Impact of Fermentation Systems on Salmonella spp. Detection in Broiler LitterABSTRACT
The reuse of poultry litter is a common practice in Brazil. However, it poses sanitary risks due to the persistence of Salmonella spp. This prospective observational study evaluated the effectiveness of two fermentation methods (windrow, T1; and flat, T2) in reducing the detection of Salmonella in broiler litter. A total of 196 litter samples were evaluated in the windrow fermentation system, and 194 in the flat fermentation system. Before fermentation, all litter samples were positive for Salmonella spp. Surface samples were collected using sterile swabs after seven days of fermentation to detect the pathogen. After fermentation, the risk of Salmonella positivity was lower in T1 (8.67%) than in T2 (20.10%). The relative risk (RR = 0.43; 95% CI: 0.25-0.73) indicated that windrow fermentation reduced Salmonella detection by 56.86% compared with flat fermentation. The prevented fraction in the exposed group (PFe = 56.86%) confirmed the protective effect of windrow fermentation. In this study, the results showed that, under the commercial conditions evaluated, windrow fermentation was associated with lower post-treatment Salmonella spp. detection than flat surface fermentation.
Keywords:
Poultry litter; public health; Salmonella; flat fermentation; sustainability; windrow fermentation
INTRODUCTION
Salmonella spp. is among the most important foodborne pathogens worldwide, and salmonellosis is a zoonotic bacterial disease with significant public health implications (Zizza et al., 2024). According to the World Health Organization, this pathogen is one of the four leading causes of diarrhea worldwide, and around 200 million to 1 billion cases of Salmonella infections are recorded globally every year (Lamichhane et al., 2024). Poultry products, including eggs, meats, and derivatives, remain the primary source of human infection (Gonzalez et al., 2015; Shaji et al., 2023).
Salmonella spp. is widely distributed in nature and has a complex epidemiology. It can be introduced into production systems through vectors such as water, feed, bedding, and contaminated equipment or footwear (Jones, 2011; Brito et al., 2019). Members of this genus can survive for extended periods in the environment, including in poultry litter (Jones, 2011; Pires et al., 2014; Voss-Rech et al., 2015; Brito et al., 2019; Frozza et al., 2022).
Although Canada and Europe recommend fresh litter bedding for every flock (Oladeinde et al., 2022), the reuse of litter across multiple broiler flocks is a widespread practice in Brazil and the United States (Muniz et al., 2014; Lopes et al., 2015; Oladeinde et al., 2022). This practice is economically and environmentally sustainable for Brazilian poultry farming (Roll et al., 2011; Toledo et al., 2020), as long as it complies with local legislation and does not pose a risk to the subsequent flock or public health (Brazil, 2007). Nevertheless, reused litter may be an important source of potentially pathogenic agents, including Salmonella (Vaz et al., 2017).
Considering that chickens remain in continuous contact with poultry litter from placement until slaughter, and that Salmonella can persist in the environment for extended periods, litter may act as a persistent source of contamination and may also contribute to the acquisition of virulence- or resistance-associated plasmids (Bucher et al., 2020; Frozza et al., 2022; Vaz, 2022). Therefore, appropriate litter management and treatment between flocks are essential to reduce microbial contamination (Roll et al., 2011; Vaz et al., 2017).
In Brazil, the most commonly adopted broiler litter treatment methods during the interval between flocks to reduce potential pathogens include quicklime application, flat fermentation with plastic tarpaulin cover, flat fermentation combined with quicklime application, and windrow fermentation, with or without plastic cover (Lopes et al., 2013; Martins et al., 2013; Liang et al., 2014; Muniz et al., 2014; Vaz et al., 2017; Voss-Rech et al., 2017). Alternative methods include ammonia gas application and competitive exclusion strategies applied to poultry litter (Bucher et al., 2020; Muniz et al., 2022; Rosa et al., 2023).
Fermentation is a biological method that involves the natural decomposition of organic matter mediated by bacterial and enzymatic action, producing heat, water vapor, ammonia, and carbon dioxide (Patterson & Adrizal, 2005; Gehring et al., 2020; Dornelas et al., 2023; Lima & Fontana, 2023). In general, the process begins with the action of mesophilic microorganisms that promote the hydrolysis of organic matter, heating the compost to approximately 65-68 °C and eliminating pathogens (Manogaran et al., 2022).
Both windrow fermentation and flat fermentation are practiced, with the latter being a common method in Brazilian poultry farming (Vaz et al., 2017). Flat fermentation requires less labor and generally reduces darkling beetle (Alphitobius diaperinus) populations. In contrast, windrow fermentation generally reduces or eliminates Salmonella spp., Campylobacter spp., and Clostridium perfringens (Lavergne et al., 2006; Dornelas et al., 2023).
Extensive literature is available on poultry litter treatments and their effects on pathogen reduction. However, most studies focus primarily on microbiological outcomes, without quantifying the magnitude of risk reduction achieved through epidemiological indicators under different management strategies. Therefore, this prospective observational study aimed to evaluate the effectiveness of two poultry litter fermentation methods-windrow and flat fermentation-in reducing the detection of Salmonella spp.
MATERIALS AND METHODS
Study Location
This prospective observational study was conducted over three months in commercial broiler chicken farms in the southern region of Brazil. This region is characterized by a humid subtropical climate, with abundant rainfall year-round and an average annual temperature of 19 °C. This study evaluated 390 poultry houses, representing 20.88% of the entire integration system of a single company. All evaluated litter samples were composed of wood shavings.
The poultry houses were randomly allocated to either the windrow or the flat fermentation treatment. All farms belonged to the same integrated poultry production system and followed standardized company protocols for management, nutrition, biosecurity, and health. The evaluated poultry houses had similar structural characteristics, measuring approximately 15 × 100 m and operating under an all-in/all-out rearing system with negative-pressure ventilation, compacted dirt floors, and an average housing capacity of approximately 19,600 birds. The company-established standard litter depth was 12 cm, the average downtime between consecutive flocks was 15 days, and stocking density ranged from 12 to 15 birds/m².
Selection Criteria
The poultry houses were selected based on a positive Salmonella spp. result detected through a drag swab evaluation conducted between 20 and 22 days of flock age, before slaughter. This evaluation is mandatory for poultry flocks under Brazilian legislation - Normative Instruction No. 20/2016 (Brazil, 2016). The detection was carried out in laboratories accredited by the Ministry of Agriculture and Livestock, following the methodology described in Ordinance No. 126/1995 (Brazil, 1995).
Experimental Design
After animal removal, the poultry houses were cleaned according to the company’s standard procedures, and residual feathers were burned using a gas flamethrower. The poultry houses were divided into two treatment groups: windrow fermentation (T1) and flat fermentation (T2). For T1 (n=196), the litter was longitudinally stacked in the center of the poultry house in a single windrow shape and then covered with a 200 µm thick plastic tarp, completely isolating it from the environment and preventing gas exchange. For T2 (n=194), the litter was covered with a 200 µm thick plastic tarp cover without prior piling. At the edges of the litter, near the side walls, poultry house partitions, and structural uprights, the tarp was manually adjusted, forming an envelope and completely isolating the litter from the environment, thereby preventing gas exchange. The fermentation time for both treatments was seven days.
During the fermentation process, temperatures were monitored in a convenience sample of 20 poultry houses from each treatment. The same poultry houses were evaluated on the second and seventh days of fermentation using a digital probe thermometer (Akso, São Leopoldo, Brazil). Temperature was measured at a single central point in each house. The probe was inserted to a depth of approximately 15 cm in the windrow treatment and 10 cm in the flat fermentation treatment, corresponding to the center of the litter mass. Additional measurements were performed at different locations within the litter on the sampling days to verify temperature uniformity. As no significant variation was observed among the different locations (data not shown), the central measurement was considered representative of the litter temperature.
Detection of Salmonella spp.
After the litter fermentation period, drag swabs were collected from the treated litter using sterile swabs placed over disposable plastic boots. Swabs were collected to cover multiple points of the litter surface. For T1, swab collection was performed directly on the windrow, and for T2, it was carried out on the litter distributed throughout the poultry house. After collection, the swabs were individually identified, placed in an isothermal box, and transported to the laboratory. Analyses were carried out within 24 hours.
The material was processed according to the methodology described in Ordinance 126/1995 (Brazil, 1995). A total of 15 mL of brain-heart infusion broth (BHI; Himedia, Kelton, PA, USA) was added to each sample. The material was homogenized and incubated at 36 ± 1 °C for 18-24 h. Then, 2 mL and 0.2 mL of this material were inoculated in 20 mL of tetrathionate broth (Oxoid, Hampshire, United Kingdom) with 4% novobiocin, and 20 mL of Rappaport-Vassiliadis broth (Merck, Darmstadt, Germany), respectively. The material was incubated at 41 ± 1 °C for 18-24 h. After the incubation period, the material was seeded on brilliant green (Merck, Darmstadt, Germany) and Hektoen (Himedia) agars and incubated at 37 ± 1 °C for 18-24 h. Characteristic colonies were selected for preliminary and complementary biochemical screening and serotyping.
Measures of Association and Impact
The risk ratio or relative risk (RR) was calculated by comparing windrow fermentation and flat fermentation to estimate the strength of the association between treatments and Salmonella spp. positivity. The RR can be estimated according to the following formula:
where p (Salmonella+| T1) represents the probability of detecting Salmonella spp. in poultry litter treated by windrow fermentation, and p (Salmonella+| T2) represents the probability of detecting Salmonella spp. in litter treated by flat fermentation. The RR estimates the association between exposure and outcome. An RR=1 indicates no difference in risk between groups; an RR>1 suggests increased risk, while an RR<1 suggests decreased risk.
The prevented fraction in the exposed group (PFe) was calculated using the following formula:
where RR is the risk ratio or relative risk.
Statistical Analysis
Data were statistically analyzed using Minitab software. RR was estimated using OpenEpi (www.openepi.com). Descriptive analysis was performed to determine the detection frequency of Salmonella spp. The Student’s t-test was used to compare the mean fermentation temperatures of both treatments. The chi-squared test was used to compare the results between the two treatments. Significance was set at p<0.05.
RESULTS
Detection of Salmonella spp.
The mean fermentation temperatures for T1 and T2 on days 2 and 7 are presented in Table 1. Statistically significant differences (p<0.0001) were observed between treatments on both days. Salmonella detection in litter after seven days of fermentation for T1 and T2 is shown in Table 1. Statistically significant differences (p=0.001) were observed between treatments.
Measures of Association and Impact
The measures of association are presented in Table 2. The risk of remaining positive for Salmonella spp. was 8.67% and 20.10% after treatments T1 and T2, respectively, indicating that T1 reduced the risk of Salmonella spp. detection in treated litter by 11.43% (risk difference in post-treatment positivity) compared with T2. The RR was 0.43.
The PFe for T1 was 56.86%, indicating that T1 reduced the risk of litter remaining positive at the end of the fermentation process by 56.86% compared with T2.
DISCUSSION
Brazilian legislation (IN 20/2016) allows the reuse of poultry litter. However, the litter must not test positive for S. Enteritidis, S. Typhimurium, S. Gallinarum, or S. Pullorum (Brazil, 2016). In the present study, none of the poultry litter samples tested positive for these regulated serovars. Therefore, according to the current Brazilian legislation, all treated litter samples were considered eligible for reuse. Despite its economic and environmental benefits, the reuse of poultry litter presents microbiological risks for the following flocks (Roll et al., 2011; Muniz et al., 2014; Oladeinde et al., 2022; Vaz, 2022). Thus, adequate treatment is needed before reuse (Toledo et al., 2020; Dornelas et al., 2023). Treatment may include litter fermentation (Palhares & Kunz, 2011) and the addition of quicklime (Lopes et al., 2015).
Studies evaluating litter treatment have adopted varied fermentation periods, ranging from 8-21 days (Palhares & Kunz, 2011; Bush et al., 2007; Sonoda et al., 2012; Martins et al., 2013). The fermentation period in this study was based on the results of a previous experimental inoculation of S. Enteritidis in poultry litter. In this experiment, bacterial counts dropped below the detection limit (100 CFU/g) after six days of fermentation for all tested groups, except for the control (Vaz et al., 2017). Thus, the fermentation period was established at seven days, which also facilitated the company’s logistical planning and the interval between flocks.
During the litter fermentation process, hydrolysis of complex elements occurs through microbial and enzymatic activities, resulting in the release of heat, ammonia, and water (Patterson & Adrizal, 2005; Amanullah et al., 2007; Muniz et al., 2014; Gehring et al., 2020). Ammonia is toxic to Salmonella spp. and to A. diaperinus, a vector for the bacteria in poultry environments (Voss-Rech et al., 2017; Gehring et al., 2020). The windrow fermentation method, adopted in T1, is based on heat generation; flat fermentation, used for T2, is based on the retention of ammonia (Vaz, 2022). Flat fermentation, a relatively recent method adopted in Brazilian poultry farms, is sustainable, cost-effective, efficient, and less labor-intensive. Nevertheless, its effectiveness depends directly on the adequate sealing of the litter to prevent ammonia volatilization and allow its sanitizing effect (Palhares & Kunz, 2011; Vaz et al., 2017).
During the fermentation process, temperature, in association with exposure time, is an effective physical agent for the inactivation of bacteria (Palhares & Kunz, 2011). According to Dumontet et al. (1999), the thermal inactivation of Salmonella spp. requires 80 min at 55 °C or 7.5 min at 60 °C. It is known that the reduction in Salmonella counts is associated with increased fermentation temperatures (Lavergne et al., 2006; Wilkinson et al., 2011). However, according to Vaz et al. (2017), other factors may also contribute to bacterial inactivation.
In this study, the mean temperature for T1 remained >50 °C throughout the seven days, while for T2 it remained <30 °C. Previous studies have demonstrated that windrow fermentation temperatures are maintained between 50 and 55 °C (Macklin et al., 2006; Macklin et al., 2008; Vaz et al., 2017). Flat fermentation, on the other hand, usually reaches temperatures ranging from 20 to 30 °C (Lavergne et al., 2006; Lopes et al., 2015; Vaz et al., 2017).
There is no consensus regarding poultry litter treatment. While Sonoda et al. (2012) demonstrated that both fermentation methods are effective in reducing Salmonella spp., Muniz et al. (2022) reported that fermentation practices commonly adopted to disinfect poultry litter prior to reuse do not reliably reduce pathogenic microorganisms, as they fail to generate ammonia gas at sufficiently high concentrations. These contrasting findings highlight the need for further investigation into fermentation-based treatments. Therefore, the present study provides additional evidence on the effectiveness of fermentation under practical poultry house conditions.
In this study, windrow fermentation (T1) exhibited significantly superior performance in Salmonella spp. inactivation when compared with flat fermentation (T2). The efficiency of T2 depends on ammonia retention, which contributes to Salmonella inactivation (Vaz et al., 2017; Gehring et al., 2020). One possible explanation for the lower performance of T2 observed in the present study is that complete sealing of the litter may have been difficult to achieve due to the poultry house structure, potentially limiting ammonia accumulation because of gas volatilization. However, because ammonia concentration, pH, and litter moisture were not measured, this hypothesis could not be directly evaluated.
Additionally, although the A. diaperinus population was not quantified, a greater number of live insects was qualitatively observed at the end of the fermentation period in T2 during field evaluations. Because these observations were not systematically recorded, they should be interpreted with caution. This observation was unexpected, as previous studies have demonstrated the effectiveness of flat fermentation in reducing the A. diaperinus population (Palhares & Kunz, 2011; Voss-Rech et al., 2017). Nevertheless, it may be related to the lower fermentation temperatures observed in T2, which remained below the recommended threshold (45 °C) (Wolf et al., 2015).
Several studies have discussed the reduction of Salmonella under different practices adopted prior to poultry litter reuse, as well as the importance of increased temperature and ammonia gas levels generated during composting (Macklin et al., 2006; Macklin et al., 2008; Pra et al., 2009; Vaz et al., 2017; Voss-Rech et al., 2017; Muniz et al., 2022; Vaz, 2022; Rosa et al., 2023). However, none of these studies employed risk-based association measures. In this study, windrow fermentation (T1) presented a markedly lower post-fermentation risk (8.67%) than flat fermentation (20.10%). The risk ratio (RR = 0.43; 95% CI: 0.25-0.73) indicates a 57% reduction in the risk of Salmonella spp. detection when using the windrow fermentation method. This effect is reinforced by the prevented fraction in the exposed population (PFe = 56.86%), which reflects the proportion of positive results prevented among the litter samples subjected to windrow fermentation. According to Dohoo et al. (2009), association measures are used to assess the magnitude of the relationship between exposure, in this case, litter fermentation, and the outcome, that is, whether the litter remained positive or became negative after treatment. These indicators are widely used in veterinary epidemiology.
Additionally, only the effects of fermentation were evaluated, as no additives (r.g. quicklime) were applied. The application of approximately 300 g/m2 of quicklime has been shown to be effective in controlling Salmonella spp. and Clostridium spp., primarily due to increased pH and reduced litter water activity (Aw) (Pra et al., 2009). In a study conducted by Lopes et al. (2015), the effect of quicklime application was greater than that of flat fermentation after 12 days of treatment, resulting in a significant reduction in Enterobacteriaceae contamination. Thus, it is suggested that additional treatments be applied to flat fermentation, such as the application of quicklime, for proper litter disinfection.
A limitation of this study is its observational design. The associations were assessed using unadjusted analyses, and potential confounding factors could not be controlled because detailed information on relevant covariates was not available. Consequently, the estimated relative risks should be interpreted with caution. In addition, litter samples were not collected immediately before the fermentation treatments; therefore, the pre-treatment Salmonella status was inferred from the mandatory pre-slaughter drag swab results obtained between 20 and 22 days of flock age. Furthermore, this study evaluated only two litter decontamination methods under the specific management conditions of a single integrated poultry production system, including the flock interval and poultry house characteristics adopted by the company. Therefore, caution should be exercised when extrapolating these findings to other production systems, and factors such as housing type, downtime between flocks, and labor availability should be considered when selecting a litter decontamination method prior to reuse. Future studies should include comprehensive baseline microbiological assessments, a broader set of explanatory variables, and multivariable statistical models to better evaluate the independent effect of litter fermentation methods on Salmonella control.
CONCLUSION
The results showed that, under the commercial conditions evaluated, windrow fermentation was associated with lower post-treatment Salmonella spp. detection than flat surface fermentation. The lower performance observed for flat fermentation may have been influenced by practical limitations affecting litter sealing; however, this hypothesis was not directly evaluated in the present study. Furthermore, the use of risk-based epidemiological measures provided a broader assessment of the sanitary impact of litter treatment strategies under commercial poultry production conditions.
ACKNOWLEDGEMENTS
None.
REFERENCES
- Amanullah MM, Somasundaram E, Vaiyapuri K, et al. Poultry manure to crops - a review. Agricultural Reviews 2007;28(3):216-22.
- Brasil. Ministério da Agricultura, Pecuária e Abastecimento. Portaria SDA nº 126, de 3 de novembro de 1995. Normas de credenciamento e monitoramento de laboratórios de diagnóstico das salmoneloses aviárias (S. Enteritidis, S. Gallinarum, S. Pullorum e S. Typhimurium). Diário Oficial da União 1995 nov 6; Seção 1:17694.
-
Brasil. Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa MAPA nº 56, de 4 de dezembro de 2007 [Internet]. Brasília, DF: Ministério da Agricultura, Pecuária e Abastecimento; 2007 [cited 2024 Oct 30]. Available from: https://www.gov.br/agricultura/pt-br/assuntos/sanidade-animal-e-vegetal/saude-animal/programas-de-saude-animal/pnsa/imagens/copy_of_INSTRUONORMATIVAN56DE4DEDEZEMBRODE2007.pdf/view
» https://www.gov.br/agricultura/pt-br/assuntos/sanidade-animal-e-vegetal/saude-animal/programas-de-saude-animal/pnsa/imagens/copy_of_INSTRUONORMATIVAN56DE4DEDEZEMBRODE2007.pdf/view -
Brasil. Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa MAPA nº 20, de 21 de outubro de 2016 [Internet]. Brasília, DF: Ministério da Agricultura, Pecuária e Abastecimento; 2016 [cited 2024 Oct 30]. Available from: https://www.gov.br/agricultura/pt-br/assuntos/sanidade-animal-e-vegetal/saude-animal/programas-de-saude-animal/pnsa/imagens/INSTRUONORMATIVAN20DE21DEOUTUBRODE2016.pdf
» https://www.gov.br/agricultura/pt-br/assuntos/sanidade-animal-e-vegetal/saude-animal/programas-de-saude-animal/pnsa/imagens/INSTRUONORMATIVAN20DE21DEOUTUBRODE2016.pdf -
Brito DAP, Sousa GLA, Souza YL, et al. Sources of paratyphoid Salmonella in the production chain of broilers in the Northern mesoregion of Maranhão State, Brazil. Semina: Ciências Agrárias 2019;40(6 Suppl 2):3021-34. https://doi.org/10.5433/1679-0359.2019v40n6Supl2p3021
» https://doi.org/10.5433/1679-0359.2019v40n6Supl2p3021 -
Bucher MG, Zwirzitz B, Oladeinde A, et al. Reused poultry litter microbiome with competitive exclusion potential against Salmonella Heidelberg. Journal of Environmental Quality 2020;49(4):869-81. https://doi.org/10.1002/jeq2.20081
» https://doi.org/10.1002/jeq2.20081 -
Bush DJ, Poore MH, Rogers GM, et al. Effect of stacking method on Salmonella elimination from recycled poultry bedding. Bioresource Technology 2007;98(3):571-8. https://doi.org/10.1016/j.biortech.2006.02.017
» https://doi.org/10.1016/j.biortech.2006.02.017 - Dohoo I, Martin W, Stryhn H. Veterinary epidemiologic research. 2nd ed. Charlottetown: VER Inc.; 2009. 865 p.
-
Dornelas KC, Mascarenhas NMH, Rocha PAS, et al. Chicken bed reuse. Environmental Science and Pollution Research 2023;30(14):39537-45. https://doi.org/10.1007/s11356-023-25850-8
» https://doi.org/10.1007/s11356-023-25850-8 -
Dumontet S, Dinel H, Baloda SB. Pathogen reduction in sewage sludge by composting and other biological treatments: a review. Biological Agriculture and Horticulture 1999;16(4):409-30. https://doi.org/10.1080/01448765.1999.9755243
» https://doi.org/10.1080/01448765.1999.9755243 -
Frozza R, Almeida LM, Brum JS. Evaluation of the active concentration of two disinfectants based on glutaraldehyde and benzalkonium chloride and antimicrobial activity in vitro against Salmonella heidelberg and Salmonella typhimurium. Arquivos do Instituto Biológico 2022;89:e0022021. https://doi.org/10.1590/1808-1657000022021
» https://doi.org/10.1590/1808-1657000022021 -
Gehring VS, Santos ED, Mendonça BS, et al. Alphitobius diaperinus control and physicochemical study of poultry litters treated with quicklime and shallow fermentation. Poultry Science 2020;99(4):2120-4. https://doi.org/10.1016/j.psj.2019.11.039
» https://doi.org/10.1016/j.psj.2019.11.039 - Gonzalez M, Lainez M, Vega S, et al. Sources for Salmonella contamination during pig production in eastern Spain. Journal of Animal and Veterinary Sciences 2015;2(5):37-42.
-
Jones FT. A review of practical Salmonella control measures in animal feed. Journal of Applied Poultry Research 2011;20(1):102-113. https://doi.org/10.3382/japr.2010-00281
» https://doi.org/10.3382/japr.2010-00281 -
Lamichhane B, Mawad AMM, Saleh M, et al. Salmonellosis: an overview of epidemiology, pathogenesis, and innovative approaches to mitigate the antimicrobial resistant infections. Antibiotics 2024;13(1):76. https://doi.org/10.3390/antibiotics13010076
» https://doi.org/10.3390/antibiotics13010076 - Lavergne TK, Stephens MF, Schellinger D, et al. In-house pasteurization of broiler litter [Publication 2955]. Baton Rouge: Louisiana State University Agricultural Center; 2006. p.1-16.
-
Liang Y, Payne JB, Penn C, et al. Systematic evaluation of in-house broiler litter windrowing effects on production benefits and environmental impact. Journal of Applied Poultry Research 2014;23(4):625-38. https://doi.org/10.3382/japr.2014-00960
» https://doi.org/10.3382/japr.2014-00960 -
Lima R, Fontana C. Eficiência do protocolo de fermentação em cama de aviário para controle de salmonela. Revista JRG de Estudos Acadêmicos 2023;6(13):1048-59. https://doi.org/10.5281/zenodo.8083041
» https://doi.org/10.5281/zenodo.8083041 -
Lopes M, Leite FL, Valente BS, et al. An assessment of the effectiveness of four in-house treatments to reduce the bacterial levels in poultry litter. Poultry Science 2015;94(9):2094-98. https://doi.org/10.3382/ps/pev195
» https://doi.org/10.3382/ps/pev195 -
Lopes M, Roll VF, Leite FL, et al. Quicklime treatment and stirring of different poultry litter substrates for reducing pathogenic bacteria counts. Poultry Science 2013;92(3):638-44. https://doi.org/10.3382/ps.2012-02700
» https://doi.org/10.3382/ps.2012-02700 -
Macklin KS, Hess JB, Bilgili SF, et al. Effects of in-house composting of litter on bacterial levels. Journal of Applied Poultry Research 2006;15(4):531-7. https://doi.org/10.1093/japr/15.4.531
» https://doi.org/10.1093/japr/15.4.531 -
Macklin KS, Hess JB, Bilgili SF. In-house windrow composting and its effects on foodborne pathogens. Journal of Applied Poultry Research 2008;17(1):121-127. https://doi.org/10.3382/japr.2007-00051
» https://doi.org/10.3382/japr.2007-00051 -
Manogaran MD, Shamsuddin R, Yusoff MHM, et al. A review on treatment processes of chicken manure. Cleaner and Circular Bioeconomy 2022;2:100013. https://doi.org/10.1016/j.clcb.2022.100013
» https://doi.org/10.1016/j.clcb.2022.100013 -
Martins RS, Hötzel MJ, Poletto R. Influence of in-house composting of reused litter on litter quality, ammonia volatilisation and incidence of broiler foot pad dermatitis. British Poultry Science 2013;54(6):669-76. https://doi.org/10.1080/00071668.2013.838747
» https://doi.org/10.1080/00071668.2013.838747 -
Muniz E, Mesa D, Cuaspa R, et al. Presence of Salmonella spp. in reused broiler litter. Revista Colombiana de Ciencias Pecuarias 2014;27(1):12-7. https://doi.org/10.17533/udea.rccp.324874
» https://doi.org/10.17533/udea.rccp.324874 -
Muniz RF, Oliveira WR, Pereira RS, et al. Ammonia gas for bacterial control in poultry litter. Pesquisa Veterinária Brasileira 2022;42:e06990. https://doi.org/10.1590/1678-5150-PVB-6990
» https://doi.org/10.1590/1678-5150-PVB-6990 -
Oladeinde A, Abdo Z, Zwirzitz B, et al. Litter commensal bacteria can limit the horizontal gene transfer of antimicrobial resistance to Salmonella in chickens. Applied and Environmental Microbiology 2022;88(9):e02517-21. https://doi.org/10.1128/aem.02517-21
» https://doi.org/10.1128/aem.02517-21 -
Palhares JCP, Kunz A. Manejo ambiental na avicultura [Internet]. Concórdia: Embrapa Suínos e Aves; 2011 [cited 2024 Oct 30]. Available from: https://www.embrapa.br/busca-de-publicacoes/-/publicacao/920466/manejo-ambiental-na-avicultura
» https://www.embrapa.br/busca-de-publicacoes/-/publicacao/920466/manejo-ambiental-na-avicultura -
Patterson PH, Adrizal. Management strategies to reduce air emissions: emphasis - dust and ammonia. Journal of Applied Poultry Research 2005;14(3):638-650. https://doi.org/10.1093/japr/14.3.638
» https://doi.org/10.1093/japr/14.3.638 -
Pires SM, Vieira AR, Hald T, et al. Source attribution of human salmonellosis: an overview of methods and estimates. Foodborne Pathogens and Disease 2014;11(9):667-76. https://doi.org/10.1089/fpd.2014.1744
» https://doi.org/10.1089/fpd.2014.1744 -
Prá MAD, Corrêa EK, Roll VF, et al. Quicklime for controlling Salmonella spp and Clostridium spp in litter from floor pens of broilers. Ciência Rural 2009;39(4):1189-94. https://doi.org/10.1590/S0103-84782009005000028
» https://doi.org/10.1590/S0103-84782009005000028 -
Roll VFB, Prá MA, Roll AP. Research on Salmonella in broiler litter reused for up to 14 consecutive flocks. Poultry Science 2011;90(10):2257-62. https://doi.org/10.3382/ps.2011-01583
» https://doi.org/10.3382/ps.2011-01583 -
Rosa C, Nascimento VP, Pizolotto W, et al. Effect of ammonia gas in poultry litter contaminated with Salmonella Heidelberg. Brazilian Journal of Poultry Science 2023;25(1):eRBCA-2022-1631. https://doi.org/10.1590/1806-9061-2022-1631
» https://doi.org/10.1590/1806-9061-2022-1631 -
Shaji S, Selvaraj RK, Shanmugasundaram R. Salmonella infection in poultry: a review on the pathogen and control strategies. Microorganisms 2023;11(11):2814. https://doi.org/10.3390/microorganisms11112814
» https://doi.org/10.3390/microorganisms11112814 -
Sonoda LT, Moura DJ, Bueno LGF, et al. Broiler litter reutilization applying different composting concepts. Brazilian Journal of Poultry Science 2012;14(3):227-32. https://doi.org/10.1590/S1516-635X2012000300011
» https://doi.org/10.1590/S1516-635X2012000300011 -
Toledo TDS, Roll AAP, Rutz F, et al. An assessment of the impacts of litter treatments on the litter quality and broiler performance: a systematic review and meta-analysis. PLoS ONE 2020;15(5):e0232853. https://doi.org/10.1371/journal.pone.0232853
» https://doi.org/10.1371/journal.pone.0232853 -
Vaz CSL, Voss-Rech D, Avila VS, et al. Interventions to reduce the bacterial load in recycled broiler litter. Poultry Science 2017;96(8):2587-94. https://doi.org/10.3382/ps/pex063
» https://doi.org/10.3382/ps/pex063 -
Vaz CSL. O manejo da cama que realizamos realmente funciona? Anais do Simpósio FACTA sobre Salmonella; 2022; Campinas, Brasil [Internet]. 2022 [cited 2024 Oct 30]. Available from: http://www.alice.cnptia.embrapa.br/alice/handle/doc/1152978
» http://www.alice.cnptia.embrapa.br/alice/handle/doc/1152978 -
Voss-Rech D, Vaz CS, Alves L, et al. A temporal study of Salmonella enterica serotypes from broiler farms in Brazil. Poultry Science 2015;94(3):433-41. https://doi.org/10.3382/ps/peu081
» https://doi.org/10.3382/ps/peu081 -
Voss-Rech D, Trevisol IM, Brentano L, et al. Impact of treatments for recycled broiler litter on the viability and infectivity of micro-organisms. Veterinary Microbiology 2017;203:308-14. https://doi.org/10.1016/j.vetmic.2017.03.020
» https://doi.org/10.1016/j.vetmic.2017.03.020 -
Wilkinson KG, Tee E, Tomkins RB, et al. Effect of heating and aging of poultry litter on the persistence of enteric bacteria. Poultry Science 2011;90(1):10-8. https://doi.org/10.3382/ps.2010-01023
» https://doi.org/10.3382/ps.2010-01023 -
Wolf J, Potrich M, Lozano ER, et al. Combined physical and chemical methods to control lesser mealworm beetles under laboratory conditions. Poultry Science 2015;94(6):1145-9. https://doi.org/10.3382/ps/pev093
» https://doi.org/10.3382/ps/pev093 -
Zizza A, Fallucca A, Guido M, et al. Foodborne infections and Salmonella: current primary prevention tools and future perspectives. Vaccines 2024;13(1):29. https://doi.org/10.3390/vaccines13010029
» https://doi.org/10.3390/vaccines13010029
