Receıved: 16/12/2025 Aceppted: 14/05/2026 Published: 02/06/2026 UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico 1 of 6 Revista Cienﬁca, FCV-LUZ / Vol. XXXVI hps://doi.org/10.52973/rcfcv-e362879 Hypoderma spp. ınvesgaon of dynamıc Thıol dısulde balance ın ınfested cale Invesgacıón del equılıbrıo dınámıco Tıol-Dısulfuro en ganado ınfestado con Hypoderma spp Şemistan Kiziltepe 1 * , Fatma Ertaş-Oğuz 1 , Oğuz Merhan 2 , Erdoğan Uzlu 3 ¹Iğdır University Tuzluca Vocaonal School, Iğdır / Türkiye. ²Kaas University, Faculty of Veterinary Medicine, Department of Biochemistry, Kars, Türkiye. ³Balıkesir University, Faculty of Veterinary Medicine, Department of Veterınary Internal Dıseases, Balıkesir/ Türkiye. *Correspondence author: semistan.kiziltepe@igdir.edu.tr ABSTRACT Hipodermiasis in cale is a parasic disease caused by Hypoderma bovis and Hypoderma lineatum type ﬂy larvae. The disease, which mostly aﬀects young cale, causes economic losses such as developmental delay, decrease in meat and milk yield, and inability to use the back skin as a result of being punctured by the larvae. This study aimed to determine serum total thiol, nave thiol, disulﬁde, interleukin-1, IL-6, and tumor necrosis factor-α levels in Hypoderma-infested cale. In the study, 15 Hypoderma infested cale diagnosed by clinical examinaon and 10 healthy cale for control purposes were used. Serum total thiol, nave thiol and disulphide levels of the sick animals were determined as 406.84 ± 8.33 μmol/L, 297.62 ± 5.24 μmol/L, 54.61 ± 4.83 μmol/L, respecvely. interleukin-1, interleukin-6 and tumor necrosis factor-α were detected as 41.98 ± 4.37 pg/mL, 94.11 ± 8.49 pg/mL, 82.29 ± 9.12 pg/mL in infested animals. Total thiol, nave thiol and disulﬁde values of infested animals were determined to be lower than the healthy control group, and interleukin-1, interleukin-6, and tumor necrosis factor-α were higher than those of healthy animals. As a result, interleukin-1, interleukin-6, and tumor necrosis factor-α values were determined to be high, and total thiol and nave thiol levels were low in cale with hipodermiasis. Key words: Hipodermiasis; interleukin-1; interleukin-6; nave thiol; bovine; tumor necrosis factor-α; total thiol. RESUMEN Hipodermiasis en el ganado es una enfermedad parasitaria causada por larvas de moscas de los pos Hypoderma bovis e Hypoderma lineatum. La enfermedad, que afecta principalmente al ganado joven, provoca pérdidas económicas como retraso en el desarrollo, disminución en la producción de carne y leche, y la incapacidad de usar la piel del lomo debido a las perforaciones causadas por las larvas. El objevo de este estudio fue determinar los niveles séricos de ol total, ol navo, disulfuro, interleucina-1, IL-6 y factor de necrosis tumoral- α en ganado infestado con Hypoderma. En el estudio se ulizaron 15 bovinos infestados con Hypoderma, diagnoscados mediante examen clínico, y 10 bovinos sanos como grupo control. Los niveles séricos de ol total, ol navo y disulfuro de los animales enfermos se determinaron como 406.84 ± 8.33 μmol/L, 297.62 ± 5.24 μmol/L, 54.61 ± 4.83 μmol/L respecvamente. interleucina-1, interleucina-6 y factor de necrosis tumoral- α se detectaron como 41.98±4.37 pg/ mL, 94.11 ± 8.49 pg/mL, 82.29 ± 9.12 pg/mL en los animales infestados. Los valores de ol total, ol navo y disulfuro de los animales infestados se determinaron como más bajos que los del grupo control sano, y los de interleucina-1, interleucina-6 y factor de necrosis tumoral- α fueron más altos que los de los animales sanos. Como resultado, los valores de interleucina-1, interleucina-6 y factor de necrosis tumoral- α se determinaron como altos, y los niveles de ol total y ol navo como bajos en el ganado con hipodermiasis. Palabras clave: Hipodermiasis; interleucina-1; interleucina-6; ol navo; bovino; factor de necrosis tumoral- α; ol total.

Hypoderma spp. ın ınfested cale / Kiziltepe et al. UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico INTRODUCTION Hypodermosis is a parasic disease caused by the larval stage of ﬂies belonging to the Hypoderma genus (Diptera, Oestridae) in cale (Bos taurus) and progresses with myiasis. Since Hypoderma bovis and Hypoderma lineatum are characterized by the presence of limited and disnct subcutaneous swellings made by the larvae on the back and waist region of cale, they can be easily detected by palpaon (clinical parasitological examinaon) on the backs of animals in spring and summer [1]. In cale aﬀected by the disease, signiﬁcant economic losses occur due to a signiﬁcant decrease in meat and milk yield, growth retardaon and irreversible damage to the skin. In addion, it is extremely diﬃcult to evaluate the possible stress caused by hipodermiasis and the immunosuppression eﬀect that may result from it, as well as the economic losses that may be caused by secondary infecons caused by bacteria, viruses, etc [2]. Development of hipodermiasis; First, the ﬁrst stage larvae (L1) of adult ﬂies penetrate the skin by deposing them on the hind legs, hind ankles and lower abdominal area of cale. In this region, they cross the skin with L1 enzymac secreons. L1, which crosses the skin, passes through the host connecve ssue. They then move through the subcutaneous ssues and migrate under the back skin. It may take 8-10 months for the larva to enter the body, migrate and leave [2]. It has been reported that the migraon of the larvae and, most recently, myiasis, which is characterized by subcutaneous boils on the back and waist of the animals during the summer months, cause inﬂammaon and stress in the host [2]. It has been reported that parasic factors cause inﬂammaon. In chronic inﬂammaon, proinﬂammatory cytokines are released from macrophages in the vascular wall. A signiﬁcant poron of these cytokines are interleukins [3]. Of these, interleukin (IL)- 1, IL-6 and tumor necrosis factor-α (TNF-α) acvate immune system cells [4 , 5]. TNF-α causes the secreon of cytokines and chemokines and the migraon and proliferaon of lymphocytes to the inﬂammaon site [6]. IL-1, in conjuncon with TNF-α, is a pro-inﬂammatory cytokine that can aﬀect almost every cell type [7]. IL-6 is both a pro- and an-inﬂammatory cytokine that has been associated with disease states and is produced by various cell types in situaons of infecon and trauma [8]. It has been determined that as a result of inﬂammaon resulng from increased skin-subcutaneous-connecve ssue damage in cale with hipodermiasis, endothelial damage, dysfuncon and oxidave stress occur due to this process [9 , 10 , 11]. It is eﬀecve in ssue damage through mechanisms such as lipid peroxidaon and protein oxidaon. An important reason for decreased anoxidant levels in the body is increases in free radicals or reacve oxygen species. These increases lead to imbalance and as a result oxidave stress occurs. It has been demonstrated by frequent studies in recent years that oxidave stress plays a role in the pathological process of many diseases in Veterinary Medicine [11]. At the cellular level, proteins funcon not only as structural building blocks but also as sensive molecular machines that respond to environmental changes. The dynamic funcons and structural integrity of proteins depend on the delicate redox balance provided by the sulfur-containing amino acids cysteine and methionine. The sulydryl (-SH) groups of these amino acids act as molecular sensors that detect oxidave changes in the cellular microenvironment [12 , 13]. Under oxidave stress condions, an increase in reacve oxygen species such as hydrogen peroxide targets these sensive sensors, iniang the oxidaon process. In the inial stage of the reacon, the -SH groups convert into sulfonic acid, an unstable and highly reacve form. As long as oxidave stress persists, the conversion of these structures into disulﬁde bonds acts as a molecular shield that protects the protein from permanent damage and maintains its funconal integrity. The thiol-disulﬁde homeostasis maintained by the reconversion of these disulﬁde bonds back into thiol groups via cellular reducve mechanisms serves not only as an early indicator of protein oxidaon but also as a crical adapve strategy for cellular survival [12 , 14]. This dynamic balance serves as a vital control mechanism in fundamental processes regulang cellular homeostasis, such as apoptosis, regulaon of enzymac acvity, anoxidant defense, and detoxiﬁcaon [13 , 14 , 15 , 16]. Changes in thiols and pro- inﬂammatory cytokines observed in parasic infecons such as hypodermosis are a systemic reﬂecon of these complex oxidave and inﬂammatory processes. Although the role of this mechanism in pathophysiological processes has been elucidated by extensive literature in human medicine, research on the clinical and pathophysiological signiﬁcance of this biochemical balance in the ﬁeld of veterinary medicine remains limited. This study aims to evaluate the systemic response that develops secondary to ssue damage caused by parasite larvae during the seasonal phase of hypodermosis, focusing on changes in the pro-inﬂammatory cytokine proﬁle (TNF-α, IL-1, IL-6) and in thiol-disulﬁde homeostasis, a sensive indicator of protein oxidaon. MATERIALS AND METHODS Ethical Statement The protocol for this research was formally sanconed by the Local Ethics Commiee for Animal Experiments at Kaas University (Reference: KAU-HADYEK/2021-080). Animal Selecon The presence of hypodermiasis in cale in Türkiye has been documented in various studies [17 , 18]. Since it has been reported that acquired immunity develops in cale exposed to Hypoderma spp. twice or more, this study was speciﬁcally conducted on animals naturally exposed to the disease for the ﬁrst me [19 , 20 , 21 , 22]. Furthermore, it has been reported that the number of warbles signiﬁcantly aﬀects the biochemical parameters obtained from such studies [20]. Based on this literature, animals presenng with 4 to 10 warbles on their dorsal and lumbar regions were preferred for the study. Animal Material The study involved a total of 25 cale, aged 18–24 months. The experimental group consisted of 15 animals naturally infested with 8–10 Hypoderma spp. larvae (warbles), while 10 healthy cale served as the control group. The sample size for the control group (n = 10) was determined following the 2 of 6

Revista Cienﬁca, FCV-LUZ / Vol. XXXV UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico ethical principle of ‘Reducon’ in animal research. Given the high homogeneity and low standard deviaon of biochemical parameters typically observed in healthy animals, this sample size was deemed suﬃcient to establish a stascally reliable baseline. In contrast, 15 animals were included in the infested group to beer account for potenal variaons in individual clinical and biochemical responses. Stascal analysis conﬁrmed that the diﬀerence in group sizes did not compromise the power or the validity of the results. To obtain serum samples, blood was drawn from the jugular vein and subjected to centrifugaon at 3000 rpm for a duraon of 10 minutes (Zenith Lab LC-04B, China). Separated sera were then transferred to storage at -80 °C (Esco Lexicon® UUS-48OB- 1-5D, Singapore) to maintain stability unl biochemical proﬁling. The age, gender, care and feeding condions of the animals included in the study were the same. Biochemical analysis Serum thiol concentraons were measured using the colorimetric spectrophotometric technique described by Erel and Neselioglu [13] with an Agilent Technologies Cary 60 UV-Vis system (USA). Addionally, pro-inﬂammatory cytokines (TNF-α, IL-1, and IL-6) were measured using commercial ELISA kits (BT Lab, China) following the manufacturer’s instrucons. Stascal analysis Data were processed using SPSS 20.0. Normal distribuon was conﬁrmed, and an independent t-test was ulized for comparisons. Results are presented as mean ± standard deviaon, with signiﬁcance set at P < 0.05. RESULTS AND DISCUSSION In the measurements made; While a general decrease was detected in the values for thiol/disulﬁde balance, stascally signiﬁcant decreases were determined only in total thiol and nave thiol values. The values obtained from the infested hypodermic group and the control group are given in TABLE I. TABLE I Total thiol, Nave thiol, Disulﬁde levels in Hypodermic Cale Parameters Infested group Control group P TT (μmol/L) 406.84 ± 8.33 459.25 ± 16.20 P < 0.01 NT (μmol/L) 297.62 ± 5.24 327.68 ± 11.72 P < 0.05 Ds (μmol/L) 54.61 ± 4.83 65.78 ± 6.89 NS Ds/NT (%) 18.66 ± 1.86 20.58 ± 2.36 NS Ds/TT (%) 13.24 ± 0.93 14.04 ± 1.18 NS NT/TT (%) 73.52 ± 1.86 71.93 ± 2.35 NS NT - nave thiol, TT - total thiol, Ds - disulﬁde, Data are presented as the mean ± SD, NS: no signiﬁcavo In the study, TNF-α, IL-1 and IL-6 parameters obtained from the Hypoderma group were found to be stascally signiﬁcantly higher than the control group. The values obtained from the hypodermic group and the control group are given in TABLE II. TABLE II Interleukin-1, Interleukin-6 and Tumor Necrosis Factor- α Parameters in Hypodermic Cale Parameters Control group Infested P TNF-α (pg/mL) 82.29 ± 9.12 177.78 ± 9.62 P < 0.001 IL-1 (pg/mL) 41.98 ± 4.37 149.80 ± 8.88 P < 0.001 IL-6 (pg/mL) 94.11 ± 8.49 129.69 ± 5.02 P < 0.01 TNF-α- tumor necrosis factor-alpha,IL-1- interleukin-1, IL-6- interleukin-6. These study demonstrates that a signiﬁcant shiﬅ in the thiol- disulﬁde balance leads to systemic oxidave stress characterized by increased protein oxidaon which drives the pathological process of hypodermosis. These ﬁndings are consistent with the exisng literature indicang that physiological abnormalies trigger free radical producon [11 , 23]. Furthermore, the crical role of thiol-disulﬁde homeostasis in apoptosis, anoxidant defense, and intracellular signaling [24 , 25 , 26 , 27] underscores the systemic impact of the infecon. These results demonstrate that this balance is not only aﬀected in human diseases [16 , 10 , 28], but also funcons as a sensive diagnosc marker for oxidave damage in cale with hypodermosis, providing further evidence of the clinical importance of thiol groups in pathological condions. In Veterinary Medicine; in calves dehorned with hot cautery [19], in dogs (Canis lupus familiaris) with distemper [29], in sheep (Ovis aries) with gastrointesnal nematodes [30], in sheep with toxoplasmosis [31]. Studies have reported that nave thiol (NT) and total thiol (TT) levels are low. In the same studies, disulphide (Ds), disulphide/nave thiol (Ds/NT), disulphide/total thiol (Ds/ TT) were reported to be high. Among the reported results, NT, TT and Ds levels obtained from sheep infested with sarcopc mange, which has high dermatological eﬀects, decreased and there was no diﬀerence in Ds/NT, Ds/TT and nave thiol / total thiol (NT/TT) raos [32]. Unlike these studies, Deveci and Erdal [33] found an increase in NT and TT levels in cale foot diseases. Studies conducted in recent years show an increase in reacve oxygen species as well as a decrease in plasma thiol concentraon as an indicator of oxidave stress [31 , 34 , 35]. In the presented study, it was determined that NT and TT values of the infested group were low. It is thought that the decrease in TT and NT levels obtained in this study can be explained by ssue damage caused by subcutaneous factors, strong oxidave stress caused by inﬂammaon, and the severity of thiol oxidaon aﬀected by oxidave stress, as noted in the studies of other researchers. The formaon of subepidermal tunnels during the developmental period of hypoderma larvae causes myiasis subcutaneous inﬂammaon accompanied by raised and serpenne lesions unl they leave the animal. As a defense reacon against parasites that cause ssue damage, pro-inﬂammatory cytokines such as TNF-α, IL-1 and IL-6 are released from acvated leukocytes in the region and from macrophages in the vessel wall as a result of chronic inﬂammaon. IL-1 plays an important role in the iniaon of inﬂammaon in the pathogenesis of skin diseases. It has been reported that levels of IL-1, its derivaves IL-1α and IL-1β, increase in humans infested with scabies mites [36]. In a study conducted in cale with anaplasma, it was determined that there was an increase in IL-6 level. It is stated 3 of 6

Hypoderma spp. ın ınfested cale / Kiziltepe et al. UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico that this increase is caused by the smulaon of macrophages by factors and the increase in the synthesis of pro-inﬂammatory cytokines [37]. In other study conducted in cale with trichophytosis, it was reported that TNF-α, IL-1 and IL-6 values were stascally signiﬁcantly higher than the control group [38]. In this study, IL-1 and IL-6 were found to be stascally higher and more signiﬁcant compared to the control group, which is thought to be due to the inﬂammaon that occurs as a result of the migraon of the larva and the perforaon in the skin. Tumor necrosis factor-α is one of the ﬁrst immune mediators released from acvated T cells and macrophages as a pro-inﬂammatory cytokine [5 , 39]. TNF-α is the predominant cytokine in bovine serum. In a study where TNF-α was used to monitor the prognosis of cale with mass, it was reported that the serum TNF-α level of sick animals was signiﬁcantly increased [40]. High TNF-α levels in the skin and serum of hypoderma- infested cale have been reported in studies [41]. It has been reported that there is an increase in cytokines aﬅer boils appear on the back in cale infested with H. lineatum [42]. In this study, 4-8 larvae were seen on the dorsal areas of young hypodermic cale and healthy samples of the same age were taken as control group. The average levels of TNF-α measured in the blood serum of the paents were determined as 177.78 pg/mL and 82.29 pg/mL, respecvely. The average TNF-α in the control group was determined as 84 pg/mL, according to Ercan et al. [43] are similar to the levels they determined in healthy cale. Similar to the ﬁndings determined in this study, the fact that TNF-α level was measured higher in the hypodermic group compared to the control group shows that TNF-α can be considered a biomarker indicang inﬂammaon in cale [22 , 44]. Tumor necrosis factor-α was found to be higher compared to the control group and this diﬀerence was found to be stascally signiﬁcant. It was determined that the results obtained in the study were compable with the results of previous studies conducted by other researchers. CONCLUSIONS AND IMPLICATIONS This study determined the levels of TT, NT, Ds (and their interacons), TNF-α, and IL-1 to IL-6 in animals with hypodermiasis. It was observed that the thiol-disulﬁde balance shiﬅed towards disulﬁde in hypodermiasis-aﬀected animals, and systemic oxidave damage occurred along with protein oxidaon. 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