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Three Months of Composting Are Enough to Eliminate the Fowl Typhoid Bacteria

ABSTRACT

The composting technique has been increasingly highlighted in poultry production units, as an efficient and low-cost solution for the destination of carcasses. The process is based on the accelerated decomposition of organic material under high temperatures, associated with eliminating pathogenic microorganisms. This study aims to evaluate the effectiveness and the time necessary for the elimination of Salmonella Gallinarum in carcasses of poultry submitted to the composting process. The composting was carried out following the models used in the field, and microbiological analysis was performed in five different periods: 45, 90, 120, 150 and 180-days after closing the composter. After 90 days of experiment and in the subsequent analysis, the elimination of the bacteria in 100% of the samples was verified, validating the composting process as an effective method for eliminating S. Gallinarum in poultry carcasses, when respecting the period necessary for the elimination of the bacteria and the good quality of the structure adopted for the process.

Keywords:
Avian salmonellosis; carcass slurry; poultry farm; Salmonella Gallinarum

INTRODUCTION

Fowl typhoid is an avian disease characterized by high mortality in mature flocks from broilers and semi-heavy laying hens (Oliveira et al., 2005Oliveira GHD, Berchieri Jr A, Fernandes AC. Experimental infection of laying hens with Salmonella enterica serovar Gallinarum. Brazilian Journal of Microbiology 2005; 36:51-56. https://doi.org/10.1590/S1517-83822005000100011
https://doi.org/10.1590/S1517-8382200500...
; Neto et al., 2007Neto OCF, Arroyave W, Alessi AC, et al. Infection of commercial laying hens with Salmonella Gallinarum: clinical, anatomopathological and haematological studies. Brazilian Journal of Poultry Science 2007; 9:133-141. https://doi.org/10.1590/S1516-635X2007000200010
https://doi.org/10.1590/S1516-635X200700...
). In general, the infection occurs orally: the bacteria crosses through the gastrointestinal pathway and evade the immune system due to its capacity to settle within avian macrophages (Huang et al., 2020Huang K, Fresno AH, Skov S, et al. Dynamics and outcome of macrophage interaction between Salmonella gallinarum, Salmonella typhimurium, and Salmonella dublin and macrophages from chicken and cattle. Frontiers in Cellular and Infection Microbiology 2020; 9:420. https://doi.org/10.3389/fcimb.2019.00420
https://doi.org/10.3389/fcimb.2019.00420...
), triggering a systemic infection, with a focus on the liver and spleen (Barrow & Neto, 2011Barrow PA, Neto OCF. Pullorum disease and fowl typhoid-new thoughts on old diseases: a review. Avian Pathology 2011; 40(1):1-13. https://doi.org/ 10.1080/03079457.2010.542575
https://doi.org/...
; Ojima et al., 2021Ojima S, Okamura M, Osawa N, et al. Characteristics of systemic infection and host responses in chickens experimentally infected with Salmonella enterica serovar Gallinarum biovar Gallinarum. The Journal of veterinary medical science 2021; 83(7):1147-1154. https://doi.or/10.1292/jvms.21-0227.
https://doi.or/10.1292/jvms.21-0227...
). Because of the systemic behaviour of infection, the carcasses of poultry stricken by fowl typhoid become a source of infection to those healthy ones (Berchieri et al., 2000).

Throughout the poultry production chain, the solid waste obtained is composed of feed, litter with excreta, incubation scraps, and chicken carcass (Costa et al., 2017Costa MSSM, Bernardi FH, Costa LAM, et al. Composting as a cleaner strategy to broiler agro-industrial wastes: Selecting carbon source to optimize the process and improve the quality of the final compost. Journal of Cleaner Production 2017; 142:2084-2092. https://doi.org/10.1016/j.jclepro.2016.11.075
https://doi.org/10.1016/j.jclepro.2016.1...
), which are a source of pathogenic bacteria, endangering the triad human-animals-environment (Chiarelotto et al., 2021Chiarelotto M, Restrepo JCPS, Lorin HEF, et al. Composting organic waste from the broiler production chain: A perspective for the circular economy. Journal of Cleaner Production 2021; 329:129717. https://doi.org/10.1016/j.jclepro.2021.129717
https://doi.org/10.1016/j.jclepro.2021.1...
). Thus, as a strategy for eliminating and inactivating pathogens, several procedures can be performed, such as alkaline hydrolysis, anaerobic digestion, incineration, and composting (Staroń et al., 2017; Arias et al., 2018Arias JZ, Reuter T, Sabir A, et al. Ambient alkaline hydrolysis and anaerobic digestion as a mortality management strategy for whole poultry carcasses. Waste Management 2018; 81:71-77. https://doi.org/10.1016/j.wasman.2018.09.049
https://doi.org/10.1016/j.wasman.2018.09...
; Avidov et al., 2021Avidov R, Varma VS, Saadi I, et al. Physical and chemical indicators of transformations of poultry carcass parts and broiler litter during short term thermophilic composting. Waste Management 2021; 119:202-214. https://doi.org/10.1016/j.wasman.2020.09.040
https://doi.org/10.1016/j.wasman.2020.09...
), preventing the spread of diseases and environmental contamination (Berge et al., 2009Berge ACB, Glanville TD, Millner PD, et al. Methods and microbial risks associated with composting of animal carcasses in the United States. Journal of the American Veterinary Medical Association 2009; 234(1):47-56. https://doi.org/ 10.2460/javma.234.1.47
https://doi.org/...
).

Composting is an easy method to perform and allows obtaining compound environmentally friendly (Singh et al., 2018Singh P, Mondal T, Sharma R, et al. Poultry waste management. International Journal of Current Microbiology and Applied Sciences 2018; 7(8):701-712. https://doi.org/10.20546/ijcmas.2018.708.077
https://doi.org/10.20546/ijcmas.2018.708...
), which is generated due to the activity of aerobic microorganisms (Prabakaran & Valavan, 2021Prabakaran R, Valavan SE. Wealth from poultry waste: an overview. World's Poultry Science Journal 2021; 77(2):389-401. https://doi.org/10.1080/00439339.2021.1901557
https://doi.org/10.1080/00439339.2021.19...
), and reducing the risk of nitrogen and phosphorus compounds spreading to water systems (Singh et al., 2018). Therefore, in view of the correct destination of poultry residues, to minimize the environmental impact and the epidemiology of avian diseases, the present study aimed to evaluate the efficiency of the composting process in the elimination of Salmonella Gallinarum from bird carcasses that died as a result of fowl typhoid.

MATERIAL AND METHODS

The study was conducted at the Laboratory of Avian Pathology of the Department of Animal Pathology from the School of Agricultural and Veterinary Sciences (FCAV/UNESP), Jaboticabal, Brazil. It was carried out following the Ethical Principles on Animal Experimentation approved by the internal Ethical Committee on the Use of Animals (Process nº 017354/18).

The composting process has been performed in five 60-liter plastic barrels (Plastienvases®, Mexico) with 695 mm height x 315 mm length x 310 mm width and with removable cover, and their structural arrangement following the distribution of layers described by (Irfan et al., 2020Irfan M, Mehmood S, Mahmud A, et al. An assessment of chemical and microbiological properties of different types of poultry waste compost prepared by bin and windrow composting system. Brazilian Journal of Poultry Science 2020; 22. https://doi.org/10.1590/1806-9061-2020-1278
https://doi.org/10.1590/1806-9061-2020-1...
): sawdust substrate, poultry litter, poultry carcasses, poultry litter, sawdust substrate, and water (Figure 1). The proportion of each layer is as follows: 1:10 part by weight of sawdust substrate, 3 parts by weight of poultry litter, 1 part by weight of poultry carcass, and 1/2 part by weight of water. The distribution pattern in the order described was successively repeated until the complete filling of the barrel, which was sealed, with no exposure of the material to the environment, vectors, or leakage of content, until its opening for sample collection. The carcasses used were from semi-heavy lineage from commercial laying chickens 22 weeks old, which died after an experimental infection by S. Gallinarum carried out within controlled environmental rooms (Rubio et al., 2021Rubio MS, Alves LBR, Viana GB, et al. Heat stress impairs egg production in commercial laying hens infected by fowl typhoid. Avian Pathology 2021; 50(2):132-137. https://doi.org/10.1080/03079457.2020.1845302
https://doi.org/10.1080/03079457.2020.18...
).

Microbiological analyses were performed at five different times: 45-, 90-, 120-, 150- and 180-days after closing the composter barrels. In each of these periods, 7 samples (5 g each) were randomly collected from each of the layers present in the barrels, totalizing 35 samples. All samples were placed into conical bottom tubes (Thermo Scientific™, Brazil) and led to the laboratory for immediate analysis.

Microbiological analyses were performed immediately after sampling at the end of each experimental period. Samples were homogenized directly into selenite broth supplemented with 0.4% of novobiocin (1:9). Then, each sample was plated on Brilliant Green agar containing nalidixic acid sodium as done previously (Rodrigues Alves et al., 2018Rodrigues Alves LB, Neto OCF, Batista DFA, et al. Inactivation of phoPQ genes attenuates Salmonella Gallinarum biovar Gallinarum to susceptible chickens. Brazilian Journal of Microbiology 2018;49(3):601-606. https://doi.org/10.1016/j.bjm.2017.09.006.
https://doi.org/10.1016/j.bjm.2017.09.00...
). After 24h of incubation, visual identification of characteristic colonies for the biovar S. Gallinarum on Brilliant Green agar plates was performed, followed by biochemical and serological confirmation (Grimont & Weill, 2007Grimont PAD, Weill FX. Antigenic formulae of the Salmonella serovars. 9th ed. Paris: WHO Collaborating Centre for Reference and Aesearch on Salmonella; 2007. p.1-166.; Brenner & Farmer, 2015Brenner DJ, Farmer, JJ. Enterobacteriaceae. In: Trujillo ME, Dedysh S, DeVos P, Hedlund B, Kämpfer P, Rainey FA, Withman WB, editors. Bergey's manual of systematics of archaea and bacteria hoboken. Hoboken: John Wiley & Sons; 2015. p. 1-24. ISBN: 9781118960608).

Figure 1
Distribution of layers: sawdust, poultry litter, carcass, and water, in the compost barrels used in this study.

RESULTS AND DISCUSSION

From all 35 samples collected from five experimental days (Figure 2), the presence of S. Gallinarum was identified in only 1/7 (14.29%) from the first experimental day (45 days of composting), which came from the bottom of the compost barrel, where the drained liquid accumulates of the process (slurry). In the following experimental periods (90-, 120-, 150, and 180-days), no bacteria were identified on the collected samples (0/28).

Figure 2
Number of positive samples from composting barrels at different collection days.

Composting can be done on-farm and is applicable in cases of mass animal deaths avoiding the spread of diseases (Wilkinson, 2006). Besides, it is considered a mitigation method of pathogens for the broiler production chain (Chiarelotto et al., 2021Chiarelotto M, Restrepo JCPS, Lorin HEF, et al. Composting organic waste from the broiler production chain: A perspective for the circular economy. Journal of Cleaner Production 2021; 329:129717. https://doi.org/10.1016/j.jclepro.2021.129717
https://doi.org/10.1016/j.jclepro.2021.1...
), in addition to promoting the biological conversion of carcasses into useful fertilizers products (Melo et al., 2022).

The correct management in poultry farms is the most effective measure used to action control fowl typhoid disease (Celis-Estupiñan et al., 2017Celis-Estupiñan ALP, Batista DFA, Cardozo MV, et al. Further investigations on the epidemiology of fowl typhoid in Brazil. Avian Pathology 2017; 46(4):416-425. https://doi.org/10.1080/03079457.2017.1299922.
https://doi.org/10.1080/03079457.2017.12...
). Standards regarding temperature, pressure, and humidity should be well-defined in the biosecurity measures when aiming for the complete elimination of pathogenic bacteria (Vaddella et al., 2016Vaddella V, Pitesky M, Cao W, et al. Assessing Salmonella typhimurium persistence in poultry carcasses under multiple thermal conditions consistent with composting and wet rendering. Poultry Science 2016; 95(3):705-714. https://doi.org/10.3382/ps/pev373
https://doi.org/10.3382/ps/pev373...
).

However, concerning the composting process, the variety of protocols used are divergent in the disposal of waste, litter material used, mixing or not of the material, and the opening or not of the biodigester during the process, which may justify the variety of results previously reported. (Orrico et al., 2010; Pandey et al., 2016Pandey P, Cao W, Wang Y, et al. Predicting Salmonella Typhimurium reductions in poultry ground carcasses. Poultry Science 2016; 95(11):2640-2646. https://doi.org/10.3382/ps/pew242
https://doi.org/10.3382/ps/pew242...
; Vaddella et al., 2016Vaddella V, Pitesky M, Cao W, et al. Assessing Salmonella typhimurium persistence in poultry carcasses under multiple thermal conditions consistent with composting and wet rendering. Poultry Science 2016; 95(3):705-714. https://doi.org/10.3382/ps/pev373
https://doi.org/10.3382/ps/pev373...
). Another important factor focusing on eliminating pathogens is the period in which the composing was closed, although the efficiency period is directly linked with the temperatures reached and their maintenance during the process of pathogens elimination (Vaddella et al., 2016). Despite no information on the temperature from the barrels having been recorded after the opening, our results showed that 90-days after the composting was closed was enough to completely eliminate Salmonella Gallinarum.

Divergent results regarding the minimum period necessary for the complete elimination of bacteria from Salmonella genus were reported using different methodologies. Orritco et al. (2010) and Esperón et al. (2020Esperón F, Albero B, Ugarte-Ruíz M, et al. Assessing the benefits of composting poultry manure in reducing antimicrobial residues, pathogenic bacteria, and antimicrobial resistance genes: a field-scale study. Environmental Science and Pollution Research 2020; 27(22):27738-27749. https://doi.org/10.1007/s11356-020-09097-1
https://doi.org/10.1007/s11356-020-09097...
), needed 100-120 days after closing the compost, while in the Paiva et al. (2011Paiva ECR, Matos AT, Sarmento AP, et al. Avaliação de sistema de tratamento de carcaças de frangos pelo método da composteira-windrow. Revista Eletrônica de Engenharia Civil 2011; 1(3):19-27. https://doi.org/10.5216/reec.v3i1.16820
https://doi.org/10.5216/reec.v3i1.16820...
) and Pandey et al. (2016Pandey P, Cao W, Wang Y, et al. Predicting Salmonella Typhimurium reductions in poultry ground carcasses. Poultry Science 2016; 95(11):2640-2646. https://doi.org/10.3382/ps/pew242
https://doi.org/10.3382/ps/pew242...
) experiments, bacteria were eliminated after 20- and 8-days, respectively. These divergences reinforce the need for a standard protocol for composting poultry carcasses since the main source of both contamination and permanence of S. Gallinarum in the poultry industry is the management in which the carcasses are improperly discarded or that they are not removed from the sheds (Oliveira et al., 2005Oliveira GHD, Berchieri Jr A, Fernandes AC. Experimental infection of laying hens with Salmonella enterica serovar Gallinarum. Brazilian Journal of Microbiology 2005; 36:51-56. https://doi.org/10.1590/S1517-83822005000100011
https://doi.org/10.1590/S1517-8382200500...
).

Despite only one positive sample having been recovered in the present study, it has come from the last layer of 45-days closed barrel, in the slurry accumulates, which highlights another composting concern: the structure of the composter. This liquid has a high concentration of organic compounds and contains highly soluble substances, it can contaminate groundwater and, consequently, the environment around the property and other crops that may be intended for human consumption (Vadella et al., 2016).

Vaz et al. (2019Vaz C, Rech D, Kramer B, et al. Cama de frango: influencia do manejo de reuso entre lotes na persistência de Salmonella Heidelberg. Avicultura Industrial 2019; 8:12-15.) described how this kind of environment can be propitious to the exchange of antimicrobial resistance elements between the bacteria present in that liquid when extravasated from the composter, accelerating both microbial adaptation and potentially leading to future problems involving the control of these pathogens. This reinforces the need to maintain correct composting sealing, to avoid the leakage of contaminated liquids into the environment, and to ensure the permanence time of the residues in the composter is respected.

To our knowledge, the composting process proved to be an effective method for eliminating S. Gallinarum in poultry carcasses. However, it is necessary to respect the period of completely closing the composter recipient to avoid environmental contamination by pathogenic microorganisms. In addition, the rigid implementation of the guidelines for the composting process can be safely adopted in poultry farms to present a financial return to the farmer without causing environmental impacts.

ACKNOWLEDGMENTS

This study was supported by São Paulo Research Foundation (FAPESP) [grant number 2019/23634-1 (GBV); in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001, and the National Council of Technological and Scientific Development (CNPq). The authors thank to LAVINESP (Laboratory of Avian Science - Unesp/FCAV) for kindly providing the structure for growing birds before the challenge.

REFERENCES

  • Rodrigues Alves LB, Neto OCF, Batista DFA, et al. Inactivation of phoPQ genes attenuates Salmonella Gallinarum biovar Gallinarum to susceptible chickens. Brazilian Journal of Microbiology 2018;49(3):601-606. https://doi.org/10.1016/j.bjm.2017.09.006
    » https://doi.org/10.1016/j.bjm.2017.09.006
  • Arias JZ, Reuter T, Sabir A, et al. Ambient alkaline hydrolysis and anaerobic digestion as a mortality management strategy for whole poultry carcasses. Waste Management 2018; 81:71-77. https://doi.org/10.1016/j.wasman.2018.09.049
    » https://doi.org/10.1016/j.wasman.2018.09.049
  • Avidov R, Varma VS, Saadi I, et al. Physical and chemical indicators of transformations of poultry carcass parts and broiler litter during short term thermophilic composting. Waste Management 2021; 119:202-214. https://doi.org/10.1016/j.wasman.2020.09.040
    » https://doi.org/10.1016/j.wasman.2020.09.040
  • Barrow PA, Neto OCF. Pullorum disease and fowl typhoid-new thoughts on old diseases: a review. Avian Pathology 2011; 40(1):1-13. https://doi.org/ 10.1080/03079457.2010.542575
    » https://doi.org/
  • Berchieri Jr A, Oliveira GHD, Pinheiro LAS, et al. Experimental Salmonella Gallinarum infection in light laying hen lines. Brazilian Journal of Microbiology 2000; 31:50-52. https://doi.org/10.1590/S1517-83822000000100012
    » https://doi.org/10.1590/S1517-83822000000100012
  • Berge ACB, Glanville TD, Millner PD, et al. Methods and microbial risks associated with composting of animal carcasses in the United States. Journal of the American Veterinary Medical Association 2009; 234(1):47-56. https://doi.org/ 10.2460/javma.234.1.47
    » https://doi.org/
  • Brenner DJ, Farmer, JJ. Enterobacteriaceae. In: Trujillo ME, Dedysh S, DeVos P, Hedlund B, Kämpfer P, Rainey FA, Withman WB, editors. Bergey's manual of systematics of archaea and bacteria hoboken. Hoboken: John Wiley & Sons; 2015. p. 1-24. ISBN: 9781118960608
  • Celis-Estupiñan ALP, Batista DFA, Cardozo MV, et al. Further investigations on the epidemiology of fowl typhoid in Brazil. Avian Pathology 2017; 46(4):416-425. https://doi.org/10.1080/03079457.2017.1299922
    » https://doi.org/10.1080/03079457.2017.1299922
  • Chiarelotto M, Restrepo JCPS, Lorin HEF, et al. Composting organic waste from the broiler production chain: A perspective for the circular economy. Journal of Cleaner Production 2021; 329:129717. https://doi.org/10.1016/j.jclepro.2021.129717
    » https://doi.org/10.1016/j.jclepro.2021.129717
  • Costa MSSM, Bernardi FH, Costa LAM, et al. Composting as a cleaner strategy to broiler agro-industrial wastes: Selecting carbon source to optimize the process and improve the quality of the final compost. Journal of Cleaner Production 2017; 142:2084-2092. https://doi.org/10.1016/j.jclepro.2016.11.075
    » https://doi.org/10.1016/j.jclepro.2016.11.075
  • Esperón F, Albero B, Ugarte-Ruíz M, et al. Assessing the benefits of composting poultry manure in reducing antimicrobial residues, pathogenic bacteria, and antimicrobial resistance genes: a field-scale study. Environmental Science and Pollution Research 2020; 27(22):27738-27749. https://doi.org/10.1007/s11356-020-09097-1
    » https://doi.org/10.1007/s11356-020-09097-1
  • Grimont PAD, Weill FX. Antigenic formulae of the Salmonella serovars. 9th ed. Paris: WHO Collaborating Centre for Reference and Aesearch on Salmonella; 2007. p.1-166.
  • Huang K, Fresno AH, Skov S, et al. Dynamics and outcome of macrophage interaction between Salmonella gallinarum, Salmonella typhimurium, and Salmonella dublin and macrophages from chicken and cattle. Frontiers in Cellular and Infection Microbiology 2020; 9:420. https://doi.org/10.3389/fcimb.2019.00420
    » https://doi.org/10.3389/fcimb.2019.00420
  • Irfan M, Mehmood S, Mahmud A, et al. An assessment of chemical and microbiological properties of different types of poultry waste compost prepared by bin and windrow composting system. Brazilian Journal of Poultry Science 2020; 22. https://doi.org/10.1590/1806-9061-2020-1278
    » https://doi.org/10.1590/1806-9061-2020-1278
  • Melo WS, Pereira N, Andrade EA, et al. Organic fertilizer produced from chicken carcasses on soybean production. International Journal of Recycling Organic Waste in Agriculture 2020; 11(3):355-362. https://doi.org/10.30486/ IJROWA.2021.1918036.1172
    » https://doi.org/10.30486/
  • Neto OCF, Arroyave W, Alessi AC, et al. Infection of commercial laying hens with Salmonella Gallinarum: clinical, anatomopathological and haematological studies. Brazilian Journal of Poultry Science 2007; 9:133-141. https://doi.org/10.1590/S1516-635X2007000200010
    » https://doi.org/10.1590/S1516-635X2007000200010
  • Ojima S, Okamura M, Osawa N, et al. Characteristics of systemic infection and host responses in chickens experimentally infected with Salmonella enterica serovar Gallinarum biovar Gallinarum. The Journal of veterinary medical science 2021; 83(7):1147-1154. https://doi.or/10.1292/jvms.21-0227
    » https://doi.or/10.1292/jvms.21-0227
  • Oliveira GHD, Berchieri Jr A, Fernandes AC. Experimental infection of laying hens with Salmonella enterica serovar Gallinarum. Brazilian Journal of Microbiology 2005; 36:51-56. https://doi.org/10.1590/S1517-83822005000100011
    » https://doi.org/10.1590/S1517-83822005000100011
  • Orrico Jr MAP, Orrico ACA, Lucas Jr J. Compostagem dos resíduos da produção avícola: cama de frangos e carcaças de aves. Engenharia Agrícola 2010; 30(3):538-545. http://dx.doi.org/10.1590/S0100-69162010000300017
    » http://dx.doi.org/10.1590/S0100-69162010000300017
  • Paiva ECR, Matos AT, Sarmento AP, et al. Avaliação de sistema de tratamento de carcaças de frangos pelo método da composteira-windrow. Revista Eletrônica de Engenharia Civil 2011; 1(3):19-27. https://doi.org/10.5216/reec.v3i1.16820
    » https://doi.org/10.5216/reec.v3i1.16820
  • Pandey P, Cao W, Wang Y, et al. Predicting Salmonella Typhimurium reductions in poultry ground carcasses. Poultry Science 2016; 95(11):2640-2646. https://doi.org/10.3382/ps/pew242
    » https://doi.org/10.3382/ps/pew242
  • Prabakaran R, Valavan SE. Wealth from poultry waste: an overview. World's Poultry Science Journal 2021; 77(2):389-401. https://doi.org/10.1080/00439339.2021.1901557
    » https://doi.org/10.1080/00439339.2021.1901557
  • Rubio MS, Alves LBR, Viana GB, et al. Heat stress impairs egg production in commercial laying hens infected by fowl typhoid. Avian Pathology 2021; 50(2):132-137. https://doi.org/10.1080/03079457.2020.1845302
    » https://doi.org/10.1080/03079457.2020.1845302
  • Singh P, Mondal T, Sharma R, et al. Poultry waste management. International Journal of Current Microbiology and Applied Sciences 2018; 7(8):701-712. https://doi.org/10.20546/ijcmas.2018.708.077
    » https://doi.org/10.20546/ijcmas.2018.708.077
  • Staron P, Kowalski Z, Staron A, et al. Thermal treatment of waste from the meat industry in high scale rotary kiln. International Journal of Environmental Science and Technology 2017; 14(6):1157-1168. https://doi.org/10.1007/s13762-016-1223-9
    » https://doi.org/10.1007/s13762-016-1223-9
  • Vaddella V, Pitesky M, Cao W, et al. Assessing Salmonella typhimurium persistence in poultry carcasses under multiple thermal conditions consistent with composting and wet rendering. Poultry Science 2016; 95(3):705-714. https://doi.org/10.3382/ps/pev373
    » https://doi.org/10.3382/ps/pev373
  • Vaz C, Rech D, Kramer B, et al. Cama de frango: influencia do manejo de reuso entre lotes na persistência de Salmonella Heidelberg. Avicultura Industrial 2019; 8:12-15.
  • Wilkinson KG. The biosecurity of on-farm mortality composting. Journal of Applied Microbiology 2007; 102(3):609-618. https://doi.org/10.1111/j.1365-2672.2006.03274.x
    » https://doi.org/10.1111/j.1365-2672.2006.03274.x

Publication Dates

  • Publication in this collection
    19 June 2023
  • Date of issue
    2023

History

  • Received
    20 Dec 2022
  • Accepted
    22 Mar 2023
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