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BY 4.0 license Open Access Published by De Gruyter Open Access February 21, 2023

The effects of in ovo injected with sodium borate on hatching performance and small intestine morphology in broiler chicks

  • Mehmet Fatih Bozkurt and Günnur Peşmen EMAIL logo
From the journal Open Chemistry

Abstract

The objective of this study was to investigate the effects of in ovo injection of sodium borate on hatching power, chick weight, chick length in fertile broiler eggs. A total of 256 fertile broiler eggs were incubated in the study. On Day 18 of incubation, two groups were injected with 0.1 mL of 0.5 mg and 1 mg of sodium borate dissolved in saline, and two groups were used as sham control (injected with 0.1 mL of saline) and uninjected control. Hatching power was apparently increased (P ≤ 0.05) by in ovo injection of sodium borate (0.5 mg) rather than control groups and sodium borate (1 mg) group. While there was no significant difference between the groups in terms of chick weights, a significant difference was found between group B and other experimental groups in terms of chick length (P < 0.05). In ovo sodium borate injection (0.5 mg) had a positive effect on villus length, crypt width, villus absorption surface (HASA), and the number of proliferating cell nuclear antigen positive crypt cells.

1 Introduction

The success of hatcheries directly affects the development of the broiler industry due to the increasing demand of commercial enterprises for quality chicks. For this reason, the production of healthy chicks in ideal environmentally controlled conditions is a necessity. The global demand for poultry meat and eggs will increase by 121 and 65%, respectively, in 2050, and the human population is projected to be 9.6 billion, requiring the development of the poultry industry and increased productivity. According to the results of in ovo feeding (IOF), productivity can be increased in poultry by continuous improvement of the practice [1].

IOF method in poultry is one of the research topics that have been emphasized in recent years. It is a method based on the injection of liquid solutions with carbohydrates, amino acids, and various protein contents into the sacs of poultry embryos during the incubation period [2]. IOF applications in incubation are used for many purposes. The first among these is to improve hatching [3], vaccinate chicks, increase digestive capacity and intestinal development [4], skeletal system [5], immune system [6], improve body weight and feed efficiency [7], reducing early embryo mortality [8], increasing muscle growth [9], manipulating sex in the early period [10], and also reducing difficulties associated with infections and oxidative stress in poultry production. It has the potential to minimize the use of synthetic antibiotic growth promoters [11]. The incubation period in chickens is 21 days and this period constitutes half of the life of 2 kg broiler chickens. Therefore, anything that promotes growth and development during the incubation period affects the post-hatching performance and health of the birds [12]. Very rapid morphological, biochemical, and cellular changes occur in the digestive system in the first 72 h after hatching. The healthy and strong start of life of the chicks significantly affects their performance and survival in the future. For this, new approaches have emerged in the direction of nutritional supplementation during the incubation period as well as early feeding. Such applications can be done within 72 h after hatching, or by injecting various nutrients and immune substances directly into the egg in the last period of the incubation [13].

Swek et al. [14] reported that an important determinant of growth performance and intestinal function in poultry is the morphology of the intestinal mucosa. The intestine is the region where nutrients are first absorbed, so it is sensitive to changes in nutrition [15]. In addition, the sooner it reaches its maximum functional capacity, the faster it will increase its ability and efficiency to use nutrients [8]. As the embryo consumes amniotic fluids late in incubation, in ovo delivery of nutrients can promote early development of the digestive system [3].

Boron is a trace mineral found in highest amount in fruits, vegetables, nuts, and legumes. At the beginning of the eighties, the opinions about boron in human and animal nutrition started to change and it has been revealed that boron can become a necessary micro-element for human and animal nutrition with the studies carried out in recent years [16].

Although boron has many beneficial functions in biological, metabolic, and physiological processes in plants and animals, it has a vital role in protecting animal health and preventing nutritional disorders. The addition of boron to the diet in animal nutrition has positive effects on bone density, wound healing, and embryonic development [17,18]. Various studies have shown that boron increases the growth in chicks with vitamin D deficiency, the absorption and balance of calcium and phosphorus are improved in rats when boron is included in the diet [18]. It indirectly affects calcium, phosphorus, and magnesium metabolism by manipulating the hormone or enzyme systems of animals. Abdelnoura et al. [17] found that boron supplementation significantly increased femur calcium, phosphorus, and magnesium levels in boron-deficient chicks [19]. Boron deficiency has also been associated with low immune function and a high incidence of osteoporosis, which increases the risk of death [18,17].

King et al. [20] reported that injecting 150 µL of boron into the air cavity of fertile turkey eggs on Day 15 of hatching increased embryonic weight, tibia length, and bone ash. Tako et al. [3] and Beiglou [13] reported that the IOF method has positive effects on the digestive capacity and intestinal development of chicks.

Givisiez et al. [21] stated that in ovo application of different nutrients to the embryo stimulates the early development of the digestive system and muscle tissues, increases the resistance against diseases in chicks, and supports the preservation of glycogen stores and vitality. In studies on the effects of IOF on the morphological and functional development of the intestinal mucosa in chickens, turkeys, and quails, it was observed that it positively affected the intestinal development after hatching [21]. Since the intestine is the region where nutrients are first absorbed, it is sensitive to changes in nutrition [22] and the sooner it reaches its maximum functional capacity, the faster it will increase the ability and efficiency of using nutrients, and the resistance against metabolic and infectious diseases [8]. Berrocoso et al. [23] found that in ovo injection of raffinose increased villus height and villus height:crypt depth ratio. It has the potential to improve ileum mucosa morphology and immunity in the small intestine. Nowaczewski et al. [24] reported that in ovo given nutrients improved the growth performance, digestive system, and increased the body weight and nutritional status. Dai et al. [25] reported that in ovo arginine injection linearly increased duodenal weight in 3-day-old chicks and jejunal weight in 14-day-old chicks. Elwan et al. [26] reported that in ovo injection of methionine and cystine improved the histomorphometric parameters of jejunum in chicks. Mohammadrezaei et al. [22] reported that in ovo administration of 40 mg methionine increased the height and width of the villi and, consequently, the villi area.

This study was carried out to examine the effect of sodium borate on hatchability and small intestine morphology using fertile eggs.

2 Materials and methods

In the study, fertile eggs from broiler chickens of Ross 308 strain from a commercial farm were used. Eggs were incubated at 37.5°C at 56% relative humidity in a commercial hatchery. On the tenth day, the eggs were checked for fertility and the eggs without embryo development were removed from the machine. Then, 256 fertile eggs were designed as in Table 1. The injection site of the eggs was cleaned with 70% ethanol. A hole was made on the blunt side of the fertile eggs with the help of a micro-motor. The prepared solutions were injected into the air sac with the help of a syringe on the 18th day of incubation. After the injection process was completed, the injection site was closed with paraffin tape. Similarly, in the negative control group, 0.1 mL/egg saline was injected into the eggs. The control group was kept outside the incubator for the same time as the other groups, without injection. Experimental groups were designed as in Table 1.

Table 1

Experimental groups

Groups Applications n
Control (K) No solution was applied 64
Negative control (NK) 0.1 mL saline/egg 64
Sodium borate (0.5 mg) (B) Including 0.5 mg sodium borate in saline: 0.1 mL/egg 64
Sodium borate (1 mg) (B1) Including 1 mg sodium borate in saline: 0.1 mL/egg 64

Hatching power (%) = number of live chicks/number of fertile eggs × 100.

Chick weight (g) was determined as grams with a digital balance with a sensitivity of 0.01 g.

Chick length (cm): the length from the tip of the beak to the tip of the finger was measured with the help of a ruler [27,28].

After hatching, chick weights and chick lengths were taken and recorded.

After necropsy of the chicks, a 1 cm long jejunum segment was removed. Each jejunum was cleaned with 5% formaldehyde solution gently. Samples taken in buffered neutral formalin solution for tissue fixation were fixed for 48 h. The tissues were processed and embedded in paraffin. Sections were taken using a microtome on normal and adhesive slides with a thickness of 4 µm. Sections taken from normal slides were stained with hematoxylin–eosin (HE) technique and examined under a light microscope (Zeiss Axio Lab.A1 Microscope-AxioCam ICc 5 Camera). The obtained results were evaluated using Image J analysis software (http://imagej.nih.gov/ij). The height of the villi was measured from the end of the villi to the junction of the villus–crypt, crypt depth was measured from the bottom up to the transition zone between the crypt and the villi, and finally the width of the villi was measured. Small intestinal absorptive surface was determined with the method described by Kisielinski et al. [29].

Samples taken on adhesive slides from the intestinal tissues were stained immunohistochemically by avidin–biotin–peroxidase (ABC) method for Proliferating Cell Nuclear Antigen (PCNA) staining. Slides, which were taken into phosphate buffered (pH 7.2) solution after deparaffinization and dehydration stages, were kept in 3% H2O2 solution for 10 min to remove endogenous peroxidase activity. Microwave boiling in 0.01 M pH 6.0 citrate buffer for 20 min to reveal antigen. Sections delimited with a hydrophobic pen were dripped with serum for endogenous serum blocking and incubated at 37°C for 15 min. Anti-PCNA (ab18197, Abcam, 1/400 dilution) primary antibody was instilled into the tissues. It was washed by incubating for 2 h in a 37°C humidity chamber. Then, the application of the ABC (TA-125-UDX, UltraVision Polyvalent HRP Kit, LabVision/Thermo Scientific, USA) kit was started. Immune bindings were colored with a red-brown colored AEC (TA-060-HA, AEC Substrate System, LabVision/Thermo Scientific, USA) peroxidase substrate. When the reaction took place, the slides were placed in distilled water and the reaction was terminated. The floor was stained with Mayer’s hematoxylin. Sections were covered with a coverslip using aqueous adhesive and examined under a light microscope. One hundred cells were counted from the base of five villi from each sample. Positive cells were scored as a percentage.

Histological absorbent surface amplification (HASA) was calculated according to the formula below [29]:

HASA = ( Villus width⁎ Villus length ) + Villus width/2 + Crypt width/2) 2 ( Villus width/2 ) 2 /Villus width/2 + Crypt width/2) 2

Research data were analyzed with SPSS 21.0 for windows package program. ANOVA was used to compare the groups in terms of chick weight and chick length, and chi-square test was used for hatching power. Tukey test was used to determine the difference between the groups. The significance level was taken as 0.05 [30].

3 Results and discussion

The comparison of the groups according to the chick weights is given in Table 2. According to the test results, it was determined that the chick weights did not show a significant difference according to the groups (P < 0.05). The mean values of the K, NK, B, and B1 groups were determined as 46.39, 47.09, 46.35, and 46.28 g, respectively (Table 2).

Table 2

Comparison of groups in terms of chick weight

Groups n Min. Max. Mean SD P-value
K 53 38.86 56.44 46.39 3.16 0.348
NK 51 37.92 53.40 47.09 3.50
B 58 38.68 52.39 46.35 2.97
B1 46 38.82 54.32 46.28 3.23

Table 3 shows the effect of sodium borate on chick length. According to Table 3, there was a significant difference between the groups in terms of chick length (P < 0.05). The mean values of the K, NK, B, and B1 groups were determined as 16.94, 17.20, 17.57, and 17.22 cm, respectively. Results shows that the B group has a highest chick length, while K group has the lowest chick lengths (Table 3).

Table 3

Comparison of groups in terms of chick length

Groups n Min. Max. Mean SD P-value
K 53 15.30 18.30 16.94 0.61 0.028
NK 51 16.00 18.00 17.20 0.50
B 58 15.00 19.50 17.57 0.78
B1 46 15.30 18.30 17.22 0.68

It was determined that there was a significant difference between the groups in terms of hatchability (P < 0.05). The mean values of the F, NK, B, and B1 groups were determined as 82.8, 79.7, 90.6, and 71.9%, respectively. Accordingly, the highest hatchability was determined in group B, and the lowest in group B1. Sodium borate (0.5 mg) application had a positive effect on hatchability.

Sodium borate when administered as in ovo into the egg at a level of 0.5 mg had a positive effect on hatching power and chick length; while administered at 1 mg level the hatching power and chick weight had a negative effect.

As a result, it can be said that IOF of sodium borate (0.5 mg) into the hatching broiler eggs causes the hatching power and chick length to increase without affecting the chick weight parameters. More studies are needed for definitive results. The highest hatchability and chick length were obtained from the B treatment, while the lowest hatchability and chick weight were obtained from the B1 treatment.

The effects of in ovo injection of sodium borate on the jejunum are compared in Table 4. Significant differences in the histological structure of the jejunum were observed as an effect of in ovo sodium borate injection. According to these findings, it was determined that there was a significant difference between the groups in terms of villus length, villus width, and villus absorption surface (P < 0.05). There was no significant difference between the groups in terms of crypt depth (P = 0.131). Villus length in K, B (0.5 mg), and B1(1 mg) groups, respectively, was determined as 941.43, 1050.60, and 1004.20 µm. Accordingly, the highest villus length was determined in the B group, and the lowest in the K group. Villus width in K, B, and B1 groups, respectively, was determined as 245.26, 162.00, and 206.11 µm. Villus absorption surface (HASA) in K, B, and B1 groups, respectively, was determined as 11.91, 15.85, 13.42. Villus absorption surface was the highest in the B group and the lowest in the K group. In histological evaluation of jejunum sections, the sodium borate group injected at 0.5 mg level showed greater villus length and absorptive surface (HASA) compared to the other groups. The number of PCNA positive crypt cells was found to be 83.74, 84.54, and 85.89% in the K, B, and B1 groups, respectively. These results revealed that sodium borate (0.5 mg) application had a positive effect on villus length, crypt depth, villus resorption surface, and the number of PCNA positive crypt cells (Figure 1).

Table 4

Effect of sodium borate injected in ovo on the intestinal morphology (jejunum) of chickens at 14 days of age

Items Treatments P-value
K Mean ± SE B Mean ± SE B1 Mean ± SE
Villus length 941.43 ± 18.29 1050.60 ± 24.44 1004.20 ± 31.82 0.015
Villus width 245.26 ± 11.83 162.00 ± 8.39 206.11 ± 12.38 0.000
Crypt depth 42.04 ± 3.16 52.00 ± 5.33 50.52 ± 3.44 0.131
HASA 11.91 ± 0.52 15.85 ± 1.05 13.42 ± 0.71 0.002
Figure 1 
               Microscopic view of the jejunal mucosa in the experimental groups. Longer villi are seen in Bor 0.5 group (B) and Bor 1 group (B1) compared to the control group (K). HE. Bar = actual length.
Figure 1

Microscopic view of the jejunal mucosa in the experimental groups. Longer villi are seen in Bor 0.5 group (B) and Bor 1 group (B1) compared to the control group (K). HE. Bar = actual length.

In this study, it is seen that the optimum amount of sodium borate to be injected into the egg air sac is 0.5 mg to achieve optimum morphology changes, since the increase in villus size leads to an increase in the absorption area (Figure 2).

Figure 2 
               Microscopic image of PCNA immunohistochemical staining of group jejunum. In Bor 0.5 (B) and Bor 1 (B1) groups, more intense PCNA positivity (nuclear red color indicates positivity) is observed compared to the control group (K). ABC-peroxidase technique, AEC chromogen, Mayer’s hematoxylin. Bar = actual length.
Figure 2

Microscopic image of PCNA immunohistochemical staining of group jejunum. In Bor 0.5 (B) and Bor 1 (B1) groups, more intense PCNA positivity (nuclear red color indicates positivity) is observed compared to the control group (K). ABC-peroxidase technique, AEC chromogen, Mayer’s hematoxylin. Bar = actual length.

The jejunum, the longest part of the small intestine, is responsible for digesting and absorbing more than 80% of ingested nutrients. The length of the villi and the width of the crypts are important indicators in the evaluation of the morphological structure of the small intestine. Moreover, a change in the ratio of the length of the intestinal villi to the width of the crypts can directly affect the morphological structure of the small intestine [31,32].

In this study, in ovo injection of sodium borate (0.5 mg) increased the villus development. The results obtained from this study are in agreement with the results of other studies. Ohta et al. [32] found that nutrient injection into the egg is an alternative method to increase the weight of the newly hatched chicks, while Şeremet [33] stated that long chicks may have better developed organs, and that the length of the digestive tract increases in parallel with the length of the chick and the intestinal tract in long chicks [34,35].

Moosanezhad et al. [35] obtained the highest chick size at 18.5 days of incubation and the highest hatchability with in ovo application at 17.5 and 18.5 days of incubation. In the same study, they recommended in ovo application for high output power at 17.5 and 18.5 days of incubation. Kurtoglu et al. [36] in their study on mineral metabolism of boron, determined that boron plays an important biological role on mineral metabolism in animals. In another study, it was found that boron supplementation increased bone ash and also increased the weight [37]. Bhasker et al. [38] found an improvement in weight gain with 40 ppm boron supplementation in Ca-deficient rats. Bai and Hunt [39] reported that boron deficiency in the diet may reduce bone development and cause bone anomalies in chickens with vitamin D deficiency, while Uysal et al. [40] and Hakki et al. [41] reported that boron has an important role in the development, mineralization, and proliferation of bones. In this study, chick height increased as a result of in ovo 0.5 mg boron application. This may be due to the effect of boron on the bones.

Molenaar et al. [42] concluded in their study that there is a positive relationship between chick height and chick weight and the development of important organs such as heart, liver, and spleen. Therefore, chick length can be considered an important indicator of chick quality for hatcheries and broiler breeder [43]. The length of the digestive system increases in parallel with the length of the chick, indicating that the intestinal system is better developed in these long chicks [42,43]. Chick length is a measure used to evaluate chick quality. Studies have suggested the use of chick length in the assessment of chick quality [45]. Based on the literature, hatching weight and length of the hatched chick are the key factors in estimating marketing weight in chickens [44,45].

King et al. [18], in their study, reported that simultaneous in ovo administration of boron and vitamin D (0.5 mg and 0.3 µg, respectively) on the eighth day of incubation increased the hatching power of embryos with vitamin D deficiency, and boron given at 0.5 mg alone reduced the hatching power. In the current study, boron given at the level of 0.5 mg increased the hatching power. This difference may be due to the difference in injection time. Embryonic deaths are higher in IOF applied in the early period. When the effects of IOF on hatching power were examined in various studies, very different results (positive or negative) were observed. Various studies show that the best time for IOF is between the 17th and 18th days (last 3 days period) [35,46]. Abdelnoura et al. [17] suggested that boron deficiency in animals impairs early embryonic development. King et al. [20] reported that the application of in ovo boron (0.5 mg) had no effect on the chick weight. In another study the addition of 100 mg/L boron to drinking water significantly increased the villus length and crypt depth of Gushi chicken jejunum [47]. This result is consistent with our study.

From the results of various studies, it is understood that the response of chicks to IOF may vary depending on factors such as injected nutrients, mechanism of action of nutrients, dose of nutrients, injection time, injection site, breeder genetics and age, egg size, and hatching conditions. According to classical feeding, it has a positive effect on the development of the animal’s digestive system. Although this technique, which is a biotechnological development, is very new, it is seen that positive results have been obtained and it can be an effective way to prevent many diseases in the future, as well as to enable earlier and healthier growth [12,21,33,46]. Mohammadrezaei et al. [22] reported that administration of 40 mg methionine to the yolk sac on the fourth day of incubation provides an increase in the overall volume of the jejunum, and an increase in the size of the villus leads to an increase in the resorption area.

An appropriate amount of boron supplementation can improve the morphology and structure of the jejunum, as well as increase the villus length and crypt depth. This may be because boron has a significant effect on oxidoreductase activity in aerobic respiration of cells, thereby increasing the aerobic respiration of cells and promoting the production of more adenosine diphosphate to provide sufficient energy for differentiation and proliferation of jejunal epithelial cells [48].

4 Conclusion

According to many studies, although IOF has positive effects on chick weight and hatching characteristics, the practice has not been sufficiently widespread and commercialized in the field. More precise results can be obtained, and the expected benefits from the application can be increased, by conducting more in-depth research on the in ovo application time, the application site, and the dose to be used. As a result, it can be said that IOF of sodium borate (0.5 mg) into the hatching broiler eggs causes the hatching power and chick length to increase without affecting the chick weight. In addition, this study revealed that sodium borate (0.5 mg) application had a positive effect on villus length, crypt depth, villus absorption surface, and the number of PCNA positive crypt cells.

More research is needed on the effect of sodium borate injected into the egg in embryonic development. Studies on the effects of boron on animals are scarce. Therefore, this study can open a window for future studies on boron. The appropriate dose of boron has not yet been determined. Effects of sodium borate application and the application dose may be clarified with new studies on the injection time and injection site. Since high doses of boron will cause cell damage and toxicity in humans and different animal species, it is important to increase the research on the usage levels.

Acknowledgements

We thank the PAK TAVUK A.Ş. for providing eggs for conducting this study.

  1. Funding information: There is no funding for this article.

  2. Author contributions: Conceptualization, G.P. and M.F.B.; methodology, G.P. and M.F.B; formal analysis, M.F.B. and G.P.; investigation, M.F.B. and G.P.; resources, M.F.B. and G.P.; data curation, G.P.; writing – original draft preparation, G.P. and M.F.B.; writing – review and editing, G.P. and M.F.B. All authors have read and agreed to the published version of the manuscript.

  3. Conflict of interest: The authors declare no conflict of interest.

  4. Ethical approval: Ethical approval for this study was obtained from Afyon Kocatepe University HADYEK.

  5. Data availability statement: Derived data supporting the findings of this study are available from the corresponding author, Günnur Peşmen, on request.

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Received: 2022-12-25
Revised: 2023-01-23
Accepted: 2023-01-25
Published Online: 2023-02-21

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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