Effect of Bee Bread on Corticosterone Level in Rat Dams Exposed to Gestational Heat Stress

Main Article Content

Nur Akmar Nadhirah Mohd Nor
Asmad Kari
Mohd Nizam Haron
Connie Fay Komilus

Abstract

Environmental temperature rises are powerful stimuli that can alter both the sympathetic nervous system and the hypothalamic-pituitary-adrenocortical axis (HPA). Heat stress has been shown to harm pregnancy outcomes such as causing spontaneous abortion, low birth weight, growth retardation and stillbirth. Supplementation of bee bread in pregnant rats under heat stress exposure has been shown to improve the pregnancy outcomes. However, whether supplementation of bee bread during heat stress exposure may also reduce the level of the stress hormone, corticosterone has yet been reported. Therefore, this study aims to determine the effect of bee bread on corticosterone level, progesterone level, oestradiol level and zonation of the adrenal cortex of pregnant rats under heat stress exposure. Pregnant rats were randomly categorised into four groups (n = 6): Control (C: standard feeding), Treatment 1 (T1: 0.5 g bee bread/kg body weight/ day), Treatment 2 (T2: standard feeding with heat exposure), and Treatment 3 (T3: 0.5 g bee bread/kg body weight/day with heat exposure). Bee bread (0.5 g/kg body weight/ day) was force-fed to pregnant rats through oral gavage beginning on day 0 of pregnancy and continuing until delivery. Heat stress was generated experimentally by putting both T2 and T3 rats in an egg incubator for 45 min daily at a temperature of 43°C till delivery. On a postnatal Day 21, dams were euthanised to assess serum corticosterone, progesterone, oestradiol levels and adrenal gland histology. Rats in the T2 group had a significantly (P < 0.05) increase in the zona fasciculata thickness (94.95 ± 1.55 ?m) and higher corticosterone levels (49.57 ± 1.57 ng/mL) compared with control. However, supplementation of bee bread during heat stress was able to show an improvement in adrenal zona fasciculata thickness by decreasing to 79.89 ± 3.08 ?m and corticosterone level reduced to 35.31 ± 1.73 ng/mL significantly (P < 0.05). Therefore, these findings may imply that bee bread is effective as a neutralizer in lowering the production of stress hormone.

Article Details

How to Cite
Effect of Bee Bread on Corticosterone Level in Rat Dams Exposed to Gestational Heat Stress. (2023). Tropical Life Sciences Research, 34(3), 151–163. https://doi.org/10.21315/tlsr2023.34.3.8
Section
Original Article

References

Abdulmajeed W I, Sulieman H B, Zubayr M O, Imam A, Amin A, Biliaminu S A, Oyewole L A, and Owoyele B V. (2016). Honey prevents neurobehavioural deficit and oxidative stress induced by lead acetate exposure in male Wistar rats: A preliminary study. Metabolic Brain Disease 31(1): 37–44. https://doi.org/10.1007/s11011-015-9733-6

Allen M J and Sharma S. (2021). Physiology, Adrenocorticotropic Hormone (ACTH) [Updated 17 August 2021]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing. https://www.ncbi.nlm.nih.gov/books/NBK500031/

Arroyo V, Díaz J, Carmon R, Ortiz C and Linares C. (2016). Impact of air pollution and temperature on adverse birth outcomes: Madrid, 2001–2009. Environmental Pollution 218: 1154–1161. https://doi.org/10.1016/j.envpol.2016.08.069

Auger N, Fraser W D, Smargiassi A, Bilodeau-Bertrand M and Kosatsky T. (2017). Elevated outdoor temperatures and risk of stillbirth. International Journal of Epidemiology 46(1): 200–208. https://doi.org/10.1093/ije/dyw077

American Veterinary Medical Association (AVMA). (2013). AVMA guidelines for the euthanasia of animals: 2013 edition. https://works.bepress.com/cgi/viewcontent. cgi?article=1014&context=cheryl_greenacre

Bakour M, Laaroussi H, Ousaaid D, El Ghouizi A, Es-Safi I, Mechchate H and Lyoussi B. (2022). Bee bread as a promising source of bioactive molecules and functional properties: An up-to-date review. Antibiotics (Basel, Switzerland) 11(2): 203. https://doi.org/10.3390/antibiotics11020203

Belina-Aldemita M D, Opper C, Schreiner M and D’Amico S. (2019). Nutritional composition of pot-pollen produced by stingless bees (Tetragonula biroi Friese) from the Philippines. Journal of Food Composition and Analysis 82: 103215. https://doi.org/10.1016/j.jfca.2019.04.003

da Silva G R, da Natividade T B, Camara C A, da Silva E M S, dos Santos F D A R and Silva T M S. (2014). Identification of sugar, amino acids and minerals from the pollen of jandara stingless bees (Melipona subnitida). Food and Nutrition Sciences 05(11): 1015–1021. https://doi.org/10.4236/fns.2014.511112

del Barrio A S, Mansilla W, Navarro-Villa A, Mica J, Smeets J, den Hartog L and García- Ruiz A. (2020). Effect of mineral and vitamin C mix on growth performance and blood corticosterone concentrations in heat-stressed broilers. Journal of Applied Poultry Research 29(1): 23–33. https://doi.org/10.1016/j.japr.2019.11.001

Donkersley P, Rhodes G, Pickup R W, Jones K C, Power E F, Wright G A and Wilson K. (2017). Nutritional composition of honey bee food stores vary with floral composition. Oecologia 185(4): 749–761. https://doi.org/10.1007/s00442-017- 3968-3

El-Ratel I T, Abdel-Khalek A E and Fouda S F. (2020). Effect of ovarian stimulation by different gonadotrophin treatments on in vivo and in vitro reproductive efficiency of rabbit does under high ambient temperature. Tropical Animal Health and Production 53(1): 22. https://doi.org/10.1007/s11250-020-02429-w

Fotsing D, Njapdounke K J, Kenneth Y A and Ngo Bum E. (2016). Effect of Nelsonia canescens (Acanthaceae) on the stress induced behavioral and reproductive changes in female rats. World Journal Pharmacy and Pharmaceutical Science 12: 31–49.

Ha S, Liu D, Zhu Y, Kim S S, Sherman S and Mendola P. (2017a). Ambient temperature and early delivery of singleton pregnancies. Environmental Health Perspectives 125(3): 453–459. https://doi.org/10.1289/EHP97

Ha S, Liu D, Zhu Y, Soo Kim S, Sherman S, Grantz K L and Mendola P. (2017b). Ambient temperature and stillbirth: A multi-center retrospective cohort study. Environmental Health Perspectives 125(6): 067011. https://doi.org/10.1289/EHP945

Haron M N, Wan F, Siti A S and Mahaneem M. (2014). Tualang honey ameliorates restraint stress-induced impaired pregnancy outcomes in rats. European Journal of Integrative Medicine 6(6): 657–663. https://doi.org/10.1016/j.eujim.2014.07.001

Huh E, Lee W, Choi Y, Lee T H and Oh M S. (2021). Geongangbuja-tang decoction and its active ingredient, aconiti lateralis radix preparata, exerts inhibitory effects on heat stress-induced inflammation in mice. Applied Sciences 11(15): 6902. https://doi.org/10.3390/app11156902

Ieko T, Sasaki H, Maeda N, Fujiki J, Iwano H and Yokota H. (2019). Analysis of corticosterone and testosterone synthesis in rat salivary gland homogenates. Frontiers in Endocrinology 10: 479. https://doi.org/10.3389/fendo.2019.00479

Kieliszek M, Piwowarek K, Kot A M, B?a?ejak S, Chlebowska-?migiel A and Wolska I. (2018) Pollen and bee bread as new health-oriented products: A review. Trends in Food Science and Technology 71: 170–180. https://doi.org/10.1016/j.tifs.2017.10.021

Levin G, Elchalal U and Rottenstreich A. (2019). The adrenal cortex: Physiology and diseases in human pregnancy. European Journal of Obstetrics, Gynecology and Reproductive Biology 240: 139–143. https://doi.org/10.1016/j.ejogrb.2019.06.036

Lucy M C. (2019). Stress, strain, and pregnancy outcome in postpartum cows. Animal Reproduction 16(3): 455–464. https://doi.org/10.21451/1984-3143-AR2019-0063

Mohammad S M, Mahmud-Ab-Rashid N and Zawawi N. (2020). Botanical origin and nutritional values of bee bread of stingless bee (Heterotrigona itama) from Malaysia. Journal of Food Quality 2020: 2845757. https://doi.org/10.1155/2020/2845757

Mohd Nor N A N and Haron M N. (2018). Effect of heat stress on pregnancy outcomes in Sprague Dawley rats. International Journal of Engineering Technology 7(4.43): 6–9.

Morsy A, Soltan Y, El-Zaiat H, Alencar S and Abdalla A. (2021). Bee propolis extract as a phytogenic feed additive to enhance diet digestibility, rumen microbial biosynthesis, mitigating methane formation and health status of late pregnant ewes. Animal Feed Science and Technology 273: 114834. https://doi.org/10.1016/j.anifeedsci.2021.114834

Nor N A N M, Komilus C F, Haron M N, Lananan F, Chew H H, Yaakub N and Kari A. (2021). Effect of bee bread on pregnancy outcomes and reproductive system of rats under heat stress exposure. Malaysian Journal of Fundamental and Applied Sciences 17(6): 781–793. https://doi.org/10.11113/mjfas.v17n6.2308

National Society for Histotechnology (NSH). (2001). Guidelines for hematoxylin and eosin staining. Maryland: NSH.

Organisation for Economic Co-operation and Development (OECD). (2008). Part 5: Preparation, reading and reporting of vaginal smears. In: OECD Guidelines for the Testing of Chemicals. OECD, 116–125. https://www.oecd.org/chemicalsafety/testing/40581357.pdf

Othman Z A, Wan Ghazali W S, Nordin L, Omar N and Mohamed M. (2019). Nutritional, phytochemical and antioxidant analysis of bee bread from different regions of Malaysia. Indian Journal Pharmacology Science 81: 955–960. https://doi.org/10.36468/pharmaceutical-sciences.590

Quinteiro-Filho W M, Gomes A V S, Pinheiro M L, Ribeiro A, Ferraz-de-Paula V, Astolfi- Ferreira C S and Palermo-Neto J. (2012). Heat stress impairs performance and induces intestinal inflammation in broiler chickens infected with Salmonella enteritidis. Avian Pathology 41(5): 421–427. https://doi.org/10.1080/03079457.2012.709315

Rakova N, Kitada K, Lerchl K, Dahlmann A, Birukov A, Daub S, Kopp C, Pedchenko, T, Zhang Y, Beck L, Johannes B, Marton A, Müller D N, Rauh M, Luft F C and Titze J. (2017). Increased salt consumption induces body water conservation and decreases fluid intake. The Journal of clinical investigation 127(5): 1932–1943. https://doi.org/10.1172/JCI88530

Sadek M T, El-Abd S S and Ibrahim M A A. (2021). Effect of chronic unpredictable mild stress on adrenal cortex of adult rat and the possible protective role of licorice extract: A histological and immunohistochemical study. Egyptian Journal of Histology 44(4): 887–901.

Schifano P, Asta F, Dadvand P, Davoli M, Basagana X and Michelozzi P. (2016). Heat and air pollution exposure as triggers of delivery: A survival analysis of population-based pregnancy cohorts in Rome and Barcelona. Environment International 88: 153–159. https://doi.org/10.1016/j.envint.2015.12.013

Sheng J A, Bales N J, Myers S A, Bautista A I, Roueinfar M, Hale T M and Handa R J. (2021). The hypothalamic-pituitary-adrenal axis: Development, programming actions of hormones, and maternal-fetal interactions. Frontiers in Behavioral Neuroscience 14(January): 1–21. https://doi.org/10.3389/fnbeh.2020.601939

Tomás A, Falcão S I, Russo-Almeida P and Vilas-Boas M. (2017). Potentialities of beebread as a food supplement and source of nutraceuticals: Botanical origin, nutritional composition and antioxidant activity. Journal of Apicultural Research 56(3): 219– 230. https://doi.org/10.1080/00218839.2017.1294526

Urcan A C, Marghitas L A, Dezmirean D S, Bobis O, Bonta V, Muresan C I and Margaoan R. (2017). Chemical composition and biological activities of beebread: Review. Bulletin of University of Agricultural Sciences and Veterinary Medicine Cluj- Napoca. Animal Science and Biotechnologies 74(1): 6–14.

Valsamakis G, Chrousos G and Mastorakos G. (2019). Stress, female reproduction and pregnancy. Psychoneuroendocrinology 100: 48–57. https://doi.org/10.1016/j.psyneuen.2018.09.031

Wagenmaker E R and Moenter S M. (2017). Exposure to acute psychosocial stress disrupts the luteinizing hormone surge independent of estrous cycle alterations in female mice. Endocrinology 158(8): 2593–2602. https://doi.org/10.1210/en.2017-00341

Wang L, Liu F, Luo Y, Zhu L and Li G. (2015). Effect of acute heat stress on adrenocorticotropic hormone, cortisol, interleukin-2, interleukin-12 and apoptosis gene expression in rats. Biomedical Reports 3(3): 425–429. https://doi.org/10.3892/br.2015.445

Xu Y, Lai X, Li Z, Zhang X and Luo Q. (2018). Effect of chronic heat stress on some physiological and immunological parameters in different breed of broilers. Poultry Science 97(11): 4073–4082. https://doi.org/10.3382/ps/pey256

Zaki S M, Abdelgawad F A, El-Shaarawy E A A, Radwan R A K and Aboul-Hoda B E. (2018). Stress-induced changes in the aged-rat adrenal cortex. Histological and histomorphometric study. Folia Morphologica (Warsz) 77(4): 629–641. https://doi.org/10.5603/FM.a2018.0035

Zhang S, Mesalam A, Lee K L, Song S H, Khan I, Yuan Y, Wenfa L V and Kong I K. (2019). Effect of predator stress on the reproductive performance of female mice after nonsurgical embryo transfer. Journal of the American Association for Laboratory Animal Science 58(3): 304–310. https://doi.org/10.30802/AALAS-JAALAS-18-000085