linearly and quadratically (p < 0.05) decreased the plasma AST, ALT, CRT, and UA levels, showing the lowest values in the 9% SP treatment group.

3.4. Hematological Parameters

The effect of SP treatments on the hematological analysis of laying hens is shown in Table 6. Results indicated that the WBC was linearly and quadratically (p < 0.05) increased as the dietary SP level increased, while the RBC was linearly (p < 0.05) increased by increasing the SP level into layer diets. Data also showed that the HB was linearly and quadratically (p < 0.05) increased as the dietary SP level increased, while the HT was linearly (p < 0.05) increased by increasing the SP level into layer diets. Furthermore, linear and quadratic elevation (p < 0.05) in the MCH and MCHC were obtained as the dietary SP levels increased. In contrast, the SP treatment did not affect the MCV of the layers (p > 0.05).

4. Discussion

In the current study, the possible effect of dietary SP inclusion into layer diets as a complementary source of protein on the hens’ performance was investigated. Therefore, approximately 3.9%, 7.7%, 11.6%, and 15.4% of the SBM as a traditional source of protein in the control basal diet was substituted with 3%, 6%, 9%, and 12% SP, considering the reformulation of the other ingredients to contain the same nutritional composition for all experimental diet groups (Table 2). The dietary SP treatment positively improved the productive performance of laying hens, characterized by increased EP, EW, FI, and decreased FCR of laying hens. The increased FI by the SP treatment may be the direct reason for the linear increase in the FBW and in the other productive parameters of the treated layers [39]. Most of the research that applied the addition of the SP into poultry diets did not indicate any changes in the productive performance of laying hens [13,30,32]. This may be due to either using low levels of the SP (1.0–2.5%) or employing older hens (age > 60 wks) in these studies, compared to the higher SP levels or younger hens used in the present study. Our results indicated that the 9% of the SP treatment group showed the best outcomes regarding the productive performance. In this group, the SBM ingredient was reduced from 275 to 159 g/kg diet, suggesting that 4.7% of SBM of layer diets could be replaced by 1% of SP to optimize the performance of laying hens.
Most of the egg-quality parameters in the present study were enhanced in proportion to the increase in the SP level into the layer diet. Linear and quadratic trends in the quality parameters were evidenced by the increase in the SP levels, especially in the egg YC. In accordance with the presented results, more than 90% of linear correlation between the YC and dietary SP treatment was found in other studies [13,32,33,40]. This correlation is often attributed to the rich SP contents of β-carotene, which is converted into retinol and deposited in egg yolks [41].
According to the nutritional composition of the SBM and SP presented in Table 1, the SP contained higher contents of CP (56.4% versus 44%) and essential amino acids, such as isoleucine (6.6% versus 2.5%), valine (6.6% versus 2.4%), lysine (4.8% versus 2.7%), methionine (2.4% versus 0.7%), and threonine (5.3% versus 1.7%), than that in the SBM. The plasma proteins (TP, ALB, and GLB) were increased by the SP treatment in the current study as well as in previous studies [42,43]. This result could be because of the high contents of SP with protein and at least five essential amino acids [44]. In addition, the increase in plasma proteins may contribute to the increase in egg AI and HU, which were recorded in the SP-treatment groups, through forming a complex with the polysaccharides, polyphenols, and β-ovomucin secreted from the hens’ oviduct [45]. In addition to the finding that the SP used in the current study contains 75% CA more than the SBM (Table 1), it has also been reported that the bioavailability of CA obtained from SP was higher than that obtained from other sources [46]. Our data displayed that SP treatment significantly increased the plasma CA and PP concentration, although the CA contents of the diets were adjusted at the same level. It is an interesting result since the higher level of CA in the plasma of layers fed with SP indicated that a higher absorption of CA occurs in the SP groups compared to the SBM group. Moreover, the increase in CA and PP can explain the high positive correlation obtained in the current study between the SP levels and the egg ST and SS [47].
On the other hand, increasing the SP treatment induced a linear and quadratic decrease in the plasma AST, ALT, CRT, and UA levels, especially when using 9% SP. Similar results were previously reported in laying hens [40], in broiler chickens [12], in other animal species [11,48], and in humans [49]. The abnormality of AST and ALT levels could be a signal to hepatocyte or muscle cell damage [50], while the abnormal levels of CRT and UA could be markers to renal dysfunction [51]. The hepatoprotective properties of SP may also regulate the proteins and amino acids metabolism [52], allowing the release of albumin from the liver to the plasma stream [53]. This finding was supported in the present study by the linear increase in plasma ALB as the dietary SP increased.
The results showed a linear and/or quadratic increase in most of the haematological parameters as the dietary SP treatment increased, and the best values were obtained in the 9% SP group. The beneficial effect of spirulina intake on the blood rejuvenation was confirmed in humans and successfully applied to ameliorate the nutritional anaemia in children and elderly people [54,55]. In poultry species, the SP supplementation at 0.5–1.0% was sufficient to improve some haematological parameters, including RBC, HB, HT, MCV, and MCH, in heat-stressed broilers [12]. An increase in the WBC, RBC, and HB were observed in fish supplemented with 3–10% SP in the diet [56,57]. The increase in WBC, RBC, HB, and, consequently, the other parameters, could be due to the presence of phycocyanin and many important minerals (i.e., iron and calcium) in the spirulina, which might directly modify the blood components [58,59]. Furthermore, the well-known antioxidant properties of SP may explain the relevant increase in blood components and haematological markers in the laying hens [60] and other animals [61,62]. It was reported that such antioxidant compounds can produce a remarkable improvement in the haematological parameters through counteracting the intravascular haemolysis, iron reduction, and erythrocyte deterioration induced by oxidative stress [63].

5. Conclusions

The study concludes that SBM of layer diets could be replaced by SP to improve the productive performance, egg quality, blood metabolites, and hematology. There are linear and quadratic effects for increasing the levels of SP inclusion into the layer diets. However, the highest values of most parameters were observed when using 9% SP (90 g/kg of the layer diets). Furthermore, the results suggests that 4.7% of SBM can be replaced by 1% of SP as a promising nutritional approach to optimize the performance of laying hens.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ani12202816/s1, File S1: The protocol description for metabolites assay.

Author Contributions

Conceptualization, A.O.A., A.A.A., G.M.K.M. and N.N.K.; methodology, A.O.A., A.A.A., G.M.K.M. and N.N.K.; validation, A.O.A., A.A.A., G.M.K.M. and N.N.K.; formal analysis, A.O.A., A.A.A., G.M.K.M. and N.N.K.; investigation, A.O.A., A.A.A., G.M.K.M. and N.N.K.; resources, A.O.A., A.A.A., G.M.K.M. and N.N.K.; data curation, A.O.A., A.A.A., G.M.K.M. and N.N.K.; writing—original draft, A.O.A. and G.M.K.M.; writing—review and editing, A.O.A., A.A.A., G.M.K.M. and N.N.K.; visualization, A.O.A., A.A.A., G.M.K.M. and N.N.K.; supervision, A.O.A.; project administration, A.O.A.; funding acquisition, A.O.A. and A.A.A. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported through funds obtained from the Deanship of Scientific Research, Vice Presidency for Graduate Studies and Scientific Research, King Faisal University, Saudi Arabia (GRANT938).

Institutional Review Board Statement

The current animal study protocol was authorized by the research ethical committee of Saudi Arabia’s King Faisal University (Ref. No. KFU-REC-2022-AUG-ETHICS137).

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

Authors would like to thank the Deanship of Scientific Research, Vice Presidency for Graduate Studies and Scientific Research, King Faisal University, Saudi Arabia for their support to this work.

Conflicts of Interest

The authors declare no conflict 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. Mohan, A.; Misra, N.; Srivastav, D.; Umapathy, D.; Kumar, S. Spirulina-The Nature’s Wonder: A Review. Sch. J. Appl. Med. Sci. 2014, 2, 1334–1339. [Google Scholar]
  2. Ravi, M.; Lata, S.; Syed, D.; Solomon, A.; Paul, F.D. The Beneficial Effects of Spirulina Focusing on Its Immunomodulatory and Antioxidant Properties. Nutr. Diet. Suppl. 2010, 2, 73–83. [Google Scholar] [CrossRef] [Green Version]
  3. Costa, J.A.V.; Freitas, B.C.B.; Rosa, G.M.; Moraes, L.; Morais, M.G.; Mitchell, B.G. Operational and Economic Aspects of Spirulina-Based Biorefinery. Bioresour. Technol. 2019, 292, 121946. [Google Scholar] [CrossRef] [PubMed]
  4. Soni, R.A.; Sudhakar, K.; Rana, R.S. Spirulina—From Growth to Nutritional Product: A Review. Trends Food Sci. Technol. 2017, 69, 157–171. [Google Scholar] [CrossRef] [Green Version]
  5. Habib, M.A.B.; Parvin, M.; Huntington, T.C.; Hasan, M.R. A Review on Culture, Production and Use of Spirulina as Food for Humans and Feeds for Domestic Animals and Fish; FAO: Rome, Italy, 2008. [Google Scholar]
  6. Vilahur, G.; Sutelman, P.; Ben-Aicha, S.; Mendieta, G.; Radiké, M.; Schoch, L.; Casaní, L.; Borrell-Pagés, M.; Padro, T.; Badimon, L. Supplementation With Spirulina Reduces Infarct Size and Ameliorates Cardiac Function in a Pig Model of STEMI. Front. Pharmacol. 2022, 13, 891801. [Google Scholar] [CrossRef] [PubMed]
  7. Liang, Y.; Huang, X.; Zhang, Z.; Deng, K.; An, S.; Gao, X.; Wang, Z.; Liu, Z.; Wang, F.; Liu, D.; et al. Spirulina Supplementation Improves Lipid Metabolism and Autophagic Activities in the Liver and Muscle of Hu Lambs Fed a High-Energy Diet. Arch. Anim. Nutr. 2020, 74, 476–495. [Google Scholar] [CrossRef]
  8. Azabji-Kenfack, M.; Dikosso, S.E.; Loni, E.G.; Onana, E.A.; Sobngwi, E.; Gbaguidi, E.; Kana, A.L.N.; Nguefack-Tsague, G.; von der Weid, D.; Njoya, O.; et al. Potential of Spirulina platensis as a Nutritional Supplement in Malnourished HIV-Infected Adults in Sub-Saharan Africa: A Randomised, Single-Blind Study. Nutr. Metab. Insights 2011, 4, NMI-S5862. [Google Scholar] [CrossRef] [Green Version]
  9. Khan, Z.; Bhadouria, P.; Bisen, P. Nutritional and Therapeutic Potential of Spirulina. Curr. Pharm. Biotechnol. 2005, 6, 373–379. [Google Scholar] [CrossRef] [Green Version]
  10. Anvar, A.A.; Nowruzi, B. Bioactive Properties of Spirulina: A Review. Microb. Bioact. 2021, 4, 134–142. [Google Scholar] [CrossRef]
  11. Ragab El-Sabagh, M.; Attia, M.; Eldaim, A.; Mahboub, D.H.; Abdel-Daim, M. Effects of Spirulina platensis Algae on Growth Performance, Antioxidative Status and Blood Metabolites in Fattening Lambs. J. Agric. Sci. 2014, 6, 92. [Google Scholar] [CrossRef] [Green Version]
  12. Moustafa, E.S.; Alsanie, W.F.; Gaber, A.; Kamel, N.N.; Alaqil, A.A.; Abbas, A.O. Blue-Green Algae (Spirulina platensis) Alleviates the Negative Impact of Heat Stress on Broiler Production Performance and Redox Status. Animals 2021, 11, 1243. [Google Scholar] [CrossRef] [PubMed]
  13. Curabay, B.; Sevim, B.; Cufadar, Y.; Ayasan, T. Effects of Adding Spirulina platensis to Laying Hen Rations on Performance, Egg Quality, and Some Blood Parameters. J. Hell. Vet. Med. Soc. 2021, 72, 2945–2952. [Google Scholar] [CrossRef]
  14. Shanmugapriya, B.; Saravana Babu, S.; Hariharan, T.; Sivaneswaran, S.; Anusha, M.B. Dietary Administration of Spirulina platensis Asprobiotics Ongrowth Performanceand Histopathology in Broilerchicks. Int. J. Recent Sci. Res. 2015, 6, 2650–2653. [Google Scholar]
  15. Shokri, H.; Khosravi, A.; Taghavi, M. Efficacy of Spirulina platensis on Immune Functions in Cancer Mice with Systemic Candidiasis. J. Mycol. Res. 2014, 1, 7–13. [Google Scholar]
  16. Şahan, A. Determination of Some Haematological and Non-Specific Im-Mune Parameters in Nile Tilapia (Oreochromis niloticus L., 1758) Fed with Spirulina (Spirulina platensis) Added Diets. J. Aquac. Eng. Fish. Res. 2015, 1, 133–139. [Google Scholar] [CrossRef]
  17. Ismail, M.F.; Ali, D.A.; Fernando, A.; Abdraboh, M.E.; Gaur, R.L.; Ibrahim, W.M.; Raj, M.H.G.; Ouhtit, A. Chemoprevention of Rat Liver Toxicity and Carcinogenesis by Spirulina. Int. J. Biol. Sci. 2009, 5, 377–387. [Google Scholar] [CrossRef] [Green Version]
  18. Coskun, Z.K.; Kerem, M.; Gurbuz, N.; Omeroglu, S.; Pasaoglu, H.; Demirtas, C.; Lortlar, N.; Salman, B.; Pasaoglu, O.T.; Turgut, H.B. The Study of Biochemical and Histopathological Effects of Spirulina in Rats with TNBS-Induced Colitis. Bratisl. Lek. Listy. 2011, 112, 235–243. [Google Scholar]
  19. Gupta, S.; Hrishikeshvan, H.J.; Sehajpal, P.K. Spirulina Protects against Rosiglitazone Induced Osteoporosis in Insulin Resistance Rats. Diabetes Res. Clin. Pract. 2010, 87, 38–43. [Google Scholar] [CrossRef]
  20. Gad, A.S.; Khadrawy, Y.A.; El-Nekeety, A.A.; Mohamed, S.R.; Hassan, N.S.; Abdel-Wahhab, M.A. Antioxidant Activity and Hepatoprotective Effects of Whey Protein and Spirulina in Rats. Nutrition 2011, 27, 582–589. [Google Scholar] [CrossRef]
  21. Altmann, B.A.; Wigger, R.; Ciulu, M.; Mörlein, D. The Effect of Insect or Microalga Alternative Protein Feeds on Broiler Meat Quality. J. Sci. Food Agric. 2020, 100, 4292–4302. [Google Scholar] [CrossRef]
  22. Tavernari, F.D.C.; Roza, L.F.; Surek, D.; Sordi, C.; Silva, M.L.B.D.; Albino, L.F.T.; Migliorini, M.J.; Paiano, D.; Boiago, M.M. Apparent Metabolisable Energy and Amino Acid Digestibility of Microalgae Spirulina platensis as an Ingredient in Broiler Chicken Diets. Br. Poult. Sci. 2018, 59, 562–567. [Google Scholar] [CrossRef] [PubMed]
  23. Velten, S.; Neumann, C.; Bleyer, M.; Gruber-Dujardin, E.; Hanuszewska, M.; Przybylska-Gornowicz, B.; Liebert, F. Effects of 50 Percent Substitution of Soybean Meal by Alternative Proteins from Hermetia Illucens or Spirulina platensis in Meat-Type Chicken Diets with Graded Amino Acid Supply. Open J. Anim. Sci. 2018, 8, 119–136. [Google Scholar] [CrossRef] [Green Version]
  24. Park, J.H.; Lee, S.I.; Kim, I.H. Effect of Dietary Spirulina (Arthrospira) Platensis on the Growth Performance, Antioxidant Enzyme Activity, Nutrient Digestibility, Cecal Microflora, Excreta Noxious Gas Emission, and Breast Meat Quality of Broiler Chickens. Poult. Sci. 2018, 97, 2451–2459. [Google Scholar] [CrossRef]
  25. Omar, A.E.; Al-Khalaifah, H.S.; Osman, A.; Gouda, A.; Shalaby, S.I.; Roushdy, E.M.; Abdo, S.A.; Ali, S.A.; Hassan, A.M.; Amer, S.A. Modulating the Growth, Antioxidant Activity, and Immunoexpression of Proinflammatory Cytokines and Apoptotic Proteins in Broiler Chickens by Adding Dietary Spirulina platensis Phycocyanin. Antioxidants 2022, 11, 991. [Google Scholar] [CrossRef]
  26. Feshanghchi, M.; Baghban-Kanani, P.; Kashefi-Motlagh, B.; Adib, F.; Azimi-Youvalari, S.; Hosseintabar-Ghasemabad, B.; Slozhenkina, M.; Gorlov, I.; Zangeronimo, M.G.; Swelum, A.A.; et al. Milk Thistle (Silybum marianum), Marine Algae (Spirulina platensis) and Toxin Binder Powders in the Diets of Broiler Chickens Exposed to Aflatoxin-B1: Growth Performance, Humoral Immune Response and Cecal Microbiota. Agriculture 2022, 12, 805. [Google Scholar] [CrossRef]
  27. Elbaz, A.M.; Ahmed, A.M.H.; Abdel-Maqsoud, A.; Badran, A.M.M.; Abdel-Moneim, A.M.E. Potential Ameliorative Role of Spirulina platensis in Powdered or Extract Forms against Cyclic Heat Stress in Broiler Chickens. Environ. Sci. Pollut. Res. 2022, 29, 45578–45588. [Google Scholar] [CrossRef] [PubMed]
  28. Hajati, H.; Zaghari, M.; Oliveira, H.C. Arthrospira (Spirulina) Platensis Can Be Considered as a Probiotic Alternative to Reduce Heat Stress in Laying Japanese Quails. Rev. Bras. Cienc. Avic. 2020, 22, 1–8. [Google Scholar] [CrossRef]
  29. Abd El-Dayem, G.A.; Saleh, G.K.; Abd El-wahab, R.A.E.-R. Impact of Dietary Spirulina (Arthrospira) Platensison Growth Performance, Gene Expression and Antioxidant Status of Quail Challenged with Salmonella Enteritidis. Mansoura Vet. Med. J. 2021, 22, 38–47. [Google Scholar] [CrossRef]
  30. Tufarelli, V.; Baghban-Kanani, P.; Azimi-Youvalari, S.; Hosseintabar-Ghasemabad, B.; Slozhenkina, M.; Gorlov, I.; Seidavi, A.; Ayaşan, T.; Laudadio, V. Effects of Horsetail (Equisetum arvense) and Spirulina (Spirulina platensis) Dietary Supplementation on Laying Hens Productivity and Oxidative Status. Animals 2021, 11, 335. [Google Scholar] [CrossRef]
  31. Rey, A.I.; De-Cara, A.; Rebolé, A.; Arija, I. Short-Term Spirulina (Spirulina platensis) Supplementation and Laying Hen Strain Effects on Eggs’ Lipid Profile and Stability. Animals 2021, 11, 1944. [Google Scholar] [CrossRef]
  32. Zahroojian, N.; Moravej, H.; Shivazad, M. Effects of Dietary Marine Algae (Spirulina platensis) on Egg Quality and Production Performance of Laying Hens. J. Agric. Sci. Technol. 2013, 15, 1353–1360. [Google Scholar]
  33. Khan, F.; Shuvo, A.A.S.; Khan, M.J.; Islam, K.M.S. Effects of Dietary Inclusion of Spirulina platensis on Egg Yolk Pigmentation. Livest. Res. Rural. Dev. 2021, 33, 101. [Google Scholar]
  34. Holman, B.W.B.; Malau-Aduli, A.E.O. Spirulina as a Livestock Supplement and Animal Feed. J. Anim. Physiol. Anim. Nutr. 2013, 97, 615–623. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. El-Ghany, W.A.A. Microalgae in Poultry Field: A Comprehensive Perspectives. Adv Anim Vet Sci. 2020, 8, 888–897. [Google Scholar] [CrossRef]
  36. NRC Nutrient Requirements of Poultry: Ninth Revised Edition; The National Academies Press: Washington, DC, USA, 1994; ISBN 978-0-309-04892-7.
  37. Association of Official Analysis Chemists International. Official Methods of Analysis of AOAC International, 18th ed.; AOAC: Washington, DC, USA, 2005; ISBN 0935584544. [Google Scholar]
  38. Drabkin, D.L.; Austin, J.H. Spectrophotometric Studies: I. Spectrophotometric Constants for Common Hemoglobin Derivatives in Human, Dog, and Rabbit Blood. J. Biol. Chem. 1932, 98, 719–733. [Google Scholar] [CrossRef]
  39. Li, F.; Xu, L.M.; Shan, A.S.; Hu, J.W.; Zhang, Y.Y.; Li, Y.H. Effect of Daily Feed Intake in Laying Period on Laying Performance, Egg Quality and Egg Composition of Genetically Fat and Lean Lines of Chickens. Br. Poult. Sci. 2011, 52, 163–168. [Google Scholar] [CrossRef]
  40. Selim, S.; Hussein, E.; Abou-Elkhair, R. Effect of Spirulina platensis as a Feed Additive on Laying Performance, Egg Quality and Hepatoprotective Activity of Laying Hens. Eur. Poult. Sci. 2018, 82, 1–13. [Google Scholar]
  41. Çalişlar, S. The Important of Beta Carotene on Poultry Nutrition. Selcuk. J. Agric. Food Sci. 2019, 33, 252–259. [Google Scholar] [CrossRef]
  42. Mariey, Y.A.; Samak, H.R.; Ibrahem, M.A. Effect of Using Spirulina platensis Algae as Afeed Additive for Poultry Diets: 1-Productive and Reproductive Performances of Local Laying Hens. Egypt. Poult. Sci. J. 2012, 32, 201–215. [Google Scholar]
  43. Seyidoglu, N.; Belenli, D. A “Super Food” for Alternative Nutrients: Spirulina platensis. Online J. Sci. Technol. 2019, 9, 1–6. [Google Scholar]
  44. Mitchell, W.K.; Wilkinson, D.J.; Phillips, B.E.; Lund, J.N.; Smith, K.; Atherton, P.J. Human Skeletal Muscle Protein Metabolism Responses to Amino Acid Nutrition. Adv. Nutr. 2016, 7, 828S–838S. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Ariana, M.; Samie, A.; Edriss, M.A.; Jahanian, R. Effects of Powder and Extract Form of Green Tea and Marigold, and α-Tocopheryl Acetate on Performance, Egg Quality and Egg Yolk Cholesterol Levels of Laying Hens in Late Phase of Production. J. Med. Plants Res. 2011, 5, 2710–2716. [Google Scholar]
  46. Ekantari, N.; Harmayani, E.; Pranoto, Y.; Marsono, Y. Calcium of Spirulina platensis Has Higher Bioavailability than Those of Calcium Carbonate and High-Calcium Milk in Sprague Dawley Rats Fed with Vitamin D-Deficient Diet. Pak. J. Nutr. 2017, 16, 179–186. [Google Scholar] [CrossRef] [Green Version]
  47. An, S.H.; Kim, D.W.; An, B.K. Effects of Dietary Calcium Levels on Productive Performance, Eggshell Quality and Overall Calcium Status in Aged Laying Hens. Asian-Australas J. Anim. Sci. 2016, 29, 1477. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  48. Bhattacharyya, S.; Mehta, P. The Hepatoprotective Potential of Spirulina and Vitamin C Supplemention in Cisplatin Toxicity. Food Funct 2012, 3, 164–169. [Google Scholar] [CrossRef] [PubMed]
  49. El-Sheekh, M.M.; Hamad, S.M.; Gomaa, M. Protective Effects of Spirulina on the Liver Function and Hyperlipidemia of Rats and Human. Braz. Arch. Biol. Technol. 2014, 57, 77–86. [Google Scholar] [CrossRef] [Green Version]
  50. Giannini, E.G.; Testa, R.; Savarino, V. Liver Enzyme Alteration: A Guide for Clinicians. Can. Med. Assoc. J. 2005, 172, 367. [Google Scholar] [CrossRef] [Green Version]
  51. Yadav, D.; Prakash Bhartiya, J.; Kumar Verma, S.; Kumar Nandkeoliar, M. Evaluation of Blood Urea, Creatinine and Uric Acid as Markers of Kidney Functions in Hypertensive Patients: A Prospective Study. Indian J. Basic Appl. Med. Res. 2014, 3, 682. [Google Scholar]
  52. Charlton, M.R. Protein Metabolism and Liver Disease. Baillieres Clin. Endocrinol. Metab. 1996, 10, 617–635. [Google Scholar] [CrossRef]
  53. Chiu, H.W.; Hua, K.F. Hepatoprotective Effect of Wheat-Based Solid-State Fermented Antrodia Cinnamomea in Carbon Tetrachloride-Induced Liver Injury in Rat. PLoS ONE 2016, 11, 1–17. [Google Scholar] [CrossRef] [Green Version]
  54. Selmi, C.; Leung, P.S.C.; Fischer, L.; German, B.; Yang, C.Y.; Kenny, T.P.; Cysewski, G.R.; Gershwin, M.E. The Effects of Spirulina on Anemia and Immune Function in Senior Citizens. Cell. Mol. Immunol. 2011, 8, 248. [Google Scholar] [CrossRef] [PubMed]
  55. Mani, U.; Sadliwala, A.; Iyer, U.; Parikh, P. The Effect of Spirulina Supplementation on Blood Haemoglobin Levels of Anaemic Adult Girls. J. Food Sci. Technol. 2000, 37, 642–644. [Google Scholar]
  56. Promya, J.; Chitmanat, C. The Effects of Spirulina platensis and Cladophora Algae on the Growth Performance, Meat Quality and Immunity Stimulating Capacity of the African Sharptooth Catfish (Clarias gariepinus). Int. J. Agric. Biol. 2011, 13, 77–82. [Google Scholar]
  57. Yeganeh, S.; Teimouri, M.; Amirkolaie, A.K. Dietary Effects of Spirulina platensis on Hematological and Serum Biochemical Parameters of Rainbow Trout (Oncorhynchus Mykiss). Res. Vet. Sci. 2015, 101, 84–88. [Google Scholar] [CrossRef]
  58. Seghiri, R.; Kharbach, M.; Essamri, A. Functional Composition, Nutritional Properties, and Biological Activities of Moroccan Spirulina Microalga. J. Food Qual. 2019, 2019, 3707219. [Google Scholar] [CrossRef] [Green Version]
  59. Wei, C.; Zhou, J.; Huang, X.; Li, M. Effects of Psychological Stress on Serum Iron and Erythropoiesis. Int. J. Hematol. 2008, 88, 52–56. [Google Scholar] [CrossRef]
  60. Hasan, R.; Sarker, S.; Islam, M.S.; Sikder, M.H.; Rahman, M.M. Efficacy Of Spirulina On Production Indices Of Advanced Age Layer Chicken. Ann. Bangladesh Agric. 2018, 22, 67–76. [Google Scholar]
  61. Elmalawany, A.M.; Salem, T.A.; Mohamed, A.H.; Osman, G.Y. Effect of Blue Green Algae on Some Biochemical and Hematological Markers in Mice. Int. J. Adv. Res. 2014, 2, 568–574. [Google Scholar]
  62. Dvm, S.E.; Olfati, A.; Emami, S. Effects of Dietary Supplementing of Spirulina platensis and Chlorella Vulgaris Microalgae on Hematologic Parameters in Streptozotocin-Induced Diabetic Rats. Iran. J. Pediatr. Hematol. Oncol. 2017, 7, 163–170. [Google Scholar]
  63. Kelkar, G.; Subhadra, K.; Chengappa, R.K. Effect of Antioxidant Supplementation on Hematological Parameters, Oxidative Stress and Performance of Indian Athletes. J. Hum. Ecol. 2008, 24, 209–213. [Google Scholar] [CrossRef]
Table
Table 1. The chemical analysis of soybean meal (SBM) and Spirulina platensisis (SP).
Table 1. The chemical analysis of soybean meal (SBM) and Spirulina platensisis (SP).
ItemContents per 100 g SBM *Contents per 100 g SP
Chemical composition
Dry matter90.0 g94.4 g
Crude protein44.0 g56.4 g
Total lipids0.5 g7.2 g
Carbohydrate-14.2 g
Crude fiber7.0 g0.02 g
Total ash-7.5 g
Gross energy-43.6 MJ
Minerals *
Calcium250.0 mg436.3 mg
Phosphorus200.0 mg124.5 mg
Sodium40.0 mg220.1 mg
Potassium1970.0 mg167.8 mg
Iron-11.5 mg
Zinc-2.4 mg
Essential amino acids *
Isoleucine2.5 g6.6 g
Leucine-8.3 g
Valine2.4 g6.6 g
Lysine2.7 g4.8 g
Tryptophan0.6 g1.1 g
Phenylalanine-4.7 g
Methionine0.7 g2.4 g
Threonine1.7 g5.3 g
Nonessential amino acids *
Cysteine0.7 g1.0 g
Tyrosine-4.5 g
Alanine-8.5 g
Arginine3.4 g7.4 g
Aspartic acid-11.5 g
Glutamic acid-10.2 g
Glycine-5.5 g
Histidine-2.5 g
Proline-4.3 g
Serine-4.9 g
* According to the commercial supplier (not analyzed).
Table
Table 2. Composition of the experimental diets 1.
Table 2. Composition of the experimental diets 1.
Ingredients (g/kg as Fed)Control3% SP6% SP9% SP12% SP
Spirulina0.030.060.090.0120.0
Soybean meal (44% CP)275.0236.4197.7159.1120.5
Yellow corn566.5575.1583.8592.4601.0
Wheat bran10.010.010.010.010.0
Soybean oil30.030.030.030.030.0
Bone meal30.030.030.030.030.0
Limestone80.080.080.080.080.0
Salt (NaCl)4.04.04.04.04.0
Premix 23.03.03.03.03.0
DL-Methionine1.51.51.51.51.5
Calculated nutrients
Metabolizable energy (MJ/kg)12.612.612.612.612.6
Calcium (g/kg)40.240.240.240.240.2
Available phosphorus (g/kg)5.25.25.25.25.2
Determined nutrients
Crude protein (g/kg)167.5170.0170.0174.5174.7
Crude fat (g/kg)66.064.563.862.161.5
Crude fiber (g/kg)47.046.546.545.845.5
1 Experimental diets: supplemented with 3% spirulina (3% SP), 6% spirulina (6% SP), 9% spirulina (9% SP), 12% spirulina (12% SP), or without spirulina (Control). 2 Premix (content per kg of the experimental diet): 8000 IU vitamin A; 1500 IU vitamin D; 4 mg riboflavin; 10 µg cobalamin; 15 mg vitamin E; 2 mg vitamin K; 500 mg choline; 25 mg niacin; 60 mg manganese; 50 mg zinc.
Table
Table 3. Effect of dietary Spirulina platensis on the productive performance of laying hens.
Table 3. Effect of dietary Spirulina platensis on the productive performance of laying hens.
Parameters 1Dietary Spirulina platensis (SP) GroupsSEMp-Value
Control3% SP6% SP9% SP12% SPTreatmentLinearQuadratic
IBW, g1550.01549.71549.81550.81550.12.260.9980.8630.981
FBW, g1597.4 b1597.0 b1599.0 ab1600.8 ab1604.7 a2.420.1530.0160.354
Hen-day EP, %89.2 c88.9 c91.4 b92.9 a91.8 b0.19<0.001<0.001<0.001
EW, g61.2 d61.2 d62.1 b62.9 a61.7 c0.09<0.001<0.001<0.001
FI, g/d99.5 c99.5 c100.9 b101.4 b104.4 a0.19<0.001<0.001<0.001
FCR1.82 b1.83 ab1.78 c1.74 d1.84 a0.006<0.0010.011<0.001
1 Parameters: IBW, initial body weight at the 40th week of age; FBW, final body weight at the 50th week of age; EP, egg production; EW, egg weight; FI, feed intake; FCR, feed conversion ratio. Data are presented as means for five replicates of 10 hens each (n = 50 per group). Means within the same row with different superscripts are significantly different (p < 0.05). SEM, pooled standard error of means.
Table
Table 4. Effect of dietary Spirulina platensis on the egg quality parameters of laying hens.
Table 4. Effect of dietary Spirulina platensis on the egg quality parameters of laying hens.
Parameters 1Dietary Spirulina platensis (SP) GroupsSEMp-Value
Control3% SP6% SP9% SP12% SPTreatmentLinearQuadratic
AI, %9.87 b10.47 ab10.93 a10.70 a10.67 a0.2460.0340.0200.037
HU81.92 b85.44 a87.80 a87.71 a85.70 a0.839<0.001<0.001<0.001
YI, %40.18 b40.95 ab41.19 ab42.60 a41.83 ab0.7020.1530.0280.464
YC7.90 e8.50 d9.87 c11.20 b12.67 a0.124<0.001<0.001<0.001
SW, %8.71 b8.89 ab9.02 ab9.18 a8.80 ab0.1410.1520.2880.042
ST, mm0.32c0.33 c0.37 b0.42 a0.42 a0.008<0.001<0.0010.439
SS, kg/cm23.84 c3.95 c4.43 b4.72 a4.49 b0.070<0.001<0.0010.001
1 Parameters: AI, albumen index; HU, Haugh units; YI, yolk index; YC, yolk color; SW, shell ratio; ST, shell thickness; SS, shell strength. Data are presented as means for five replicates of six eggs each (n = 30 per group). Means within the same row with different superscripts are significantly different (p < 0.05). SEM, pooled standard error of means.
Table
Table 5. Effect of dietary Spirulina platensis on the blood biochemicals of laying hens.
Table 5. Effect of dietary Spirulina platensis on the blood biochemicals of laying hens.
Parameters 1Dietary Spirulina platensis (SP) GroupsSEMp-Value
Control3% SP6% SP9% SP12% SPTreatmentLinearQuadratic
TP, g/dL4.62 e5.27 d6.16 c7.68 a6.81 b0.138<0.001<0.001<0.001
ALB, g/dL2.97 c3.42 b3.52 b4.32 a4.09 a0.106<0.001<0.0010.096
GLB, g/dL1.65 c1.85 c2.64 b3.36 a2.72 b0.122<0.001<0.001<0.001
CA, mg/dL25.58 d28.59 c31.21 b32.56 a31.76 ab0.384<0.001<0.001<0.001
PP, mg/dL6.40 b6.35 b6.50 b7.08 a6.90 a0.084<0.001<0.0010.608
AST, U/mL63.70 a62.15 a58.52 b57.19 b57.55 b0.755<0.001<0.0010.035
ALT, U/mL36.86 a32.68 b29.57 c22.17 e25.31 d0.660<0.001<0.001<0.001
CRT, mg/dL0.28 a0.27 ab0.26 bc0.25 d0.26 cd0.005<0.001<0.0010.037
UA, mg/dL5.71 a5.43 b5.24 c4.94 d5.13 cd0.068<0.001<0.0010.002
1 Parameters: TP, total protein; ALB, albumin; GLB, globulin; CA, calcium; PP, phosphorus; AST, aspartate transferase; ALT, alanine transferase; CRT, creatinine; UA, uric acid. Data are presented as means for five replicates of two hens each (n = 10 per group). Means within the same row with different superscripts are significantly different (p < 0.05). SEM, pooled standard error of means.
Table
Table 6. Effect of dietary Spirulina platensis on the blood hematology of laying hens.
Table 6. Effect of dietary Spirulina platensis on the blood hematology of laying hens.
Parameters 1Dietary Spirulina platensis (SP) GroupsSEMp-Value
Control3% SP6% SP9% SP12% SPTreatmentLinearQuadratic
WBC, 103/µL36.18 e42.73 d51.60 c66.78 a58.08 b1.375<0.001<0.001<0.001
RBC, 106/µL2.24 c2.25 c2.29 bc2.39 a2.34 ab0.022<0.001<0.0010.454
HB, g/dL10.85 b10.68 b12.90 a13.36 a11.61 b0.329<0.001<0.001<0.001
HT, %30.58 c30.49 c31.51 bc32.86 a31.76 b0.380<0.001<0.0010.240
MCV, fL136.36135.89137.59137.63136.162.3280.9730.8550.677
MCH, pg/cell48.38 b47.60 b56.30 a55.97 a49.80 b1.548<0.0010.0270.001
MCHC, g/dL35.49 b35.11 b41.02 a40.64 a36.61 b1.109<0.0010.0320.002
1 Parameters: WBC, white blood cells; RBC, red blood cells; HB, hemoglobin; HT, hematocrit; MCV, mean corpuscular volume; MCH, mean corpuscular hemoglobin; MCHC, mean corpuscular hemoglobin concentration. Data are presented as means for five replicates of two hens each (n = 10 per group). Means within the same row with different superscripts are significantly different (p < 0.05). SEM, pooled standard error of means.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Abbas, A.O.; Alaqil, A.A.; Mehaisen, G.M.K.; Kamel, N.N. Effect of Dietary Blue-Green Microalgae Inclusion as a Replacement to Soybean Meal on Laying Hens’ Performance, Egg Quality, Plasma Metabolites, and Hematology. Animals 2022, 12, 2816. https://doi.org/10.3390/ani12202816

AMA Style

Abbas AO, Alaqil AA, Mehaisen GMK, Kamel NN. Effect of Dietary Blue-Green Microalgae Inclusion as a Replacement to Soybean Meal on Laying Hens’ Performance, Egg Quality, Plasma Metabolites, and Hematology. Animals. 2022; 12(20):2816. https://doi.org/10.3390/ani12202816

Chicago/Turabian Style

Abbas, Ahmed O., Abdulaziz A. Alaqil, Gamal M. K. Mehaisen, and Nancy N. Kamel. 2022. "Effect of Dietary Blue-Green Microalgae Inclusion as a Replacement to Soybean Meal on Laying Hens’ Performance, Egg Quality, Plasma Metabolites, and Hematology" Animals 12, no. 20: 2816. https://doi.org/10.3390/ani12202816

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop