Newell DG et al. 2010. Food-borne diseases—the challenges of 20 years ago still persist while new ones continue to emerge. Int J Food Microbiol 139: S3–S15.
Scallan E, Kirk M, Griffin PM, 2013. Chapter 1: estimates of disease burden associated with contaminated food in the United States and globally. In: Foodborne Infections and Intoxications. 4th edition. Amsterdam, The Netherlands: Elsevier Inc., 3–18.
Kirk MD et al. 2015. World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis. PLoS Med 12: e1001940. Erratum in: PLoS Med 12, e1001940.
Global Foodborne Infections Network, 2010. Global Foodborne Infections Network: Strategic Plan 2011–2015. Geneva, Switzerland: Global Foodborne Infections Network.
Pickering AJ, Julian TR, Marks SJ, Mattioli MC, Boehm AB, Schwab KJ, Davis J, 2012. Fecal contamination and diarrheal pathogens on surfaces and in soils among Tanzanian households with and without improved sanitation. Environ Sci Technol 46: 5736–5743.
Rosas I, Báez A, Coutiño M, 1984. Bacteriological quality of crops irrigated with wastewater in the Xochimilco plots, Mexico City, Mexico. Appl Environ Microbiol 47: 1074–1079.
Ensink JHJ, Mahmood T, Dalsgaard A, 2007. Wastewater-irrigated vegetables: market handling versus irrigation water quality. Trop Med Int Health 12: 2–7.
Amoah P, Drechsel P, Abaidoo RC, Ntow WJ, 2006. Pesticide and pathogen contamination of vegetables in Ghana’s urban markets. Arch Environ Contam Toxicol 50: 1–6.
Beuchat LR, Farber JM, Garrett EH, Harris LJ, Parish ME, Suslow TV, Busta FF, 2001. Standardization of a method to determine the effiacy of sanitizers in inactivating human pathogenic microorganisms on raw fruits and vegetables. J Food Prot 64: 1079–1084.
Ravaliya K, Gentry-Shields J, Garcia S, Heredia N, Fabiszewski de Aceituno A, Bartz FE, Leon JS, Jaykus L-A, 2014. Use of Bacteroidales microbial source tracking to monitor fecal contamination in fresh produce production. Appl Environ Microbiol 80: 612–617.
Armon R, Dosoretz CG, Azov Y, Shelef G, 1994. Residual contamination of crops irrigated with effluent of different qualities: a field study. Water Sci Technol 30: 239–248.
Antwi-Agyei P, Cairncross S, Peasey A, Price V, Bruce J, Baker K, Moe C, Ampofo J, Armah G, Ensink J, 2015. A farm to fork risk assessment for the use of wastewater in agriculture in Accra, Ghana. PLoS One 10: 1–19.
Amoah P, Drechsel P, Henseler M, Abaidoo RC, 2007. Irrigated urban vegetable production in Ghana: microbiological contamination in farms and markets and associated consumer risk groups. J Water Health 5: 455–466.
Beuchat LR, Ryu J, 1997. Produce handling and processing practices. Emerg Infect Dis 3: 459–465.
Yakub GP, Castric DA, Stadterman-knauer KL, Tobin MJ, Blazina M, Heineman TN, Yee GY, Frazier L, 2002. Applications evaluation defined of colilert substrate and enterolert for methodology applications wastewater. Water Environ Res 74: 131–135.
Characklis GW, Dilts MJ, Simmons OD, Likirdopulos CA, Krometis L-AH, Sobsey MD, 2005. Microbial partitioning to settleable particles in stormwater. Water Res 39: 1773–1782.
Levy K, Hubbard AE, Nelson KL, Eisenberg JNS, 2009. Drivers of water quality variability in northern coastal Ecuador. Environ Sci Technol 43: 1788–1797.
Harris A, Pickering AJ, Harris M, Doza S, Islam MS, Unicomb L, Luby S, Davis J, Boehm AB, 2016. Ruminants contribute fecal contamination to the urban household environment in Dhaka, Bangladesh. Environ Sci Technol 50: 4642–4649.
Furness NH, Upadhyaya A, Upadhyaya MK, 2002. Comparison of three nondestructive methods for determination of vegetable surface area. HortScience 37: 550–553.
Siefring S, Varma M, Atikovic E, Wymer L, Haugland RA, 2008. Improved real-time PCR assays for the detection of fecal indicator bacteria in surface waters with different instrument and reagent systems. J Water Health 6: 225–237.
Reischer GH, Kasper DC, Steinborn R, Mach RL, Farnleitner AH, 2006. Quantitative PCR method for sensitive detection of ruminant fecal pollution in freshwater and evaluation of this method in alpine karstic regions. Appl Environ Microbiol 72: 5610–5614.
Cao Y, Griffith JF, Dorevitch S, Weisberg SB, 2012. Effectiveness of qPCR permutations, internal controls and dilution as means for minimizing the impact of inhibition while measuring Enterococcus in environmental waters. J Appl Microbiol 113: 66–75.
Arceneaux K, Nickerson DW, 2009. Modeling certainty with clustered data: a comparison of methods. Polit Anal 17: 177–190.
Harris LJ, Farber JN, Beuchat LR, Parish ME, Suslow TV, Garrett EH, Busta FF, 2003. Chapter 3: outbreaks associated with fresh produce: incidence, growth, and survival of pathogens in fresh and fresh-cut produce. Compr Rev Food Sci Food Saf 2: 78–141.
Beattie GA, Lindow SE, 1995. The secret life of foliar bacterial pathogens on leaves. Annu Rev Phytopathol 33: 145–172.
Ansari SA, Sattar SA, Springthorpe VS, Wells GA, Tostowaryk W, 1988. Rotavirus survival on human hands and transfer of infectious virus to animate and nonporous inanimate surfaces. J Clin Microbiol 26: 1513–1518.
Marples RR, Towers AG, 1979. A laboratory model for the investigation of contact transfer of micro-organisms. J Hyg (Lond) 82: 237–248.
Patrick DR, Findon G, Miller TE, 1997. Residual moisture determines the level of touch-contact-associated bacterial transfer following hand washing. Epidemiol Infect 119: 319–325.
Luby SP, Kadir MA, Yushuf Sharker MA, Yeasmin F, Unicomb L, Sirajul Islam M, 2010. A community-randomised controlled trial promoting waterless hand sanitizer and handwashing with soap, Dhaka, Bangladesh. Trop Med Int Health 15: 1508–1516.
Reller ME, Nelson JM, Ackman DM, Schoonmaker-bopp DJ, Root TP, Mintz EDA, 2006. Large, multiple-restaurant outbreak of infection with Shigella flexneri serotype 2a traced to tomatoes. Clin Infect Dis 42: 163–169.
Holvoet K, Sampers I, Seynnaeve M, Uyttendaele M, 2014. Relationships among hygiene indicators and enteric pathogens in irrigation water, soil and lettuce and the impact of climatic conditions on contamination in the lettuce primary production. Int J Food Microbiol 171: 21–31.
Pickering AJ, Julian TR, Mamuya S, Boehm AB, Davis J, 2011. Bacterial hand contamination among Tanzanian mothers varies temporally and following household activities. Trop Med Int Health 16: 233–239.
Mattioli MC, Boehm AB, Davis J, Harris AR, Mrisho M, Pickering AJ, 2014. Enteric pathogens in stored drinking water and on caregiver’s hands in Tanzanian households with and without reported cases of child diarrhea. PLoS One 9: e84939.
Luby SP, Halder AK, Huda T, Unicomb L, Johnston RB, 2011. The effect of handwashing at recommended times with water alone and with soap on child diarrhea in rural Bangladesh: an observational study. PLoS Med 8.
Soller JA, Schoen ME, Bartrand T, Ravenscroft JE, Ashbolt NJ, 2010. Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of faecal contamination. Water Res 44: 4674–4691.
WHO, 2004. Waterborne Zoonoses: Identification, Causes, and Control. London: IWA Publishing, Alliance House.
Hossain Z, 2001. Farmer’s view on soil organic matter depletion and its management in Bangladesh. Nutr Cycl Agroecosyst 61: 197–204.
Cordier J, 2013. Chapter 4: Microbiological Criteria and Indicator Microorganisms. In: Doyle MP, Buchanan R, eds. Food Microbiology: Fundamentals and Frontiers. 4th edition. Washington, DC: American Society for Microbiology Press, 81–90.
Mundt JO, 1963. Occurrence of enterococci on plants in a wild environment. Appl Microbiol 11: 141–144.
Leclerc H, Devriese LA, Mossel DAA, 1996. Taxonomical changes in intestinal (faecal) enterococci and streptococci: consequences on their use as indicators of faecal contamination in drinking water. J Appl Bacteriol 81: 459–466.
Müller T, Ulrich A, Ott EM, Müller M, 2001. Identification of plant-associated enterococci. J Appl Microbiol 91: 268–278.
Byappanahalli MN, Roll BM, Fujioka RS, 2012. Evidence for occurrence, persistence, and growth potential of Escherichia coli and enterococci in Hawaii’s soil environments. Microbes Environ 27: 164–170.
Byappanahalli MN, Yan T, Hamilton MJ, Ishii S, Fujioka RS, Whitman RL, Sadowsky MJ, 2012. The population structure of Escherichia coli isolated from subtropical and temperate soils. Sci Total Environ 417–418: 273–279.
Brennan FP, Grant J, Botting CH, O’Flaherty V, Richards KG, Abram F, 2013. Insights into the low-temperature adaptation and nutritional flexibility of a soil-persistent Escherichia coli. FEMS Microbiol Ecol 84: 75–85.
Weigand MR, Ashbolt NJ, Konstantinidis KT, Santo Domingo JW, 2014. Genome sequencing reveals the environmental origin of enterococci and potential biomarkers for water quality monitoring. Environ Sci Technol 48: 3707–3714.
World Health Organization, 2006. A Guide to Healthy Food Markets. Geneva, Switzerland: WHO
James J, ed., 2006. Microbial Hazard Identification in Fresh Fruits and Vegetables. New Jersey: John Wiley & Sons.
Olaimat AN, Holley RA, 2012. Factors influencing the microbial safety of fresh produce: a review. Food Microbiol 32: 1–19.
Ramos B, Miller FA, Brandão TRS, Teixeira P, Silva CLM, 2013. Fresh fruits and vegetables—an overview on applied methodologies to improve its quality and safety. Innov Food Sci Emerg Technol 20: 1–15.
Sapers GM, 2009. Chapter 16: Disinfection of contaminated produce with conventional washing and sanitizing technology. In: Matthews KR, Sapers GM, Gerba CP, eds. The Produce Contamination Problem: Causes and Solutions. 1st edition. Burlington, MA: Elsevier Inc., 393–424
Bartz JA, Yuk H, Mahovic MJ, Warren BR, Sreedharan A, Schneider KR, 2015. Internalization of Salmonella enterica by tomato fruit. Food Control 55: 141–150.
Penteado ANAL, Eblen BS, Miller AJ, 2004. Evidence of Salmonella internalization into fresh mangos during simulated postharvest insect disinfestation procedures. J Food Prot 67: 181–184.
Past two years | Past Year | Past 30 Days | |
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Abstract Views | 1732 | 1454 | 267 |
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Fresh produce items can become contaminated with enteric pathogens along the supply chain at the preharvest (e.g., irrigation water, soil, fertilizer) or postharvest (e.g., vendor handling or consumer handling) stages. This study assesses the concentrations of fecal indicator bacteria Escherichia coli, enterococci (ENT), and Bacteriodales on surfaces of carrots, eggplants, red amaranth leaves, and tomatoes obtained from both a wholesale market (recently harvested) and neighborhood retail markets in Dhaka, Bangladesh. We detected E. coli in 100% of carrot and red amaranth rinses, 92% of eggplant rinses, and 46% of tomato rinses. Using a molecular microbial source tracking assay, we found that 32% of produce samples were positive for ruminant fecal contamination. Fecal indicator bacteria were more likely to be detected on produce collected in retail markets compared with that in the wholesale market; retail market produce were 1.25 times more likely to have E. coli detected (P = 0.03) and 1.24 times more likely to have ENT detected (P = 0.03) as compared with wholesale market produce. Bacteriodales was detected in higher concentrations in retail market produce samples compared with wholesale market produce samples (0.40 log10 gene copies per 100 cm2 higher, P = 0.03). Our results suggest that ruminant and general fecal contamination of produce in markets in Dhaka is common, and suggest that unsanitary conditions in markets are an important source of produce fecal contamination postharvest.
Financial support: This work was supported by funding from the UPS Endowment Fund at Stanford, the US Agency for International Development, and the Center for International Security and Cooperation at Stanford University. Angela Harris was funded by an NSF Graduate Research Fellowship and a Stanford Graduate Fellowship.
Authors’ addresses: Angela R. Harris, Alexandria B. Boehm, Stephen Luby, and Jennifer Davis, Stanford University, Stanford, CA, E-mails: angelaharris@stanford.edu, aboehm@stanford.edu, sluby@stanford.edu, and jennadavis@stanford.edu. Mohammad Aminul Islam and Leanne Unicomb, International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh, E-mails: maislam@icddrb.org and leanne@icddrb.org. Amy J. Pickering, Tufts University, Medford, MA, E-mail: amyjanel@gmail.com.
Newell DG et al. 2010. Food-borne diseases—the challenges of 20 years ago still persist while new ones continue to emerge. Int J Food Microbiol 139: S3–S15.
Scallan E, Kirk M, Griffin PM, 2013. Chapter 1: estimates of disease burden associated with contaminated food in the United States and globally. In: Foodborne Infections and Intoxications. 4th edition. Amsterdam, The Netherlands: Elsevier Inc., 3–18.
Kirk MD et al. 2015. World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis. PLoS Med 12: e1001940. Erratum in: PLoS Med 12, e1001940.
Global Foodborne Infections Network, 2010. Global Foodborne Infections Network: Strategic Plan 2011–2015. Geneva, Switzerland: Global Foodborne Infections Network.
Pickering AJ, Julian TR, Marks SJ, Mattioli MC, Boehm AB, Schwab KJ, Davis J, 2012. Fecal contamination and diarrheal pathogens on surfaces and in soils among Tanzanian households with and without improved sanitation. Environ Sci Technol 46: 5736–5743.
Rosas I, Báez A, Coutiño M, 1984. Bacteriological quality of crops irrigated with wastewater in the Xochimilco plots, Mexico City, Mexico. Appl Environ Microbiol 47: 1074–1079.
Ensink JHJ, Mahmood T, Dalsgaard A, 2007. Wastewater-irrigated vegetables: market handling versus irrigation water quality. Trop Med Int Health 12: 2–7.
Amoah P, Drechsel P, Abaidoo RC, Ntow WJ, 2006. Pesticide and pathogen contamination of vegetables in Ghana’s urban markets. Arch Environ Contam Toxicol 50: 1–6.
Beuchat LR, Farber JM, Garrett EH, Harris LJ, Parish ME, Suslow TV, Busta FF, 2001. Standardization of a method to determine the effiacy of sanitizers in inactivating human pathogenic microorganisms on raw fruits and vegetables. J Food Prot 64: 1079–1084.
Ravaliya K, Gentry-Shields J, Garcia S, Heredia N, Fabiszewski de Aceituno A, Bartz FE, Leon JS, Jaykus L-A, 2014. Use of Bacteroidales microbial source tracking to monitor fecal contamination in fresh produce production. Appl Environ Microbiol 80: 612–617.
Armon R, Dosoretz CG, Azov Y, Shelef G, 1994. Residual contamination of crops irrigated with effluent of different qualities: a field study. Water Sci Technol 30: 239–248.
Antwi-Agyei P, Cairncross S, Peasey A, Price V, Bruce J, Baker K, Moe C, Ampofo J, Armah G, Ensink J, 2015. A farm to fork risk assessment for the use of wastewater in agriculture in Accra, Ghana. PLoS One 10: 1–19.
Amoah P, Drechsel P, Henseler M, Abaidoo RC, 2007. Irrigated urban vegetable production in Ghana: microbiological contamination in farms and markets and associated consumer risk groups. J Water Health 5: 455–466.
Beuchat LR, Ryu J, 1997. Produce handling and processing practices. Emerg Infect Dis 3: 459–465.
Yakub GP, Castric DA, Stadterman-knauer KL, Tobin MJ, Blazina M, Heineman TN, Yee GY, Frazier L, 2002. Applications evaluation defined of colilert substrate and enterolert for methodology applications wastewater. Water Environ Res 74: 131–135.
Characklis GW, Dilts MJ, Simmons OD, Likirdopulos CA, Krometis L-AH, Sobsey MD, 2005. Microbial partitioning to settleable particles in stormwater. Water Res 39: 1773–1782.
Levy K, Hubbard AE, Nelson KL, Eisenberg JNS, 2009. Drivers of water quality variability in northern coastal Ecuador. Environ Sci Technol 43: 1788–1797.
Harris A, Pickering AJ, Harris M, Doza S, Islam MS, Unicomb L, Luby S, Davis J, Boehm AB, 2016. Ruminants contribute fecal contamination to the urban household environment in Dhaka, Bangladesh. Environ Sci Technol 50: 4642–4649.
Furness NH, Upadhyaya A, Upadhyaya MK, 2002. Comparison of three nondestructive methods for determination of vegetable surface area. HortScience 37: 550–553.
Siefring S, Varma M, Atikovic E, Wymer L, Haugland RA, 2008. Improved real-time PCR assays for the detection of fecal indicator bacteria in surface waters with different instrument and reagent systems. J Water Health 6: 225–237.
Reischer GH, Kasper DC, Steinborn R, Mach RL, Farnleitner AH, 2006. Quantitative PCR method for sensitive detection of ruminant fecal pollution in freshwater and evaluation of this method in alpine karstic regions. Appl Environ Microbiol 72: 5610–5614.
Cao Y, Griffith JF, Dorevitch S, Weisberg SB, 2012. Effectiveness of qPCR permutations, internal controls and dilution as means for minimizing the impact of inhibition while measuring Enterococcus in environmental waters. J Appl Microbiol 113: 66–75.
Arceneaux K, Nickerson DW, 2009. Modeling certainty with clustered data: a comparison of methods. Polit Anal 17: 177–190.
Harris LJ, Farber JN, Beuchat LR, Parish ME, Suslow TV, Garrett EH, Busta FF, 2003. Chapter 3: outbreaks associated with fresh produce: incidence, growth, and survival of pathogens in fresh and fresh-cut produce. Compr Rev Food Sci Food Saf 2: 78–141.
Beattie GA, Lindow SE, 1995. The secret life of foliar bacterial pathogens on leaves. Annu Rev Phytopathol 33: 145–172.
Ansari SA, Sattar SA, Springthorpe VS, Wells GA, Tostowaryk W, 1988. Rotavirus survival on human hands and transfer of infectious virus to animate and nonporous inanimate surfaces. J Clin Microbiol 26: 1513–1518.
Marples RR, Towers AG, 1979. A laboratory model for the investigation of contact transfer of micro-organisms. J Hyg (Lond) 82: 237–248.
Patrick DR, Findon G, Miller TE, 1997. Residual moisture determines the level of touch-contact-associated bacterial transfer following hand washing. Epidemiol Infect 119: 319–325.
Luby SP, Kadir MA, Yushuf Sharker MA, Yeasmin F, Unicomb L, Sirajul Islam M, 2010. A community-randomised controlled trial promoting waterless hand sanitizer and handwashing with soap, Dhaka, Bangladesh. Trop Med Int Health 15: 1508–1516.
Reller ME, Nelson JM, Ackman DM, Schoonmaker-bopp DJ, Root TP, Mintz EDA, 2006. Large, multiple-restaurant outbreak of infection with Shigella flexneri serotype 2a traced to tomatoes. Clin Infect Dis 42: 163–169.
Holvoet K, Sampers I, Seynnaeve M, Uyttendaele M, 2014. Relationships among hygiene indicators and enteric pathogens in irrigation water, soil and lettuce and the impact of climatic conditions on contamination in the lettuce primary production. Int J Food Microbiol 171: 21–31.
Pickering AJ, Julian TR, Mamuya S, Boehm AB, Davis J, 2011. Bacterial hand contamination among Tanzanian mothers varies temporally and following household activities. Trop Med Int Health 16: 233–239.
Mattioli MC, Boehm AB, Davis J, Harris AR, Mrisho M, Pickering AJ, 2014. Enteric pathogens in stored drinking water and on caregiver’s hands in Tanzanian households with and without reported cases of child diarrhea. PLoS One 9: e84939.
Luby SP, Halder AK, Huda T, Unicomb L, Johnston RB, 2011. The effect of handwashing at recommended times with water alone and with soap on child diarrhea in rural Bangladesh: an observational study. PLoS Med 8.
Soller JA, Schoen ME, Bartrand T, Ravenscroft JE, Ashbolt NJ, 2010. Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of faecal contamination. Water Res 44: 4674–4691.
WHO, 2004. Waterborne Zoonoses: Identification, Causes, and Control. London: IWA Publishing, Alliance House.
Hossain Z, 2001. Farmer’s view on soil organic matter depletion and its management in Bangladesh. Nutr Cycl Agroecosyst 61: 197–204.
Cordier J, 2013. Chapter 4: Microbiological Criteria and Indicator Microorganisms. In: Doyle MP, Buchanan R, eds. Food Microbiology: Fundamentals and Frontiers. 4th edition. Washington, DC: American Society for Microbiology Press, 81–90.
Mundt JO, 1963. Occurrence of enterococci on plants in a wild environment. Appl Microbiol 11: 141–144.
Leclerc H, Devriese LA, Mossel DAA, 1996. Taxonomical changes in intestinal (faecal) enterococci and streptococci: consequences on their use as indicators of faecal contamination in drinking water. J Appl Bacteriol 81: 459–466.
Müller T, Ulrich A, Ott EM, Müller M, 2001. Identification of plant-associated enterococci. J Appl Microbiol 91: 268–278.
Byappanahalli MN, Roll BM, Fujioka RS, 2012. Evidence for occurrence, persistence, and growth potential of Escherichia coli and enterococci in Hawaii’s soil environments. Microbes Environ 27: 164–170.
Byappanahalli MN, Yan T, Hamilton MJ, Ishii S, Fujioka RS, Whitman RL, Sadowsky MJ, 2012. The population structure of Escherichia coli isolated from subtropical and temperate soils. Sci Total Environ 417–418: 273–279.
Brennan FP, Grant J, Botting CH, O’Flaherty V, Richards KG, Abram F, 2013. Insights into the low-temperature adaptation and nutritional flexibility of a soil-persistent Escherichia coli. FEMS Microbiol Ecol 84: 75–85.
Weigand MR, Ashbolt NJ, Konstantinidis KT, Santo Domingo JW, 2014. Genome sequencing reveals the environmental origin of enterococci and potential biomarkers for water quality monitoring. Environ Sci Technol 48: 3707–3714.
World Health Organization, 2006. A Guide to Healthy Food Markets. Geneva, Switzerland: WHO
James J, ed., 2006. Microbial Hazard Identification in Fresh Fruits and Vegetables. New Jersey: John Wiley & Sons.
Olaimat AN, Holley RA, 2012. Factors influencing the microbial safety of fresh produce: a review. Food Microbiol 32: 1–19.
Ramos B, Miller FA, Brandão TRS, Teixeira P, Silva CLM, 2013. Fresh fruits and vegetables—an overview on applied methodologies to improve its quality and safety. Innov Food Sci Emerg Technol 20: 1–15.
Sapers GM, 2009. Chapter 16: Disinfection of contaminated produce with conventional washing and sanitizing technology. In: Matthews KR, Sapers GM, Gerba CP, eds. The Produce Contamination Problem: Causes and Solutions. 1st edition. Burlington, MA: Elsevier Inc., 393–424
Bartz JA, Yuk H, Mahovic MJ, Warren BR, Sreedharan A, Schneider KR, 2015. Internalization of Salmonella enterica by tomato fruit. Food Control 55: 141–150.
Penteado ANAL, Eblen BS, Miller AJ, 2004. Evidence of Salmonella internalization into fresh mangos during simulated postharvest insect disinfestation procedures. J Food Prot 67: 181–184.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 1732 | 1454 | 267 |
Full Text Views | 1060 | 12 | 0 |
PDF Downloads | 217 | 18 | 0 |