Effects of hawthorn (Crataegus oxycantha) fruit extract on tibia bone properties in broiler chickens subjected to heat stress
Resumen
The aim of this study was to investigate the effects of different doses of hawthorn (Crataegus oxyacantha) fruit extract (HFE) supplementation to experimentally heat stressed broiler drinking water on tibia morphology, biomechanics and mineral levels. 300 one-day-old male broiler were randomly allocated to 6 experimental groups according to 2x3 factorial experimental design with two different ambient temperatures (24 and 35oC) and three different HFE additions (0, 0.2 and 0.4 mL/L). Each experimental group contained five replicates of 10 chicks each. Heat stress (HS) decreased tibia dry weight, length, wet weight, volume, seedor index, cortex thickness, shear force and shear stress and increased dry matter percentage (P<0.05). HS also caused a decrease in tibia Ca, Mg, Cu, Fe, Zn and K (P<0.05) levels. The addition of HFE to the water of broilers housed under HS didn’t affect the morphological and biomechanical properties of tibia. Ca level of tibia increased with 0.2 mL/L HFE addition and Mg and Zn levels increased with both 0.2 and 0.4 ml/L HFE additions compared to the control (P<0.05), while Fe and Mn levels of tibia decreased with 0.2 mL/L HFE addition and K level decreased with both levels of HFE addition compared to the control (P<0.05). On the other hand, tibia Cu level decreased with 0.2 mL/L HFE addition and increased with 0.4 mL/L HFE addition. It was concluded that the addition of 0.2 mL/L HFE to the water of broilers exposed to high ambient temperature would be sufficient and recommendable to improve bone quality characteristics.
Article Details
- Cómo citar
-
Kaya, H., & Karaalp, M. (2025). Effects of hawthorn (Crataegus oxycantha) fruit extract on tibia bone properties in broiler chickens subjected to heat stress. Journal of the Hellenic Veterinary Medical Society, 76(3), 9751–9762. https://doi.org/10.12681/jhvms.40144
- Número
- Vol. 76 Núm. 3 (2025)
- Sección
- Research Articles
Esta obra está bajo una licencia internacional Creative Commons Atribución-NoComercial 4.0.
Authors who publish with this journal agree to the following terms:
· Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
· Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
· Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.
Descargas
Los datos de descargas todavía no están disponibles.
Citas
Abdelaziz MAM (2015) Effect of phosphorus restriction in presence
of organic acid salt on bone quality and mineral digestibility of
broilers. Egyptian Poultry Science Journal, 35(4):961-968.
Ahmadipour B, Kalantar M, Hosseini SM, Yang LG, Kalantar MH,
Raza SHA, Schreurs NM (2017) Hawthorn (Crataegus oxyacantha)
extract in the drinking water of broilers on growth and incidence
of pulmonary hypertension syndrome (PHS). Brazilian Journal of
Poultry Science, 19(4):639-644. https://doi.org/10.1590/1806-9061-
-0558
Alharbi K, Ekesi N, Hasan A, Asnayanti A, Liu J, Murugesan
R, Ramirez S, Rochell S, Kidd MT, Alrubaye A (2024). Deoxynivalenol
and fumonisin predispose broilers to bacterial chondronecrosis
with osteomyelitis lameness. Poultry Science, 103(5):103598.
AOAC-Association of Official Analytical Chemists (1994) Official
Methods of Analysis.16th ed. Association of Analytical Chem.
Washington, DC. USA.
Armstrong TA, Flowers WL, Spears JW, Nielsent, FH (2002) Long-term
effects of boron supplementation on reproductive characteristics
and bone mechanical properties in gilts. Journal of Animal Science,
(1):154-161. https://doi.org/10.2527/2002.801154x
ASAE-American Society of Agricultural Engineers (2001) Shear And
Three-Point Bending Test of Animal Bone: St. Joseph, MO, USA.
Attard E, Attard H (2019) Hawthorn: Crataegus oxyacantha, Crataegus
monogyna and related species. In Nonvitamin and Nonmineral Nutritional
Supplements; Nabavi, S.M., Silva, A.S., Eds.; Academic
Press: Cambridge, MA, USA. https://doi.org/10.1016/B978-0-12-
-8.00041-2
Attia YA, Aldhalmi AK, Youssef IM, Bovera F, Tufarelli V, El-Hack
MEA, El-Kholy KH, Shukry, M (2024) Climate change and its
effects on poultry industry and sustainability. Discover Sustainability,
Attia YA, Al-Harthi MA, El-Shafey AS, Rehab YA, Kim WK (2017)
Enhancing tolerance of broiler chickens to heat stress by supplementation
with vitamin E, vitamin C and/or probiotics. Annals of Animal
Science, 17(4):1155. https://doi.org/10.1515/aoas-2017-0012
Aviagen (2009) Ross broiler management manual, aviagen broiler
breeders, Midlothian, Scotland, UK, pp. 1–114, www.aviagen.com
Bartell SM, Kim HN, Ambrogini E, Han L, Iyer S, Serra Ucer S, Rabinovitch
P, Jilka RL, Weinstein RS, Zhao H, O’Brrien CA, Manolagas
SC, Almeida M (2014) FoxO proteins restrain osteoclastogenesis
and bone resorption by attenuating H2O2 accumulation. Nature
communications, 5(1):3773. https://doi.org/10.1038/ncomms4773
Baysan G, Yilmaz PA, Husemoglu RB, Albayrak AZ, Sisman AR,
Havitcioglu H (2024) Elderberry (Sambucus nigra) and hawthorn
(Crataegus oxyacantha) extract additives in carboxymethyl chitosan
scaffolds for osteochondral tissue engineering applications. Journal
of Applied Polymer Science, e55637. https://doi.org/10.1002/
app.55637
Bolduc JA, Collins JA, Loeser RF (2019) Reactive oxygen species,
aging and articular cartilage homeostasis. Free Radical Biology
and Medicine, 132:73-82. https://doi.org/10.1016/j.freeradbiomed.
08.038
Cardinali R, Cullere M, Dal Bosco A, Mugnai C, Ruggeri S, Mattioli S,
Castellini C, Trabalza Marinucci M, Dalle Zotte A (2015) Oregano,
rosemary and vitamin E dietary supplementation in growing rabbits:
Effect on growth performance, carcass traits, bone development
and meat chemical composition. Livestock Science, 175(5):83-89.
Cartoni Mancinelli A, Mattioli S, Dal Bosco A, Aliberti A, Guarino
Amato M, Castellini C (2020) Performance, behavior, and welfare
status of six different organically reared poultry genotypes. Animals,
(4):550. https://doi.org/10.3390/ani10040550
Chen K, Liu Y, He J, Pavlos N, Wang C, Kenny J, Yuan J, Zhang Q, Xu
j, He W (2020) Steroid-induced osteonecrosis of the femoral head
reveals enhanced reactive oxygen species and hyperactive osteoclasts.
International journal of biological sciences, 16(11):1888.
Chen Y, Cheng Y, Du M, Zhou Y (2021) Protective effects of dietary
synbiotic supplementation on meat quality and oxidative status in
broilers under heat stress. Environmental Science and Pollution
Research, 28(23):30197-30206. https://doi.org/10.1007/s11356-
-12535-3
Cimrin T, Tunca RI, Avsaroglu MD, Ayasan T, Küçükersan S (2020)
Effects of an antibiotic and two phytogenic substances (cinnamaldehyde
and 1, 8-cineole) on yolk fatty acid profile and storage
period-associated egg lipid peroxidation level. Revista Brasileira de
Zootecnia, 49, e20190270. https://doi.org/10.37496/rbz4920190270
Cuevas-Bernardino JC, Lobato-Calleros C, Román-Guerrero A, Alvarez-
Ramirez J, Vernon-Carter EJ (2016) Physicochemical characterisation
of hawthorn pectins and their performing in stabilising oilin-
water emulsions. Reactive and Functional Polymers, 103:63–71.
Çetin CR (2014) Investigation of protective effects of hawthorn (Crataegus
tanacetifolia) fruit extract and hawthorn fruit vinegar against
experimental hyperlipidemia and possible endothelial damage in
rats. MSc Thesis. Inönü University, Institute of Health Sciences,
Department of Biochemistry, Sivas, Türkiye.
Dahmer S, Scott E (2010) Health effects of hawthorn. American
Family Physician, 81(4):465-468. www.aafp.org/pubs/afp/issues/
/0215/p465.pdf
El-Faham AI, Nematallah GMA, Abdelaziz MAM (2017) Effects of
dietary threonine level, methionine sources, sex of broiler chicks
and their interactions on carcass tissue distribution and chemical
composition. Egyptian Poultry Science Journal, 37(1):155-167.
Elnesr SS, Elwan HAM, Xu QQ, Xie C, Dong XY, Zou XT (2019)
Effects of in ovo injection of sulfur-containing amino acids on heat
shock protein 70, corticosterone hormone, antioxidant indices, and
lipid profile of newly hatched broiler chicks exposed to heat stress
during incubation. Poultry Science, 98(5):2290-2298. https://doi.
org/10.3382/ps/pey609
Gajewska J, Chełchowska M, Rychłowska-Pruszyńska M, Klepacka
T, Ambroszkiewicz J (2022) Oxidative and antioxidative status
expressed as OSI index and GSH/GSSG ratio in children with bone
tumors after anticancer therapy completion. Journal of Clinical
Medicine, 11(6):1663. https://doi.org/10.3390/jcm11061663
Gonz´alez-Jim´enez FE, Salazar-Montoya JA, Calva-Calva G, Ramos-
Ram´ırez EG (2018) Phytochemical characterization, ın vitro
antioxidant activity, and quantitative analysis by micellar electrokinetic
chromatography of hawthorn (Crataegus pubescens)
Fruit. Journal of Food Quality, 2018(1), 2154893. https://doi.
org/10.1155/2018/2154893
Goo D, Kim, JH, Park GH, Delos Reyes JB, Kil DY (2019) Effect of
heat stress and stocking density on growth performance, breast meat
quality, and intestinal barrier function in broiler chickens. Animals,
(3):107. https://doi.org/10.3390/ani9030107
Hamada Y, Kitazawa S, Kitazawa R, Fujii H, Kasuga M, Fukagawa
M (2007) Histomorphometric analysis of diabetic osteopenia
in streptozotocin-induced diabetic mice: a possible role of oxidative
stress. Bone, 40(5):1408-1414. https://doi.org/10.1016/j.
bone.2006.12.057
Hasan MN, Chand N, Naz S, Khan RU, Ayaşan T, Laudadio V, Tufarell
V (2022) Mitigating heat stress in broilers by dietary dried
tamarind (Tamarindus indica L.) pulp: Effect on growth and blood
traits, oxidative status and immune response. Livestock Science,
Hatipoğlu M, Sağlam M, Köseoğlu S, Köksal E, Keleş A, Esen HH
(2015) The effectiveness of Crataegus orientalis M Bieber (Hawthorn)
extract administration in preventing alveolar bone loss in
rats with experimental periodontitis. PLoS One,10(6):e0128134.
Henneicke H, Gasparini SJ, Brennan-Speranza TC, Zhou H, Seibel
MJ (2014) Glucocorticoids and bone: local effects and systemic
implications. Trends in Endocrinology & Metabolism, 25(4):197-
Hosseini SJ, Kermanshahi H, Nassirimoghaddam H, Nabipour A,
Mirakzeh MT, Saleh H, Kazemifard M (2016) Effects of 1.25-dihydroxycholecalciferol
and hydroalcoholic extract of Withania coagulans
fruit on bone mineralization and mechanical and histological
properties of male broiler chickens. Brazilian Journal of Poultry
Science, 18(1):73-86. https://doi.org/10.1590/18069061-2015-0016
Hosseini-Vashan SJ, Golian A, Yaghobfar A (2016) Growth, immune, antioxidant, and bone responses of heat stress-exposed broilers
fed diets supplemented with tomato pomace. International Journal
of Biometeorology, 60(8):1183-1192. https://doi.org/10.1007/
s00484-015-1112-9
Huang C, Jiao H, Song Z, Zhao J, Wang X, Lin H (2015) Heat stress
impairs mitochondria functions and induces oxidative injury in
broiler chickens. Journal of Animal Science, 93(5):2144-2153.
Huang J, Tong XF, Yu ZW, Hu YP, Zhang L, Liu Y, Zhou ZX (2020)
Dietary supplementation of total flavonoids from Rhizoma drynariae
improves bone health in older caged laying hens. Poultry Science,
(10):5047-5054. https://doi.org/10.1016/j.psj.2020.06.057
Iantomasi T, Romagnoli C, Palmini G, Donati S, Falsetti I, Miglietta F,
Aurilia C, Marini F, Giusti F, Brandi ML (2023) Oxidative stress
and inflammation in osteoporosis: molecular mechanisms involved
and the relationship with microRNAs. International journal of molecular
sciences, 24(4):3772. https://doi.org/10.3390/ijms24043772
Jankowski J, Mikulski D, Tatara MR, Krupski W (2015) Effects of
increased stocking density and heat stress on growth, performance,
carcase characteristics and skeletal properties in turkeys. Veterinary
Record, 176(1):21-21. https://doi.org/10.1136/vr.102216
Jurikova T, Sochor J, Rop O, Mlcek J, Balla S, Szekeres L (2012)
Polyphenolic profile and biological activity of Chinese hawthorn
(Crataegus pinnatifida BUNGE) fruits. Molecules, 17(12):14490–
Karadağoğlu Ö, Şahin T (2023) A Strategic Approach to Nutrition of
Poultry Exposed to Heat Stress: Probiotics. In: Ölmez, M. (ed.),
Therapeutic, Prophylactic, and Functional Use of Probiotics in
Veterinary Sciences. Özgür Publications. https://doi.org/10.58830/
ozgur.pub358.c1522
Kaya H (2023a). The effects of hawthorn (Crataegus oxyacantha) fruit
extract on performance, carcass and some serum parameters of broilers
reared under heat-stress conditions. Indian Journal of Animal
Research, 57(9):1244-1250. https://doi.org/10.18805/IJAR.BF-1657
Kaya H (2023b). The effect of organic hawthorn (Crataegus tanacetifolia)
fruit vinegar supplement on growth performance, carcass
characteristics and some serum parameters in broiler chickens
subjected to cyclic heat stress. Indian Journal of Animal Research,
(8):1011-1017. https://doi.org/10.18805/IJAR.BF-1652
Kaya Z (2019). The effects of pickle juice supplementation in drinking
water of quails on fecal microbiota. MSc Thesis. Kırsehir Ahi Evran
University, Science and Engineering Institute, Animal Science Department,
Kırşehir, Türkiye.
Kimball JS, Johnson JP, Carlson DA (2021) Oxidative stress and osteoporosis.
The Journal of Bone and Joint Surgery 103(15):1451-1461.
Kwiecieñ M, Winiarska-Mieczan A (2009) Effect of addition of herbs
on body weight and assessment of physical and chemical alterations
in the tibia bones of broiler chickens. Journal of Elementology,
(4):705-715.
Kwiecień M, Winiarska-Mieczan A, Pałyszka M, Kwiatkowska K
(2014) Effects of chicken feed herbal additives on the breeding
performance, slaughter yield and mechanical and morphometric
parameters of chicken tibia bones. Medycyna Weterynaryjna,
(05):280-286.
Leskovec J, Levart A, Žgur S, Jordan D, Pirman T, Salobir J, Rezar V
(2017) Effects of olive leaf and marigold extracts on the utilization
of nutrients and on bone mineralization using two different
oil sources in broilers. The Journal of Poultry Science, 0170059.
Li F, Yuan Q, Rashid F (2009) Isolation, purification and immunobiological
activity of a new water-soluble bee pollen polysaccharide from
Crataegus pinnatifida Bge. Carbohydrate Polymers, 78(1):80-88.
Li Y, Li C, Xu W, Zhao J, Liu K, Liu X, Li Y, Tang Z, Li A, Zhang
H (2025) Chondroitin sulfate reverses tibial dyschondroplasia,
broiler chondrocyte proliferation and differentiation dysfunction
via the CHST11/β-Catenin pathway. International Journal of Biological
Macromolecules, 144488. https://doi.org/10.1016/j.ijbiomac.
144488
Liang X, Yang X, Liu J, Tu L, Wei W, Wang H, Wu M, Cai L, Zheng Y,
Chen, Y. (2024). ROS-scavenging bioactive scaffold orchestrates
bone regeneration for osteoporotic bone defect repair. Composites
Part B: Engineering, 281, 111528. https://doi.org/10.1016/j.compositesb.
111528
Liu PZ, Kallio H, Lu D, Zhou CS, Yao B (2011) Quantitative analysis
of phenolic compounds in Chinese hawthorn (Crataegus spp.) fruits
by high performance liquid chromatography-electrospray ionisation
mass spectrometry. Food Chemistry, 127(3):1370–1377. https://doi.
org/10.1016/j.foodchem.2011.01.103
Liu W, Yuan Y, Sun C, Balasubramanian B, Zhao Z, An L (2019) Effects
of dietary betaine on growth performance, digestive function,
carcass traits, and meat quality in indigenous yellow-feathered
broilers under long-term heat stress. Animals,9(8):506. https://
doi.org/10.3390/ani9080506
Magwere T, Myatt SS, Burchill SA (2008) Manipulation of oxidative
stress to induce cell death in Ewing’s sarcoma family of tumours.
European Journal of Cancer, 44(15), 2276-2287. https://doi.
org/10.1016/j.ejca.2008.06.008
Malila Y, Jandamuk A, Uopasai T, Buasook T, Srimarut Y, Sanpinit
P, Phasuk Y, Kunhareang S (2021) Effects of cyclic thermal
stress at later age on production performance and meat quality
of fast-growing, medium-growing and thai native chickens. Animals,
(12):3532. https://doi.org/10.3390/ani11123532
Marcinčáková D, Čertík M, Marcinčák S, Popelka P, Šimková J, Klempová
T, Tučková M, Bača M (2011) Effect of dietary supplementation
of Melissa officinalis and combination of Achillea millefolium
and Crataegus oxyacantha on broiler growth performance, fatty acid
composition and lipid oxidation of chicken meat. Italian Journal,
Marcucci G, Domazetovic V, Nediani C, Ruzzolini J, Favre C, Brandi
ML (2023) Oxidative stress and natural antioxidants in osteoporosis:
novel preventive and therapeutic approaches. Antioxidants, 12(2):
Marques-Carvalho A, Kim HN, Almeida M (2023) The role of reactive
oxygen species in bone cell physiology and pathophysiology. Bone
Reports, 19(2):101664. https://doi.org/10.1016/j.bonr.2023.101664
Martínez Y, Rodríguez R, Pupo GE, Rosabal O, Colmo C, Valdivié
M (2020) Phytobiotic effect of Psidium guajava leaf powder on
productivity and quality of the egg of laying hens. Cuban Journal
of Agricultural Science, 54(4):557-568. https://www.cjascience.
com/index.php/CJAS/article/view/989
Mertens D (2005) AOAC Official Method 975.03. Metal in Plants and
Pet Foods. Official Methods of Analysis, 18th edit. Horwitz, W.,
and G.W. Latimer, (Eds).Chapter 3, pp 3-AOAC- International
Suite 500, 481. North Frederick Avenue, Gaitherburg, Maryland
-2417, USA.
Mirakzehi MT, Hosseini SJ, Saleh H (2018) Effects of two plant extracts
and vitamin D3 on bone mechanical and histological properties of
broiler chickens. Journal of Animal & Plant Sciences, 28(3):686-
Mishra B, Jha R (2019) Oxidative stress in the poultry gut: Potential
challenges and interventions. Frontiers in Veterinary Science,
Mohammed AA, Zaki RS, Negm EA, Mahmoud MA, Cheng HW (2021)
Effects of dietary supplementation of a probiotic (Bacillus subtilis)
on bone mass and meat quality of broiler chickens. Poultry
Science, 100(3):100906. https://doi.org/10.1016/j.psj.2020.11.073
Mutlu Sİ, Baykalir Y, Azman MA, Şimşek ÜG, Özçelik M, Bayraktar O,
Çiftçi M, Erişir Z (2021) The effects of dietary supplementation of
olive leaf extract and eggshell with membrane on performance, egg
quality, blood biochemical, and bone parameters in laying Japanese
quail. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 68(3):251-
Nkukwana TT, Muchenje V, Masika PJ, Hoffman LC, Dzama K (2014)
The effect of Moringa oleifera leaf meal supplementation on tibia
strength, morphology and inorganic content of broiler chickens.
South African Journal of Animal Science, 44(3):228-239. https://
doi.org/10.4314/sajas.v44i3.4
Olgun O (2016) The effect of dietary essential oil mixture supplementation
on performance, egg quality and bone characteristics in laying
hens. Annals of Animal Science,16(4):1115. https://doi.org/10.1515/
aoas-2016-0038
Olgun O, Gül ET, Tüzün AE, Yıldız A (2022) Effect of maca powder
supplementation to growing quail diets on performance, carcass,
serum constituents and hormones, and bone and ileum characteristics.
Tropical Animal Health and Production, 54(4):1-11. https://
doi.org/10.1007/11250-022-03230-7
Özcan M, Hacıseferogulları H, Marakoglu T, Arslan D (2005) Hawthorn
(Crataegus spp.) fruit: some physical and chemical properties. Jour nal of Food Engineering 69(4): 409-415. https://doi.org/10.1016/j.
jfoodeng.2004.08.032
Pečjak M, Levart A, Salobir J, Rezar V (2020) Effect of the supplementation
of olive leaves and olive cake on growth performance
and bone mineralisation of broiler chickens.Acta Fytotech. Zootech,
(2020):105-111. https://doi.org/10.15414/afz.2020.23.mifpap.
-111
Pritchard A, Robison C, Nguyen T, Nielsen BD (2020) Silicon supplementation
affects mineral metabolism but not bone density or
strength in male broilers. PLoS One, 15(12): e0243007. https://doi.
org/10.1371/journal.pone.0243007
Reisenfeld A (1972) Metatarsal robusticity in bi-pedal rats. American
Journal of Physiology and Anthropology, 40:229–234. https://doi.
org/10.1002/ajpa.1330360211
Rocchi A, Ruff J, Maynard CJ, Forga AJ, Señas-Cuesta R, Greene ES,
Tellez-Isaias G (2022) Experimental cyclic heat stress on ıntestinal
permeability, bone mineralization, leukocyte proportions and
meat quality in broiler chickens. Animals, 12(10):1273. https://doi.
org/10.3390/ani12101273
Sahin K, Orhan C, Tuzcu M, Sahin N, Hayirli A, Bilgili S, Kucuk O
(2016) Lycopene activates antioxidant enzymes and nuclear transcription
factor systems in heat-stressed broilers. Poultry Science,
(5):1088-1095. https://doi.org/10.3382/ps/pew012
Sanchez-Rodriguez E, Benavides-Reyes C, Torres C, Dominguez-Gasca
N, Garcia-Ruiz AI, Gonzalez-Lopez S, Rodriguez-Navarro AB
(2019) Changes with age (from 0 to 37 D) in tibiae bone mineralization,
chemical composition and structural organization in
broiler chickens. Poultry science, 98(11):5215-5225. https://doi.
org/10.3382/ps/pez363
Santos MN, Widowski TM, Kiarie EG, Guerin MT, Edwards AM, Torrey
S (2022) In pursuit of a better broiler: walking ability and incidence
of contact dermatitis in conventional and slower growing strains
of broiler chickens. Poultry Science, 101(4):101768. https://doi.
org/10.1016/j.psj.2022.101768
Saracila M, Panaite T, Tabuc C, Soica C, Untea A, Ayasan T, Criste RD
(2020). Dietary ascorbic acid and chromium supplementation for
broilers reared under thermoneutral conditions vs. high heat stress.
Scientific Papers-Animal Science Series: Lucrări Ştiinţifice - Seria
Zootehnie, 73(1):41-47.
Savón L, Scull I, Orta M, Martínez M (2007) Harinas de follajes integrales
de tres leguminosas tropicales para la alimentación avícola.
Composición química, propiedades físicas y tamizaje fitoquímico.
Revista Cubana de Ciencia Agrícola,41(4):359-361.
Seedor JG, Quartuccio HA, Thompson DD (1991) The bisphosphonate
alendronate (MK‐217) inhibits bone loss due to ovariectomy in rats.
Journal of Bone and Mineral Research, 6(4):339-346. https://doi.
org/10.1002/jbmr.5650060405
Sellmeyer DE, Civitelli R, Hofbauer LC, Khosla S, Lecka-Czernik B,
Schwartz AV (2016) Skeletal metabolism, fracture risk, and fracture
outcomes in type 1 and type 2 diabetes. Diabetes, 65(7), 1757-1766.
Shakeri M, Cottrell JJ, Wilkinson S, Le HH, Suleria HA, Warner RD,
Dunshea FR (2019) Growth performance and characterization of
meat quality of broiler chickens supplemented with betaine and
antioxidants under cyclic heat stress. Antioxidants, 8(9):336-354.
Shim MY, Karnuah AB, Mitchell AD, Anthony NB, Pesti GM, Aggrey
SE (2012) The effects of growth rate on leg morphology and tibia
breaking strength, mineral density, mineral content, and bone ash in
broilers. Poultry Science, 91(8):1790-1795. https://doi.org/10.3382/
ps.2011-01968
Snezhkina AV, Kudryavtseva AV, Kardymon OL, Savvateeva MV, Melnikova
NV, Krasnov GS, Dmitriev AA (2019) ROS generation and
antioxidant defense systems in normal and malignant cells. Oxidative
medicine and cellular longevity, 2019(1): 6175804. https://
doi.org/10.1155/2019/6175804
Song Y, Zhu J, Wang T, Zhang C, Yang F, Guo X, Liu P, Cao H, Hu G
(2018) Effect of ultra-fine traditional chinese medicine compounds
on regulation of lipid metabolism and reduction in egg cholesterol
of laying hens. Brazilian Journal of Poultry Science, 20(1):153-
Sultan A, Khan S, Khan S, Chand N, Khan MS, Maris H (2018) Effect
of organic acid blend on carcass yield, nutrient digestibility and
tibia ash during starter phase of broiler chicks. Pakistan Journal
of Zoology, 50(4):1483-1488. http://doi.org/10.17582/journal.
pjz/2018.50.4.1483.1488
Tahami Z, Hosseini S M, Valizadeh Ghalebeig A (2021) Effects of
mixed Cinnamomum cassia (L.) J. Presl, Mentha pulegium L., and
Capsicum annuum L. extracts on gastrointestinal and tibia characteristics,
and blood of broilers. Iranian Journal of Medicinal and
Aromatic Plants Research, 37(3):487-501. https://doi.org/10.22092/
ijmapr.2021.351822.2869
Tang LP, Liu YL, Zhang JX, Ding KN, Lu MH, He YM (2022) Heat
stress in broilers of liver injury effects of heat stress on oxidative
stress and autophagy in liver of broilers. Poultry Science,
(10):102085. https://doi.org/10.1016/j.psj.2022.102085
Tekce E, Bayraktar B, Aksakal V, Dertli E, Kamiloğlu A, Çinar Topcu
K,Takma Ç, Gül M, Kaya H (2020) Response of Japanese quails
(Coturnix coturnix japonica) to dietary inclusion of Moringa
oleifera essential oil under heat stress condition. Italian Journal
of Animal Science, 19(1):514-523. https://doi.org/10.1080/1828
X.2020.1760740
Tian Y, Ma X, Yang C, Su P, Yin C, Qian AR (2017) The impact of
oxidative stress on the bone system in response to the space special
environment. International Journal of Molecular Sciences, 18(10):
TSE. 1991. Hayvan Yemleri Metabolik Enerji Tayini, TSE No:9610.
Türk Stant. Enst; Ankara.
Wauquier F, Leotoing L, Coxam V, Guicheux J, Wittrant Y (2009) Oxidative
stress in bone remodelling and disease. Trends in molecular
medicine, 15(10):468-477.
Wilson JH, Ruszler PL (1996) Effects of dietary boron supplementation
on laying hens. British Poultry Science, 37(4):723-729. https://doi.
org/10.1080/00071669608417902
Wruck CJ, Fragoulis A, Gurzynski A, Brandenburg LO, Kan YW, Chan
K, Hassenpflug J, Freitag-Wolf s, Varoga D, Lippross S,Pufe T
(2011) Role of oxidative stress in rheumatoid arthritis: insights
from the Nrf2-knockout mice. Annals of the rheumatic diseases,
(5):844-850. https://doi.org/10.1136/ard.2010.132720
Xu W, Xu Q, Chen J, Lu Z, Xia R, Li G (2011) Ligustrazine formation
in zhenjiang aromatic vinegar: Changes during fermentation and
storing process. Journal of the Science of Food and Agriculture,
(9):1612-1617. https://doi.org/10.1002/jsfa.4356
Yan FF, Mohammed AA, Murugesan GR, Cheng HW (2019) Effects of
a dietary synbiotic inclusion on bone health in broilers subjected
to cyclic heat stress episodes. Poultry Science, 98(3):1083-1089.
Yehia M, Askri A, Achour A, Prus JMA, Ouellet V, Alnahhas N (2025)
Rectal temperature and heat transfer dynamics in the eye, face, and
breast of broiler chickens exposed to moderate heat stress. Poultry
Science, 104(2): 104748. https://doi.org/10.1016/j.psj.2024.104748
Yılmaz E (2022) Effects of dietary supplementation of cuminum (Cuminum
cyminum L.) essential oil on growth performance, blood biochemistry,
gene expression, and slaughter traits in heat-stressed
broiler. PhD Thesis, Atatürk University, Institute of Health Sciences,
Department of Animal Nutrition and Nutritional Diseases, Erzurum,
Türkiye.
Zhang H, Majdeddin M, Gaublomme D, Taminiau B, Boone M, Elewaut
D, Daube G, Josipovic I, Zhang K, Michiels J (2021) 25-hydroxycholecalciferol
reverses heat induced alterations in bone quality
in finisher broilers associated with effects on intestinal integrity
and inflammation. Journal of Animal Science and Biotechnology,
Zhang Y, Zhang L, Geng Y, Geng Y (2014) Hawthorn fruit attenuates
atherosclerosis by improving the hypolipidemic and antioxidant activities
in apolipoprotein e-deficient mice. Journal of Atherosclerosis
and Thrombosis, 21(2):119-128. https://doi.org/10.5551/jat.19174
