Scholarly article on topic 'Phage FR38 Treatment on Sprague Dawley Rat Inferred from Blood Parameters and Organ Systems'

Phage FR38 Treatment on Sprague Dawley Rat Inferred from Blood Parameters and Organ Systems Academic research paper on "Agriculture, forestry, and fisheries"

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Academic research paper on topic "Phage FR38 Treatment on Sprague Dawley Rat Inferred from Blood Parameters and Organ Systems"

HAYATI Journal of Biosciences September 2012 Vol. 19 No. 3, p 131-136 EISSN: 2086-4094

Available online at: http://journal.ipb.ac.id/index.php/hayati DOI: 10.4308/hjb.19.3.131

Phage FR38 Treatment on Sprague Dawley Rat Inferred from Blood Parameters and Organ Systems

DEWI SARTIKA1, SRI BUDIARTI2*, MIRNAWATI SUDARWANTO3

1Department of Food Technology, Faculty of Agriculture, Lampung University, Gedong Meneng Campus,

Bandar Lampung, 35147, Indonesia 2Department of Biology, Faculty of Mathematics and Natural Sciences, Bogor Agricultural University,

Darmaga Campus, Bogor, 16680, Indonesia 3Faculty of Veterinary Medicine, Bogor Agricultural University, Darmaga Campus, Bogor, 16680, Indonesia

Received March 8, 2012/Accepted August 27, 2012

The ability of phage FR38 to lysis indigenous Salmonella P38 from feces of diarrheal patient has been studied. However, effects of phage FR38 on organ system were not revealed as yet. This study was conducted to observe the effect of phage FR38 on blood chemistry, kidney functions, and liver functions. Twelve Sprague-Dawley rats were used as a model for this study that were divided into two groups; (i) control and (ii) treated group with phage FR38. For treated phage group, each rat was administered by 5 ml/kg bw of 1.59-107 pfu/ml of phage intragastric. The blood parameters were analysed on day 16. The results revealed that body and organs weight, erythrocyte, hematocrit, hemoglobin, leukocyte, total protein, creatinine, SGOT, and SGPT of phage treatment rats were not significantly different with the control rats on day 16 (P > 0.05). Therefore, this study showed was no effect of phage FR38 on body weight, blood chemistry, kidney and liver functions of the rat (P > 0.05).

Key words: phage FR38, blood chemistry, kidney functions, liver functions

INTRODUCTION

Salmonella is a food borne pathogenic bacteria that cause food borne and water borne disease (Delibato 2006). Salmonella were used as an indicator of food hygiene and food safety (Abedon 2008). Salmonella P38 that performed antibiotic resistant had been isolated from feces of diarrheal patient.

Contamination of Salmonella on food had been reported in orange juice and fresh orange (Castillo et al. 2006), apple cider product (Zhuang et al. 2005), beverage product (Li & Mustapha 2005), milk (Tadesse et al. 2005), apple juice (Izzo & House 2011), and fresh shrimp (Ray (2001). In Indonesia, chemical preservatives mostly were used to decrease microbe, however the chemical preservatives showed toxic effect. Food producers currently used illegal preservative such as, formaldehyde, aluminate and hydrogen peroxyde due to the high price of the legal preservatives. Illegal preservative, such formaldehyde, also cause a negative effect on organ and body cell. Base on presentation upon, other alternative to decrease microbe on food is needed.

Phage lytic is a preservative alternative on food processing (Rode et al. 2011), have an environmentally-friendly characteristic (Castro et al. 1991), non toxic and is easy to be isolated, such as from humans, cattle, pigs, and chickens (Duijkeren et al. 2002) and can be produced

'Corresponding author. Phone: +62-251-8622833, Fax: +62-251-8318942, E-mail: s_budiarti@yahoo.com

(Brenner et al. 1991; Maura & Debarbieux 2011). Phage lytic can be isolated from the environment as well such as soil, water, human body, fermented food (Lu et al. 2003a), vegetable fermentation (Lu et al. 2003b) and food products. Isolate of phage lytic can be taken from various food products e.g. cheese and yoghourt (Binneti & Reinheimer 2000), salad, crisp and lettuce (Kennedy 1986).

Phage application as a biocontrol food had been used to decrease a microbe contaminant on food, such as, Bacillus cereus phage in outbreaks of food poisoning (Ahmed et al. 1995), psychrotrophic phage to prevent spoilage process on food (Greer 2005), Xanthomonas phage to prevent a spot on tomato (Flaherty 2000), Listeria phage (Leverentz et al. 2004) and Salmonella enteriditis phage on melon and apple slices (Leverentz et al. 2001). Staphylococcus aureus phage also had been applied on milk as well as Salmonella enteritidis phage on cheese (Greer 2005), E. coli phage on beef steak (O'Neill et al. 2001) and on food processing (Rode et al. 2011), Flavobacterium columnare phage on fish (Laanto et al. 2011), Listeria and E. coli phage on meat (Anani et al. 2011), and on milk (ellis et al. 1973).

The other application of phage was as a microbe therapy (Chairns & Payne 2009), such as, by using Salmonella enterica phage (Pang et al. 2011), Yersinia pestis (Schofield et al. 2009), cancer cell (Browska et al. 2010), Mycobacterium phage (Foddai et al. 2011), Vibrio cholerae phage (Chakrabarti et al. 2000), Actinomycetes phage (Nerney et al. 2004), phage of methicillin resistant S. Aureus (O'Neill et al. 2001; Murchan et al. 2004),

Bacillus antrachis phage (Abshire et al. 2005), Listeria monocytogenes phage (Kim et al. 2012), phage of bacterial resistance to antibiotic (Edgar et al. 2011), and E. coli O18:K1:H7 phage (Bull et al. 2011). Phage therapy on poultry had been done by using of Salmonella enteriditis phage Sillankorva et al. (2010). The result of Budynek et al. (2010) points out that phage therapy on cancer patient can decrease the incident of microbe infection significantly. Ghaemi et al. (2010) reported that phage therapy on tumor can be done by use of ^-phage. Budiarti et al. (2011) reported that EPEC (Enteropathogenic Escherichia coli) can be degraded by phage isolated from the environment.

On preliminary study, phage FR38 had been used to decrease of Salmonella P38, an indigenous contaminant, on fresh milk and sausage. Nevertheless, the effect of phage FR38 on body damage was still unrevealed. Therefore, the aim of this study was to observe the effect of Salmonella P38 phage (phage FR38) on organs system by use Sprague Dawley's rat as the animal model.

MATERIALS AND METHODS

Phage Production. Palette of Salmonella P38 indigenous culture (OD=1) 108 cfu/ml were dropped by phage FR38 (1 ml) (collection of the second author), and were incubated at 37 oC for 30 minutes. The cocktail of Salmonella P38 phage were cultivated in 49 ml of nutrient broth (NB) medium, and incubated at 37 oC for 24 hours. After 24 hours incubation, bacteria-phage cocktail were centrifugated with 2800 rpm speed (Backman GPR Centrifuge), at 4 oC for 20 minutes. Supernatant (3 ml) were taken by using a 5 ml syringe and filtered by using Millipore membrane 0.22 ^m (Whatmann). The supernatant from filtration process were transferred into sterile tube (Clokie & Kropinski 2009). After double overlay process, the phage were counted by use Clokie and Kropinski formula, i.e., phage total = 1.59-107 + 2.449-107 pfu/ml (Figure 1).

Experimental Design. A total of 12 Sprague Dawley rats, all were in the same two months age rats were obtained from Veterinary Medicine Faculty, Bogor Agricultural University. Experimental rats were aclimitated at rat cage for 15 days, and then divided into two groups. The first group was rats as control and the other group was given by phage treatment. During adaptation, all of rat was fed with Japfa animal feed with standard drink (Table 1).

Research designs were the randomized control group post test design. The treatments of this research were control and phage treatment (5 ml phage FR38/kg bw; 1 ml = 1.59 x 107 pfu). Layout of experiment was arranged by coding of the sample, such as, control treatment code

(K1, K2, K3, K4, K5, and K6) and phage treatment code (P1, P2, P3, P4, P5, and P6). After treatment coding, rat code were placed in random position (Table 2).

Phage Treatment. All rats were weighed and were labeled with treatment codes. Body weights of rats were measured every two days for 15 days. The doses of treatment were (i) control group and (ii) Phage FR38 group. Each group was administered (5 ml kg-1 bw) by phage FR38 every day for 15 days.

Intragastric Administration. Treatment on rat (control group and Phage FR38 group) was carried out using 16 G intra-gastric syringe. For safety intra-gastric administration, the syringes were manipulated and added a bulbed needle.

Data Administration. After given the treatment for 15 days, data collected on day 16 by surgical technique on rat's body. The euthanasia processes of rat were used ether. The blood was taken from the posterior vena cava. The blood chemistry was analyzed for red cell (erythrocyte) and white cell number, hemoglobin, hematocrit, leukocyte differentiation (lymphocyte, neutrophil, eosinophil, and basophil), Serum Glutamic

Figure 1. The appearance of plaque phage FR38.

Table 2. Treatment and lay out design Lay out design

Location code Control lay out Location code Treatment lay out

1 K4 7 P2

2 K5 8 P1

3 K1 9 P6

4 K6 10 P5

5 K3 11 P3

6 K2 12 P4

Table 1. Feed and treatment given to the rats

Treatment Period (for 15 days)

Treatment Adaptation period (tor 14 days) -i-J—L-

Feed Treatment

Control Phage

Platelet from Jafpa

Platelet from Jafpa

phage = 1 ml/200g bw

Oxaloacetic Transaminase (SGOT), Serum Glutamic Pyruvic Transaminase (SGPT), creatinin, and total protein (Djojosoebagio 2007). The performances (shape and color) of rat feces also were collected for 16 days.

Statistical Analysis. Statistical analysis was carried out using Student's t-test. The results were presented as the mean differences between individual groups with P (less than or equal to) 0.05 consider statistically significant.

RESULTS

Body Weight. Body weights of rat were not significantly different for each group. We found that not significantly different in body weight between the two group treatments (P > 0.05) on day 0, 2, 4, 6, 8, 10, 12, 14, and 16. The average values of the body weight for each group were presented in Table 3. The body weight of phage treatment and control rat showed a normal growth characteristic. On day 1, the mean values of body growth control rat was 214.5 g (n = 6) and the body growth phage treatment rat was 212 g (n = 6). In the fact, the phage and control treatment, on day 1 up to 16, showed not significantly effect on body weight (P > 0.05) with the mean values of control rat was 250.47 g (n = 6) and phage FR38 rat was 255.83 g (n = 6). All of the phage treatment rats shown that the body growth rats were also tend in normal characteristics. The body growth of all controls the same high as all treatment rats. On the last treatment day, the body growth of phage treatment (SD = 8.295) and control (SD = 8.710) rat were uniform (Table 3).

Feces. Data of feces performances on day 0, 2, 4, 6, 8, 10, 12, 14, and 16 showed no difference among rats which had given by phage FR38 treatment and control (Table 4). The feces of phage FR38 rat and control rat were normal on day 0 up to 16.

Organ Weight. Large intestine, spleen, right kidney, left kidney, stomach, small intestine, heart, lung and liver weight the same for the groups (P > 0.05) on day 16 (Table 5). The organ weight of phage treatment was normal as well.

Erythrocyte. Hemoglobin and erythrocyte of rat blood for 16 day were not different for each group (control and phage group). We found not significantly effect in hemoglobin and erythrocyte in the two group treatments (P > 0.05). Hemoglobin number of control rat (n = 6) was similar as the phage treatment rat (n = 6) (P > 0.05) on day 16 day. Erythrocyte of control rat (n = 6) was as much as those in phage treatment rats (n = 6) (P > 0.05) on day 16. Median values of the hemoglobin and erythrocyte for each rat groups were presented in Table 6. Hematocrit value of control rat (n = 6) was also the same as phage treatment rat (n = 6) (P > 0.05).

The research results showed that thrombocyt value was not significantly different in the two group treatment (P > 0.05). Thrombocyt value of control rat (n = 6) was as much as phage treatment rat (n = 6) (P > 0.05) (Table 6) on day 16.

Leukocyte. Leukocyte total number of control rat was not significantly different in the two group treatments (P > 0.05). In this research, we also observed the

Table 3. Effect of phage treatment on body weight of rat

Day Control (g) Phage treatment (g)

0 214.5 + 3.782a 212.00 + 1.291a

2 217.55 + 4.579b 219.33 + 4.308b

4 219.86 + 5.317c 223.16 + 2.409c

6 224.19 + 6.156d 227.17 + 2.671d

8 227.78 + 6.494e 232.67 + 5.153e

10 233.47 + 7.360f 237.83 + 4.524f

12 239.05 + 5.007g 244.33 + 4.642g

14 244.3 + 8.335h 248.83 + 5.757h

16 250.47 + 8.710i 255.83 + 8.295i

The same letter in each row indicated not significantly different at P > 0.05.

Table 5. Effect of phage treatment on organ weight values of rat

Organ Control (g) Phage FR38 treatment (g)

Large intestine 22.573 + 2.292a 21.683 + 1.951a

Spleen 0.702 + 0.100b 0.673 + 0.210b

Right kidney 1.852 + 0.093c 1.842 + 0.055c

Left kidney 1.822 + 0.129d 1.840 + 0.069d

Stomach 9.760 + 1.615d 7.065 + 1.845d

Small intestine 7.007 + 0.776e 6.872 + 1.529e

Liver 10.103 + 0.761f 10.002 + 0.798f

Lung 1.992 + 0.126g 1.970 + 0.204g

Heart 0.813 + 0.065h 0.807 + 0.070h

The same letter in each row indicated not significantly different at P > 0.05.

Table 4. Effect of phage treatment on rat feces

Tre atm ent _0__2 4 6 8 10 12 14 16

Fs Fs Fs Fs Fs Fs Fs Fs Fs

F1 N N N N N N N N N

F2 N N N N N N N N N

F3 N N N N N N N N N

F4 N N N N N N N N N

F5 N N N N N N N N N

F6 N N N N N N N N N

K1 N N N N N N N N N

K2 N N N N N N N N N

K3 N N N N N N N N N

K4 N N N N N N N N N

K5 N N N N N N N N N

K6 N N N N N N N N N

N = Normal.

differentiation of white cell blood, such as, neutrophil, monocyte, eosinophil, lymphocyte, and basophil. The monocyte values of control rat were not significantly different in the two group treatment (P > 0.05). The monocyte value of control rat (n = 6) was as much as phage treatment rat (n = 6) (P > 0.05) on day 16 (Table 6).

The number of neutrophil after given the phage treatment was not increased. The neutrophil values of control rat showed not significantly different in the two group treatment (P > 0.05). The neutrophil value of control rat (n = 6) was as much as phage treatment rat (n = 6) (P > 0.05) on day 16. The result point out that the eosinophil count of controls (n = 6) showed not different value with the phage treatment (n = 6) on day 16 (P > 0.05). The basophil values of control rat also showed not significantly different in the two group treatments (P > 0.05). The neutrophil value of control rat (n = 6) as much as phage treatment rat (n = 6) (Table 6).

Lymphocyte value was not significantly different in the two group treatment (P > 0.05). The lymphocyte value of control rat (n = 6) as much as phage treatment rat (n = 6). Median values of the hemoglobin, hematocrit and erythrocyte for each rat group are presented in Table 6.

Total Protein. The value of protein total shown a total of the globulin and albumin value. Overall structure of the immunoglobulin molecule was determined by the sequence of amino acids. In this research, the protein total value was not significantly different in the two group treatment (P > 0.05). Protein total value of control rat was (n = 6) was as much as phage treatment rat (n = 6) (P > 0.05) (Figure 2) on day 16.

f l u i 1 1

40 -.39 .30 37 -.36 -.35 -34 .33 .32 -.31 ■ .30 -,29

1.394 + 0.743

1.331 + 0.527

Figure

Flia^ Control

Treatment

2. Effect phage FR38 treatment on creatinine value of rat.

Kidney Functions. Kidney functions parameter can be observed from blood, such as, creatinine. Increasingly of creatinine on the blood indicate an abnormal of kidney function. The result showed that the creatinine value was also not significantly different in the two group treatment (P > 0.05). The creatinine value of control rat (n = 6) as much as phage treatment rat (n = 6) on day 16 (P > 0.05) (Figure 3).

Liver Functions. Liver functions parameter can be observed from blood, such as, SGOT and SGPT values. Increasing of SGOT and SGPT on the blood indicate an abnormal of liver function. The result research showed that SGOT and SGPT value were also not significantly different between the two group treatments (P > 0.05). SGOT value of control rat (211.67 + 65.503 IU L-1) (n = 6) similar to phage treatment rat (193.50 + 34.735 IU L-1) (n = 6) (P > 0.05) on day 16. SGPT value ofcontrol rat (177.00 + 3 6.630 IU L-1) (n = 6) as much as phage treatment rat (176.67 +27.95 IU L-1) (n= 6) (P > 0.05) on day 16 (Table 7).

DISCUSSION

On the last day treatment, all of the treatments (phage and control) had no significantly effect on the body

6.43 6.42 6.42 ■

£ 6.41 -S

I 6.40 H 6.40 ■ 6.39 6.39

6.423 + 0.59

6.4 + 0.458

Control

Treatment

Figure 3. Effect of phage FR38 treatment on total protein values of rat.

Table 7. Effect of phage treatment on SGOT values of rat

Parameter Phage FR38 Control

SGOT 193.50 + 34.735a 211.67 + 65.503a

SGPT 176.67 + 27.955b 177.00 + 36.630b

The same letter in each row indicated not significantly different at P > 0.05.

Table 6. Effect of phage treatment on blood cell of rat

Blood cell differentiation Phage FR38 Control

Erythrocyte (106/mm3) 8.363 + 0.437a 8.922 + 1.358a

Hb (%) 12.643 + 0.798b 12.58 + 0.776b

PCV (%) 36.125 + 1.910c 37.125 + 2.032c

Thrombocyte (106/mm3) 119.167 + 13.86d 123.5 + 19.670d

Leukocyte (thousand/mm3) 8.425 + 0.687e 8.2 + 2.905e

Neutrophil (%) 20.667 + 9.331f 18.167 + 10.000f

Eosinophils (%) 1.333 + 1.033g 1.333 + 0.512g

Basophil (%) 0 0

Lymphocyte (%) 76.167 + 8.377h 78.167 + 11.600h

Monocyt (%) 1.833 + 1.329i 2.333 + 1.584i

The same letter in each row indicated not significantly different at P > 0.05.

weight (P > 0.05) with the mean values of control was 250.47 g (n = 6) and the body growth phage treatment rat was 255.83 g (n = 6). The mean values of normal body weight of adult rat (for 40-60 days) are 200-250 g, but, it is various depend on strain (Derelanko & Hollinger 2004). The normal body weights of rat (2.5-3.5 month old) are 267-500 g (male) and 225-325 g (female) (Meredith & Anna 2002). All of the phage treatment rat shown that the body growth rat were tend normal trend.

The result showed that organ weight of controls treatment as weight as phage FR38 treatment, at confidence level 99%, on day 16. This result was similar to the previous studies on rat that reported by Derelanko and Hollinger (2004), recorded that normal weight of right kidney were 1.839 + 0.222 g and left kidney were 1.717 + 0.155 g.

Erythrocyte, Hb, thrombocyte, and PCV values of rat were normal (P > 0.05). Based on research on rat that reported by Meredith and Anna (2002), the normal rat had hemoglobin (Hb) values = (11.1-18) g dl-1 and Hematocrit (PCV) = (36-52)%. It was similarly number from the previous study by Derelanko and Hollinger (2004) that the normal Hb of rat = (11-18) g dl-1; Erythrocyte = (6-10) x 106 mm-3-and PCV = (34-48)%. This showed that the mean of Hb, erythrocyte, PCV values of phage treatment rat were normal.

The results point out that the differentiation of white blood of control treatment was as much as in the phage treatment, at confidence level 99%, on day 16. It was not significantly different (P > 0.05) than the control treatment. The value was similarly from Derelanko and Hollinger (2004) study showed that a normal rat had values of leukocyte = (7-14) x 103 mm-3; neutrophils = (4-50)%; lymphocytes = (40-95)%; monocytes = (0-8)%; eosinophils = (0-2)%; basophils = (0-2)%; and total protein = (5.9-8.4) g dl-1. The results mean that the white blood and total protein values of phage treatment rat were normal; the phage FR38 had no effect on body rat.

Creatinin values of rat that had given phage treatment were not significantly different than control as well. The normal rat had a creatinin values = (0.39-2.29) mg dl-1 (Meredith & Anna 2002). The rat that had given phage treatment had SGOT values = (193.50 ± 34.735) IU L-1 and SGPT values = (176.67 + 27.955) IU L-1 were not significantly different than control (P > 0.05).

In conclusion, all parameters studied above showed not significantly different of P value between the two groups of rat (P > 0.05). Therefore, those indicated that the phage FR38 treatment did not effect to the rat body. Paracetamol treatment on rat increased of SGOT and SGPT values (Jawi et al. 2008), but natural functional drink did not effect on SGOT and SGPT values (Safithri et al. 2012).

ACKNOWLEDGEMENT

This research have been supported by Ministry of National Education Republic of Indonesia through Competitive Research Grant Team for Post Graduate Program (multi years program of Bogor Agricultural University), for which the authors are grateful.

REFERENCES

Abedon ST. 2008. Bacteriophage Ecology. Cambridge: Cambridge

Univ Pr. http://dx.doi.org/10.1017/CBO9780511541483 Abshire TG, Brown JE, Ezzell JW. 2005. Production and validation of the use of gamma phage for identification of Bacillus anthracis. J Clin Microbiol 43:4780-4788. http://dx.doi.org/ 10.1128/JCM.43.9.4780-4788.2005 Ahmed R, Mistry PS, Jackson. 1995. Bacillus cereus phage typing as an epidemiological tool in outbreaks of food poisoning. J Clin Microbiol 33:636-640. Anani H, Chen W, Pelton R. 2011. Biocontrol of L. monocytogenes and E. coli in meat by using phages immobilized on modified cellulose membranes. Appl Env Microbiol 77:6379-6387. http://dx.doi.org/10.1128/AEM.05493-11 Binetti AG, Reinheimer JA. 2000. Thermal and chemical inactivation of indigenous Streptococcus thermophilus bacteriophages isolated from Argentinian dairy plants. J Food Prot 63:509-515. Brenner FH, Stubbs AD, Farmer JJ. 1991. Phage typing of Salmonella enteritidis in the United States. J Clin Microbiol 29:2817-2823.

Browska K, Aski M, Owczarek B. 2010. The effect phage lysate on cancer cells in vitro. Clinic Exp Med 10:81-86. http:// dx.doi.org/10.1007/s10238-009-0066-9 Budiarti S, Pratiwi RH, Rusmana I. 2011. Infectivity of lytic phage to enteropathogenic Escherichia coli from Diarrheal patients in Indonesia. J US-China Med Sci 8:273-282. Budynek P, Dabrowska K, Skaradzinski G, Gorski A. 2010. Bacteriophages and cancer. Arch Microbiol 192:315-320. http://dx.doi.org/10.1007/s00203-010-0559-7 Bull JJ, Otto G, Molineaux IJ. 2011. In vivo growth rates are poorly correlated with phage therapy success in a mouse infection model. Antimicrob Agents Chem 56:949-954. http:/ /dx.doi.org/10.1128/AAC.05842-11 Cairns T, Payne J. 2009. Quantitative models of in vitro phage-host dynamics and their application to phage therapy. PLoS Pathogen J 5:20-25. Castillo A, Lopez M, Hidalgo G, Vitella. 2006. Salmonella and Shigella in orange juice and fresh orange. J Food Protect 69:2595-2599.

Castro D, Morinigo MA, Manzanares EM, Cornax R. 1991. Development and application of a new scheme of phages for typing and differentiating Salmonella strains from different sources. J Clin Microbiol 30:1418-1423. Chakrabarti AK, Ghosh AN, Nair GB. 2000. Bacteriology development and evaluation of a phage typing scheme for Vibrio cholerae O139. J Clin Microbiol 38:44-49. Clokie MRJ, Kropinski AM. 2009. Bacteriophages: Method and Protocols. UK: Humana Pr. http://dx.doi.org/10.1007/978-1-60327-565-1

Delibato E. 2006. Development of a SYBR green real-time PCR and multichannel electrochemical immunosensor for specific detection of Salmonella enterica. Anal Lett J 39:1611-1620. http://dx.doi.org/10.1080/00032710600713354 Derelanko MJ, Hollinger MA. 2004. Handbook Toxicology (2nd

Ed). USA: CRC Pr. Djojosoebagio S. 2007. Veterinary Physiology. Bogor: Bogor

Agricultural Univ. Duijkeren V, Wannet WJ, Houwers C. 2002. Serotype and phage type distribution of Salmonella strains isolated from humans, cattle, pigs, and chickens in the Netherlands from 1984 to 2001. J Clin Microbiol 40:3980-3985. http://dx.doi.org/ 10.1128/JCM.40.11.3980-3985.2002 Edgar R, Friedman R, Mor SM. 2011. Reversing bacterial resistance to antibiotic by phages-mediated delivery of dominant sensitive genes. Appl Env Microbiol 78:3744-3751. Ellis DE, Whitman PA, Marshall RT. 1973. Effects homologous bacteriophage on growth of Pseudomonas fragi WY in milk. Appl Env Microbiol 25:24-27. Flaherty JE, Jones JB, Harbaugh BK, Somodi GC, Jackson LE. 2000. Control of bacterial spot on tomato in the greenhouse and field with bacteriophages. Hort Sci 35:882-884.

Foddai A, Strain S, Whitlock RH, Elliott CT, Irene R, Grant. 2011. Clinical veterinary microbiology notes: application of a peptide-mediated magnetic separation-phage assay for detection of viable Mycobacterium vium subsp. paratuberculosis to bovine bulk tank milk and feces samples. J Clin Microbiol 49:2017-2019. http://dx.doi.org/10.1128/ JCM.00429-11

Gast RK, Benson ST. 1995. Comparative virulence for chicks of Salmonella. Avian Disease J 10:567-574. http://dx.doi.org/ 10.2307/1591810

Ghaemi A, Gill P, Jahromy SR, Roohvand F. 2010. Recombinant X-Phage Nanobioparticles for tumor therapy in mice models. Gen Vaccine Therapy J 8:3-10. http://dx.doi.org/10.1186/ 1479-0556-8-3

Greer G. 2005. Bacteriophage control of foodborne bacteria. J Food Prot 68:1102-1111.

Izzo MM, House JK. 2011. Prevalency of mayor enteric pathogen in Australian dairy calves. Australian Veterinary J 169:8-5.

Jawi K, Indrayani S, Sumardika, Yasa. 2008. Paracetamol effect on SGPT and SGOT of mice. Medicine J 21:57-59.

Kennedy JE. 1986. Methodology for enumeration of coliphage in food. App Environ Microbiol 51:956-962.

Kim JW, Dutta V, Elhanafi D. 2012. A novel restriction-modification system is responsible for temperature-dependent phage resistance in L. monocytogenes. Appl Env Microbiol 78:1995-2004. http://dx.doi.org/10.1128/AEM.07086-11

Laanto E, Sundberg LR, Bamford KH. 2011. Phage specificity of the fresh water fish pathogen F. columnar. Appl Env Microbiol 77:7868-7872. http://dx.doi.org/10.1128/AEM.05574-11

Leverrentz B, Conway WS, Alavidze Z. 2001. Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit. J Food Prot 64:1116-1121.

Leverrentz B, Conway WS, Jannisiewics W, Camp MJ. 2004. Optimizing concentration and timing phage spray on honeydew melon. J Food Prot 67:1682-1686.

Li R, Mustapha. 2005. Application PCR for detection E. coli, Shigella and Salmonella in raw and ready to eat meat product. Meat Sci J 20:402-406.

Lu Z, Breidt F, Flemming JR. 2003a. Bacteriophage ecology in commercial sauerkraut fermentation. Appl Environ Microbiol 69:3192-3202. http://dx.doi.org/10.1128/AEM.69.6.3192-3202.2003

Lu Z, Breidt F, Flemming JR. 2003b. Isolation and characterization of L. Plantarun bacteriophage. From cucumbar fermentation. Int J Food Microbiol 84:225-235. http://dx.doi.org/10.1016/ S0168-1605(03)00111-9

Maura D, Debarbieux L. 2011. Phages as twenty-first century antibacterial tools for food and medicine. Appl Microbiol Biotech J 90:851-860. http://dx.doi.org/10.1007/s00253-011-3227-1

Meredith, Anna. 2002. BSAVA Manual of Exotic Pets (4th Ed). British: BSAVA Pr.

Murchan S, Aucken HM, O'Neill GL. 2004. Emergence, spread, and characterization of phage variants of epidemic methicillin-resistant Staphylococcus aureus 16 in England and Wales. J Clin Microbiol 42:5154-5160. http://dx.doi.org/ 10.1128/JCM.42.11.5154-5160.2004

Nerney R, Kambashi R, Kinkese J. 2004. Mycobacteriology and aerobic actinomycetes development of a bacteriophage phage replication assay for diagnosis of pulmonary tuberculosis. J Clin Microbiol 42:52115-52120.

O'Neill GL, Murchan S, Setas AG. 2001. Epidemiology identification and characterization of phage variants of a strain of epidemic methicillin-resistant Staphylococcus aureus (EMRSA-15). J Clin Microbiol 39:1540-1548. http://dx.doi. org/10.1128/JCM.39.4.1540-1548.2001

Pang S, Octavia S, Reevers PR. 2011. Genetic relationship polymorphism typing of Salmonella enterica. J Clin Microbiol 50:3727-3734.

Ray B. 2001. Fundamental Food Microbiology. Washington DC: CRC Pr.

Rode TM, Axelsson L, Granum PE. 2011. High stability of stx2 phage in food and under food processing condition. Appl Env Microbiol 77:5336-5341. http://dx.doi.org/10.1128/AEM. 00180-11

Safithri M, Yasni S, Bintang M, Ranti AS. 2012. Toxicity study of antidiabetics functional drink of piper crocatum and cinnamomum burmannii. Hayati J Biosci 19:31-36. http:// dx.doi.org/10.4308/hjb.19.1.31

Schofield DA, Molineux IJ, Westwater C. 2009. Diagnostic bioluminescent phage for detection of Yersinia pestis. J Clin Microbiol 47:3887-3894. http://dx.doi.org/10.1128/JCM. 01533-09

Sillankorva S, Shaburova O, Santos S. 2010. Salmonella enteritidis phage candidates for phage therapy of poultry. J Appl Microbiol 108:1175-1187. http://dx.doi.org/10.1111/j.1365-2672.2009.04549.x

Tadesse G, Ashenafi M, Ephraim E. 2005. Survival E. coli, Shigella and Salmonella in Fermenting Borde (beverage). Meat Sci J 5:189-196.

Zhuang Z, Yu L, Mustapha A. 2005. Simultaneous detection of E.

coli, Salmonella, Shigella in apple cider. J Food Protect 67:27-33.

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