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�:	Antiviral and antioxidant role of wild Egyptian artichoke and neem extracts on turkeys experimentally infected with Turkey Pox Virus 

Samah M. Mosad1, Mohamed El-Adl2, Mohamed F. Salama2*, Mahmoud F. Elsebai3, Mayar Ali4

1Department of Virology, Faculty of Veterinary Medicine, Mansoura University, Egypt.
2Department of Biochemistry, Faculty of Veterinary Medicine, Mansoura University, Egypt
3Department of Pharmacology, Faculty of Pharmacy, Mansoura University, Egypt. 
4Department of Animal Husbandry and Reproduction, Faculty of Veterinary Medicine, Mansoura University, Egypt. 













* Corresponding Author:
Work address: Department of Biochemistry, Faculty of Veterinary Medicine, Mansoura University, Egypt. Postal code: 35516
E-mail:  HYPERLINK "mailto:drmohamedalymaher@hotmail.com" mfisalama@gmail.com � mfouda@mans.edu.eg 





Abstract
The current experiment was conducted to investigate the effect of artichoke (WEA) and neem (NE) extracts on turkeys that were experimentally infected with turkey pox virus (TPV). Thirty turkey poults were equally divided into six groups. In the first group, turkeys were intradermally inoculated with PBS, while birds in the second to the sixth group were intradermally inoculated with 104.9 EID50 of TPV. Group 2 was left without treatment. Group 3 was pretreated with WEA for one week before inoculation and continued for 4 weeks. Therapeutic effects of WEA and/or NE against TPV infection were assessed in group 4, 5 and 6, respectively. Weekly serum samples were collected from each bird for determination of antibody titer. After 4 weeks, samples were collected from bursa, liver and lung and used for assessing antioxidant status. Serum antibody titer was significantly elevated in group 4 at the 1st, 2nd and 4th week, while in group 6 the increase was only observed at the 3rd week. Characteristic pox lesions were observed in featherless area in group 2 with a significant decrease in the antioxidant enzymatic activities and increased lipid peroxidation in tissues. Pretreatment with WEA alleviated oxidative stress; however, the combination of WEA and NE was more efficient and associated with lower morbidity rate than NE alone. These findings suggest that artichoke supplementation can provide enough protection against TPV infection. Moreover, the combined use of WEA and NE is recommended to improve the healing of lesions and ameliorate oxidative stress associated with TPV infections. 




Keywords: Fowl pox; turkey; artichoke; neem; oxidative stress


Introduction
The interest in turkey breeding and turkey meat is increasing over the last decades. Turkey meat is rich in proteins, essential amino acids and has less fat content compared to other poultry meats. Moreover, turkey meat is rich in vitamins and minerals required for different body functions of the consumers (Ribarski Stara Zagora et al., 2001){Ribarski Stara Zagora, 2001 #37}(Ribarski et al. 2001; Biesalski 2005; Baggio et al. 2002). Despite its importance as a source of good quality food, studies on turkey diseases are scarce.
Fowl pox is a contagious disease of chicken and turkey caused by Fowl pox virus; genus Avipoxvirus; subfamily Chordopoxvirinae of the family Poxviridae (Murphy et al. 1999; Tripathy and Reed 2013). Most of researchers believe that Turkey pox virus (TPV) is identical to Fowl pox virus (FPV), while others consider it as a distinct strain. However, susceptibility of ducks to TPV but not FPV can be used to differentiate between these closely related viruses (Cunningham 1978; Murphy et al. 1999). Moreover, the genome of TPV is about 188.53 Kb in size, while that of FPV is about 288.54 Kb (Haydar et al. 2017). TPV can be isolated on chorioallantoic membranes (CAMs) of 12 days old chicken embryo producing pock lesions (OIE 2016).
The disease occurs in two forms, cutaneous (dry form) and diphtheritic (wet) forms. The dry form is characterized by proliferative lesions in unfeathered areas of the skin. On the other hand, the diphtheritic form is characterized by formation of a diphtheritic membrane on the mucous membranes of respiratory and/or digestive tracts (Fenner et al. 1993; OIE 2016).
The disease in turkey is characterized by formation of lesions around the eyes which usually cause blindness and starvation as the bird becomes unable to see the food and water with subsequent emaciation and death (Forrester and Spalding 2003). Pox virus infection in turkeys usually occurs over a longer duration than FPV infection (Wakenell 2001). However, currently there is no treatment for turkey pox and the disease control mainly depends on vaccination by thigh-stick method with FPV vaccine (Jacob et al. 1998).
Artichokes have been used in ancient medicine as they are rich in pharmaceutically active compounds, such as flavonoids, sesquiterpene lactones and caffeoylquinic acid derivatives (Lattanzio et al. 2009). The wild Egyptian artichockes (WEA) {Cynaracardunculus L. var. sylvestris (lam.) Fiofi} leaves extracts have two unique compounds, cynaropicin and grosheimol which have potent antiviral activities (Elsebai et al. 2016).
Neem (Azadirachta indica A juss) is considered as a nature�s pharmacy (Vietmeyer 1992). It is dubbed as "a wonder tree" by many researchers as it elaborates many biologically active compounds (Kaur et al. 2004; Senthil et al. 2006). More than 140 compounds were isolated from different parts of neem tree.
The medicinal properties of neem have been attributed to the presence of sulphur containing compounds as well as primary and secondary amines (Mubarak and Kulatilleke 1990; Atawodi and Spiegelhalder 1994; Koul 2004).
Neem is used in the treatment of different skin diseases (Dhawan and Ratnaik 1993), and it has been shown to possess an antibiotic activity (Sharma 1993). It also acts as anti-inflammatory (Kaur et al. 2004), antiulcer (Dorababu et al. 2004), antimicrobial (SaiRam et al. 2000; Parida et al. 2002; Siddiqui et al. 1992), and immunomodulatory agent (Arivazhagan et al. 2000). Moreover, neem also exhibits potent antimutagenic and anticarcinogenic effects (Kusamran et al. 1998). 
In the present study, we aimed to study the potential antiviral and immune-stimulating effects of artichoke and neem extracts against TPV experimental infection in turkey. Here we studied the possible protective effect of artichoke extract as well as the therapeutic effects of artichoke and/or neem extracts against TPV infection in turkey. 
Materials and methods
Plant materials and extraction procedures
The extraction procedures were conducted as previously described (Elsebai et al. 2016). Briefly, plant materials were collected from Sinai, powdered, boiled, and freeze-dried to obtain a dry water leaf-extract of WEA and neem. For the phytochemical profile, 20 mg of extract was homogenized with 1.5 mL of 80% methanol containing umbelliferon (10 �g/ml as the internal standard) by sonication for 20 min. Each extract was then vortexed vigorously and centrifuged at 10000 xg for 5 min, 1 ml was aliquoted and filtered through a 22 �m Millipore filter. 
Collection and preparation of virus samples
Clinical sample was collected from the characteristic pox virus skin lesions in 7 months old turkey that was then homogenized in phosphate buffered saline (PBS) supplemented with an antibiotic mixture (penicillin 50 IU/ml and streptomycin 50 �g/ml) to produce 10% suspension. Homogenate was then centrifuged at 4000 rpm for 15 minutes at 4(C. Supernatant fluid was used for virus isolation (Diallo et al. 2010; Nayeri Fasaei et al. 2014).
Virus isolation
Supernatant fluid (0.2 ml) was inoculated on the CAM of 12 day old ECE. Inoculated eggs were incubated at 35oC for 6 days and were then examined for specific pock lesions (Nayeri Fasaei et al. 2014). CAMs with pock lesions were stored at -20oC until their use in PCR and experimental infection.
DNA extraction
Viral DNA was extracted from pock lesions-containing CAMs using a commercial kit (QIAamp� MinElut� Virus Spin Kit; QIAGEN GmbH, Germany) according to the manufacturer�s instructions.
PCR
To confirm the existence of TPV in the isolated DNA from pock lesions, PCR was carried out by using a previously published set of primers that were designed to amplify 4b gene of the Avian pox virus (Masola et al. 2015). The primer sequences were as follows: 4b forward 5�-CAGCAGGTGCTAAACAACAA-3�, and 4b reverse 5�-CGGTAGCTTAACGCCGAATA-3�. The primers were synthesized by Metabion International AG (Germany). PCR was performed by using Dream Taq Green PCR Master Mix (Thermo Scientific). The reaction mixture contained 25�l Dream Taq Green PCR Master Mix (2X), 0.5�M of each primer, 0.5�g of the extracted DNA, and nuclease free water that was added to a final volume of 50�l. Two control tubes, one with FPV DNA as a positive control and the other tube with nuclease free water instead of the extracted DNA was included as a negative control.
The PCR cycling conditions included an initial denaturation step of 94oC for 2 min followed by 35 cycles of denaturation at 94oC for 1 min, annealing at 61oC for 1 min, and extension at 72oC for 1 min. The cycles were followed by final extension step at 72oC for 10 min.
Agarose gel electrophoresis of the PCR product
The 578 bp PCR product was separated on a 1.5% agarose gel that was stained with 0.5 �g/ml ethidium bromide using Tris-Borate EDTA (TBE) buffer. Samples were loaded next to 100 bp DNA ladder (Jena Bioscience, Germany). Gel was then visualized on a UV transilluminator and an image was then captured by a digital camera.
Virus titration
TPV isolate was titrated in specific pathogen-free (SPF) ECEs at the Animal Health Research Institute, Dokki, Giza, Egypt. Ten-fold serial dilutions of the isolate were prepared. Each dilution (0.2 ml) was then inoculated onto the CAM of five embryos (10 days old). Any deaths before 24 hrs were discarded. On the 5th day post inoculation (PI), EID50 was calculated as described by Reed and Munch (1938) and the virus titer was 104.9 EID50.
Experimental design
About 30 turkeys poults (7 weeks old, 500 g in body weight, and TPV free) were used in the present study. All birds received human care according to the national association of laboratory animal care. Moreover, food and water were supplied ad libitum.
Birds were randomly divided into six groups of 5 birds each as follows: 
Birds in group 1 (control group) were intradermally inoculated with PBS and were physically separated from experimentally infected birds to avoid cross infection.
Groups 2-6 were intradermally inoculated with 104.9 EID50 of TPV (El-Abasy et al. 2016). The inoculated birds were closely monitored for the appearance of characteristic pox lesions. 
Birds in group 2 were infected with TPV and left without any treatment and served as a control infected group.
Birds in group 3 were used to examine the possible protective effect of WEA extract against TPV infection. Birds received a daily dose of 20 mg WEA extract/100g body weight dissolved in 1 ml PBS according to Oghenesuvwe et al. (2014) for 6 days before TPV inoculation and continued for 4 weeks afterwards (Wei et al. 2015).
Birds in group 4 were used to study the potential therapeutic effect of WEA extract against TPV infection. Upon the appearance of pox lesions after viral inoculation, birds were treated by oral administration of 20 mg WEA extract/100g body weight dissolved in 1 ml PBS for 4 weeks. 
In group 5, TPV-infected birds were used to assess the effect of topical application of neem extract on the healing of pox lesions as neem may be toxic when administrated orally as previously reported by Gandhi et al. (1988). Birds were treated by local administration of neem extract paste on the skin lesions.
In group 6, infected birds were used to examine the combined effect of oral WEA extract and topical neem administration for the treatment of turkey pox. After the appearance of pox lesions, birds were treated with oral WEA extract together with topical neem extract as described in groups 4 and 5 above. 
Serum samples were collected from each bird before virus inoculation and weekly afterwards until the end of the experiment (4 weeks) to assess antibodies against TPV. At the end of experimental period, birds were euthanized and internal organs (liver, bursa, and lung) were collected for measuring oxidative stress biomarkers.


Passive hemagglutination test
The test was carried out according to Tripathy et al. (1970) and Vasudevachari et al. (1989) with some modifications as follows: sheep RBCs were collected in a sterile Alsever�s solution and were then washed three times with sterile PBS. Washed sheep RBCs were fixed by adding 1.2 ml PBS and 0.25 ml of 0.6% glutaraldehyde in water to each 0.1 ml RBCs. This mixture was incubated for 2 hours at room temperature with gentle stirring, and was then washed three times with PBS. Fixed 2.5% sheep RBCs were then added to an equal volume of tannic acid (1: 25,000), incubated at 37oC for 30 minutes, and washed 3 times with PBS. For antigen sensitization, TPV (filtered by 0.45 �m filter) was added to an equal volume of 5% tannic acid-treated sheep RBCs and incubated at 37oC for 2 hours. The mixture was then washed three times with PBS and re-suspended to 1% concentration in stabilizing solution (PBS containing 1% sucrose, 1% normal rabbit serum and 0.2% sodium azide).
All tested sera were heat inactivated at 56oC for 30 minutes then a two-fold serial dilution from each serum sample was prepared in a U shape microtiter plate, and 25 �l of sensitized sheep RBCs was added to each serum dilution. Plates were then incubated at 37oC for 15 minutes and up to one hour.
Determination of oxidative stress markers associated with experimental pox infection.
The collected tissue samples were homogenized in ice-cold phosphate buffer saline (PBS), centrifuged at 3000 rpm for 30 minutes at 4�C, and the supernatants were collected and stored at -20�C. Tissue activities of superoxide dismutase (SOD), catalase (CAT), and glutathione s transferase (GST) as well as the levels of reduced glutathione (GSH) and malondialdehyde (MDA) were estimated according to the instructions of the kits� provider (Bio-diagnostic, Co, Dokki, Giza, Egypt).



Statistical analysis
Data for antioxidant and oxidative stress markers are expressed as means (SEM and analyzed for statistical significance at p<0.05 by one way ANOVA and Tukey�s Post-hoc test by using GraphPad Prism software (GraphPad Software, Incorporated, La Jolla, CA, USA).  
Results
Virus isolation
Pox virus was isolated on the CAM of 12 days old ECEs for three successive passages, producing characteristic pock lesions (Fig. 1).
PCR results for Avian pox 4b gene 
To confirm the isolated TPV, PCR amplification of the avian pox virus 4b gene was carried out. As shown in Fig. 2, our isolate produced specific band at approximately 578 bp.
Progression of turkey pox infection
The disease progression and antibody titers were monitored for up to four weeks PI and the results were recorded for all of the experimental groups. Morbidity rate was 0% in group 1, 60% in group 3, and 100% in groups 2, 4 and 5 with no mortalities in all groups (Table 1).
Characteristic pox lesions (nodules which progressed to discrete wart like nodules followed by the development of brown crust) appeared on the 4th day PI in featherless areas under the wings, around the eyes (leading to total closer of the eye), ears, vent area and in mouth commissures. In WEA protected group (group 3), two bids did not show any lesions, while the other three birds developed pox lesions on the 4th, 6th and 8th day PI. Interestingly, the observed lesions were very mild that appeared only on the head of two birds and under the wing of the 3rd one (Fig. 3 C and D).
Of note, a bird in group 6 developed a large nodule on the eyelid that became caseated and caused complete eye closure. However, the lesion disappeared after a combined treatment by oral administration of WEA extract and local neem application (Fig. 3I and J).
The observed clinical signs disappeared within 12 days in protected group (group 3), 19 days in group 6, 22 days in group 4, 24 days in group 5. However, in group 2, the observed pox lesions were still existing 4 weeks PI (time of sacrifice) (Table 1; Fig. 3B)
Passive hemagglutination
In the first week, group 3 revealed a significant decrease in comparison with group 4 with a non-significant change between other groups (pe"0.05). After 2 weeks, the antibody titer of group 4 and 6 was the highest among the other studied groups (pd"0.05). Antibody titer in group 6 was elevated by nearly 20-fold after 21 days and was significantly higher than other groups (pd"0.05). The antibody titer was started to decrease in the 4th week in all groups with no differences among groups 4, 5 and 6 (pe"0.05) that were significantly higher than groups 1, 2 and 3 (pd"0.05). 
WEA and neem extract ameliorate the oxidative stress associated with TPV infection
As shown in fig. 4, TPV infection was associated with a marked oxidative stress as indicated by decreased enzymatic activities of SOD, CAT, GST and GSH level in infected birds. Lipid peroxidation secondary to oxidative stress was also observed as indicated by increased MDA levels. Pre-treatment with oral WEA was sufficient to avoid such an oxidative stress. Similarly, a combined treatment with oral WEA extract and local neem extract was also effective in preventing tissue oxidative stress. Treatment with either oral WEA or local neem extract caused a mild but significant improvement of oxidative stress to the same extent compared to untreated birds. 
Discussion
The present study aimed to examine the possible antiviral effects of WEA and neem extracts on turkeys experimentally infected with pox virus. In the current study, both local and generalized pox lesions were observed after viral inoculation. These results were in agreement with previous reports in poultry (Tripathy and Cunningham 1984; Siddique et al. 2011; Fenner et al. 1993).
Characteristic nodules which progressed to discrete wart like nodules then brown crust was developed in featherless areas under the wings, on the head, vent area and in mouth commissures at four days PI except in the protected group, where some birds showed mild lesions that appeared 4-8 days PI and others did not show any lesions. In previous reports, lesions appeared on the 5th (El-Abasy et al. 2016), or the 6th (Kabir et al. 2015) day. In another study, lesions appeared after 4-10 days (Kirmse 1969).
Presence of lesions on the eyelids may cause mortality as birds become unable to visualize food and water and eventually die from starvation (Forrester and Spalding 2003). Therefore, effective treatment during the course of TPV infection is crucial to avoid mortalities.
The disease duration varies between turkey and chicken. In avian pox, the disease persists for about four weeks in chickens (van Riper III and Forrester 2007). On the other hand, the disease duration in turkeys is longer and lesions could take up to 6-12 weeks to disappear after initial infection (Davidson and Doster, NWTF).
Forrester (1991) followed the development of cutaneous lesions on a sentinel domestic turkey in Florida. On day six post-exposure, small areas of swelling were observed followed by small lesions by day 8 that had considerably grown by day 15. Lesions began to cover the eye at day 20 and the bird was blind after 50 days. However, in our experiment, the lesions disappeared within 24 days from all the experimental groups except in untreated group where lesions were still present at the time of sacrifice (4 weeks PI). More importantly, a combined treatment with artichoke and neem extracts was efficient to recover a blind bird within one week. Therefore, complications and mortalities associated with TPV can be avoided by a combined treatment with artichoke and neem extracts. Our results also demonstrated that the use of artichoke extract was effective and provided protection against TPV infection. 
To assess the immunity in infected birds, serum samples were collected from all birds at different time points after viral inoculation, and antibody titers were measured by passive hemagglutination test. The lowest antibody titers were observed in birds pretreated with artichoke extract. This could possibly be due to the antiviral effect of artichoke that inhibits viral replication and hence antibody titer. On the other hand, the highest antibody titer was observed in birds treated with a combination of neem and artichoke extracts. High viral loads in that group together with the immune-stimulating effect of artichoke extract could be the reason behind the observed elevation in the antibody titer. NE was accompanied with a significant increase in antibody titer in chicks infected with Newcastle disease virus and other group infected with infectious bursal disease virus (Jawad et al. 2013) as it was advised that NE can potentially increase both humeral and cell mediated immunity as well as it could kill and inhibit the growth of microorganisms (Sadekar et al. 1998). In a similar experiment in rats, different doses of neem flower extract were capable of increasing antibody titer in a dose dependent manner (Shah et al. 2009). Similar results were also observed in artichoke supplementation in broiler that was exposed to heat stress, where a significant improvement in antibody titer was observed (Effati et al. 2014).  
In sheep, Pox virus induced oxidative stress and increased the production of MDA with a significant reduction in total antioxidant capacity in serum of infected animals (Kirmizigul et al. 2016) due to imbalances between oxidant and antioxidant system levels. This imbalance between antioxidant and pro-oxidants levels within the cells causes oxidative stress that could potentially leads to tissue damage (Voljc et al. 2011). Oxygen is required for different metabolic processes inside the body and tissue respiration; however, incomplete reduction of oxygen during metabolism yields highly reactive oxidizing molecules that are called reactive oxygen species (ROS). Oxidative stress occurs as a result of failure of the organism�s antioxidant system to neutralize ROS that is associated with several poultry diseases (Surai 2003; Avanzo et al. 2001; Iqbal et al. 2001). Oxidative stress has been linked to some poultry diseases, such as fatty liver, hemorrhagic disease, coccidiosis, and arthritis (Bottje and Wideman 1995; Papas 1999; Iqbal et al. 2002). The antioxidant system in birds could be enzymatic and non-enzymatic system (Surai 1999). The enzymatic antioxidants include SOD, CAT, GST (Fang et al. 2002). On the other hand, non-enzymatic antioxidants include GSH, vitamin E, C, selenium, and carotenoids. Oxidative stress and elevated ROS levels are associated with lipid peroxidation and MDA formation that causes membrane damage and cell death. Therefore, measuring the levels of tissue antioxidant and MDA levels is considered as a useful biomarker for oxidative stress (Surai 2003; Panda et al. 2008). Birds are frequently exposed to oxidative stress in farms that can damage DNA, proteins, lipids (McCall and Frei 1999) with subsequent health problems and poor performance (Lykkesfeldt and Svendsen 2007).  Here, we showed that TPV infection was associated with a remarkable oxidative stress as evidenced by a decrease in the enzymatic activities of SOD, CAT, GST and decreased GSH levels. Moreover, increased lipid peroxidation was also observed in infected birds as shown by increased MDA levels. Pre-treatment with artichoke extract and combined treatment with artichoke and neem extracts have shown a potent antioxidant effect as the levels of antioxidant enzymes, GSH and MDA were restored. Moreover, treatment with either artichoke or neem alone slightly restored the observed alterations in antioxidant levels.
Neem extract has previously been shown to possess antioxidant (Brahmachari 2004; Prakash et al. 2007) and anti-inflammatory (Schumacher et al. 2011) roles in the body by suppressing oxidative stress against infection through inhibiting the production of reactive oxygen species. Similarly, artichoke is rich in natural antioxidant, such as vitamin C, hydroxycinnamic acids, and flavones that revealed a good efficiency in the inhibition in vitro of LDL oxidation (Jim�nez-Escrig et al. 2003). Therefore, neem and artichoke were capable of alleviating the oxidative stress produced by pox virus in turkey.
In conclusion, artichoke extract can be given as a dietary supplement to provide an effective protection against pox viral infection during outbreaks. Moreover, when infected, birds can be treated with a combination of oral artichoke extract together with topical neem extract to alleviate lesions and oxidative stress associated with TPV infection.


Conflict of interest 
The authors have no conflict to declare.
Ethical approval 
The current study complies with national and international guidelines. All experimental procedures were approved by the research ethics committee at Mansoura University. 
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Figure Legends
Figure 1. Isolation of pox virus on embryonated chicken egg chorioallantoic membrane. Virus was isolated on CAM of 12 day old ECE for 3 passages with characteristic pock lesions. 
Figure 2. Agarose gel electrophoresis of PCR products for avian pox 4b gene. PCR products from negative control (lane 1), positive control (lane 2), and isolated virus (lane 3) were resolved in 1.5 % agarose gel stained with ethidium bromide; the sizes of the DNA ladder in bp (lane M) are shown.  
Figure 3. Disease progression in different experimental groups. Photos of birds from group 1 (A) and group 2 (B) four weeks PI are shown. Lesions in group 3 (C, D) were mild and appeared on head and under the wing (black arrows). Photos of birds from group 4 and 5 two weeks PI (E, G) and 22 days PI (F, H) are also shown. A photo of a bird in group 6 with a large nodule on the eyelid that became caseated and led to eye closure (I) that completely disappeared after oral administration of artichoke extract and local neem application (J).
Figure 4. Tissue antioxidants and oxidative stress markers in all studied groups. Activities of SOD (A), CAT (B), GST (C), as well as the levels of GSH (D) and MDA (E) were measured in tissue homogenates from liver, lung, and bursa. Bars labeled with different letters in each tissue denotes a �������&Fj56@PVWXY`{���������?��ϾϾϾ��ϾϾ���������n�n�n�T3hj|h�}�5�B*CJKH$OJPJQJ\�aJph+hj|h�}�5�B*CJOJQJ\�aJph%h�8�5�B*CJOJQJ\�aJphh
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