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Comparative meta-analysis of feline leukemia virus and feline immunodeficiency virus seroprevalence correlated with GDP per capita around the globe
Research in Veterinary Science 125 (2019) 89–93
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Research in Veterinary Science journal homepage: www.elsevier.com/locate/rvsc
Comparative meta-analysis of feline leukemia virus and feline immunodeficiency virus seroprevalence correlated with GDP per capita around the globe
T
Kristen Ludwicka, , Jeffrey W. Clymerb ⁎
a b
Miami University, 501 E High St, Oxford, OH 45056, 6249 Aspen Ave, Cincinnati, OH 45224, United States of America Ethicon, Inc. 4545 Creek Rd, Cincinnati, OH 45242, United States of America
ARTICLE INFO
ABSTRACT
Keywords: Feline leukemia virus Feline immunodeficiency virus Feline infectious disease
Feline Leukemia Virus (FeLV) and Feline Immunodeficiency Virus (FIV) are two prevalent transmittable diseases for domestic cats. This paper reports the frequency of these two diseases compared globally across Gross Domestic Product (GDP) at purchasing power parity per capita (PPP). Information around FeLV and FIV rates of infection in specific locations around the world was analyzed from 47 published articles. Results show that based on the data available, the statistical model indicates that the highest percentage of FeLV or FIV infected cats live in areas of lower PPP (p ≤.001) with a decreasing rate of infection of FeLV and FIV with increasing income. Two theories for this could be that the lower PPP locations in this study were also in areas of greater feral cat and cat colony populations, as well as were areas with less emphasis on animal welfare and animal control programs. Additional research should be conducted to strengthen the study size in South America and Africa before further conclusions can be drawn.
1. Introduction Feline Leukemia Virus (FeLV) and Feline Immunodeficiency Virus (FIV) are two widespread infectious diseases that impact domestic cats all over the globe. These diseases cause immunosuppressive infections in cats and are linked to lymphomas, leukopenia, and tumors (Normand and Urbanek, 2017). Infection rates increase in cats with these diseases. Additionally, cats living in colonies, whether in shelters or in the wild, are the most susceptible. There is a direct association of virus infection to age, lifestyle, and health status (Oguzoglu et al., 2013). Methods of preventing these two retroviral infections in the feline population exist. Angtigenemia has been found in protected cats after receiving FeLV vaccines (Hofmann-Lehmann et al., 1995), and several different methods of vaccine administration are available (Grosenbaugh et al., 2004). Neutering has been shown to reduce aggression and therefore reduce the risk of FIV transmission in cat populations (Finker et al., 2011). Sexually intact free-roaming cats are at the highest risk of retroviral disease infection, so sterilization programs can assist with population control as well as reducing the spread of infectious disease. Cats are exceedingly adaptable creatures and live on all continents excluding Antarctica. Therefore, cats can live in any biome except tundra (Randerson, 2006). This paper focuses on the relationship
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between a country's income and disease seroprevalence rates of cats. Income was compared using an indicator that measures the amounts of goods and services that income could purchase in that country, Gross Domestic Product (GDP) at purchasing power parity per capita (PPP). The mission of this paper is to explore the incidence of FeLV and FIV in cats across PPP and draw conclusions from existing literature. Due to the complex interactions of animal welfare priorities compared to GDP at PPP, the anticipated findings are that there will be the highest seroprevalence of infectious disease rates in countries with lower PPP, as they are frequently in areas with less governing bodies, fewer capital, and smaller financial reserves. It is hypothesized that the lack of finances, and the increase in poverty and crime rates in these areas leave fewer resources for feral and domestic cat shelter, treatment, and population control. 2. Methods Articles were found through The Public Library of Cincinnati, using Google Scholar, and EBSCOhost Research Platform/EBSCO Industries online databases on the incidence of FeLV and FIV in various locations. Searches were conducted using the keywords “feline infectious disease” or “feline virus”, and articles were chosen based on abstracts, dates of
Corresponding author. E-mail addresses: [email protected] (K. Ludwick), [email protected] (J.W. Clymer).
https://doi.org/10.1016/j.rvsc.2019.05.013 Received 26 September 2018; Received in revised form 20 May 2019; Accepted 21 May 2019 0034-5288/ © 2019 Elsevier Ltd. All rights reserved.
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Fig. 1. Map of locations researched. Red shows the countries from which data was used in this report. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 2. FIV Probability of Infection as a Function of PPP. The odds ratio of FIV infection per USD thousand dollars of income was 0.954.
study, and topics discussed. The main criteria for acceptance of a study was that the study was conducted between 1989 and 2018, and reported FeLV and FIV rates of infection in specific locations around the world. If duplicative studies were found from the same specific location, data from the more current study was used in this analysis. Multiple studies were used, when available, if they were in the same region but different cities. After locations were established, PPP was assigned to each location/article using the International Monetary Fund World Economic Outlook (2018). The chosen articles were analyzed, data extruded, and transcribed into an Excel spreadsheet. Data points extracted included the sample size of the study, the number positive for FeLV and FIV, and the number of co-infections, if listed. Binary logistic regression statistics were conducted on the incidence of FeLV and FIV in
the various countries using Minitab 17.1. These findings were compared among per capita incomes. 3. Results Information regarding FeLV and FIV infection rates was found in 47 regions (Fig. 1). Ten articles address the seroprevalence of FIV and FeLV in Asia, three in Africa, seventeen in Europe, nine in North America, four in Oceania, and four in South America (see Table 1, Appendix A). FeLV and FIV rates of infection were modeled via binary logistic regression using PPP (income) as the predictor. Based on the data available, the statistical models indicate that the results were highly significant (p < .001) with a decreasing rate of infection of both FeLV and 90
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Fig. 3. FeLV Probability of Infection as a Function of PPP. The odds ratio of FeLV infection per USD thousand dollars of income was 0.965.
the highest PPP of all locations researched, it did not have the lowest rates for FeLV or FIV. Rather, the locations in Oceania had the lowest rates of FeLV at 2.34% (Fig. 4) and North America had the lowest rates of FIV at 7.70% (Fig. 5), compared to 10.13% and 12.40% respectively, for Europe. 4. Discussion The region with the highest percentage of FeLV was Africa, with the lowest percentage of FeLV seroprevalence in Oceania. The region with the highest percentage of FIV was also Africa, with the lowest percentage of disease seroprevalence in North America. Conclusions can be drawn from this information, as lower PPP economies have limited flexibility in regards to available finances allotted towards animal control, vaccines, or spay/neuter programs for cats, compared to high PPP economies. The locations with higher PPP have funding and resourcing available for shelters, veterinary care, and sterilization programs for feral cats. Overall, there are more resources and better programs in place for owned and feral cats in these locations (de Boo and Knight, 2002). Statistics on cat ownership and feral cat populations are lacking for much of the globe, due to lax rules and regulations in regards to companion animals and animal control. The World Society for the Protection of Animals (WSPA) states that countries in Europe and the United States place far more emphasis on animal welfare and sterilization of cats than other countries around the world (de Boo and Knight, 2002). The low PPP locations researched in this study are on the WSPA list of locations where animal care resources are low compared to the resources of higher PPP locations. One potential issue with this study is the smaller sample sizes of some regions. Studies in Africa only discuss the seroprevalence of disease in 315 cats, compared to the sample size of 28,575 cats in Europe. Regions in South America had smaller sample sizes as well, at 1627 cats surveyed, where by contrast, North American regions surveyed 20,077 cats. A lack of data from Africa and South America could have impacted the results of this study. However, GDP at PPP could play into the availability of resources to research and conduct studies on cat infectious diseases in these locations.
Fig. 4. FeLV rates of disease pervalence per PPP by region.
Fig. 5. FIV rates of disease pervalence per PPP by region.
FIV with increasing income (Figs. 4 and 5). The odds ratio for FIV infection per thousand dollars of income was 0.954 (95% CI: 0.952–0.957) (Fig. 2), and the odds ratio for FeLV infection per thousand dollars of income was 0.963 (95% CI: 0.960–0.965) (Fig. 3). Of the locations analyzed in this paper, the location with the lowest PPP was Africa (Fig. 4), at an average of $6033.00 PPP between the three African countries with data on FeLV and FIV disease seroprevalence. FeLV rates were the highest of all regions researched in Africa, at 22.80%, with South America being second highest (14.88%) (Fig. 4). FIV was the highest also in Africa, at 33.91% (Fig. 5). The location with the highest average PPP was Europe (Figs. 4 and 5), with an average $42,366.08 across seventeen locations. While Europe had
5. Conclusion In conclusion, the anticipated findings of this study were mostly 91
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supported by the data. There is a higher seroprevalence of infectious disease in locations with low PPP compared to locations of higher PPP. This could be because the lower income economies in this study have a higher percentage of feral cats and cat colonies, and there is less emphasis on animal welfare and animal control programs in these locations. Additional research should be conducted to strengthen the study size in South America and Africa before further conclusions can be drawn.
Acknowledgements Dr. Rachel Yoho for her encouragement and Stephanie Atkins for manuscript editing support. Funding This research did not receive any special grant from funding agencies in the public, commercial, or not-for-profit sectors.
Declarations of interest None. Appendix A Table 1
Articles containing disease seroprevalence rates of FIV and FeLV used in this research, organized by region. Based on available research, the following articles were used from each region. Region Asia
Africa Europe
North America
Oceania
South America
Article Akhtardanesh, B., Ziaali, N., Sharifi, H., & Rezaei, S. (2010). Bande, F., Arshad, S.S., Hassan, L., Zakaria, Z., Sapian, N.A., Rahman, N.A., & Alazawy, A. (2012). Baneth, G., Kass, P.H., Steinfeld, D., & Besser, M. (1999). Cong, W., Meng, Q.F., Blaga, R., Villena, I., Zhu, X.Q., & Qian, A.D. (2016). Hwang, J., Gottdenker, N., Min, M.S., Lee, H., & Chun, M.S. (2016). Lin, D., Lai, S., Bowman, D.D., Jacobson, R.H., Barr, M.C., Giovengo, S.L. (1990). Maruyama, S., Kabeya, H., Nakao, R., Tanaka, S., Sakai, T., Xuan, X. … Mikami, T. (2003). Nakamura, K., Miyazawa, T., Ikeda, Y., Sato, E., Nishimura, Y., Nguyen, N.T.P., … Mikami, T. (2000). Nakamura, K., Suzuki, Y., Ikeo, K., Ikeda, Y., Sato, E., Nguyen, N.T.P., … Miyazawa, T. (2003). Nedumpun, T., Piamsomboon, P., Chanchaithong, P., Taweethavonsawat, P., Chungpivat, S., & Suradhat, S. (2015). Muchaamba, F., Mutiringindi, T.H., Tivapasia, M.T., Dhliwayo, S., & Matope, G. (2014). Tiao, N., Darrington, C., Molla, B., Savielle, W.J.A., Tilahun, G., Kwok, O.C.H. … Dubey, J.P. (2013). Al-Kappany, Y.M., Lappin, M.R., Kwok, O.C.H., Abu-Elwafa, A., Hilali, M., & Dubey, J.P. (2011). Arjona A, Escolar E, Soto I, Barquero N, Martin D, Gomez-lucia E. (2000). Bandecchi, P., Matteucci, D., Baldinotti, F., Guidi, G., Abramo, F. Tozzini, F., & Bendinelli, M. (1992). Duarte, A., Castro, I., da Fonseca, I.M.P., Almeida, V., de Carvalho, L.M., Meireles, J., Fazendeiro, M.I., … Vaz, Y. (2009). Firth, C.L., Mostl, K. (2015). Gleich, S.E., & Hartmann, K. (2009). Gleich, S.E., Krieger, S., & Harmann, K. (2009). Hosie, M.J., Robertson, C., & Jarrett, O. (1989). Lutz, H., Lehmann, R., Winkler, G., Kottwitz, B., Dittmer, A., Wolfensberger, C., & Arnold, P. (1990). Lopes, A.P., Cardoso, L., & Rodrigues, M. (2008). Natasa, T., Svete A., N., Zemljic, M., Zakosek, M., & Darja, B.M. (2008). Oguzoglu, T.C., Muz, D., Timurkan, M.O., Maral, N., & Gurcan, I.S. (2013). Pavlova, E.V., Kirilyku, V.E., & Naidenko, S.V. (2015). Peri, E.V., Ponti, W., Dall'ara, P., Rocchi, M., Zecconi, A., Bonizzi, L. (1994) Spada, E., Proverbio, D., della Pepa, A., Perego, R., Baggiani, L., DeGiorgi, G.B., … Cremonesi, F. (2012). Tekelioglu, B.K., Berriatua, E., Turan, N., Helps, C.R., Kocak, M., Yilmaz, H. (2015). Ueland, K., & Lutz, H. (1992). Vilhena, H., Martinez-Diaz, V.L., Cardoso, L., Vieira, L., Altet, L., Francino, O., … Silvestre-Ferreira, A.C. (2013). Blanco, K., Prendas, J., Cortes, R., Jimenez, C., & Dolz, G. (2009). Danner, R.M., Goltz, D.M., Hess, S.C., & Banko, P.C. (2007). Dubey, J. P., Lappin, M.R., Kwok, O.C.H., Mofya, S., Chikweto, A., Baffa, A., Doherty, D, … Sharma, R. N. (2009). Kelly, P.J. Moura, L., Miller, T., Thurk, J., Perreault, N., Weil, A., Maggio, R., … Breitschwerdt, E. (2009). Levy, J.K., Scott, H.M., Lachtara, J.L., & Crawford, P.C. (2006). Little, S. (2011). Ortega-Pacheco, A., Aguilar-Caballero, A.J., Colin-Flores, R.F., Acosta-Viana, K.Y., Guzman-Marin, E., & Jimenez-Coello, M. (2014). Ravi, M., Wobeser, G.A., Taylor, S.M., & Jackson, M.L. (2010). Stojanovic, V., & Foley, P. (2011). Chang-Fung-Martel, J., Gummow, B., Burgess, G., Fenton, E., & Squires, R. (2013). Norris, J.M., Bell, E.T., Hales, L., Toribio, J.A., White, J.D., Wigney, D.I., … Malik, R. (2007). Luckman, C., & Gates, M.C. (2017). Westman, M.E., Paul, A., Malik, R., McDonagh, P., Ward, M.P., Hall, E., & Norris, J.M. (2016). de Almeida, N.R., Danelli, M.G.M., da Silva, L.H.P., Hagiwara, M.K., & Mazur, C. (2012). Lacerda, L.C., Silva, A.N., Freitas, J.S., Cruz, R.D.S., Said, R.A., & Munhoz, A.D. (2017). Mora, M., Napolitano, C., Ortega, R., Poulin, E., & Pizarro-Lucero, J. (2015). Nova, S.G., Bucafusco, D., Diaz, L.M., & Bratanich, A.C. (2016).
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Research in Veterinary Science journal homepage: www.elsevier.com/locate/rvsc
Comparative meta-analysis of feline leukemia virus and feline immunodeficiency virus seroprevalence correlated with GDP per capita around the globe
T
Kristen Ludwicka, , Jeffrey W. Clymerb ⁎
a b
Miami University, 501 E High St, Oxford, OH 45056, 6249 Aspen Ave, Cincinnati, OH 45224, United States of America Ethicon, Inc. 4545 Creek Rd, Cincinnati, OH 45242, United States of America
ARTICLE INFO
ABSTRACT
Keywords: Feline leukemia virus Feline immunodeficiency virus Feline infectious disease
Feline Leukemia Virus (FeLV) and Feline Immunodeficiency Virus (FIV) are two prevalent transmittable diseases for domestic cats. This paper reports the frequency of these two diseases compared globally across Gross Domestic Product (GDP) at purchasing power parity per capita (PPP). Information around FeLV and FIV rates of infection in specific locations around the world was analyzed from 47 published articles. Results show that based on the data available, the statistical model indicates that the highest percentage of FeLV or FIV infected cats live in areas of lower PPP (p ≤.001) with a decreasing rate of infection of FeLV and FIV with increasing income. Two theories for this could be that the lower PPP locations in this study were also in areas of greater feral cat and cat colony populations, as well as were areas with less emphasis on animal welfare and animal control programs. Additional research should be conducted to strengthen the study size in South America and Africa before further conclusions can be drawn.
1. Introduction Feline Leukemia Virus (FeLV) and Feline Immunodeficiency Virus (FIV) are two widespread infectious diseases that impact domestic cats all over the globe. These diseases cause immunosuppressive infections in cats and are linked to lymphomas, leukopenia, and tumors (Normand and Urbanek, 2017). Infection rates increase in cats with these diseases. Additionally, cats living in colonies, whether in shelters or in the wild, are the most susceptible. There is a direct association of virus infection to age, lifestyle, and health status (Oguzoglu et al., 2013). Methods of preventing these two retroviral infections in the feline population exist. Angtigenemia has been found in protected cats after receiving FeLV vaccines (Hofmann-Lehmann et al., 1995), and several different methods of vaccine administration are available (Grosenbaugh et al., 2004). Neutering has been shown to reduce aggression and therefore reduce the risk of FIV transmission in cat populations (Finker et al., 2011). Sexually intact free-roaming cats are at the highest risk of retroviral disease infection, so sterilization programs can assist with population control as well as reducing the spread of infectious disease. Cats are exceedingly adaptable creatures and live on all continents excluding Antarctica. Therefore, cats can live in any biome except tundra (Randerson, 2006). This paper focuses on the relationship
⁎
between a country's income and disease seroprevalence rates of cats. Income was compared using an indicator that measures the amounts of goods and services that income could purchase in that country, Gross Domestic Product (GDP) at purchasing power parity per capita (PPP). The mission of this paper is to explore the incidence of FeLV and FIV in cats across PPP and draw conclusions from existing literature. Due to the complex interactions of animal welfare priorities compared to GDP at PPP, the anticipated findings are that there will be the highest seroprevalence of infectious disease rates in countries with lower PPP, as they are frequently in areas with less governing bodies, fewer capital, and smaller financial reserves. It is hypothesized that the lack of finances, and the increase in poverty and crime rates in these areas leave fewer resources for feral and domestic cat shelter, treatment, and population control. 2. Methods Articles were found through The Public Library of Cincinnati, using Google Scholar, and EBSCOhost Research Platform/EBSCO Industries online databases on the incidence of FeLV and FIV in various locations. Searches were conducted using the keywords “feline infectious disease” or “feline virus”, and articles were chosen based on abstracts, dates of
Corresponding author. E-mail addresses: [email protected] (K. Ludwick), [email protected] (J.W. Clymer).
https://doi.org/10.1016/j.rvsc.2019.05.013 Received 26 September 2018; Received in revised form 20 May 2019; Accepted 21 May 2019 0034-5288/ © 2019 Elsevier Ltd. All rights reserved.
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Fig. 1. Map of locations researched. Red shows the countries from which data was used in this report. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 2. FIV Probability of Infection as a Function of PPP. The odds ratio of FIV infection per USD thousand dollars of income was 0.954.
study, and topics discussed. The main criteria for acceptance of a study was that the study was conducted between 1989 and 2018, and reported FeLV and FIV rates of infection in specific locations around the world. If duplicative studies were found from the same specific location, data from the more current study was used in this analysis. Multiple studies were used, when available, if they were in the same region but different cities. After locations were established, PPP was assigned to each location/article using the International Monetary Fund World Economic Outlook (2018). The chosen articles were analyzed, data extruded, and transcribed into an Excel spreadsheet. Data points extracted included the sample size of the study, the number positive for FeLV and FIV, and the number of co-infections, if listed. Binary logistic regression statistics were conducted on the incidence of FeLV and FIV in
the various countries using Minitab 17.1. These findings were compared among per capita incomes. 3. Results Information regarding FeLV and FIV infection rates was found in 47 regions (Fig. 1). Ten articles address the seroprevalence of FIV and FeLV in Asia, three in Africa, seventeen in Europe, nine in North America, four in Oceania, and four in South America (see Table 1, Appendix A). FeLV and FIV rates of infection were modeled via binary logistic regression using PPP (income) as the predictor. Based on the data available, the statistical models indicate that the results were highly significant (p < .001) with a decreasing rate of infection of both FeLV and 90
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Fig. 3. FeLV Probability of Infection as a Function of PPP. The odds ratio of FeLV infection per USD thousand dollars of income was 0.965.
the highest PPP of all locations researched, it did not have the lowest rates for FeLV or FIV. Rather, the locations in Oceania had the lowest rates of FeLV at 2.34% (Fig. 4) and North America had the lowest rates of FIV at 7.70% (Fig. 5), compared to 10.13% and 12.40% respectively, for Europe. 4. Discussion The region with the highest percentage of FeLV was Africa, with the lowest percentage of FeLV seroprevalence in Oceania. The region with the highest percentage of FIV was also Africa, with the lowest percentage of disease seroprevalence in North America. Conclusions can be drawn from this information, as lower PPP economies have limited flexibility in regards to available finances allotted towards animal control, vaccines, or spay/neuter programs for cats, compared to high PPP economies. The locations with higher PPP have funding and resourcing available for shelters, veterinary care, and sterilization programs for feral cats. Overall, there are more resources and better programs in place for owned and feral cats in these locations (de Boo and Knight, 2002). Statistics on cat ownership and feral cat populations are lacking for much of the globe, due to lax rules and regulations in regards to companion animals and animal control. The World Society for the Protection of Animals (WSPA) states that countries in Europe and the United States place far more emphasis on animal welfare and sterilization of cats than other countries around the world (de Boo and Knight, 2002). The low PPP locations researched in this study are on the WSPA list of locations where animal care resources are low compared to the resources of higher PPP locations. One potential issue with this study is the smaller sample sizes of some regions. Studies in Africa only discuss the seroprevalence of disease in 315 cats, compared to the sample size of 28,575 cats in Europe. Regions in South America had smaller sample sizes as well, at 1627 cats surveyed, where by contrast, North American regions surveyed 20,077 cats. A lack of data from Africa and South America could have impacted the results of this study. However, GDP at PPP could play into the availability of resources to research and conduct studies on cat infectious diseases in these locations.
Fig. 4. FeLV rates of disease pervalence per PPP by region.
Fig. 5. FIV rates of disease pervalence per PPP by region.
FIV with increasing income (Figs. 4 and 5). The odds ratio for FIV infection per thousand dollars of income was 0.954 (95% CI: 0.952–0.957) (Fig. 2), and the odds ratio for FeLV infection per thousand dollars of income was 0.963 (95% CI: 0.960–0.965) (Fig. 3). Of the locations analyzed in this paper, the location with the lowest PPP was Africa (Fig. 4), at an average of $6033.00 PPP between the three African countries with data on FeLV and FIV disease seroprevalence. FeLV rates were the highest of all regions researched in Africa, at 22.80%, with South America being second highest (14.88%) (Fig. 4). FIV was the highest also in Africa, at 33.91% (Fig. 5). The location with the highest average PPP was Europe (Figs. 4 and 5), with an average $42,366.08 across seventeen locations. While Europe had
5. Conclusion In conclusion, the anticipated findings of this study were mostly 91
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supported by the data. There is a higher seroprevalence of infectious disease in locations with low PPP compared to locations of higher PPP. This could be because the lower income economies in this study have a higher percentage of feral cats and cat colonies, and there is less emphasis on animal welfare and animal control programs in these locations. Additional research should be conducted to strengthen the study size in South America and Africa before further conclusions can be drawn.
Acknowledgements Dr. Rachel Yoho for her encouragement and Stephanie Atkins for manuscript editing support. Funding This research did not receive any special grant from funding agencies in the public, commercial, or not-for-profit sectors.
Declarations of interest None. Appendix A Table 1
Articles containing disease seroprevalence rates of FIV and FeLV used in this research, organized by region. Based on available research, the following articles were used from each region. Region Asia
Africa Europe
North America
Oceania
South America
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