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Suggested Title: Prevalence of caseous lymphadenitis in sheep in Argentina (Patagonia).

Authors: Estevao Belchior, Silvia Graciela ; Abalos, María Andrea; Mas, Mirta ; Clapera, Eduardo ; Gallardo, Adriana Alicia; Alvarez, Laura Alejandra.

ID: 296125-2011



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4.REPORT: A large cohort has been used to determine the prevalence of ovine caseous lymphadenitis in southern Argentina. This is large sheep production region and the results which rely on a very large sample of 1 million animals appear to be accurate. The macroscopic and microscopic methods  confirmed the presence of CLA from carcass samples. The results should be of interest to the sheep and abbatoir industries. The survey would be of interest to many world agricultural organizations for comparison purposes and disease prevention.  However, the paper is not well written with numerous grammatical errors and these have been pinpointed in the attached text below.. The abstract is quite confusing and the authors have left out basic results (see alternative below), The introduction is relevant with  few minor changes required.  Matwerials and methods have grammar mistakes. The findings justify the conclusions.  Accept with minor modifications as suggested below.

 

Suggested ABSTRACT

A total of 1,023,793 Merino lambs and 196,737 adults (122,774 males and 73,963 females) carcasses were examined for caseous lymphadenitis (CLA).  Lamb, ewe and ram carcasses were examined visually and by palpation of   lymph nodes, lungs, liver and kidneys.  CLA was detected in 946 lambs (0.09%) and  19,798 adults (10.06%), with the thoracic cavity being involved in most cases. The lymph nodes more frequently affected were the pre-scapular, pre-femoral and supra-mammary and mediastinal lymph nodes. Visceral CLA was observed in 89% of cases with abscesses in the lung and liver. There was no significant increase in incidence during the study period.

INTRODUCTION

Sheep production is an economically important activity in Argentina, mainly in the Patagonian region. Sheep products such as wool, meat, hide and milk are supplied to the domestic and foreign markets (www.sagpya.mecon.gov.ar, 2005). However, infectious diseases are the major sources of morbidity and mortality in sheep, leading to substantial economic  losses. Among these, caseous lymphadenitis (CLA), also called boils, cheesy gland or thin ewe syndrome, is a common cause of sheep condemnation at slaughter, mainly affecting adults. The occurrence of CLA in sheep flocks may be as high as 30%, with an average of about 10% among adult sheep culled at abattoirs (Hollins 2008).

 

Corynebacterium pseudotuberculosis is the causative agent of CLA. The purulent contents of ruptured lesions are an important source of cross-infection between animals. The organism can be transmitted by contamination of skin wounds or acquired by penetration of intact skin and, probably, through mucous membranes of the digestive and respiratory tracts (Severini and others 2003; Fontaine and Baird 2008).  In Argentina there is very little epidemiological information on the prevalence of CLA, despite its impact on economy and human health. The aim of this short communications was to evaluate the occurrence of CLA and the distribution of associated lesions in culled sheep from Argentine Patagonia, on the basis of data collected from a sheep abattoir.

 

The frequency of the typical lesions caused by C. pseudotuberculosis was evaluated in the context of a survey carried out over the last few years in a slaughterhouse processing Merino and Corriedale sheep, located in Comodoro Rivadavia City, province of Chubut, southern Patagonia, Argentina.

Suggested MATERIALS and METHODS

Data sampling was performed between January 2000 and April 2007. The study design was non-experimental and cross-sectional. Animals < 6 mth age were classified as lambs and those over, as adult ewes or rams. Post-mortem inspection of animals was done following national standard criteria (Res. 475/07 de Ministerio de Economía y Producción de la Nación, SAGPYA). This included visual examination, palpation and incision of the main lymph nodes and other affected organs. Lymph nodes, lungs and liver were removed and kept at -20ºC until further analysis. Samples were cut with disinfected stainless steel knifes and contents were then exposed and characterized. The same were examined macroscopically for morphology, size, color and external/internal condition. Bacteriological examinations were performed on nodule and abscess samples (Estevao Belchior and others 2007).

 

         A case of CLA was recorded when visual inspection and palpation of lymph channels, organs and viscera showed consistency, abnormal size, purulent abscesses or cheese like matter.  Unaffected sheep did not show those characteristics. Confirmation of CLA was verified by isolation of bacterial cultures characterized by native strains of C. pseudotuberculosis biovar ovis.

 

         Univariate and multivariate statistical analyses were used to analyze changes in the variables of culled sheep; sheep affected by CLA, condemned carcasses and condemned viscera over the study period. Statistical analyses were performed using v. 15.0 Statistical Package for Social Sciences.

The seasonal variation in parasite prevalence was investigated using Analysis of Variance (ANOVA), Scheffe's test and Fisher's Least Significant Difference (LSD) test. A p value of <0.05 or less was considered statistically significant.

RESULTS

 

A total of 1,023,793 merino lambs and 196,737 merino adults (122,774 males and 73,963 females) were examined. Caseous lymphadenitis cases were detected in 946 lambs (0.09% of lambs examined) and in 19,798 adult sheep (10.06% of adults examined). The characterization established the distinctive features of the lesions of pseudotuberculosis in sheep from the southern Patagonian region of Argentina. The samples sizes were between 2 and 15 centimeter of diameter. Macroscopic observations showed a fibrous membrane enclosing necrotic tissue. Macroscopic observations showed a fibrous membrane enclosing necrotic tissue.

 

The lesions were classified into two types according to macroscopic characteristics of its contents: nodules (87%) and abscesses (13%). The content of the nodules were differentiated by the following features: 47% with caseous content, 21% with calcified foci, and 19% with necrotic tissue arranged in onion-like concentric layers. In pseudotuberculosos abscesses, necrotic tissue showed consistency of green thick pus. Bacteriological examination revealed the presence of C pseudotuberculosis in the nodules and abscesses analyzed. The number of sheep having abscesses and their location were as follows: 1,841 (93%) in carcasses, 16,752 (85%) in liver and 18,209 (92%) in lungs.

         Figure 1 shows the number of adult sheep slaughtered and the percentages of occurrence (number of positive cases per 100 cases examined) of CLA recorded from the harvest 1999-2000 to the harvest 2006-2007.

 

Figure 1. Number of sheep slaughtered and percentage of occurrence of CLA abscesses by harvest period (from July 1 of a year to June 30 of the following year).

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

After post-mortem veterinary inspection, half or quarter carcasses were condemned and sent to digesters. The mean monthly weight of condemned meat was 196 kg and that of condemned viscera was 208 kg. Figure 2 shows the mean monthly weights of meat and viscera condemned and processed in digesters during the study period.

 

Figure 2. Distribution of mean monthly weight of meat and viscera condemned and processed in digesters during the study period.

 

 

 

There was a positive association between the number of adult sheep slaughtered and the number of adult sheep with CLA each year (p<0.001). The weight of condemned meat was positively associated with the number of sheep exhibiting lesions (p<0.001). The analysis revealed a significant increase in prevalence in summer and autumn.

 

DISCUSSION

 

Published data show that ovine pseudotuberculosis is prevalent worldwide, and although it is accepted that CLA is present in the majority of the sheep-rearing areas, variations in prevalence have been observed in different geographic regions (Baird and Fontaine, 2009; Severini et al., 2003). The present study revealed a CLA frequency of 10% in adult sheep, with the thoracic cavity being involved in most cases.

 

No significant increase was found in the incidence of the disease in the study period. The lymph nodes more frequently affected were the superficial lymph nodes (prescapular, prefermoral and supramammary) and mediastinal lymph nodes. The visceral form was observed in 89% of the cases and abscesses occurred in lungs and liver. The predominance of visceral abscess is significant by the serious systemic effects in sheep and associated with significant economic losses by trimming and carcass rejection at abbatoir.

 

ACKNOWLEDGEMENTS

We acknowledge the owner and the staff of the slaughterhouse.

 

REFERENCES

 

Baird, G. J., Fontaine, M. C. (2007) Corynebacterium pseudotuberculosis and its Role in Ovine Caseus Lymphadenitis. Journal of Comparative Pathology 137, 179-210.

Estevao Belchior, S., Gallardo, A., Abalos, A., Diaz, Y., Alvarez, L., Callejo, R., Prieto, M., Jodor, N., Jensen, O. (2007) Diagnosis of caseous lymphadenitis in sheep from Patagonia. Revista Argentina de Microbiología 39, 44-46.

Fontaine, M.C., Baird, G.J. (2008) Caseous lymphadenitis. Small Ruminant Research 76, 42–48.

Hollins, J.D. (2008) Boils – Caseous Lymphadenitis (CLA) In: Farm Management Handbook, Falkland Islands Government, Department of Agriculture, Falkland Islands, pp. 1-3.

Severini, M., Ranucci, D., Miraglia, D., Cenci goga, B.T. (2003) Pseudotuberculosis in sheep as a concern of veterinary public health.  Veterinary Research Communities 27, 315–318.Abstract

This study was performed to determine the prevalence of antibodies to Neospora  caninum in dairy cattle herds in Shiraz, Fars province, southern Iran. Related risk factors for N. caninum infection as well as association of N. caninum seropositivity with abortion in the study herds were also investigated. A total of 32 herds were selected from dairy herds in the region and in each herd, blood samples were collected from nearly 10% of the herd population. Overall, 169 serum samples were obtained and detection of antibodies to N. caninum was undertaken using a commercial ELISA test. Data regarding to the history of recent abortion, keeping dogs on the farm, history of repeated abortion and accessibility of dogs or wild carnivores to feed stuff or aborted materials were obtained by questionnaire. Individual cow- and herd-level prevalence was 58 (95% CI: 50-66%) and 78% (95% CI: 63-93%), respectively. Thirty percent of the study herds had history of recent abortion and 8.7% of them had history of recurrent abortion. No association was observed between serologic status for N. caninum and abortion or recurrent abortion. No significant association was observed between keeping dogs on the farm and serologic status for N. caninum. The association between abortion and accessibility of wild carnivores to aborted materials was significant (P=0.006). Our results indicated that seroprevalence of N. caninum in our study herds is relatively high. However, further epidemiological studies are needed to evaluate the definite role of the infection in the region.

Keywords: abortion, Iran, Neospora  caninum, risk factors, seroprevalence.

 

 Introduction

Neospora caninum is an apicomplexan parasite and obligate intracellular parasite of animals with a wide host range (Dubey, 2003). It was first recognized in 1984 in dogs in Norway and subsequently has emerged as a serious disease of cattle and dogs worldwide (Dubey et al. 2007). Neospora caninum is now regarded as a major cause of bovine abortion with negative economic and reproductive impacts in the cattle industry (Dubey and Lindsay, 1996; Dubey, 1999). The economic impacts of infection with N. caninum in cattle herds include costs associated with abortion (Anderson et al. 1991; Hernandez et al. 2002), increased number of culled cows (Thurmond and Hietala, 1996) and decreased milk production (Thurmond and Hietala, 1997; Hernandez et al. 2001).

In the N. caninum life cycle, dogs (McAllister et al. 1998) and coyotes (Gondim et al. 2004) are both definitive hosts; cattle and other mammals are natural intermediate hosts (Dubey et al. 2007).

Seroprevalence of N. caninum in dogs, dairy cattle, beef cattle and other domestic animals have been determined in many countries (Dubey and Lindsay, 1996; Dubey, 2003). In Iran, there are several reports from various parts of the country about the seroprevalence of N. caninum antibodies in dairy and beef cattle farms (Sadrebazzaz et al. 2004; Razmi et al. 2006; Nourollahi Fard et al. 2008; Youssefi et al. 2009). Seroprevalence in individual cattle ranging from 12.6% in Kerman, south east of Iran (Nourollahi Fard et al. 2008) to 46% in Mashhad, north east of the country (Razmi et al. 2006) has been reported.  However, to the best knowledge of the authors, there is no report from Fars province concerning the seroepidemiologic status of dairy cattle regarding to the N. caninum infection. Therefore, this study was performed to determine the prevalence of antibodies to N. caninum in dairy herds in Shiraz, southern Iran. Related risk factors for N. caninum infection as well as association of N. caninum seropositivity with abortion in the herds were also investigated.

 

Materials and methods

This cross sectional study was conducted in Shiraz, the capital of Fars province, southern Iran during May to July 2009. Target population consisted of all dairy herds which were registered by Veterinary Organization of the province for brucellosis and tuberculosis control program. Overall, 32 herds were selected and in each herd, blood samples were collected from nearly 10% of the population. A total of 169 serum samples were obtained and sera were stored at -20ºC until use.

For serological examination and detection of antibodies to N. caninum, a commercial enzyme linked immunosorbent assay (ELISA) kit (Svanova Biotech AB, Sweden) was used. All sera were diluted 1:100 in PBS solution and according to the instruction of the manufacturer, samples with an absorbance value above the cut-off level of 0.20 were considered as positive.

A brief questionnaire was prepared and data regarding to the history of recent abortion in the herd, keeping dogs on the farm, history of repeated abortion and accessibility of dogs or wild carnivores to feed stuff or aborted materials were obtained by interview with the farmers.  

For statistical analysis, herd- and cow-level prevalence with 95% confidence interval (CI) was calculated. A herd with at least one individual positive sample was considered as positive. Association of suggested risk factors with N. caninum seroprevalence as well as association of N. caninum seropositivity with abortion in the herds was investigated using chi-square or Fisher's exact analysis. In all analysis, a P-value less than 0.05 was considered as statistically significant.

 

 Results

From 169 serum samples, a total of 98 samples (58%, 95% CI: 50-66%) were positive for antibody to N. caninum by ELISA. Twenty five out of 32 herds were positive with herd-level prevalence of 78% (95% CI: 63-93%). Dogs were kept in 55% of the herds. Nearly 87.5% of herds with dogs were positive for N. caninum in comparison with 69.2% of herds without dogs. However, the difference was not significant (P=0.23). More than 80% of farmers who keep dogs in the farm reported that their dogs were in closed situation and were not free in the farm; also more than 88% of dogs had not accessibility to feed stuff in the farm (Table 1).  

 Thirty percent of the study herds had history of recent abortion and 8.7% of them had history of recurrent abortion. No association was observed between serologic status for N. caninum and history of abortion (P=0.53) or recurrent abortion in the herds (P=0.49). Nearly 19% of farmers reported the possible accessibility of wild carnivores to aborted materials, and 53% refused to answer to this question. No association was observed between this variable and serologic status for N. caninum (Table 1).

No significant association was observed between keeping dogs on the farm and abortion problem. However, the association between abortion and accessibility of wild carnivores to aborted materials was highly significant (P=0.006); all herds (100%) with this risk factor had history of abortion compared with 20% of the herds without this risk factor. No significant relationship was observed between keeping dogs on the farm and accessibility of wild carnivores to aborted materials (P=0.14).

 

 Discussion

The serologic prevalences of N.  caninum in different countries indicate that there are considerable differences among countries, within countries and between regions (Dubey et al. 2007). Based on the results of the present study, the individual cow-level and herd-level prevalence of N. caninum in dairy cattle in Shiraz, southern Iran was 58 and 78%, respectively. Results of the present study indicate that the individual- and herd-level seroprevalence for N. caninum in Shiraz is relatively high. Neospora caninum has been detected in dairy herds in some other parts of the country. Razmi et al. (2006) reported a cow-level seroprevalence of 46% in 337 dairy cattle from 30 dairy herds in Mashhad, north eastern of the country; all selected dairy herds were positive in their study. The individual cow-level and herd-level prevalences in the present study are comparable with seroprevalences in Mashhad, but is relatively higher than prevalences reported from other parts of the country (Nourollahi Fard et al. 2008; Youssefi et al. 2009). As suggested by Dubey et al., the observed discrepancies may be due to differences in serologic techniques, study design and sample size in different regions (Dubey et al. 2007).   

Many studies have assessed risk factors for infection by N. caninum on the herd level. Presence and number of farm dogs have been associated with seropositivity in dairy herds in several epidemiologic studies (Corbellini et al. 2006; Pare´ et al. 1998; Schares et al. 2004), but no association has been detected in some other studies (Aguiar et al. 2006). The results of the present work did not show association for keeping dogs on the farm with N. caninum seroprevalence. Lack of association in this study may be related to the keeping conditions of dogs on the farms; most of the dogs were in closed status with no accessibility to feed stuff or aborted materials.

Studies on the association between N. caninum prevalence and abortion are numerous with conflicting results (Dubey et al. 2007). While many studies revealed a positive association between N. caninum and abortion on herd level (Hobson et al. 2005; Bartels et al. 1999; Sager et al. 2001), not all herds with a high seroprevalence suffer from N. caninum-associated abortion (Schares et al. 2004; Jensen et al. 1999; Dubey et al. 2007). It has been suggested that recent exposure to N. caninum infection as evidenced by seroconversion, does not necessarily result in increased abortion; furthermore this supports the hypothesis that some factors, other than the infection, may influence the abortion risk (Dubey et al. 2007).

The results showed that the risk of abortion was increased in farms with possibility of wild carnivores to feed on aborted materials. Although there was no significant relationship between presence and absence of dogs with accessibility of wild carnivores to aborted materials, the possibility of confounding effect of keeping dogs could not be eliminated due to the missing data for the latter variable.

 

Conclusion

The results indicated that seroprevalence of N. caninum in our studied herds is relatively high, but at least based on the present results it seems that this situation. From the epidemiologic point of view, retrospective assessment generally allows the identification of putative risk or protective factors, but conclusive data can be obtained only by prospective cohort or experimental studies (Dubey et al. 2007). Therefore, further epidemiological studies are needed to evaluate the definite role of the infection in the region. 

 

Acknowledgment

This study was supported by a grant from Shiraz University research council. The authors wish to thanks staff of Shiraz Veterinary Organization for valuable help in making this study possible.

 

References

Aguiar, D. M., Cavalcante, G. T., Rodrigues, A. A. R.,  Labruna, M. B.,  Camargo, L. M. A., Camargo, E. P. and Gennari, S. M. 2006. Prevalence of anti-Neospora caninum antibodies in cattle and dogs from Western Amazon, Brazil, in association with some possible risk factors. Vet. Parasitol. 142: 71–77.

Anderson, M.L., Blanchard, P.C., Barr, B.C., Dubey, J.P., Hoffman, R.L. and Conrad, P.A. 1991. Neospora-like protozoan infection as a major cause of abortion in California dairy cattle. J. of  Am. Vet. Med. Assoc. 198: 241–244.

Bartels, C.J.M., Wouda, W. and Schukken, Y.H. 1999. Risk factors for Neospora caninum-associated abortion storms in dairy herds in the Netherlands (1995 to 1997). Theriogenology 52: 247–257.

Corbellini, L. G., Smith, D.R., Pescador, C.A., Schmitz, M., Correa, A., Steffen, D.J. and Driemeier, D. 2006. Herd-level risk factors for Neospora caninum seroprevalence in dairy farms in southern Brazil. Prev. Vet. Med. 74: 130–141.

Dubey, J.P. and Lindsay, D.S. 1996. A review of Neospora caninum and neosporosis, Vet. Parasitol. 67: 1-59.

Dubey, J.P. 1999. Recent advances in Neospora and neosporosis. Vet. Parasitol. 84: 349–67.

Dubey, J.P., Schares, G., Ortega-Mora, L.M. 2007. Epidemiology and control of neosporosis and Neospora caninum.Clin. Microbiol. Rev., 20: 323–367

Dubey, J.P. 2003. Review of Neospora caninum and neosporosis in animals. Korean J. of  Parasitol. 41: 1-16.

 Gondim, L.F., McAllister, M.M., Pitt, W.C. and Zemlicka, D.E. 2004. Coyotes (Canis latrans) are definitive hosts of Neospora caninum. Int. J. of Parasitol. 34: 159–161.

Hernandez, J. and Risco, C., Donovan, A. 2001. Association between exposure to Neospora caninum and milk production in dairy cows. J. of Am. Vet. Med. Assoc. 219: 632–635.

Hernandez, J., Risco, C. and Donovan, A. 2002. Risk of abortion associated with Neospora caninum during different lactations and evidence of congenital transmission in dairy cows. J. of Am. Vet. Med. Assoc.221: 1742–1746.

Hobson, J. C., Duffield, T. F., Kelton, D., Lissemore, K., Hietala, S. K., Leslie, K. E.,  McEwen, B. and Peregrine, A. S. 2005. Risk factors associated with Neospora caninum abortion in Ontario Holstein dairy herds. Vet. Parasitol. 127: 177–188.

Jensen, A. M., Björkman, C., Kjeldsen, A. M., Wedderkopp, A., Willadsen, C., Uggla, A. and Lind, P. 1999. Associations of Neospora caninum seropositivity with gestation number and pregnancy outcome in Danish dairy herds. Prev. Vet. Med. 40:151–163.

McAllister, M.M., Dubey, J.P., Lindsay, D.S., Julley, W.R., Wills, R.A. and McGuire, A.M. 1998. Dogs are definitive hosts of Neospora caninum. Int. J. of Parasitol. 28: 1473–1478.

Nourollahi Fard, S.R., Khalili, M. and Aminzadeh, A. 2008. Prevalence of antibodies to Neospora caninum in cattle in Kerman province, South East Iran. Veterinarski Archiv, 78: 253-259.

Pare´, J., Fecteau, G., Fortin, M. and Marsolais. G. 1998. Seroepidemiologic study of Neospora caninum in dairy herds. J. of Am. Vet. Med.. Assoc. 213: 1595–1598.

Razmi, G.R., Mohammadi, G.R., Garrosi, T., Farzaneh,N., Fallah, A.H. and Maleki, M. 2006. Seroepidemiology of Neospora caninum infection in dairy cattle herds in Mashhad area, Iran. Vet. Parasitol. 135: 187–189.

Sadrebazzaz, A., Haddadzadeh, H., Esmailnia, K., Habibi, G., Vojgani, M. and Hashemifesharaki, R. 2004. Serological prevalence of Neospora caninum in healthy and aborted dairy cattle in Mashhad, Iran. Vet. Parasitol. 124: 201–204.

Sager, H., Fischer, I., Furrer, K., Strasser, M., Waldvogel, A., Boerlin, P., Audige´, L., and Gottstein, B. 2001. A Swiss case-control study to assess Neospora caninum-associated bovine abortions by PCR, histopathology and serology. Vet. Parasitol. 102: 1–15.

Schares, G., Ba¨rwald, A., Staubach, C., Ziller, M., Klo¨ss, D., Schroder, R., Labohm, R., Dra¨ger, K., Fasen, W., Hess, R.G., and Conraths, F.J. 2004. Potential risk factors for bovine Neospora caninum infection in Germany are not under the control of the farmers. Parasitol. 129:301–309.

Thurmond, M.C. and Hietala, S.K. 1996. Culling associated with Neospora caninum infection in dairy cows. Am. J. of Vet. Res. 57: 1559–1562.

Thurmond, M.C. and Hietala, S.K. 1997. Effect of congenitally acquired Neospora caninum infection on risk of abortion and subsequent abortions in dairy cattle. Am. J of Vet. Res 58: 1381–1385.

Youssefi, M.R., Arabkhazaeli, F. and Hassan, A.T.M. 2009. Seroprevalence of Neospora caninum infection in rural and industrial cattle in northern Iran. Iran. J.of Prasitol. 4: 15-18. 

 

Table 1. Distribution of risk factors for Neospora caninum antibodies in study dairy herds from Shiraz, southern Iran (2009)

 

 

Risk factors              Neospora positive herds                              Neospora negative herds       

                     N          %                     N          %

History of recent abortion                                                           

No                 17        85                    3          15

Yes                6          75                    2          25

                                                                    

History of recurrent abortion                                                                  

No                 21        80.8                 5          19.2

Yes                2          100                  0          0

                                                                    

Keeping dogs on the farm                                                           

No                 9          69.2                 4          30.8

Yes                14        87.5                 2          12.5

                                                                    

Keeping status of dogs a                                                              

Closed                      11        84.6                 2          15.4

Free              3          100                  0          0

                                                                    

Accessibility of dogs to feed stuff a                                                         

No                 11        78.6                 3          21.4

Yes                2          100                  0          0

                                                                    

Accessibility of wild carnivores to aborted materials                                                                 

No                 4          80                    1          20

Yes                4          66.7                 2          33.3

Refuse to answer                 15        88.2                 2         11.7

a: only for herds with keeping dogs 


©1996-20011All Rights Reserved. Online Journal of Veterinary Research.  You may not store these pages in any form except for your own personal use. All other usage or distribution is illegal under international copyright treaties. Permission to use any of these pages in any other way besides the  before mentioned must be gained in writing from the publisher. This article is exclusively copyrighted in its entirety to OJVR publications. This article may be copied once but may not be, reproduced or  re-transmitted without the express permission of the editors. Linking: To link to this page or any pages linking to this page you must link directly to this page only here rather than put up your own page


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