Investigation of Aopp, Total Sulphydryl Group (T-sh), Seroplasmin Levels in Sheep Wi̇th Zoonotic Liver Parasitosis

doi:10.21203/rs.3.rs-4194862/v1

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Investigation of Aopp, Total Sulphydryl Group (T-sh), Seroplasmin Levels in Sheep Wi̇th Zoonotic Liver Parasitosis

https://doi.org/10.21203/rs.3.rs-4194862/v1

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The aim of inthe present study was to investigate aopp, total sulfhydryl group (t-sh) and seroplasmin levels in zoonotic liver parasitosis in sheep. this study was carried out in Iğdır province. For this purpose, 75 sheep were grouped as healthy, Fasciola spp., Echinococcus spp., Dicrocoelium spp., Echinococcus spp. + Dicrocoelium spp. The levels of the specified parameters were measured in these groups. According to the results, AOPP level in the fasciolosis group was remarkably higher than all other groups (p < 0.05). The serum AOPP level in the E + D group was found to be significantly higher compared to the control and dicrocoelium spp. groups (p < 0.05). Echinococcus spp. group was s remarkably higher than the dicrocoelium spp. group (p < 0.05). The ceruloplasmin level in the control group was found to be significantly lower compared to the Echinococcosis, fasciolosis and dicrocoeliosis groups (p < 0.05). Total sulfhydryl level was found to be lower in the patient groups compared to the healthy group, but this value was not significant. According to these results, it can be said that cellular damage occurs in liver parasitism. These parameters are thought to be valuable in terms of prognosis in parasitic infections. It is also thought that oxidative cell damage occurs in the attack of zoonotic liver parasites in which the immune response decreases. It is thought that this study will serve as a guide for future research.

Antioxidant

Iğdir

Sheep

Oxidative stress

Parasitos

Parasitic diseases have an important place in small ruminant farming (Ayaz et al., 2006; Ertaş et al., 2022) It is reported that there is a significant morbidity and mortality due to parasitic infections and these diseases in developing or underdeveloped countries in the modern era (Çınar et al., 2018; Ertaş et al., 2022). Moreover, this problem is further complicated by the fact that pets are infected with more than one species at the same time (Ayaz et al., 2006). Parasitic agents that choose the liver as a host in ruminants cause productivity and financial losses in animals. Among these agents, Fasciolosis, a zoonotic disease of humans and livestock, is caused by digenean trematodes, Fasciola hepatica and Fasciola gigantica. The economic effect of fasciolosis in livestock is estimated to be more than 3 billion dollars a year. Globally, this parasite has been recorded to infect 17 million people in endemic areas and 180 million people are at risk of becoming ill (Calvani et al., 2018; Ertaş and Kırmızıgül 2021).

In contrast to Fasciola spp., the zoonotic agent Dicrocoelium dendriticum, also known as "lancet parasite" or "small liver parasite", causes the disease called dicrocoeliosis (Piegari, 2021). Cystic echinococcosis (CE), also known as hydatidosis, is another name for it. Canine worm is one of the most important zoonotic parasitic infections of humans and mammals caused by the larval stage of Echinococcus granulosus. In addition, this disease is of great financial and human health importance on a global scale (Rokni, 2009).

Tissue damage, inflammation and infections in the organism activate many cells with phagocytic activity such as monocytes and macrophages. Phagocytic cells play an important role in live defense. While performing these functions, they generate free radicals (such as hydrogen peroxide, super oxide anion) due to excessive oxygen consumption (Bozukluhan et al., 2016; Çenesiz 2020). Oxidative stress caused by free radicals and reactive oxygen species are involved in the pathogenesis of many tissue-damaging diseases (Ergönül and Kontaş Aşkar, 2009; Erkılıç et al., 2017; Merhan et al., 2020; Ertaş and Kırmızıgül, 2021; Öner et al., 2022).

Protein oxidation can be described as the covalent modification of proteins induced directly by reactive oxygen species such as OH˙, H₂O₂ or indirectly by reaction with secondary products of oxidative stress (Polat, et al., 2012). (AOPP) is another marker of oxidative stress and are advanced oxidation protein products that define oxidative damage in proteins (Bottari et al., 2015). In recent years (AOPP) has come under scrutiny by a number of scientists. They have also been registered as cross-linked protein products containing dtyrosine. Detection of advanced oxidation protein parameters is used to diagnose the degree of protein oxidation (Polat, et al., 2012).

Maintaining a balance in thiol-disulfide homeostasis is crucial, as levels of thiols and disulfides - which serve as markers of overall oxidant status - have been observed to rise during inflammatory infections (Erel and Neşelioğlu, 2014; Üstüner et al., 2018). Thiols, which are also referred to as mercaptans, are a type of organic compounds that contain a sulfhydryl group (-SH) consisting of a sulfur atom, a hydrogen atom, and a carbon atom. Recently, researchers have started to investigate the impact of thiols on protein metabolism and their active role in oxidative stress. Thiols are crucial molecules in protein metabolism within the body and are the first line of defense against oxidative stress as antioxidants. They exist in a state of equilibrium known as dynamic thiol/disulfide homeostasis (Erel and Neşelioğlu, 2014).

Ceruloplasmin (Cp) is a protein that plays a crucial role in transporting copper in the bloodstream (Milanovic et al., 2018). Ceruloplasmin (Cp) is primarily synthesized in the liver, but it can also be produced in other areas of the body, including extrahepatic regions and pulmonary epithelium. Cp plays a crucial role in catalyzing the oxidation of toxic iron. By catalyzing the conversion of ferrous iron (Fe2+) to ferric iron (Fe3+), ceruloplasmin helps to safeguard tissues from damage caused by free radicals (Sevgisunar et al., 2014; Karabulut and Gülay, 2016; Kırmızıgül and Arslan, 2020). Ceruloplasmin also exhibits its protective activity by safeguarding polyunsaturated fatty acids present in erythrocyte membranes from the harmful effects of reactive oxygen species (Karabulut and Gülay, 2016).

The aim of this study was to investigate aopp, total sulfhydryl group (t-sh) and seroplasmin levels in sheep infected with zoonotic liver parasites in Igdir province.

These three parasitic diseases in sheep cause significant liver damage and activate oxidative stress mechanisms. Knowledge of these defense mechanisms is important in understanding pathogenicity and immunity. They are also important markers for monitoring the treatment process. Since these parasites are zoonotic, it is medically important to know the pathogenesis of the diseases caused by these parasites in order to manage disease processes.

Animals

The animal material of the study was carried out in a total of 75 sheep, including 60 patients and 15 controls, which were registered with the Provincial Directorate of Agriculture and Forestry in the center and districts of Igdir and diagnosed with endoparasites.

Clinical examination

Routine examination of the animals whose anamnesis information was obtained before slaughter was performed. Eye mucosa, lymph nodes were checked. Respiration and heart were listened with a stethoscope. Body temperatures were measured with a digital thermometer. The results were documented.

The groups to be used in the study are shown in Table 1(Table 1).

Table 1

Experimental groups
1st group; (n = 15)	2nd group (n = 15)	2nd group (n = 15).	3rd group (n = 15)	4th group (n = 15).
Healthy	Fasciola spp	Echinococcus spp.	Dicrocelium spp.	Echinococcus spp.+Dicrocoelium spp.

Laboratory Diagnostic Methods

Fasciola spp.

Identification was carried out macroscopically in the livers of the slaughtered sheep by looking for the causative agent itself macroscopically or by using the native and sedimentation method and microscopically by looking for eggs in the feces.

Echinococcus spp.

Cyst fluid was extracted from macroscopically detected cysts in the livers of slaughtered sheep with a syringe and this fluid was examined under a microscope.

Dicrocoelium spp

Macroscopic identification of the causative agent itself in the livers of the slaughtered sheep or microscopic identification of the causative agent in the feces by using the native and sedimentation method and microscopic egg detection method.

Echinococcus spp.+Dicrocoelium spp.

Positive for both parasites were accepted.

Biochemical Analysis

Seroplasmin, Thiol Disulfate, AOPP were measured spectrophotometrically.

Statistical Analysis

Descriptive statistics were used to evaluate the parameters between the groups. Data were given as arithmetic mean ± standard deviation (X ± SX). Statistical significance level was accepted as P < 0.05 and SPSS 20.0 statistical package program (SPSS 10.0 for Windows) was used for calculations.

In this study, as a result of the sections taken from the liver and bile ducts of sheep slaughtered in the slaughterhouse, the adult form of fasciola spp is shown in image A and the egg of fasciola spp in the feces taken from the same sheep is shown in image B (Fig. 1).

Table 2 shows the AOPP level in the fasciolosis group was significantly higher than all other groups (p < 0.05). The serum AOPP level in the E + D group was found to be significantly higher compared to the control and Dicrocoelium spp. groups (p < 0.05). The Echinococcus spp. group was significantly higher than the Dicrocoelium spp. group (p < 0.05). Although the serum AOPP level in the Echinococcus spp. group was higher than in the control group, this increase was not found to be significant (p > 0.05). Although the serum AOPP level in the Dicrocoelium spp. group was lower than in the control group, this decrease was not found to be significant (Table 2)

Table 2

*Oxidative stress parameters measure*
Parameter	Groups
Parameter	Healty	Fasciola spp.	Echinococcus spp.	Dicrocoelium spp.	Echinococcus spp.+ Dicrocoelium spp.
AOPP	29.37 ± 3.50 ^a	62.02 ± 4.39 ^b	39.14 ± 15.76 ^a,c	27.66 ± 4.12 ^a	49.30 ± 4.41 ^d,a
^a,b,c,d There is no statistical significance for the parameters in the same row in the table with the same upper letters. If the letters are different, there is meaning.

Table 3 shows, Total sulfdril group (T-SH) level was similar in all groups (p > 0.05) (Table 3)

Table 3

*Measured antioxidant parameters*
Parameter	Groups
Parameter	Healty	Fasciola spp.	Echinococcus spp.	Dicrocoelium spp.	Echinococcus spp. + Dicrocoelium spp.
T-SH	0.49 ± 0.10 ^a	0.49 ± 0.03 ^a	0.44 ± 0.09 ^a	0.42 ± 0.13 ^a	0.47 ± 0.13 ^a
^a There is no statistical significance for the parameters in the same row in the table with the same upper letters. If the letters are different, there is meaning.

In this study Table 4 shows, The ceruloplasmin level in the control group was found to be significantly lower compared to the Echinococcosis, fasciolosis and dicrocoeliosis. groups (p < 0.05). Although the ceruloplasmin level in the control group was lower than in the E + D group, it was not significant (p > 0.05) (Table 4)

Table 4

*Measured positive acute phase protein parameters*
Parameter	Groups
Parameter	Healty	Fasciola spp.	Echinococcus pp.	Dicrocoelium spp.	Echinococcus spp. +Dicrocoelium spp.
Ceruloplasmin	3.63 ± 1.70 ^b	6.81 ± 1.08 ^a	6.67 ± 1.61 ^a	6.20 ± 8.77 ^a	5.54 ± 1.97 ^{a, b}
^a,b There is no statistical significance for the parameters in the same row in the table with the same upper letters. If the letters are different, there is meaning.

Liver parasites cause infections that can be lethal, especially by damaging the bile ducts and liver tissue. If we talk about parasites, the effects of parasitic agents are usually manifested as clinical symptoms such as weakness, loss of appetite, depression, malaise, edema under the chin and abdomen, anemia and jaundice and decreased milk production (Değer and Biçek, 2005; Doğanay, 2017; Acıöz and Aydın, 2020; Ertaş and Kırmızıgül, 2021). Such as the cases we observed in the present is in parallel with the mentioned studies. Parasitic invasions in ruminants cause severe economic losses in these animalsMany parasites similarly have a complex system of host immuno-modulation and immuno-avoidance, Here, a repertoire of proteins is secreted to simultaneously defend against and distract the host's immune reply (Calvani, 2022).

After any kind of tissue damage, whether it's caused by physical, mechanical, or chemical trauma, the body responds with an inflammatory reaction. This same response is also seen in conditions like autoimmune diseases and inflammatory bowel infections. The inflammatory stimuli produced by granulocytes, lymphocytes, and macrophages, such as prostaglandins, reactive oxygen species, and free radicals, can contribute to tissue damage. Additionally, oxidative stress has been linked to impaired immune response in several studies (Abd Ellah, 2013).

The immune response is crucial in protecting the host against parasitic diseases, but it comes with a cost. Building an immune defense requires energy that could otherwise be used for other important functions such as growth, reproductive performance, and sexual signaling. During an immune response, oxidants can be formed in two ways. Firstly, immune cells produce oxidants as part of their cytotoxic activity to eliminate the pathogen. Secondly, oxidants can also be by-products of oxygen consumption, which can contribute to the production of toxic oxidants in addition to the increased metabolic activity during the immune response (Van de Crommenacker et al., 2010).

Although metabolic activity and oxidant production are linked, the relationship is not always straightforward. Animals tend to use alternative methods for mitochondrial respiration to reduce oxidant production. Therefore, parasites may be responsible for oxidant synthesis directly through the degradation products of their own metabolism (Van de Crommenacker et al., 2012). According to a number of studies, levels of reactive oxygen species have been reported to rise in the cells of sick hosts attacked by parasites (Abd Ellah, 2013; Öner at al., 2022). The elevation of free radicals in parasite-infected cells is related to the host's diet, the amount of parasite infestation and the destructive effect on tissue. Parasitic diseases are associated with blood-borne protozoan agents such as Babesiosis, Theileriosis and Trypanosomosis. In addition, Fasciola sp., Eimeria sp. and Trichostrongylus sp. have been reported to be associated with lipid peroxidation, and this assessment provides a guide to parasitic diseases associated with oxidative stress and their deleterious effects (Abd Ellah, 2013).

AOPP is a marker of oxidative stress and an advanced oxidation protein product that identifies oxidative damage in proteins (Bottari et al., 2015). Although different results were obtained in studies in which the change in AOPP level was determined (Polat, et al., 2012). AOPP value was found to be significantly higher in parasitic diseases (Polat, et al., 2012; Bottari et al., 2015; Milanovic et al. 2018). In the currend study particularly Fasciola spp., Echinococcus spp., Dicrocoelium spp. affecting the liver, AOPP level was significantly higher in naturally infected sheep sera compared to the control group. This is in line with Bottari et al., (2015). It was concluded that oxidative stress in the liver increased and protein damage occurred with increasing AOPP level.

The acute phase response is a non-specific response of the individual to different tissue injuries. Acute phase proteins are a group of proteins of varying concentration in animals exposed to external or internal problem such as infection, inflammation, surgical trauma or stress (Nazifi et al., 2009). Ceruloplasmin concentrations are increased in some but not all spontaneous inflammatory diseases. Ceruloplasmin carry copper and are role in iron metabolism. Ceruloplasmin has been described as an acute phase protein in multiple species (Feldman et al., 2000). Ceruloplasmin has functions such as increasing various enzyme (cytochrome C oxidase and Cu-Zn superoxide dismutase) activities with copper, providing higher antimicrobial power in phagocytic cells and protecting against oxidative damage (Bayyit and Merhan, 2020). moreover, ceruloplasmin is an indicator of the presence of infection (Bozukluhan et al., 2016; Bayyit and Merhan, 2020).

Ceruloplasmin, which is involved in the antioxidant system, is a moderately important acute phase protein in addition to its functions such as protecting cells against oxidative damage and antimicrobial activity (Bozukluhan et al., 2020). Bozukluhan et al., (2020) reported that the value of ceruloplasmin was found to be high in sheep with toxoplasmosis, but this was statistically insignificant. Similarly, in another study, Nispet et al., (2008) compared the serum ceruloplasmin level in cattle with echinococcosis with the healthy group and reported that the difference in ceruloplasmin values was insignificant.

In Holstein cattle with bovine tropical theilerosis, it has been shown that there is an increase in serum ceruloplasmin levels as parasitemia increases (Nazifi et al., 2009). Mohammadi et al., (2021) showed that serum ceruloplasmin level was significantly increased in cattle with natural infection of Babesia bigemina in relation to the parasitemia load compared to the control group. In a study in humans with pulmonary cystic echinococcus, the serum ceruloplasmin level of infected humans was shown to be significantly higher compared to healthy controls, and it was reported that the serum ceruloplasmin level of infected constructs decreased significantly after surgical intervention compared to the value before surgery. It has been suggested that chronic inflammation may cause this increase and may be an immune response of the host (Mohammadi et al., 2021). In the study conducted by Nisper et al., (2009), although serum ceruloplasmin level was high in cattle with Echinococcus spp., this elevation was not found to be significant. They reported that elevated ceruloplasmin levels may be excreted from the liver into the circulation in response to tissue damage caused by echinococcosis host (Eser et al., 2013). In the current study, it was found that ceruloplasmin value was significantly high in liver parasitosis, but this high value was not significant in echinococcosis and dicrocoeliosis infected sheep. According to these results, liver damage and oxidative stress are thought to occur in liver parasitism.

There are antioxidant systems in the body that act as protectors against free radical damage at various rates. These antioxidants are negatively affected by impaired body balance and oxidative stress caused by free radicals (Yazıcı et al., 2002). Thiols, which are antioxidant molecules, constitute one of the important links in the extracellular defense system chain (Değirmençay et al., 2021). Thiol groups, which try to prevent the damaging effect of free radicals, can not maintain plasma and tissue levels during these effects. Proteins in the cell wall and extracellular fluid are oxidized by the cysteine residue of thiols in the presence of oxidant molecules. In this reversible reaction thiols are metabolized to disulfide bonds (Ulrich and Jakob, 2019; Değirmençay et al., 2021). It has been suggested that proteins are exposed to oxidative stress, resulting in a decrease in -SH groups and functional defects. In studies conducted in different structures and patients, a decrease in -SH groups is generally expected with oxidative stress (Yazıcı et al., 2002). Çetinkaya et al., (2020) reported that total thiol parameter was significantly lower in rat models of Alzheimer's disease compared to the control group. Similarly, Çamkerten et al., (2019) reported that total sulfhydryl group was importantly lower in pigs with sarcoptyx mange compared to healthy pigs. Değirmençay et al., (2021) revealed that thiol levels were low in dogs with canine distemper. In another study Tarhan et al., (2023) hey compared babesian dogs with a healthy group and measured total thiol levels. As a result, he stated that he found the level of this parameter to be low but not significant. This study is in parallel with the mentioned studies and is also similar to the study conducted by Tarhan et al., (2023) İn the present study total sulfhydryl level was found to be lower in the patient groups compared to the control group, but this value was not significant. Although this decrease is not significant, it is likely that the reduction of the sulfhydryl group indicates oxidative damage.

As a result, the oxidative parameter AOPP, antioxidant parameter T-SH and acute phase protein ceruloplasmin were measured in naturally infected sheep with fasciolosis, echinococcosis, dicrocoeliosis and mixed echinococcosis and dicrocoeliosis. Aopp parameter was found to be significantly higher in liver parasites and ceruloplasmin value was found to be significantly lower. According to these results, it can be said that cellular damage occurs in liver parasitism. It is thought that these parameters can be used in parasitic infections in terms of prognosis. It is also thought that oxidative cell damage occurs in the attack of zoonotic liver parasites in which the immune response decreases.

This is the first report showing Iğdır Türkiye groups with various zoootic parasitic liver diseases were formed for the first time and Aopp, Total Sulfidryl Group (T-Sh), Seroplasmine Levels were measured in sheep. In addition, it is thought that oxidative cell damage occurs in the attack of zoonotic liver parasites in which the immune response is reduced.

Ethical Statement

This study was carried out with the approval of the ethics committee numbered 2022/127 of (KAÜ-HADYEK).

Conflict of Interest

The authors declare no conflict of interest.

Author Contributions

FE planned, designed and supervised the research. AY, ÖOK performed parasitological tests. AUK, FE analyzed the biochemical parameters, interpretation of the results, statistical analysis, AUK, FE, NY, checked and finalized the manuscript.

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Investigation of Aopp, Total Sulphydryl Group (T-sh), Seroplasmin Levels in Sheep Wi̇th Zoonotic Liver Parasitosis

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INTRODUCTİON

MATERIAL AND METHODS

Animals

Laboratory Diagnostic Methods

Biochemical Analysis

Statistical Analysis

RESULTS

DISCUSSION

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