Indian Journal of Animal Research

  • Chief EditorK.M.L. Pathak

  • Print ISSN 0367-6722

  • Online ISSN 0976-0555

  • NAAS Rating 6.50

  • SJR 0.263

  • Impact Factor 0.4 (2024)

Frequency :
Monthly (January, February, March, April, May, June, July, August, September, October, November and December)
Indexing Services :
Science Citation Index Expanded, BIOSIS Preview, ISI Citation Index, Biological Abstracts, Scopus, AGRICOLA, Google Scholar, CrossRef, CAB Abstracting Journals, Chemical Abstracts, Indian Science Abstracts, EBSCO Indexing Services, Index Copernicus
Submit

Full Research Article

Molecular Characterization of the Presence of Bovine Papillomavirus in Cattle Teat Warts and a Different Treatment Approach

K. Atlı1,*, Y.S. Orta1, S. Kant1, M. Kale1, O. Yapıcı2
1Department of Virology, Faculty of Veterinary Medicine, Burdur Mehmet Akif Ersoy University, Burdur, Turkey.
2Department of Virology, Faculty of Veterinary Medicine, Selcuk University, Konya, Turkey.

ABSTRACT

Background: Papillomatosis is a skin condition that is distinguished by benign proliferative tumors with a complicated etiology and epithelial proliferation. There is a need to perform a more thorough study on bovine papillomavirus and identify the virological properties of the agent in detail since a definitive treatment approach against this infection has not yet been completely identified and the suggested treatment outcomes differ.

Methods: Samples were collected from warts developing on the teats of 500 cattle raised for milk production in Burdur Center and its districts. The samples were defrosted in order to extract DNA and the Dneasy Blood and Tissue Kit was used for the extraction procedure. By using a PCR assay, wart sample extracts were examined for 13 different BPV types (excluding BPV Type 7). For BPV type-specific primers, a protocol was utilized. Amplification products were demonstrated using agarose gel electrophoresis.

Result: In the PCR test of 500 wart samples, BPV types (type 1-type 13) were detected in 378 (75.6%). In the general distribution of BPV types (single or mixed types) in teat warts, BPV-2 (n=85; 22.49%), BPV-8 (n=45; 11.90%), BPV-9 (n=48; 12.70%) and BPV-10 (n=52; 13.76%) were determined to be more common. In the study; it was determined that three different combined treatments provided 100% regression or complete recovery in warts developing on the teat of cattle. In conclusion; one of these three treatment combinations may be preferred for teat wart lesions in cattle.

INTRODUCTION

Papillomatosis; Papovaviridae, found in all mammals and birds It is a disease caused by members of the PV family. Cattle are the most affected domestic animals (Campo, 2006). BPVs have been classified into five genera and one unclassified genus. These are: BPV-1, BPV-2, BPV-13 and BPV-14 in the Deltapapillomavirus genus; BPV-5 and BPV-8 in the Epsilonpapillomavirus genus; BPV-7 in the Dyoxipapillomavirus genus; BPV-16, BPV-18, BPV-22 and Xipapillomavirus in the Yokappapillomavirus genus. BPV-3, BPV-4, BPV-6, BPV-9, BPV-10, BPV-11, BPV-12, BPV-15 and BPV-23 in the genus and BPV-17, BPV-19 and BPV-20 in the unclassified group. BPV-21 and BPV-24 types (Araldi et al., 2017; Daudt et al., 2016; Knipe and Howley, 2013).
       

Anthropogenic activities, changes in farming systems and environmental changes all contribute to the development, reemergence and geographical spread of infectious illnesses (Kumar et al., 2023). Among many diseases that cause loss of productivity in meat and dairy farming, papillomatosis cases have an important place. Papillomatosis is a disease characterized by epithelial proliferation in the skin and benign proliferative tumors with a complex pathogenesis and etiology. Papillomas are benign tumors, but sometimes they can transform into malignant epithelial tumors and cause significant disorders (Araldi et al., 2017). Bovine papillomavirus (BPV); Mastitis reduces milk output and quality, which results in significant financial losses for milk producers (Safak et al., 2023). Mastitis causes economic losses due to decreased milk yield, blunting of the teats, inability of the teats to enter the milking machines due to deformities and inability to milk due to pain (Atasever et al., 2005, Yıldırım et al., 2022; Özmen and Kale, 2023).      

In research, BPV has been detected in blood as well as in papilloma tissues. It has also been stated that it can be transmitted through milk, urine, semen and uterine lavages and vertical transmission has been observed. The presence of viral genomes was also found in the offspring’s waste and blood (Bocaneti et al., 2016; Lindsey et al., 2009). BPV can be transmitted from animal to animal through direct skin contact; Contaminated feed and materials, milking machines, ear tagging, procedures, castration devices, tuberculin injections, heredity, malnutrition, hormonal imbalance and mutation and arthropod vectors also indirectly play an important factor in the spread of the disease (Atasever et al., 2005). In addition to negatively affecting animal health, BPV has also been reported in recent years to show that it can be transmitted from animals to humans due to its zoonotic nature (Gallina et al., 2020). The polymerase chain reaction (PCR) test in the diagnosis of BPV infection is the most widely used method for detecting viral DNA in blood and  tissue samples taken from BPV-infected animals (Ataseven et al., 2016; Tomita et al., 2008; Wobeser et al., 2012). Therefore, the conventional PCR method is preferred (Guo et al., 2012; Melo et al., 2014). Since no definitive treatment method has been defined against BPV infections, different treatment methods are applied for BPV infections.
       
In this study, BPV types of warts developing on the teats of cattle were determined by PCR tests without classifying macroscopic appearance, virus type, or papilloma/fibropapilloma and the results were evaluated by applying three different combined treatment methods to these animals.

MATERIALS AND METHODS

Animals
 
All samples were collected from warts developing on the teats of 500 cattle (Holstein, Simmental and Native Breed) raised for milk production in Burdur-Center and its districts between June 2022 and September 2023. Following the application of a surgical ligature using 0/2 silk thread to the areas where the wart samples meet the normal mucosa, the broken tissue piece was taken and sent to the Burdur Mehmet Akif Ersoy University, Faculty of Veterinary Medicine, Department of Virology Laboratory for diagnostic purposes. Wart samples were collected and kept at -20°C until extraction.
 
Extraction and PCR
 
The samples were frozen for DNA extraction, which was done using the Dneasy Blood and Tissue Kit (Qiagen). Extracts of wart samples were evaluated for 13 types of BPV (except BPV Type-7) by PCR. The procedure of Silva et al., (2016) was applied to BPV, specific primers (Table 1). PCR reaction conditions were initial denaturation at 94°C for 3 min, (denaturation at 94°C for 60 s, 35 cycles of 60-68°C annealing, extension at 72°C for 60 s) and final extension at 72°C for 3 min (Thermo). Using ethidium bromide dye and Tris-acetate buffer (2%) agarose gel electrophoresis, amplification products were demonstrated.
 

Table 1. Spesific primers for BPV.


 
Treatment
 
Three trial groups were established without classification of macroscopic appearance, virus type, or papilloma or fibropapilloma of warts. These trial groups were selected from animals that were positive as a result of the PCR test. The randomization of the treatment groups, consisting of 85 animals each, was determined by lot. Animals with positive PCR test results who were not selected for treatment groups were also determined as the control group. Among the treatment methods compared, PAPILENDTM,® cream (Almer Kimya İlaç San.Tic.Ltd.Şti., Ankara, Turkey), ivermectin once daily for 10 days (Zolimectin®, Zolenat İlaç A.Ş., İstanbul, Turkey), levamizol (Levatek® %10, Teknovet İlaç San. Tic., İstanbul, Turkey) and autohemotherapy (right-left scapula bone area; total 20 mL) subcutaneously total of 2 times with an interval of 15 days and AlquermoldTM premix powder (Biovet, S.A., 25 Poligono Industrial, Tarragona, Spain) was determined as 150 grams once a day for 10 days. The treatment protocol is given in Table 2. No treatment was applied to the animals in the control group.
 

Table 2: Applied treatment methods.

RESULTS AND DISCUSSION

As a result of the PCR test of 500 animals included in the study, 378 (75.6%) were found to be positive and 122 (24.4%) were negative. 122 (24.4%) animals that were found to be negative were considered the control group in the study (Table 3).
 

Table 3: PCR (Type-spesific primers) test results.


       
In the general distribution of BPV types (single or mixed types) in teat warts; BPV-2 (n=85; 22.49%), BPV-8 (n=45; 11.90%), BPV-9 (n=48; 12.70%) and BPV-10 (n=52; 13.76%) were determined to be more common (Table 4).
 

Table 4: General view of single or mixed types.


       
In the study; it was determined that three different combined treatments provided 100% regression or complete recovery in warts developing on the teat of cattle (without classification of macroscopic appearance, virus type, or papilloma/fibropapilloma) (Fig 1, Fig 2, Fig 3). No recurrence of warts was detected in all treatment groups during the six-month period.
 

Fig 1: Results of treatment I (A: Before; B: After).


 

Fig 2: Results of Treatment II (A: Before; B: After).


 

Fig 3: Results of treatment III (A: Before; B: After).


       
The most important function of the teat is to ensure the discharge of produced milk. Its meaning for the calf is that it is the place where milk is absorbed. Mammary papillomatosis cases are one of the most important diseases affecting cattle health and lesions that occur, especially on the udder and teat, cause significant financial losses in the dairy sector.
       
In this study, BPV types (type 1-type 13) were detected in 378 (75.6%) of 500 wart samples in the PCR test. In the general distribution of BPV types (single or mixed types) in teat warts; BPV-2 (n=85; 22.49%), BPV-8 (n=45; 11.90%), BPV-9 (n=48; 12.70%) and BPV-10 (n=52; 13.76%) were determined to be more common. Jana (2015) emphasized that BPV 1-2 are the viral agents in udder and cutaneous papillomas. As a result of the studies, it has been stated that BPV-6 and BPV-9 are common and responsible for udder papillomatosis (Hatama et al., 2009). Rai et al., (2011) reported that other types were not detected in the udders of cows in a dairy farm in India and only the presence of BPV-10 was identified. Dağalp et al., (2017) explained that BPV-6-7-9-10 are frequently encountered in udder papillomas. Özmen and Kale (2023) determined the highest levels of BPV-2, BPV-9 and BPV-10 in single types of udder papillomas. When Özmen and Kale (2023) determining the general distribution, single and mixed types are seen together in the mammary warts of Holstein breed dairy cattle; BPV-2 (37.7%), BPV-6 (26.4%), BPV-8 (28.3%), BPV-9 (34%), they determined that BPV-10 (30.3%) and BPV-12 (20.8%) were more common.
       
In teat papillomas where mixed types are seen; Lindholm et al., (1984) detected 28% BPV-1, 89% BPV-5 and 92% BPV-6. Another group of researchers (Borzacchiello and Roperto, 2008; Tozato et al., 2013) identified BPV-1, BPV-5, BPV-6, BPV-9 and BPV-10 in the udder and teats. Ataseven et al., (2016) detected BPV-1, BPV-4, BPV-8, BPV-6 and BPV-9. Lunardi et al., (2016) found BPV-6 45%, BPV-7 5%, BPV-8 2.5%, BPV-9 5% and BPV-10 32.5%. Ogawa et al., (2004) BPV-1, BPV-3, BPV-5. Savini et al., (2016) found 52.3% BPV-7, 38.6% BPV-9 and 59.1% BPV-10. Jana (2015) BPV-1, BPV-2, BPV-5, BPV-9 and BPV-10. Bianchi et al., (2020) detected BPV-4, BPV-6, BPV-7, BPV-8, BPV-9, BPV-10, BPV-11, BPV-12.
       
In the study; PAPILENDTM,® cream, used in three different combined treatment applications for warts developing on the teat of cattle (without classification of macroscopic appearance, virus type and papilloma/fibropapilloma) is a skin care product consisting of glacial acetic acid, salicylic acid and herbal oils, developed to soften the wart-like formations seen in cattle and reduce their disturbing effects by hardening (Yigitarslan et al., 2023). The product composition; It comprises salicylic acid, glacial acetic acid, garlic oil, glyceryl monostearate, tea tree oil, podophyllum,  cetyl stearyl alcohol, stearic acid,  water and hydrogenated castor oil. As main ingredients; they stated that tea tree oil (Melaleuca alternifolia) has antiviral, antifungal and antiseptic properties (monoterpenes terpinen-4-ol, γ-terpinene and linalool) (Alsanad and Alkhamees, 2016). They explained that garlic oil (Allium sativum) has antiviral, anti-inflammatory effects, increases natural killer cells and cellular immunity and that its high allicin substance has anti-DNA activity (Mousavi et al., 2018). Apart from these, podophyllum has an antimitotic effect (Rivera and Tyring 2004), glacial acetic acid has a chemical coagulation of 80-90% of proteins in wart tissues, salicylic acid cleans infected tissues without damaging the epidermis layer and glyceryl monostearate has a stabilizing effect. It has been stated that stearic acid acts as an emulsifier and cetyl stearyl alcohol and hydrogenated castor oil have viscosity increasing properties (Pekcan, 2014; Tırnaksız et al., 2015).
       
BPV is not a good immunogen for the mammalian organism and since it does not cause inflammation, it cannot create a signal to stimulate the immune system (except for the formation of local cellular immunity) regarding the presence of the virus. For this reason, the main goals are the development of neutralizing antibodies against the virus, stimulation of cellular immunity, destruction of infected cells that produce early proteins and introducing the virus to keratinocytes (Campo and Roden, 2010; Bocaneti et al., 2016). For this purpose, to stimulate the immune system, Ivermectin, Levamisole and autohemotherapy applications that stimulate the immune system were carried out. Ivermectin has a positive effect on the cellular immune response (T-cell cytotoxicity, natural killer cell cytotoxicity, macrophage activation) of animals with papilloma lesions (Uhlir and Volf, 1992; Nicholls and Stanley, 2000; Campo, 2006). As a matter of fact, ivermectin, used in the treatment of bovine papillomas, increased serum TNF-α levels synthesized by macrophages, endothelial cell and T lymphocytes and IL-6 levels secreted by monocytes, macrophages and T lymphocytes on the 7th day, indicating that ivermectin has an activating role on the immune system, especially T lymphocytes (Bekdur et al., 2018). Ivermectin has a cytotoxic effect on papilloma carcinogenic cells (Kim et al., 1992). Levamisole is the tetramisole isomer and has been used for viral diseases, tumor treatments and as an immunomodulator in humans and animals for more than 20 years (Miwa and Orita, 1978; Brunner and Muscoplat, 1980; Scheinfeld et al., 2004). It has been explained that it is used as a non-specific immune stimulant in many diseases (Ganguly, 2014). It causes an increase in macrophages after blood is taken from the jugular vein and injected directly into the muscle (Lopes et al., 2021). While the standard macrophage rate in the blood is 5%, it has been reported that this rate can increase to 20-22% about 8 hours after application (Teixeira, 1940; Ottobelli et al., 2016). It is explained that autohemotherapy stimulates RES and increases macrophages in circulating blood (Namgyel et al., 2021). It has been reported that autohemotherapy is a complementary treatment method that provides 90% success in the treatment of papillomas in cattle (Jana and Jana, 2009; Jana, 2015). According to Orta et al., (2023); AlquermoldTM premix powder, which contains vitamin E, selenium, copper and zinc, was given to sick animals as part of the study in order to boost their resistance to illness (Spears and Weiss, 2008). The main source of vitamin E is food (Baldi et al., 2000). The amount of vitamin E diminishes when prepared feed is processed or kept for an extended period of time. Furthermore, grazing may prevent them from getting enough vitamin E from plants (Baldi, 2005). Selenium levels in the soil or in plants may not be adequate (Sharma et al., 1983). Selenium is a vital component of the antioxidant defense mechanism of the organism (Kieliszek and Błażejak, 2016). Selenium and vitamin E have a synergistic impact (Willshire and Payne, 2011). Zinc is essential for keratin synthesis (Tomlinson et al., 2004). Copper and zinc are crucial for fighting microbes and boosting the immune system (Spears, 2000). Regardless of the macroscopic appearance, virus type and papilloma/fibropapilloma classification of warts developing on the teat of cattle, successful results were obtained as a result of the combined use of PAPILEND cream + immune stimulating drugs + vitamin/premix powders containing vitamin E, zinc, selenium and copper.

CONCLUSION

Regardless of the macroscopic appearance, virus type and papilloma/fibropapilloma classification of warts developing on the teat of cattle, successful results were obtained as a result of the combined use of PAPILENDTM,® cream + immune stimulating drugs or immune system stimulating applications (autohematherapy) + vitamin/premix powders containing vitamin E, zinc, selenium and copper.

ACKNOWLEDGEMENT

All procedures were approved by the Animal Ethics Committee (AEC) Burdur Mehmet Akif University, Turkey (No:29.03.2023-1029). This study was presented as an presentation at the XV. National Veterinary Microbiology Congress (with International Participation) held in Þanlýurfa /Turkey between 26th October and 28th October 2022.

CONFLICT OF INTEREST

All authors declared that they have no conflict of interest.

REFERENCES


  1. Alsanad, S.M., Alkhamees, O.A. (2016). Tea tree oil (Melaleuca alternifolia)-an efficient treatment for warts: Two case reports. International Archives of BioMedical and Clinical Research. https://iabcr.org/index.php/iabcr/article/view/130. Published.

  2. Araldi, R.P., Assaf, S.M.R., Carvalho, R.F.D., Carvalho, M.A.C.R.D., Souza, J.M.D., Magnelli, R.F., Módolo G.D., Roperto, F.P., Stocco, R.D.C., Beçak, W. (2017). Papillomaviruses: A systematic review. Genetics and Molecular Biology. 40: 1-21.

  3. Ataseven, V.S., Kanat, O., Ergun, Y. (2016). Molecular identification of bovine papillomaviruses in dairy and beef cattle: First description of Xi-and Epsilonpapillomavirus in Turkey. Turk J. Vet Anim Sci. 40: 757-763.

  4. Atasever, A., Çam, Y., Atalay, O. (2005). Bir sığır sürüsünde deri papillomatosis olguları. Ankara Üniv Vet Fak Derg. 52: 197-200.

  5. Baldi, A., Savoini, G., Pinotti, L., Monfardini, E., Cheli, F., Orto, V.D. (2000). Effects of vitamin E and different energy sources on vitamin E status, milk quality and reproduction in transition cows. Journal of Veterinary Medicine Series A. 47: 599- 608.

  6. Baldi, A. (2005). Vitamin E in dairy cows. Livestock Production Science. 98: 117-122.

  7. Bekdur, Y., Aslan, Ö., Şentürk, M., Çiğdem, M. (2018). “Sığır papillomatozisinde sağaltım amacıyla uygulanan ivermektinin serum TNF-α ve IL-6 düzeylerine etkisinin belirlenmesi”. Sağ. Bil. Derg. 26: 156-161.

  8. Bianchi, R.M., Alves, C.D.B.T., Schwertz, C.I., Panziera, W., De Lorenzo, C., da Silva, F.S., de Cecco, B.S., Daudt, C., Chaves, F.R., Canal, C.W., Pavarini, S.P., Driemeier, D. (2020). Molecular and pathological characterization of teat papillomatosis in dairy cows in Southern Brazil. Brazilian Journal of Microbiology. 51: 369-375.

  9. Brunner, C.J., Muscoplat, C.C. (1980). Immunomodulatory effects of levamisole. Journal of the American Veterinary Medical Association. 176(10 Spec No): 1159-1162.

  10. Bocaneti, F., Altamura, G., Corteggio, A. (2016). Bovine papillomavirus: New insights into an old disease. Transboundary and Emerging Diseases. 63: 14-23.

  11. Borzacchiello, G., Roperto, F. (2008). Bovine papillomaviruses, papillomas and cancer in cattle. Vet Res. 39: 45. doi: 10.1051/vetres:2008022.

  12. Campo, M.S. (2006). Bovine Papillomavirus: Old System, New Lessons? In: Papillomavirus Research: From Natural History to Vaccine and Beyond Chap 23, [Campo, M.S. (Eds)], England: Caister Academic Press. p: 459-472.

  13. Campo, M.S., Roden, R.B.S. (2010). Papillomavirus prophylactic vaccines: Established successes, new approaches. Journal of Virology. 2: 1214-1220.

  14. Dağalp, S.B., Dogan, F., Farzani, T.A., Salar, S., Bastan, A. (2017). The genetic diversity of bovine papillomaviruses (BPV) from different papillomatosis cases in dairy cows in Turkey. Archives of Virology. 162: 1507-1518.

  15. Daudt, C., da Silva, F.R.C., Streck, A.F., Weber, M.N., Mayer, F.Q., Cibulski, S.P., Canal, C.W. (2016). How many papillomavirus species can go undetected in papilloma lesions? Sci. Rep. 6: 36480. doi: 10.1038/srep36480.

  16. Gallina, L., Savini, F., Canziani, S., Frasnelli, M., Lavazza, A., Scaglianiri, A., Lelli, D. (2020). Bovine papillomatosis hiding a zoonotic infection: Epitheliotropic viruses in bovine skin lesions. Patogenes. 9: 583. doi: 10.3390/pathogens9070583.

  17. Ganguly, S. (2014). Efficacy of levamisole as non-specificý mmuno modulator: A review. Annals of Biomedicines Natural Products. 1(1): 22-23. 

  18. Guo, F., Liu, Y., Wang, X., He, Z., Weiss, N., Madeleine, M., Liu, F., Tian, X., Song, Y., Pan, Y., Ning, T., Yang, H., Shi, X., Lu, C., Cai, H., Ke, Y. (2012). Human papillomavirus infection and esophageal squamous cell carcinoma: A case control study. Cancer Epidemiol Biomarkers. 21: 780-785.

  19. Hatama, S., Nishida, T., Kadota, K., Uchida, I., Kanno, T. (2009). Bovine papillomavirus type 9 induces epithelial papillomas on the teat skin of heifers. Vet Microbiol. 136: 347-351.

  20. Jana, D., Jana, M. (2009). Autohaemotherapy for cutaneous papillomatosis in buffaloes. Indian Veterinary Journal. 86(11).

  21. Jana, D. (2015). Studies on bovine and bubaline papillomatosis with special reference to its epidemiology, clinicopathology and therapeutics. PhD Thesis, Kayani University, India. pp. 1-455.

  22. Kieliszek, M., Błażejak, S. (2016). Current knowledge on the importance of selenium in food for living organisms: A review.  Molecules. 21: 609. doi: 10.3390/molecules21050609.

  23. Kim, B.K., Kwun, J.Y., Park, Y.I., Bok, J.W., Choi, E.C. (1992). Anti- tumor components of the cultured mycelia of Calvatia craniformis. J. Korean Cancer Assoc. 24(1): 1-18.

  24. Knipe, D.N., Howley, P.M. (2013). Fields Virology, 8th Edition, Philadelphia: Lippincott Williams and Wilkins.

  25. Kumar, S., Dutta, T.K. and Roychoudhury, P. (2023). Transboundary animal diseases in the perspective of North East India: A review. Indian Journal of Animal Research. 57(12): 1577- 1585. doi: 10.18805/IJAR.B-4402.

  26. Lindholm, I., Murphy, J., O’Neil, B.W., Campo, M.S., Jarrett, W.F. (1984). Papillomas of the teats and udder of cattle and their causal viruses. Vet Rec. 115: 574-577.

  27. Lindsey, C.J., Almeida, M.E., Vicari, C.F., Carvalho, C., Yaguiu, A., Freitas, A.C., Beçak, W., Stocco, R.C. (2009). Bovine papillomavirus DNA in milk, blood, urine, semen and spermatozoa of bovine papillomavirus-infected animals. Gen Mol Res. 8: 310-318.

  28. Lopes, P.R., Batista, M.A., Soares, R.P., de Oliveira, J.G., Leme, F.D.O.P., Martins-Filho, O.A., Maranhao, P.A.R., Wenceslau, R.R., Palhares, M.S, Araújo, M.S.S. (2021). Autohemotherapy increases phagocytic activity of neutrophils and promotes cytokine production by lymphocytes in horses. Brazilian Journal of Veterinary Medicine. 43(1): e000821-e000821.

  29. Lunardi, M., Tozato, C.C., Alfieri, A.F., Alcantara, B.K., Vilas-Boas, L.A., Otonel, R.A.A., Headley, S.A., Alfieri, A.A. (2016). Genetic diversity of bovine papillomavirus types, including two putative new types, in teat warts from dairy cattle herds. Arch. Virol. 161: 1569-1577.

  30. Melo, T., Carvalho, R., Mazzucchelli-de-Souza, J., Diniz, N., Vasconcelos, S., Assaf, S., Araldi, R., Ruiz, R., Kerkis, I., Beçak, W., Stocco, R.C. (2014). Phylogenetic classification and clinical aspects of a new putative deltapapillomavirus associated with skin lesions in cattle. Genetics and Molecular Research. 13(2): 2458-2469.

  31. Miwa, H., Orita, K. (1978). Cancer immunotherapy with levamisole.  Acta Medica Okayama. 32(3): 239-245.

  32. Mousavi, Z.B., Mehrabian, A., Golfakhrabadi, F., Namjoyan, F. (2018). A clinical study of efficacy of garlic extract versus cryotherapy in the treatment of male genital wart. Dermatologica Sinica. 36(4): 196-199.

  33. Namgyel, U., Wangdi, K., Pem, R., Rinchen, S. (2021). Effectiveness of different treatment protocols against cutaneous bovine papillomatosis (wart): A clinical trial study. Bhutan Journal of Animal Science. 5(1): 95-102.

  34. Nicholls, P.K., Stanley, M.A. (2000). The immunology of animal papillomavirüses. Vet Immun Immunopathol. 73: 101-127.  

  35. Ogawa, T., Tomita, Y., Okada, M. (2004). Broad-spectrum detection of papillomaviruses in bovine teat papillomas and healthy teat skin. J. Gen Virol. 85: 2191-2197.

  36. Orta, Y.S., Kaya, G.B., Atlý, K., Kale, M., Özmen, Ö., Yıldırım, Y. (2023). Molecular diagnosis and application of combined alternative treatment in lesions developing in the oral region due to orf virus in sheep and goats. Indian Journal of Animal Research. doý: 10.18805/IJAR.BF-1665.

  37. Ottobelli, G.A., Sa, A.R.N.D., Pavanelli, M.F. (2016). Autohemotherapy: Hematological and histological changes in wistar rats. J. Health Sci Inst. 34(1): 33-37.

  38. Özmen, G., Kale, M. (2023). Searching bovine papillomavirus presence in lesions seen on teats of cows. Pesquisa Veterinária Brasileira. 43: e07150. https://doi.org/10.1590/1678-5150-PVB-7150.   

  39. Pekcan, A.N. (2014). Majistral Makaleler. 1. Basım, Emek Ofis Ltd. şti. Ankara. pp. 1-375.

  40. Rai, G.K., Saxena, M., Singh, V., Somvanshi, R., Sharma, B. (2011). Identification of bovine papilloma virus 10 in teat warts of cattle by DNase-SISPA. Vet. Microbiol. 147: 416-419.

  41. Rivera, A., Tyring, S.K. (2004). Therapy of cutaneous human papillomavirus infections. Dermatologic Therapy. 17(6): 441-448.

  42. Safak, T., Risvanli, A., and Asci-Toraman, Z. (2023). Impact of subclinical mastitis-causing bacterial species on the composition and chemical properties of milk. Indian Journal of Animal Research. 57(1): 131-135. doi: 10.18805/ IJAR.B-1396.

  43. Savini, F., Mancini, S., Gallina, L., Donati, G., Casa, G., Peli, A., Scagliarini, A. (2016). Bovine papillomatosis: First detection of bovine papilllomavirus types 6, 7, 8, 10 and 12 in Italian cattle herds. The Veterinary Journal. 210: 82-84.

  44. Scheinfeld, N., Rosenberg, J.D., Weinberg, J.M. (2004). Levamisole in dermatology: A review. American Journal of Clinical Dermatology. 5: 97-104.

  45. Sharma, S., Singh, R., Nielson, G.G. (1983). Selenium in soil, plant and animal systems. Critical Reviews in Environmental Science and Technology. 13: 23-50.

  46. Silva, F.R.C., Cibulski, S.P., Daudt, C., Weber, M.N., Guimaraes, L.L.B., Streck, A.F., Mayer, F.Q., Roehe, P.M., Canal, C.W. (2016). Novel bovine papilomavirustype discoveredby roling-circle amplification coupled with next-generation sequencing. Plos One. 11(9): e0162345.  doi: 10.1371/ journal.pone.0162345.

  47. Spears, J.W. (2000). Micronutrients and immune function in cattle. Proceedings of the Nutrition Society. 59: 587-594.

  48. Spears, J.W., Weiss, W.P. (2008). Role of antioxidants and trace elements in health and immunity of transition dairy cows. The Veterinary Journal. 176: 70-76.

  49. Teixeira, J. (1940). Autohemotransfusão: Complicações pulmonares pós-operatório. Rev Brasil-Cirúrgico. 2(3): 213-230.

  50. Tırnaksız, F., Karataþ, A., Arslan Akkuş, Ş., Tugcu Demiröz, F., İlbasmış Tamer, S., Algan, A.H. (2015). Majistral İlaç Rehberi. Türk Eczacıları Birliği Yayınları, Fersa Ofset, Ankara. Pp. 1-385.

  51. Tomita, N., Mori, Y., Kanda, H., Notomi, T. (2008). Loop-mediated isothermal amplification (LAMP) of gene sequences and simple visual detection of products. Nat Protoc. 3: 877- 882.

  52. Tomlinson, D.J., Mülling, C.H., Fakler, T.M. (2004). Invited review: Formation of keratins in the bovine claw: Roles of hormones, minerals and vitamins in functional claw integrity. Journal of Dairy Science. 87: 797-809.

  53. Tozato, C.C., Lunardi, M., Alfieri, A.F., Otonel, R.A.A., Di Santis, G.W., de Alcântara, B.K., Headley, S.A, Alfieri, A.A. (2013). Teat papillomatosis associated with bovine papillomavirus types 6, 7, 9 and 10 in dairy cattle from Brazil. Braz J. Microbiol. 44(3): 905-909.

  54. Uhlir, J., Volf, P. (1992). Ivermectin: its effect on the immune system of rabbits and rats infested with ectoparasites. Vet Immunol Immunopathol. 34(3-4): 325-336.

  55. Wobeser, B.K., Hill, J.E., Jackson, M.L., Kidney, B.A., Mayer, M.N., Townsend, H.G.G., Allen, A.L. (2012). Localization of bovine papillomavirus in equine sarcoids and inflammatory skin conditions of horses using laser microdissection and two forms of DNA amplification. J. Vet Diagn Invest. 24(1): 32-41.

  56. Willshire, J.A., Payne, J.H. (2011). Selenium and vitamin E in dairy cows-a review. Cattle Practice. 19: 22-30.

  57. Yıldırım, Y., Kale, M., Özmen, Ö., Çağırgan, A.A., Hasırcıoğlu, S., Küçük, A., Usta, A., Sökel, S. (2022). Phylogenetic analysis and searching bovine papillomaviruses in teat papillomatosis cases in cattle by performing histopathology, immunohistochemistry and transmission electron microscopy. Microbial Pathogenesis. 170: 105713. doi: 10.1016/ j.micpath.2022.105713. 

  58. Yigitarslan, K., Kale, M., Ozturk, D., and Mamak, N. (2023). Evaluating the efficiency of newly formulated pomade® and ceftiofur hydrochloride for treating foot rot in dairy cattle. Indian Journal of Animal Research. 57(2): 236- 240. doý: 10.18805/IJAR.BF-1410.
Reviewed By

Download Article
In this Article
    Contact us
    Follow us

    Editorial Board

    View all (0)