Araştırma Makalesi
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Propilparabenin Tavuk (Gallus gallus gallus, Linnaeus 1758) Embriyosunda Yol Açtığı Embriyonik Gelişim Bozuklukları

Yıl 2025, Cilt: 20 Sayı: 3, 117 - 125, 25.12.2025
https://doi.org/10.17094/vetsci.1696554

Öz

Propilparaben, gıda, kozmetik ve ilaçlarda koruyucu olarak yaygın olarak kullanılmaktadır. Potansiyel teratojenik etkileri konusunda endişeler ortaya çıkmıştır. Bu çalışma, propilparabenin tavuk embriyosu gelişimi üzerindeki teratojenik etkilerini araştırmaktadır. Yumurtalar yatay pozisyonda 36,8 °C'de 68 saat inkübe edildi. 68 saat bekletilen tavuk embriyoları altı gruba ayrıldı: pozitif kontrol (%0,9 NaCl), negatif kontrol Dimetil Sülfoksit (DMSO) ve 1, 5, 10 ve 20 ppm konsantrasyonlarında propilparaben. Her grup 3 embriyodan oluşuyordu. İşlemden sonra embriyolar 24 saat daha inkübe edildi ve toplam inkübasyon süresi 92 saate ulaştı. Veriler tanımlayıcı-karşılaştırmalı yaklaşım kullanılarak analiz edildi. İstatistiksel analiz SPSS 25 yazılımı kullanılarak, parametrik veriler için One-way ANOVA ve ardından Duncan testi, parametrik olmayan veriler için ise Kruskal-Wallis ve ardından Mann-Whitney U testi kullanılarak gerçekleştirildi (P ≤ ,05). Sonuçlar, propilparabenin mezensefalon ve telensefalonda, tamamlanmamış kapanma ve azalmış vücut uzunluğu ile gösterildiği gibi anormalliklere neden olduğunu gösterdi. Pozitif kontrol (%0,9 NaCl) en büyük vücut uzunluğuna (18,97 ± 1,56 mm) sahipken, en küçüğü 10 ppm'di (9,18 ± 1,20 mm). En büyük mezensefalon alanı pozitif kontrolde (1,66 ± 0,02 mm²) ve en küçüğü 20 ppm'di (0,73 ± 0,18 mm²). En büyük telensefalon alanı pozitif kontrolde (1,13 ± 0,05 mm²) idi. En büyük göz alanı pozitif kontrolde (1,17±0,07 mm²), en küçük göz alanı ise 20 ppm'de (0,45±0,10 mm²) bulundu. Bu bulgular, propilparabenin tavuk embriyolarında gelişimsel anormalliklere neden olabileceğini düşündürmektedir.

Kaynakça

  • 1. Simorangkir HC, Rusdi B, Suarantika F. Analisis pengawet metilparaben dan propilparaben pada beberapa sediaan toner yang beredar di toko online dengan menggunakan metode spektrofotometri UV-Vis. Bandung Conf Ser Pharm. 2023;50-55.
  • 2. Fransway AF, Fransway PJ, Belsito DV. Parabens. Dermatitis. 2019;30(1):3-31.
  • 3. González-Mariño I, Quintana JB, Rodríguez I, Cela R. Evaluation of the occurrence and biodegradation of parabens and halogenated by-products in wastewater by accurate-mass liquid chromatography-quadrupole-time-of-flight-mass spectrometry (LC-QTOF-MS). Water Res. 2011;45(20):6770-6780.
  • 4. Bereketoglu C, Pradhan A. Comparative transcriptional analysis of methylparaben and propylparaben in zebrafish. Sci Total Environ. 2019;671:129-139.
  • 5. Nishihama Y, Yoshinaga J, Iida A, et al. Association between paraben exposure and menstrual cycle in female university students in Japan. Reprod Toxicol. 2016;63:107-113.
  • 6. Balwierz R, Biernat P, Jasińska-Balwierz A, et al. Potential carcinogens in makeup cosmetics. Int J Environ Res Public Health. 2023;20(6):4780.
  • 7. El Sherbiny D, Wahba MEK. Development and validation of liquid chromatographic methods for the estimation of the acceptance values of some hazardous preservatives in pharmaceutical formulations. A comparative study. J Taibah Univ Sci. 2020;14(1):294-304.
  • 8. Mikula P, Kružíková K, Dobšíková R, Haruštiaková D, Svobodová Z. Influence of propylparaben on vitellogenesis and sex ratio in juvenile zebrafish (Danio rerio). Acta Vet Brno. 2009;78(2):319-326.
  • 9. Tregaskes CA, Kaufman J. Chickens as a simple system for scientific discovery: The example of the MHC. Mol Immunol. 2021;135:12-20.
  • 10. Blake JP, Hess KS. Chicken embryo development. Tuscaloosa, USA: Alabama University;2011.
  • 11. Ribatti D, Annese T. Chick embryo in experimental embryology and more. Pathol Res Pract. 2023;245:154478.
  • 12. Hill M.A. Embryology carnegie stage comparison. Accessed May 8, 2025. https://embryology.med.unsw.edu.au/embryology/index.php/Carnegie_Stage_Comparison.
  • 13. Institutional Animal Care and Use Committee. Policies and procedures of University of Louisville. Accessed May 6, 2025. https://louisville.edu/research/iacuc/policy-files/UseofChickenAvianEmbryos.
  • 14. ACUC Guideline. The use and euthanasia procedures of chicken/avian embryos. Accessed May 6, 2025. https://www.cpp.edu/research/research-compliance/iacuc/docs/iacuc-guidelines-on-euthanasia-of-chicken-and-embryos.pdf.
  • 15. Pratama SF, Ana ID, Retnoaji B. The effect of Carbonate Hydroxyapatite (CHA) dental implant material on the early development of zebrafish embryos (Danio rerio). In: 3rd KOBI Congress, International and National Conferences (KOBICINC 2020). Atlantis Press; 2021:307-312.
  • 16. Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. J Morphol. 1951;88(1):49-92.
  • 17. Saragih HTTSSG, Empra DEP, Rahmadian D, et al. Congenital malformations in chicken embryos after oxybenzone exposure. Hayati J Biosci. 2025;32(3):589-598.
  • 18. Boleli IC, Morita VS, Matos JB Jr, Thimotheo M, Almeida VR. Poultry egg incubation: integrating and optimizing production efficiency. Rev Bras Cienc Avic. 2016;18(spe 2):1-16.
  • 19. Henshel DS, DeWitt J, Troutman A. Using chicken embryos for teratology studies. Curr Protoc Toxicol. 2002;14(1):13-4.
  • 20. Wachholz GE, Varela APM, Teixeira TF, et al. Zika virus‐ induced brain malformations in chicken embryos. Birth Defects Res. 2021;113(1):22-31.
  • 21. Saragih HTSSG, Primahesa A, Oktaviana S, et al. The effect of paracetamol on the development of chicken embryos. Biol Med Nat Prod Chem. 2024;13(2):559-564.
  • 22. Abràmoff MD, Magalhães PJ, Ram SJ. Image processing with ImageJ. Biophotonics Int. 2004;11(7):36-42.
  • 23. Utomo H. Perbandingan tabel mortalita Indonesia dan tabel mortalita CSO menggunakan uji Mann-Whitney dan uji Kruskal-Wallis. Syntax Literate J Ilm Indones. 2021;6(3):1210-1215.
  • 24. Stern CD. The chick embryo-past, present and future as a model system in developmental biology. Mech Dev. 2004;121:1011-1013.
  • 25. Roto SM, Kwon YM, Ricke SC. Applications of in ovo technique for the optimal development of the gastrointestinal tract and the potential influence on the establishment of its microbiome in poultry. Front Vet Sci. 2016;3:63.
  • 26. Perugini M, Merola C, Amorena M, D'Angelo M, Cimini A, Benedetti E. Sublethal exposure to propylparaben leads to lipid metabolism impairment in zebrafish early-life stages. J Appl Toxicol. 2020;40 (4):493-503.
  • 27. Kodani SD, Overby HB, Morisseau C, Chen J, Zhao L, Hammock BD. Parabens inhibit fatty acid amide hydrolase: a potential role in paraben-enhanced 3T3-L1 adipocyte differentiation. Toxicol Lett. 2016;262:92-99.
  • 28. Merola C, Lai O, Conte A, et al. Toxicological assessment and developmental abnormalities induced by butylparaben and ethylparaben exposure in zebrafish early-life stages. Environ Toxicol Pharmacol. 2020;80:103504.
  • 29. Costa JR, Campos MS, Lima RF, et al. Endocrine-disrupting effects of methylparaben on the adult gerbil prostate. Environ Toxicol. 2017;32(6):1801-1812.
  • 30. Gaidhani PM, Chakraborty S, Ramesh K, Chellam PV, van Hullebusch, ED. Molecular interactions of paraben family of pollutants with embryonic neuronal proteins of Danio rerio: a step ahead in computational toxicity towards adverse outcome pathway. Chemosphere. 2024;351:141155.
  • 31. Yang C, Lim W, Bazer FW, Song G. Butyl paraben promotes apoptosis in human trophoblast cells through increased oxidative stress-induced endoplasmic reticulum stress. Environ Toxicol. 2018;33(4):436-445.
  • 32. Guo Y, Yang Y, Zhou Z, et al. Propylparaben induces reproductive toxicity in human extravillous trophoblast cells via apoptosis and cell cycle pathways. Environ Health. 2024;2(5):301-310.
  • 33. Lite C, Guru A, Juliet M, Arockiaraj J. Embryonic exposure to butylparaben and propylparaben induced developmental toxicity and triggered anxiety-like neurobehavioral response associated with oxidative stress and apoptosis in the head of zebrafish larvae. Environ Toxicol. 2022;37(8):1988-2004.
  • 34. Kolšek K, Mavri J, Sollner Dolenc M, Gobec S, Turk S. Endocrine disruptome - an open source prediction tool for assessing endocrine disruption potential through nuclear receptor binding. J Chem Inf Model. 2014;54(4):1254-1267.
  • 35. Cohen A, Popowitz J, Delbridge-Perry M, Rowe CJ, Connaughton VP. The role of estrogen and thyroid hormones in zebrafish visual system function. Front Pharmacol. 2022;13:837687.
  • 36. Gölz L, Baumann L, Pannetier P, Braunbeck T, Knapen D, Vergauwen L. AOP Report: Thyroperoxidase inhibition leading to altered visual function in fish via altered retinal layer structure. Environ Toxicol Chem. 2022;41(11):2632-2648.
  • 37. Shibata M, Makihara N, Iwasawa A. The yolk sac’s essential role in embryonic development. Rev Agric Sci. 2023;11:243-258.

Propylparaben Induced Embryonic Developmental Abnormalities in Chicken (Gallus gallus gallus, Linnaeus 1758)

Yıl 2025, Cilt: 20 Sayı: 3, 117 - 125, 25.12.2025
https://doi.org/10.17094/vetsci.1696554

Öz

Propylparaben is widely used as a preservative in food, cosmetics, and pharmaceuticals. Concerns regarding its potential teratogenic effects have been raised. This study investigates the teratogen effects of propylparaben on chicken embryo development. The eggs were incubated at 36.8°C for 68 hours in a horizontal position. Chicken embryos aged 68 hours were divided into six groups: positive control (0.9% NaCl), negative control Dimethyl Sulfoxide (DMSO), propylparaben at the concentration of 1, 5, 10, and 20 ppm. Each group consisted of 3 embryos. Following treatment, the embryos were incubated for an additional 24 hours, leading to a total incubation time of 92 hours. Data were analyzed using descriptive-comparative approach. Statistical analysis was performed using SPSS 25 software, employing One-way ANOVA followed by Duncan test for parametric data and Kruskal-Wallis followed by Mann-Whitney U test for non-parametric data (P ≤ .05). The results showed propylparaben causes abnormalities in mesencephalon and telencephalon, showed by incomplete closure and reduced body length. The positive control (0.9% NaCl) had the largest body length (18.97 ± 1.56 mm), while the smallest was at 10 ppm (9.18 ± 1.20 mm). The largest mesencephalon area was in the positive control (1.66 ± 0.02 mm²), and the smallest in 20 ppm (0.73 ± 0.18 mm²). The largest telencephalon area was in the positive control (1.13 ± 0.05 mm²). The largest eye area was in the positive control (1.17 ± 0.07 mm²) and the smallest in 20 ppm (0.45 ± 0.10 mm²). These findings suggest that propylparaben may induce developmental abnormalities in chicken embryos.

Teşekkür

Dear Editors of Veterinary Science and Practices, We sincerely thank you for the opportunity to submit our manuscript entitled "Propylparaben Induced Embryonic Developmental Abnormalities in Chicken (Gallus gallus gallus, Linnaeus 1758)." It is an honor to contribute our work to your esteemed journal. We appreciate your time and consideration. We hope that our research findings will be a valuable addition to the field of veterinary anatomy and physiology. We look forward to your feedback.

Kaynakça

  • 1. Simorangkir HC, Rusdi B, Suarantika F. Analisis pengawet metilparaben dan propilparaben pada beberapa sediaan toner yang beredar di toko online dengan menggunakan metode spektrofotometri UV-Vis. Bandung Conf Ser Pharm. 2023;50-55.
  • 2. Fransway AF, Fransway PJ, Belsito DV. Parabens. Dermatitis. 2019;30(1):3-31.
  • 3. González-Mariño I, Quintana JB, Rodríguez I, Cela R. Evaluation of the occurrence and biodegradation of parabens and halogenated by-products in wastewater by accurate-mass liquid chromatography-quadrupole-time-of-flight-mass spectrometry (LC-QTOF-MS). Water Res. 2011;45(20):6770-6780.
  • 4. Bereketoglu C, Pradhan A. Comparative transcriptional analysis of methylparaben and propylparaben in zebrafish. Sci Total Environ. 2019;671:129-139.
  • 5. Nishihama Y, Yoshinaga J, Iida A, et al. Association between paraben exposure and menstrual cycle in female university students in Japan. Reprod Toxicol. 2016;63:107-113.
  • 6. Balwierz R, Biernat P, Jasińska-Balwierz A, et al. Potential carcinogens in makeup cosmetics. Int J Environ Res Public Health. 2023;20(6):4780.
  • 7. El Sherbiny D, Wahba MEK. Development and validation of liquid chromatographic methods for the estimation of the acceptance values of some hazardous preservatives in pharmaceutical formulations. A comparative study. J Taibah Univ Sci. 2020;14(1):294-304.
  • 8. Mikula P, Kružíková K, Dobšíková R, Haruštiaková D, Svobodová Z. Influence of propylparaben on vitellogenesis and sex ratio in juvenile zebrafish (Danio rerio). Acta Vet Brno. 2009;78(2):319-326.
  • 9. Tregaskes CA, Kaufman J. Chickens as a simple system for scientific discovery: The example of the MHC. Mol Immunol. 2021;135:12-20.
  • 10. Blake JP, Hess KS. Chicken embryo development. Tuscaloosa, USA: Alabama University;2011.
  • 11. Ribatti D, Annese T. Chick embryo in experimental embryology and more. Pathol Res Pract. 2023;245:154478.
  • 12. Hill M.A. Embryology carnegie stage comparison. Accessed May 8, 2025. https://embryology.med.unsw.edu.au/embryology/index.php/Carnegie_Stage_Comparison.
  • 13. Institutional Animal Care and Use Committee. Policies and procedures of University of Louisville. Accessed May 6, 2025. https://louisville.edu/research/iacuc/policy-files/UseofChickenAvianEmbryos.
  • 14. ACUC Guideline. The use and euthanasia procedures of chicken/avian embryos. Accessed May 6, 2025. https://www.cpp.edu/research/research-compliance/iacuc/docs/iacuc-guidelines-on-euthanasia-of-chicken-and-embryos.pdf.
  • 15. Pratama SF, Ana ID, Retnoaji B. The effect of Carbonate Hydroxyapatite (CHA) dental implant material on the early development of zebrafish embryos (Danio rerio). In: 3rd KOBI Congress, International and National Conferences (KOBICINC 2020). Atlantis Press; 2021:307-312.
  • 16. Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. J Morphol. 1951;88(1):49-92.
  • 17. Saragih HTTSSG, Empra DEP, Rahmadian D, et al. Congenital malformations in chicken embryos after oxybenzone exposure. Hayati J Biosci. 2025;32(3):589-598.
  • 18. Boleli IC, Morita VS, Matos JB Jr, Thimotheo M, Almeida VR. Poultry egg incubation: integrating and optimizing production efficiency. Rev Bras Cienc Avic. 2016;18(spe 2):1-16.
  • 19. Henshel DS, DeWitt J, Troutman A. Using chicken embryos for teratology studies. Curr Protoc Toxicol. 2002;14(1):13-4.
  • 20. Wachholz GE, Varela APM, Teixeira TF, et al. Zika virus‐ induced brain malformations in chicken embryos. Birth Defects Res. 2021;113(1):22-31.
  • 21. Saragih HTSSG, Primahesa A, Oktaviana S, et al. The effect of paracetamol on the development of chicken embryos. Biol Med Nat Prod Chem. 2024;13(2):559-564.
  • 22. Abràmoff MD, Magalhães PJ, Ram SJ. Image processing with ImageJ. Biophotonics Int. 2004;11(7):36-42.
  • 23. Utomo H. Perbandingan tabel mortalita Indonesia dan tabel mortalita CSO menggunakan uji Mann-Whitney dan uji Kruskal-Wallis. Syntax Literate J Ilm Indones. 2021;6(3):1210-1215.
  • 24. Stern CD. The chick embryo-past, present and future as a model system in developmental biology. Mech Dev. 2004;121:1011-1013.
  • 25. Roto SM, Kwon YM, Ricke SC. Applications of in ovo technique for the optimal development of the gastrointestinal tract and the potential influence on the establishment of its microbiome in poultry. Front Vet Sci. 2016;3:63.
  • 26. Perugini M, Merola C, Amorena M, D'Angelo M, Cimini A, Benedetti E. Sublethal exposure to propylparaben leads to lipid metabolism impairment in zebrafish early-life stages. J Appl Toxicol. 2020;40 (4):493-503.
  • 27. Kodani SD, Overby HB, Morisseau C, Chen J, Zhao L, Hammock BD. Parabens inhibit fatty acid amide hydrolase: a potential role in paraben-enhanced 3T3-L1 adipocyte differentiation. Toxicol Lett. 2016;262:92-99.
  • 28. Merola C, Lai O, Conte A, et al. Toxicological assessment and developmental abnormalities induced by butylparaben and ethylparaben exposure in zebrafish early-life stages. Environ Toxicol Pharmacol. 2020;80:103504.
  • 29. Costa JR, Campos MS, Lima RF, et al. Endocrine-disrupting effects of methylparaben on the adult gerbil prostate. Environ Toxicol. 2017;32(6):1801-1812.
  • 30. Gaidhani PM, Chakraborty S, Ramesh K, Chellam PV, van Hullebusch, ED. Molecular interactions of paraben family of pollutants with embryonic neuronal proteins of Danio rerio: a step ahead in computational toxicity towards adverse outcome pathway. Chemosphere. 2024;351:141155.
  • 31. Yang C, Lim W, Bazer FW, Song G. Butyl paraben promotes apoptosis in human trophoblast cells through increased oxidative stress-induced endoplasmic reticulum stress. Environ Toxicol. 2018;33(4):436-445.
  • 32. Guo Y, Yang Y, Zhou Z, et al. Propylparaben induces reproductive toxicity in human extravillous trophoblast cells via apoptosis and cell cycle pathways. Environ Health. 2024;2(5):301-310.
  • 33. Lite C, Guru A, Juliet M, Arockiaraj J. Embryonic exposure to butylparaben and propylparaben induced developmental toxicity and triggered anxiety-like neurobehavioral response associated with oxidative stress and apoptosis in the head of zebrafish larvae. Environ Toxicol. 2022;37(8):1988-2004.
  • 34. Kolšek K, Mavri J, Sollner Dolenc M, Gobec S, Turk S. Endocrine disruptome - an open source prediction tool for assessing endocrine disruption potential through nuclear receptor binding. J Chem Inf Model. 2014;54(4):1254-1267.
  • 35. Cohen A, Popowitz J, Delbridge-Perry M, Rowe CJ, Connaughton VP. The role of estrogen and thyroid hormones in zebrafish visual system function. Front Pharmacol. 2022;13:837687.
  • 36. Gölz L, Baumann L, Pannetier P, Braunbeck T, Knapen D, Vergauwen L. AOP Report: Thyroperoxidase inhibition leading to altered visual function in fish via altered retinal layer structure. Environ Toxicol Chem. 2022;41(11):2632-2648.
  • 37. Shibata M, Makihara N, Iwasawa A. The yolk sac’s essential role in embryonic development. Rev Agric Sci. 2023;11:243-258.
Toplam 37 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Veteriner Anatomi ve Fizyoloji
Bölüm Araştırma Makalesi
Yazarlar

Hendry Saragih 0000-0003-0696-6191

Shuha Ma'muriyah Halim 0009-0003-9203-0476

Siti Aeniah 0009-0005-8102-776X

Wiwin Ariesti 0009-0007-2729-0780

Fianicha Shalihah 0009-0005-9459-6865

Desti Rahmadian 0009-0002-4863-9375

Ardaning Nuriliani 0000-0001-6782-4694

Gönderilme Tarihi 10 Mayıs 2025
Kabul Tarihi 31 Ekim 2025
Yayımlanma Tarihi 25 Aralık 2025
Yayımlandığı Sayı Yıl 2025 Cilt: 20 Sayı: 3

Kaynak Göster

APA Saragih, H., Halim, S. M., Aeniah, S., … Ariesti, W. (2025). Propylparaben Induced Embryonic Developmental Abnormalities in Chicken (Gallus gallus gallus, Linnaeus 1758). Veterinary Sciences and Practices, 20(3), 117-125. https://doi.org/10.17094/vetsci.1696554
AMA Saragih H, Halim SM, Aeniah S, vd. Propylparaben Induced Embryonic Developmental Abnormalities in Chicken (Gallus gallus gallus, Linnaeus 1758). Veterinary Sciences and Practices. Aralık 2025;20(3):117-125. doi:10.17094/vetsci.1696554
Chicago Saragih, Hendry, Shuha Ma’muriyah Halim, Siti Aeniah, Wiwin Ariesti, Fianicha Shalihah, Desti Rahmadian, ve Ardaning Nuriliani. “Propylparaben Induced Embryonic Developmental Abnormalities in Chicken (Gallus gallus gallus, Linnaeus 1758)”. Veterinary Sciences and Practices 20, sy. 3 (Aralık 2025): 117-25. https://doi.org/10.17094/vetsci.1696554.
EndNote Saragih H, Halim SM, Aeniah S, Ariesti W, Shalihah F, Rahmadian D, Nuriliani A (01 Aralık 2025) Propylparaben Induced Embryonic Developmental Abnormalities in Chicken (Gallus gallus gallus, Linnaeus 1758). Veterinary Sciences and Practices 20 3 117–125.
IEEE H. Saragih, S. M. Halim, S. Aeniah, W. Ariesti, F. Shalihah, D. Rahmadian, ve A. Nuriliani, “Propylparaben Induced Embryonic Developmental Abnormalities in Chicken (Gallus gallus gallus, Linnaeus 1758)”, Veterinary Sciences and Practices, c. 20, sy. 3, ss. 117–125, 2025, doi: 10.17094/vetsci.1696554.
ISNAD Saragih, Hendry vd. “Propylparaben Induced Embryonic Developmental Abnormalities in Chicken (Gallus gallus gallus, Linnaeus 1758)”. Veterinary Sciences and Practices 20/3 (Aralık2025), 117-125. https://doi.org/10.17094/vetsci.1696554.
JAMA Saragih H, Halim SM, Aeniah S, Ariesti W, Shalihah F, Rahmadian D, Nuriliani A. Propylparaben Induced Embryonic Developmental Abnormalities in Chicken (Gallus gallus gallus, Linnaeus 1758). Veterinary Sciences and Practices. 2025;20:117–125.
MLA Saragih, Hendry vd. “Propylparaben Induced Embryonic Developmental Abnormalities in Chicken (Gallus gallus gallus, Linnaeus 1758)”. Veterinary Sciences and Practices, c. 20, sy. 3, 2025, ss. 117-25, doi:10.17094/vetsci.1696554.
Vancouver Saragih H, Halim SM, Aeniah S, Ariesti W, Shalihah F, Rahmadian D, vd. Propylparaben Induced Embryonic Developmental Abnormalities in Chicken (Gallus gallus gallus, Linnaeus 1758). Veterinary Sciences and Practices. 2025;20(3):117-25.

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