Phenotypic evaluation for disposal in laying hens and asymptomatic infections by Salmonella spp. in the final production cycle

Phenotypic evaluation for disposal in laying hens and asymptomatic infections by Salmonella spp.... Abstract At the end of the production cycle, laying hens are intended for industrial slaughter; however, they may be also being sold to small farmers and thereby transmit pathogens under uncontrolled production practices. This study was developed with the objective of evaluating the physical characteristics of laying birds in the final cycle and investigating Salmonella presence. A total of 22 flocks of commercial laying hens over 76 wk of age were evaluated. For each flock, 20 birds were randomly selected. A total of 440 birds underwent visual evaluation of the comb, wattle, leg spur, beak, and cloaca appearance and distance measurement between the pubic bones and between the pubis and keeled sternum. After euthanasia and necropsy, ovarian follicles, liver fragment, spleen, heart, colon content, and oviduct swabs were evaluated for their normal aspects and changes. Six organ samples collected from each of 4 birds were pooled, respectively, and 24 pooled samples per flock totaled 528. Salmonella spp. were isolated in at least 2 samples from 7 of the 22 flocks (31.8%) sampled and in most of the productive birds (up to 71%). A total of 31 isolates were distributed in this way: 29.1% Salmonella Gallinarum, 19.3% Salmonella Heideberg, 16.1% Salmonella Enteritidis, 12.9% Salmonella Schwarzengrund; 9.7% Salmonella Cerro, 6.5% Salmonella Thiphimurium, 3.2% Salmonella Johannesburg, and 3.2% Salmonella Montevideo. It is concluded that individual phenotypic evaluations in laying hens over 76 wk of age can be used before birds are discarded related to end of production and phenotypic changes. The disposed, unproductive birds should not be sold to small breeders, follow-up current legislation, because Salmonella serovars have been identified. There was no correlation between asymptomatic Salmonella spp. and phenotypic alterations evaluated for disposal. DESCRIPTION OF PROBLEM The advanced age of laying hens causes a decrease in posture, quality of eggs, and an increase in feed conversion [1]. Because of the loss of productivity, laying hens are eliminated and sent to slaughterhouses. Layers of discard age are birds of low economic value and are one of the main economic and environmental problems of the poultry industry due to the high cost of transportation, the volume of biological material, and labor costs. Age advancement and productivity reduction are related to different physiological factors that reflect physical changes in birds, such as distance between pelvic bones, cloaca visual appearance, rump and barb color, legs and beak pigmentation [2]. Despite the existing sanitary regulations, the destination of laying hens for small rural producer which use the residual production of the laying hen for sale can be considered a risk factor for the occurrence of asymptomatic Salmonella infections [3]. Asymptomatic infections in birds are a problem for animal health, public health, and the environment, as these can be contaminating other birds and people. The acquisition of Salmonella-bearing birds presents a risk of infection by ingestion of raw or undercooked eggs or ingestion of prepared foods with unsatisfactory hygienic measures. According to Tahergorabi et al. [4], it is estimated that 96% of cases of salmonellosis in humans occur because of consumption of animal products. In addition, even adult birds, which are more resistant to infection, can, in stress situations, excrete the pathogen and infect other animal hosts, contaminating the environment and vegetables. Considering that the characteristics of the laying hens in final production can be evaluated in the period of the discard and that there are no reports on Salmonella occurrence in disposal layers, this study was developed to evaluate the physical characteristics of poultry in the final production cycle and investigate the presence of Salmonella in laying hens over 76 wk of age. MATERIALS AND METHODS The study was developed in the Bird Diseases Laboratory and the Bacteriology Laboratory of the Veterinary and Zootechnical School of the Federal University of Goiás and was approved by the Ethics Commission on the Use of Animals (IACUC) CEUA-PRPPG-UFG n° 034/13. Totaling 440 birds, 22 flocks of commercial laying hens over 76 wk of age were collected from 20 egg-producing companies with the same health conditions, considering at this age some birds that still produced eggs (productive) and others significantly decreased their production rate (final production). A total of 20 poultry were randomly selected from each flock (10% a total flock), which were subjected to physical evaluation of the combs and wattles color for normal (standard), leg spur and beak pigmentation for normal (standard) color patterns for productive birds and normal (standard) skin pigmentation, cloaca appearance eversion (ease of cloacal eversion under manual pressure), and distance measurement between the pubic bones and between the pubic and keeled sternum, according to Rosa et al. [2], to compare the changes among birds that still produced eggs from those that did not produce more eggs. After physical evaluation, the birds were submitted to euthanasia with carbon dioxide asphyxiation and subsequent cervical dislocation and necropsy. During the necropsy, the ovarian with the presence of viable follicles was counted, considering the birds that still had follicles (productive) and the birds that had no viable follicles (final production). Fragments corresponding to 20% for each organ were collected from liver, spleen, heart, and ovarian follicles, and 10% of the colon content and oviduct swabs with local scrub (collecting material by rubbing the swab) were taken with 3 swabs per bird, for Salmonella tests. The 6 organ samples collected from each of 4 birds were pooled, respectively, and composed 24 samples analyzed (4 samples × 6 organs) per flocks and 528 samples (24 pools × 22 flocks) in total. Each pooled sample was macerated with a spatula and homogenized in a sterile becker, and 1 g was transferred to 9 mL of 1% sterilized peptone water [5] and incubated at 37°C for 18–24 h. Samples were processed for the isolation of Salmonella according to a procedure used by the Georgia Poultry Laboratory, with some modifications [6]. Respectively, 1.0 and 0.1 mL of this peptone water were transferred to 9.0 mL of cystine selenite broth [5] and to 10 mL of Vassiliadis Rappaport [5] broth and incubated at 37°C for 24 h. Then, with a nickel-chromium loop, aliquots were plated as streaks onto XLT4 agar [5], Hektoën agar [5], and brilliant green agar [5] and again incubated at 37°C for 24 h. A reading was performed by the selection of colony-forming units (CFU) with morphological characteristics of Salmonella. Three to five CFU per plate were transferred to tubes containing triple sugar iron (TSI) [5] and incubated at 37°C for 24 h. Isolates from the tubes containing TSI with growth suggestive of Salmonella were submitted to the following tests: urease, indole production, methyl red, malonate, Simmon's citrate, motility, and lysine decarboxylase. When the biochemical reactions were compatible with Salmonella, the samples were submitted for a serological test with polyvalent anti-O serum [7] to agglutination test on a glass slide, applying 1 drop of the bacterial isolate suspension and 1 drop of the polyvalent serum, stirring the mixture for 2 min, with positive agglutination for presence, and those that presented positive results were sent to the Oswaldo Cruz Foundation (FIOCRUZ-RJ) in agar nutrient for serotype classification. RESULTS AND DISCUSSION The phenotypic characteristics associated with productive and final productive birds of 440 chickens from 22 lots older than 76 wk are set out in Table 1. The highest frequencies were for comb and wattle standard color (77.3%) compared to frequencies in the birds not exhibiting standard color (22.7%) and leg spur and beak color (78.4%) for (21.6%) not exhibiting standard color. The yellow coloration of the beak and leg spur is due to the deposition of xanthophylls. If the bird is in the productive phase, xanthophylls are mainly deposited in the egg yolk, resulting in paler beaks and leg spurs. This statement is consistent with a hierarchical evaluation of the ovarian follicles, with 326 (74.1%) ovaries with viable follicles in a total of 440 ovary birds analyzed, 325 (73.9%) cloaca easily eversible analyzed at the physical evaluation (with ease of reversal under pressure) in a total of 440 ovary birds analyzed, and 328 (74.5%) analyzed birds out the total of 440 birds and normal body weight within the standard as recommended for the breed. Table 1. Distribution of physical evaluations of 440 laying hens over 76 wk of age.   Productive birds  Final productive birds3  Characteristics  Number (%) exhibiting standard traits  Number (%) not exhibiting standard traits  Ovaries exhibiting follicles  326 (74.1)  –4  Ovaries without follicles  –  114 (25.9)  Comb and wattle color  340 (77.3)  100 (22.7)  Ease of cloacal eversion  325 (73.9)  115 (26.1)  Leg spur and beak color  345 (78.4)  95 (21.6)  Body weight  328 (74.5)  112 (25.5)  Vertical distance1 > 5 cm  322 (73.2)  –  Vertical distance < 5 cm  –  118 (26.8)  Horizontal distance2 > 5 cm  314 (71.4)  –  Horizontal distance < 5 cm  –  126 (28.6)    Productive birds  Final productive birds3  Characteristics  Number (%) exhibiting standard traits  Number (%) not exhibiting standard traits  Ovaries exhibiting follicles  326 (74.1)  –4  Ovaries without follicles  –  114 (25.9)  Comb and wattle color  340 (77.3)  100 (22.7)  Ease of cloacal eversion  325 (73.9)  115 (26.1)  Leg spur and beak color  345 (78.4)  95 (21.6)  Body weight  328 (74.5)  112 (25.5)  Vertical distance1 > 5 cm  322 (73.2)  –  Vertical distance < 5 cm  –  118 (26.8)  Horizontal distance2 > 5 cm  314 (71.4)  –  Horizontal distance < 5 cm  –  126 (28.6)  1Vertical distance = distance between the end of the pubic bones and the keeled sternum. 2Horizontal distance = distance between the end of the pubic bones according ROSA et al. [2]. 3Laying hens not producing eggs. 4Note detected. View Large Table 1. Distribution of physical evaluations of 440 laying hens over 76 wk of age.   Productive birds  Final productive birds3  Characteristics  Number (%) exhibiting standard traits  Number (%) not exhibiting standard traits  Ovaries exhibiting follicles  326 (74.1)  –4  Ovaries without follicles  –  114 (25.9)  Comb and wattle color  340 (77.3)  100 (22.7)  Ease of cloacal eversion  325 (73.9)  115 (26.1)  Leg spur and beak color  345 (78.4)  95 (21.6)  Body weight  328 (74.5)  112 (25.5)  Vertical distance1 > 5 cm  322 (73.2)  –  Vertical distance < 5 cm  –  118 (26.8)  Horizontal distance2 > 5 cm  314 (71.4)  –  Horizontal distance < 5 cm  –  126 (28.6)    Productive birds  Final productive birds3  Characteristics  Number (%) exhibiting standard traits  Number (%) not exhibiting standard traits  Ovaries exhibiting follicles  326 (74.1)  –4  Ovaries without follicles  –  114 (25.9)  Comb and wattle color  340 (77.3)  100 (22.7)  Ease of cloacal eversion  325 (73.9)  115 (26.1)  Leg spur and beak color  345 (78.4)  95 (21.6)  Body weight  328 (74.5)  112 (25.5)  Vertical distance1 > 5 cm  322 (73.2)  –  Vertical distance < 5 cm  –  118 (26.8)  Horizontal distance2 > 5 cm  314 (71.4)  –  Horizontal distance < 5 cm  –  126 (28.6)  1Vertical distance = distance between the end of the pubic bones and the keeled sternum. 2Horizontal distance = distance between the end of the pubic bones according ROSA et al. [2]. 3Laying hens not producing eggs. 4Note detected. View Large These parameters indicate that most of the layers analyzed were in the productive phase and reflected the characteristics indicated by Rosa et al. [2], such as soft and elastic comb and wattle, wet and augmented cloaca, pale leg spurs and beaks, distance between pubic bones and keeled sternum, soft abdomen, and adequate body weight. The phenotypic characteristics that were addressed in this study can be used individually or together to exclude productive individuals or batches. According to Yasmeen et al. [1], a gradual decrease in the rate of egg production, egg shell quality, production inconstancy, and lower feed conversion efficiency should be considered as reasons to discard hens with advanced age. In this study, 7 of the 22 flocks (31.8%) were positive for Salmonella. It was verified in the literature that the frequency of this pathogen has been studied predominantly in laying hens in production, using the feces as samples. Studies on the presence of serovars of Salmonella spp. in fecal samples from commercial egg-producing hens in the State of California (USA) presented positive results for Salmonella Enteritidis presence in 10.5% of the evaluated lots [8]. Another survey carried out by a European multinational company indicated that 20.4% of the plots were positive for Salmonella Enteritidis or Salmonella Typhimurium [9]. Gama et al. [10] studied 12 commercial laying lots up to 76 wk of age and obtained 4 (33.3%) lots positive for Salmonella. Kottwitz et al. [11] isolated Salmonella in 8 (23%) of the 30 commercial egg farms in poultry aged 17 to 76 wk in the state of Paraná, Brazil. Salles et al. [12] detected 2 positive samples from the 32 fecal pool samples (6.25%) when performing monitoring in 8 poultry companies for layers up to 40 wk of age in the state of Ceará, Brazil. Considering the results found in the colon contents, it was verified that the bacteria (Table 2) were isolated from 3 lots with a frequency of 3.4%, and strains of Salmonella Schwarzengrund and Salmonella Cerro serovars were identified (Table 3), and that chickens have the potential to spread the bacteria, including these serovars incriminated in food outbreaks. Chickens infected and stressed by the catch during transport and slaughter can eliminate the pathogen in the feces and infect other birds and other animals, and these results are consistent with the findings of Forshel and Wierup [13] who reported that contamination of food by feces is a source of Salmonella infection for humans, other animals, and the environment [13, 14]. Table 2. Salmonella-positive samples found in 440 laying hens from 22 flocks over 76 wk of age and in their final production cycle. Samples  Positive flocks  Positive samples/N1  Liver  7  9/88 (10.2%)  Spleen  6  10/88 (11.4%)  Heart  5  5/88 (5.7%)  Oviducts swab  4  4/88 (4.5%)  Colon content  3  3/88 (3.4%)  Ovarian follicles  2  2/88 (2.3%)  Samples  Positive flocks  Positive samples/N1  Liver  7  9/88 (10.2%)  Spleen  6  10/88 (11.4%)  Heart  5  5/88 (5.7%)  Oviducts swab  4  4/88 (4.5%)  Colon content  3  3/88 (3.4%)  Ovarian follicles  2  2/88 (2.3%)  1Total analized sample. View Large Table 2. Salmonella-positive samples found in 440 laying hens from 22 flocks over 76 wk of age and in their final production cycle. Samples  Positive flocks  Positive samples/N1  Liver  7  9/88 (10.2%)  Spleen  6  10/88 (11.4%)  Heart  5  5/88 (5.7%)  Oviducts swab  4  4/88 (4.5%)  Colon content  3  3/88 (3.4%)  Ovarian follicles  2  2/88 (2.3%)  Samples  Positive flocks  Positive samples/N1  Liver  7  9/88 (10.2%)  Spleen  6  10/88 (11.4%)  Heart  5  5/88 (5.7%)  Oviducts swab  4  4/88 (4.5%)  Colon content  3  3/88 (3.4%)  Ovarian follicles  2  2/88 (2.3%)  1Total analized sample. View Large Table 3. Salmonella serovars and their numbers isolated from organs collected from 22 flocks (440 birds) of laying hens in the final production cycle. Serovars  Liver  Spleen  Heart  Oviduct  Colon  Follicle  Total isolates N (%)  Flocks (+)  Gallinarum  2  3  2  1  –1  1  9 (29.1)  2  Heidelberg  1  2  –  1  –  2  6 (19.3)  2  Enteritidis  1  1  1  1  1  –  5 (16.1)  1  Schwarzengrund  2  1  –  –  1  –  4 (12.9)  2  Cerro  1  1  –  –  1  –  3 (9.7)  1  Typhimurium  –  2  –  –  –  –  2 (6.5)  2  Johannesburg  –  –  –  1  –  –  1 (3.2)  1  Montevideo  –  –  1  –  –  –  1 (3.2)  1  Total  7  10  4  4  3  3  31 (100)    Serovars  Liver  Spleen  Heart  Oviduct  Colon  Follicle  Total isolates N (%)  Flocks (+)  Gallinarum  2  3  2  1  –1  1  9 (29.1)  2  Heidelberg  1  2  –  1  –  2  6 (19.3)  2  Enteritidis  1  1  1  1  1  –  5 (16.1)  1  Schwarzengrund  2  1  –  –  1  –  4 (12.9)  2  Cerro  1  1  –  –  1  –  3 (9.7)  1  Typhimurium  –  2  –  –  –  –  2 (6.5)  2  Johannesburg  –  –  –  1  –  –  1 (3.2)  1  Montevideo  –  –  1  –  –  –  1 (3.2)  1  Total  7  10  4  4  3  3  31 (100)    1Not detected. View Large Table 3. Salmonella serovars and their numbers isolated from organs collected from 22 flocks (440 birds) of laying hens in the final production cycle. Serovars  Liver  Spleen  Heart  Oviduct  Colon  Follicle  Total isolates N (%)  Flocks (+)  Gallinarum  2  3  2  1  –1  1  9 (29.1)  2  Heidelberg  1  2  –  1  –  2  6 (19.3)  2  Enteritidis  1  1  1  1  1  –  5 (16.1)  1  Schwarzengrund  2  1  –  –  1  –  4 (12.9)  2  Cerro  1  1  –  –  1  –  3 (9.7)  1  Typhimurium  –  2  –  –  –  –  2 (6.5)  2  Johannesburg  –  –  –  1  –  –  1 (3.2)  1  Montevideo  –  –  1  –  –  –  1 (3.2)  1  Total  7  10  4  4  3  3  31 (100)    Serovars  Liver  Spleen  Heart  Oviduct  Colon  Follicle  Total isolates N (%)  Flocks (+)  Gallinarum  2  3  2  1  –1  1  9 (29.1)  2  Heidelberg  1  2  –  1  –  2  6 (19.3)  2  Enteritidis  1  1  1  1  1  –  5 (16.1)  1  Schwarzengrund  2  1  –  –  1  –  4 (12.9)  2  Cerro  1  1  –  –  1  –  3 (9.7)  1  Typhimurium  –  2  –  –  –  –  2 (6.5)  2  Johannesburg  –  –  –  1  –  –  1 (3.2)  1  Montevideo  –  –  1  –  –  –  1 (3.2)  1  Total  7  10  4  4  3  3  31 (100)    1Not detected. View Large In the current study, Salmonella Enteritidis was detected in the all organ samples processed, except in a single batch of ovarian follicles. These findings are consistent with Gast et al. [15], who isolated the pathogen from the gastrointestinal tract, liver, spleen, ovary, and oviduct of apparently healthy laying hens that were inoculated experimentally with Salmonella Enteritidis. Salmonella Schwarzengrund, Salmonella Cerro, and Salmonella Johannesburg serovars were detected in the colon and reproductive organs (Table 3), indicating that chickens may produce eggs that can be contaminated by infection of the reproductive tract or by feces in the passage through the sewer [16]. The presence of Salmonella serovars isolated from apparently healthy birds in viscera such as the heart (18.2% (4/22)), liver (27.3% (6/22)), and ovarian follicles (9.1% (2/22)) (Table 2) demonstrates the possibility that poultry may be carriers of Salmonella, which points to the need for implementation of control measures that minimize the potential risk to food animals and human health. Hygienic sanitary measures in the handling of poultry are necessary or their products may promote cross-contamination and contaminate edible products of both animal and plant origin [11]. Sterzo et al. [17] identified Salmonella in the follicles’ ovaries, oviduct, and colon, and, therefore, the pathogen potentially can be incorporated into the yolk and white during the formation of the egg, or even on the shell during its passage through the cloaca, or in the nest contaminated with the feces. Although the hosts do not present clinical signs, they are asymptomatic carriers and potential disseminators of the agent, which confirms the importance of adult birds in the spreading of the agent [18, 19]. The following serovars were identified in the colon content: Salmonella Enteritidis, Salmonella Schwarzengrund, and Salmonella Cerro. These serovars are different from those found in the United Kingdom, which identified Salmonella Enteritidis, and Salmonella Typhimurium, Salmonella Mbandaka, Salmonella Havana, and Salmonella Enterica in the stool [20]. In comparison with other studies carried out in Brazil, Salmonella Enteritidis, Salmonella Javiana, and Salmonella Mbandaka, Salmonella Infantis were identified by Gama et al. [10] and Salmonella Enterica, Salmonella Mbandaka, Salmonella Infantis, and Salmonella Newport have also been identified [10, 11]. The results obtained here are similar to those obtained by Poppe [14] and Snow et al. [20], who reported that differences in geography, climate, egg production practices, and laying hens management in a given region reflect the presence of different serovars. Salmonella Heidelberg serovars were identified in the liver, spleen, oviduct, and ovarian follicles in 2 lots of the 22 studied, with a frequency of 19.3% (6/31) among the different serovars identified (Table 3). The Salmonella Heidelberg serovar is cited as the third most frequently isolated in poultry in Canada and the fourth in foodborne diseases in the United States [21]. In Brazil, since 1962, Salmonella Heidelberg has been identified in poultry and by-products [22]. Among the Salmonella that cause infections in humans, Salmonella Heidelberg seems to be more invasive and causes diseases with greater severity than other paratyphoid serovars [23]. It is considered an agent with a high invasive capacity, which constitutes a risk to public health and compromises food safety. Results reinforce the idea that the commercialization of old laying hens may promote an unsafe strategy. Salmonella Gallinarum serovar, agent of fowl typhoid, was detected in 2 lots with a frequency of 29.1% (9/31) in this study (Table 3). Salmonella Gallinarum mainly affects birds, being considered one of the main pathogens of the commercial poultry industry in the infection of chickens (Gallus gallus) [24]. This agent has caused serious animal health problems for the Brazilian poultry industry due to the occurrence of mortality during the rearing and production phase, loss of productive performance of chickens, increased mortality, and decrease in egg production. However, in this study the samples were collected at random and the birds had no clinical signs. Knowledge of the prevalence Salmonella serovars in a likely source of infection, such as discarded chickens, is important for the success of a control program. CONCLUSION It is concluded that individual phenotypic evaluations can be used before the birds are discarded because phenotypic changes are related to the final production. Laying hens over 76 wk of age should not be marketed to small breeders since, in asymptomatic birds, Salmonella serovars have been identified, which are important both for public health and for animal health. A relation was not found between asymptomatic birds for Salmonella and phenotypic evaluations, indicating that the changes were due to age. Footnotes Primary Audience: Production hen REFERENCES 1. Yasmeen F., Mahmood S., Hassan M., Akhtar N., Yaseen M.. 2008. Comparative productive performance and egg characteristics of pullets and spent layers. Pak. Vet. J.  28: 5– 8. 2. Rosa P. S., Albino J. J., Bassi L. J., Saatkamp M. G.. 2007. Identificação e descarte de poedeiras improdutivas. Pages 1– 2 in Instrução técnica para o produtor , Embrapa Suínos e Aves, Santa Catarina, BR. 3. Namata H., Méroc E., Aerts M., Faes C., Abrahantes J. C., Imberechts H., Mintiens K.. 2008. Salmonella in Belgian laying hens: an identification of risk factors. Prev. Vet. Med.  83: 323– 336. Google Scholar CrossRef Search ADS PubMed  4. Tahergorabi R., Matak K. E., Jaczynski J.. 2012. Application of electron beam to inactivate Salmonella in food: recent developments. Food Res. Int.  45: 685– 694. Google Scholar CrossRef Search ADS   5. Merck KGaA, Darmstadt, Germany. http://www.merckmillipore.com/BR/pt/products/industrial-microbiology/culture-media/dLWb.qB.5kgAAAFAX8JkiQpx,nav. 6. Anonymous. 1997. Monitoring and detection of Salmonella. Pages 256 in Poultry and Poultry Environments . Georgia Poultry Laboratory, Oakwood, GA. 7. Probac do Brasil - Produtos bacteriológicos Ltda. Soro Salmonella polivalente, São Paulo, BR. http://probac.com.br/Produto/Detalhe/pt-BR/457. 8. Castellan D. M., Kinde H., Kass P. H., Cutler G., Breitmeyer R. E., Bell D. D., Ernst R. A., Kerr D. C., Little H. E., Willoughby D., Riemann H. P., Ardans A., Snowdon J. A., Kuney D. R.. 2004. Descriptive study of California egg layer premises and analysis of risk factors for salmonella enterica serotype Enteritidis as characterized by manure drag swabs. Avian Dis.  48: 550– 561. Google Scholar CrossRef Search ADS PubMed  9. EFSA 2007. Report of the task force on zoonoses data collection on the analysis of the baseline survey on the prevalence of Salmonella in broiler flocks of Gallus gallus in the EU 2005 - 2006. Pages 1– 85, in European Food Safety Authority . EFSA J. Publishing, Parma, IT. 10. Gama N. M. S. Q., Berchieri A. Jr, Fernandes S. A.. 2003. Occurrence of Salmonella sp in laying hens. Rev. Bras. Cienc. Avic.  5: 15– 21. Google Scholar CrossRef Search ADS   11. Kottwitz L. B. M., Oliveira T. C. R. M., Alcocer I., Farah S. M. S. S., Abrahão W. S. M., Rodrigues D. P.. 2010. Avaliação epidemiológica de surtos de salmonelose ocorridos no período de 1999 a 2008 no Estado do Paraná, Brasil. Acta Sci. Health Sci.  32: 9– 15. 12. Salles R. P. R., Teixeira R. S. C., Siqueira A. A., Silva E. E., Castro S. B., Cardoso W. M.. 2008. Monitoramento bacteriológico para Salmonella spp. em poedeira comercial na recria e produção de empresas avícolas da região metropolitana de Fortaleza, CE, Brasil. Ci. An. Bras.  9: 427– 432. 13. Forshell L. P., Wierup M.. 2006. Salmonella contamination: a significant challenge to the global marketing of animal foods products. Rev. Sci. Tech. Office Int. Epizoot.  25: 541– 554. Google Scholar CrossRef Search ADS   14. Poppe C. 2000. Salmonella infections in the domestic fowl. Pages 107– 132 in Book Salmonella in Domestic Animals . CABI Publishing, UK. Google Scholar CrossRef Search ADS   15. Gast R. K., Guraya R., Guard-Bouldin J., Holt P. S., Moore R. W.. 2007. Colonization of specific regions of the reproductive tract and deposition at different locations inside eggs laid by hens infected with Salmonella Enteritidis or Salmonella Heidelberg. Avian Dis.  51: 40– 44. Google Scholar CrossRef Search ADS PubMed  16. Gast R. K. 1993. Detection of Salmonella enteritidis in experimentally infected laying hens by culturing pools of egg contents. Poult. Sci.  72: 267– 274. Google Scholar CrossRef Search ADS PubMed  17. Sterzo E. V., Varzone J. R. M., Ferrari R.. 2008. Salmoneloses aviárias. Ensaios e Ciência. Ci. Biol. Ag. Saúde.  12: 129– 138. 18. Chappell L., Kaiser P., Barrow P., Jones M. A., Johnston C., Wigley P.. 2009. The immunobiology of avian systemic salmonellosis. Vet. Immunol. Immunopathol.  128: 53– 59. Google Scholar CrossRef Search ADS PubMed  19. Sadeyen J. J., Trotereau P., Velge J., Marly C., Beaumont P. A., Barrow N., Bumstead A., Lalmanach A. C.. 2004. Salmonella carrier state in chicken: comparison of expression of immune response genes between susceptible and resistant animals. Microbes Infect.  6: 1278– 1286. Google Scholar CrossRef Search ADS PubMed  20. Snow L. C., Davies R. H., Christiansen K. C., Carrique-Mas J. J., Wales A. D., O’connor J. L., Cook A. J. C., Evans S. J.. 2007. Survey of the prevalence of Salmonella species on commercial laying farms in the United Kingdom. Vet. Rec.  161: 471– 476. Google Scholar CrossRef Search ADS PubMed  21. Chittick P., Sulka A., Tauxe R. V., Fry A. M.. 2006. A summary of national reports of foodborne outbreaks of Salmonella Heidelberg infections in the United States: clues for disease prevention. J. Food Prot.  69: 1150– 1153. Google Scholar CrossRef Search ADS PubMed  22. Hofer E., Silva Filho S. J., E.M.F. R.. 1997. Prevalência de sorovares de Salmonella isolados de aves no Brasil. Braz. J. Vet. Res . 17: 55– 62. 23. PHAC 2007. Salmonella Heidelberg Ceftiofur-Related Resistance in Human and Retail Chicken Isolates . Public Health Agency of Canada. http://www.phac-aspc.gc.ca/cipars-picra/heidelberg/pdf/heidelberg_e.pdf. 24. Jeong J. H., Song M., Park S. I., Cho K. O., Rhee J. H., Choy H. E.. 2008. Salmonella enterica serovar Gallinarum requires ppGpp for internalization and survival in animal cells. J. Bacteriol.  190: 6340– 6350. Google Scholar CrossRef Search ADS PubMed  © 2018 Poultry Science Association Inc. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Applied Poultry Research Oxford University Press

Phenotypic evaluation for disposal in laying hens and asymptomatic infections by Salmonella spp. in the final production cycle

Loading next page...
 
/lp/ou_press/phenotypic-evaluation-for-disposal-in-laying-hens-and-asymptomatic-WoTtREIjxf
Publisher
Applied Poultry Science, Inc.
Copyright
© 2018 Poultry Science Association Inc.
ISSN
1056-6171
eISSN
1537-0437
D.O.I.
10.3382/japr/pfy019
Publisher site
See Article on Publisher Site

Abstract

Abstract At the end of the production cycle, laying hens are intended for industrial slaughter; however, they may be also being sold to small farmers and thereby transmit pathogens under uncontrolled production practices. This study was developed with the objective of evaluating the physical characteristics of laying birds in the final cycle and investigating Salmonella presence. A total of 22 flocks of commercial laying hens over 76 wk of age were evaluated. For each flock, 20 birds were randomly selected. A total of 440 birds underwent visual evaluation of the comb, wattle, leg spur, beak, and cloaca appearance and distance measurement between the pubic bones and between the pubis and keeled sternum. After euthanasia and necropsy, ovarian follicles, liver fragment, spleen, heart, colon content, and oviduct swabs were evaluated for their normal aspects and changes. Six organ samples collected from each of 4 birds were pooled, respectively, and 24 pooled samples per flock totaled 528. Salmonella spp. were isolated in at least 2 samples from 7 of the 22 flocks (31.8%) sampled and in most of the productive birds (up to 71%). A total of 31 isolates were distributed in this way: 29.1% Salmonella Gallinarum, 19.3% Salmonella Heideberg, 16.1% Salmonella Enteritidis, 12.9% Salmonella Schwarzengrund; 9.7% Salmonella Cerro, 6.5% Salmonella Thiphimurium, 3.2% Salmonella Johannesburg, and 3.2% Salmonella Montevideo. It is concluded that individual phenotypic evaluations in laying hens over 76 wk of age can be used before birds are discarded related to end of production and phenotypic changes. The disposed, unproductive birds should not be sold to small breeders, follow-up current legislation, because Salmonella serovars have been identified. There was no correlation between asymptomatic Salmonella spp. and phenotypic alterations evaluated for disposal. DESCRIPTION OF PROBLEM The advanced age of laying hens causes a decrease in posture, quality of eggs, and an increase in feed conversion [1]. Because of the loss of productivity, laying hens are eliminated and sent to slaughterhouses. Layers of discard age are birds of low economic value and are one of the main economic and environmental problems of the poultry industry due to the high cost of transportation, the volume of biological material, and labor costs. Age advancement and productivity reduction are related to different physiological factors that reflect physical changes in birds, such as distance between pelvic bones, cloaca visual appearance, rump and barb color, legs and beak pigmentation [2]. Despite the existing sanitary regulations, the destination of laying hens for small rural producer which use the residual production of the laying hen for sale can be considered a risk factor for the occurrence of asymptomatic Salmonella infections [3]. Asymptomatic infections in birds are a problem for animal health, public health, and the environment, as these can be contaminating other birds and people. The acquisition of Salmonella-bearing birds presents a risk of infection by ingestion of raw or undercooked eggs or ingestion of prepared foods with unsatisfactory hygienic measures. According to Tahergorabi et al. [4], it is estimated that 96% of cases of salmonellosis in humans occur because of consumption of animal products. In addition, even adult birds, which are more resistant to infection, can, in stress situations, excrete the pathogen and infect other animal hosts, contaminating the environment and vegetables. Considering that the characteristics of the laying hens in final production can be evaluated in the period of the discard and that there are no reports on Salmonella occurrence in disposal layers, this study was developed to evaluate the physical characteristics of poultry in the final production cycle and investigate the presence of Salmonella in laying hens over 76 wk of age. MATERIALS AND METHODS The study was developed in the Bird Diseases Laboratory and the Bacteriology Laboratory of the Veterinary and Zootechnical School of the Federal University of Goiás and was approved by the Ethics Commission on the Use of Animals (IACUC) CEUA-PRPPG-UFG n° 034/13. Totaling 440 birds, 22 flocks of commercial laying hens over 76 wk of age were collected from 20 egg-producing companies with the same health conditions, considering at this age some birds that still produced eggs (productive) and others significantly decreased their production rate (final production). A total of 20 poultry were randomly selected from each flock (10% a total flock), which were subjected to physical evaluation of the combs and wattles color for normal (standard), leg spur and beak pigmentation for normal (standard) color patterns for productive birds and normal (standard) skin pigmentation, cloaca appearance eversion (ease of cloacal eversion under manual pressure), and distance measurement between the pubic bones and between the pubic and keeled sternum, according to Rosa et al. [2], to compare the changes among birds that still produced eggs from those that did not produce more eggs. After physical evaluation, the birds were submitted to euthanasia with carbon dioxide asphyxiation and subsequent cervical dislocation and necropsy. During the necropsy, the ovarian with the presence of viable follicles was counted, considering the birds that still had follicles (productive) and the birds that had no viable follicles (final production). Fragments corresponding to 20% for each organ were collected from liver, spleen, heart, and ovarian follicles, and 10% of the colon content and oviduct swabs with local scrub (collecting material by rubbing the swab) were taken with 3 swabs per bird, for Salmonella tests. The 6 organ samples collected from each of 4 birds were pooled, respectively, and composed 24 samples analyzed (4 samples × 6 organs) per flocks and 528 samples (24 pools × 22 flocks) in total. Each pooled sample was macerated with a spatula and homogenized in a sterile becker, and 1 g was transferred to 9 mL of 1% sterilized peptone water [5] and incubated at 37°C for 18–24 h. Samples were processed for the isolation of Salmonella according to a procedure used by the Georgia Poultry Laboratory, with some modifications [6]. Respectively, 1.0 and 0.1 mL of this peptone water were transferred to 9.0 mL of cystine selenite broth [5] and to 10 mL of Vassiliadis Rappaport [5] broth and incubated at 37°C for 24 h. Then, with a nickel-chromium loop, aliquots were plated as streaks onto XLT4 agar [5], Hektoën agar [5], and brilliant green agar [5] and again incubated at 37°C for 24 h. A reading was performed by the selection of colony-forming units (CFU) with morphological characteristics of Salmonella. Three to five CFU per plate were transferred to tubes containing triple sugar iron (TSI) [5] and incubated at 37°C for 24 h. Isolates from the tubes containing TSI with growth suggestive of Salmonella were submitted to the following tests: urease, indole production, methyl red, malonate, Simmon's citrate, motility, and lysine decarboxylase. When the biochemical reactions were compatible with Salmonella, the samples were submitted for a serological test with polyvalent anti-O serum [7] to agglutination test on a glass slide, applying 1 drop of the bacterial isolate suspension and 1 drop of the polyvalent serum, stirring the mixture for 2 min, with positive agglutination for presence, and those that presented positive results were sent to the Oswaldo Cruz Foundation (FIOCRUZ-RJ) in agar nutrient for serotype classification. RESULTS AND DISCUSSION The phenotypic characteristics associated with productive and final productive birds of 440 chickens from 22 lots older than 76 wk are set out in Table 1. The highest frequencies were for comb and wattle standard color (77.3%) compared to frequencies in the birds not exhibiting standard color (22.7%) and leg spur and beak color (78.4%) for (21.6%) not exhibiting standard color. The yellow coloration of the beak and leg spur is due to the deposition of xanthophylls. If the bird is in the productive phase, xanthophylls are mainly deposited in the egg yolk, resulting in paler beaks and leg spurs. This statement is consistent with a hierarchical evaluation of the ovarian follicles, with 326 (74.1%) ovaries with viable follicles in a total of 440 ovary birds analyzed, 325 (73.9%) cloaca easily eversible analyzed at the physical evaluation (with ease of reversal under pressure) in a total of 440 ovary birds analyzed, and 328 (74.5%) analyzed birds out the total of 440 birds and normal body weight within the standard as recommended for the breed. Table 1. Distribution of physical evaluations of 440 laying hens over 76 wk of age.   Productive birds  Final productive birds3  Characteristics  Number (%) exhibiting standard traits  Number (%) not exhibiting standard traits  Ovaries exhibiting follicles  326 (74.1)  –4  Ovaries without follicles  –  114 (25.9)  Comb and wattle color  340 (77.3)  100 (22.7)  Ease of cloacal eversion  325 (73.9)  115 (26.1)  Leg spur and beak color  345 (78.4)  95 (21.6)  Body weight  328 (74.5)  112 (25.5)  Vertical distance1 > 5 cm  322 (73.2)  –  Vertical distance < 5 cm  –  118 (26.8)  Horizontal distance2 > 5 cm  314 (71.4)  –  Horizontal distance < 5 cm  –  126 (28.6)    Productive birds  Final productive birds3  Characteristics  Number (%) exhibiting standard traits  Number (%) not exhibiting standard traits  Ovaries exhibiting follicles  326 (74.1)  –4  Ovaries without follicles  –  114 (25.9)  Comb and wattle color  340 (77.3)  100 (22.7)  Ease of cloacal eversion  325 (73.9)  115 (26.1)  Leg spur and beak color  345 (78.4)  95 (21.6)  Body weight  328 (74.5)  112 (25.5)  Vertical distance1 > 5 cm  322 (73.2)  –  Vertical distance < 5 cm  –  118 (26.8)  Horizontal distance2 > 5 cm  314 (71.4)  –  Horizontal distance < 5 cm  –  126 (28.6)  1Vertical distance = distance between the end of the pubic bones and the keeled sternum. 2Horizontal distance = distance between the end of the pubic bones according ROSA et al. [2]. 3Laying hens not producing eggs. 4Note detected. View Large Table 1. Distribution of physical evaluations of 440 laying hens over 76 wk of age.   Productive birds  Final productive birds3  Characteristics  Number (%) exhibiting standard traits  Number (%) not exhibiting standard traits  Ovaries exhibiting follicles  326 (74.1)  –4  Ovaries without follicles  –  114 (25.9)  Comb and wattle color  340 (77.3)  100 (22.7)  Ease of cloacal eversion  325 (73.9)  115 (26.1)  Leg spur and beak color  345 (78.4)  95 (21.6)  Body weight  328 (74.5)  112 (25.5)  Vertical distance1 > 5 cm  322 (73.2)  –  Vertical distance < 5 cm  –  118 (26.8)  Horizontal distance2 > 5 cm  314 (71.4)  –  Horizontal distance < 5 cm  –  126 (28.6)    Productive birds  Final productive birds3  Characteristics  Number (%) exhibiting standard traits  Number (%) not exhibiting standard traits  Ovaries exhibiting follicles  326 (74.1)  –4  Ovaries without follicles  –  114 (25.9)  Comb and wattle color  340 (77.3)  100 (22.7)  Ease of cloacal eversion  325 (73.9)  115 (26.1)  Leg spur and beak color  345 (78.4)  95 (21.6)  Body weight  328 (74.5)  112 (25.5)  Vertical distance1 > 5 cm  322 (73.2)  –  Vertical distance < 5 cm  –  118 (26.8)  Horizontal distance2 > 5 cm  314 (71.4)  –  Horizontal distance < 5 cm  –  126 (28.6)  1Vertical distance = distance between the end of the pubic bones and the keeled sternum. 2Horizontal distance = distance between the end of the pubic bones according ROSA et al. [2]. 3Laying hens not producing eggs. 4Note detected. View Large These parameters indicate that most of the layers analyzed were in the productive phase and reflected the characteristics indicated by Rosa et al. [2], such as soft and elastic comb and wattle, wet and augmented cloaca, pale leg spurs and beaks, distance between pubic bones and keeled sternum, soft abdomen, and adequate body weight. The phenotypic characteristics that were addressed in this study can be used individually or together to exclude productive individuals or batches. According to Yasmeen et al. [1], a gradual decrease in the rate of egg production, egg shell quality, production inconstancy, and lower feed conversion efficiency should be considered as reasons to discard hens with advanced age. In this study, 7 of the 22 flocks (31.8%) were positive for Salmonella. It was verified in the literature that the frequency of this pathogen has been studied predominantly in laying hens in production, using the feces as samples. Studies on the presence of serovars of Salmonella spp. in fecal samples from commercial egg-producing hens in the State of California (USA) presented positive results for Salmonella Enteritidis presence in 10.5% of the evaluated lots [8]. Another survey carried out by a European multinational company indicated that 20.4% of the plots were positive for Salmonella Enteritidis or Salmonella Typhimurium [9]. Gama et al. [10] studied 12 commercial laying lots up to 76 wk of age and obtained 4 (33.3%) lots positive for Salmonella. Kottwitz et al. [11] isolated Salmonella in 8 (23%) of the 30 commercial egg farms in poultry aged 17 to 76 wk in the state of Paraná, Brazil. Salles et al. [12] detected 2 positive samples from the 32 fecal pool samples (6.25%) when performing monitoring in 8 poultry companies for layers up to 40 wk of age in the state of Ceará, Brazil. Considering the results found in the colon contents, it was verified that the bacteria (Table 2) were isolated from 3 lots with a frequency of 3.4%, and strains of Salmonella Schwarzengrund and Salmonella Cerro serovars were identified (Table 3), and that chickens have the potential to spread the bacteria, including these serovars incriminated in food outbreaks. Chickens infected and stressed by the catch during transport and slaughter can eliminate the pathogen in the feces and infect other birds and other animals, and these results are consistent with the findings of Forshel and Wierup [13] who reported that contamination of food by feces is a source of Salmonella infection for humans, other animals, and the environment [13, 14]. Table 2. Salmonella-positive samples found in 440 laying hens from 22 flocks over 76 wk of age and in their final production cycle. Samples  Positive flocks  Positive samples/N1  Liver  7  9/88 (10.2%)  Spleen  6  10/88 (11.4%)  Heart  5  5/88 (5.7%)  Oviducts swab  4  4/88 (4.5%)  Colon content  3  3/88 (3.4%)  Ovarian follicles  2  2/88 (2.3%)  Samples  Positive flocks  Positive samples/N1  Liver  7  9/88 (10.2%)  Spleen  6  10/88 (11.4%)  Heart  5  5/88 (5.7%)  Oviducts swab  4  4/88 (4.5%)  Colon content  3  3/88 (3.4%)  Ovarian follicles  2  2/88 (2.3%)  1Total analized sample. View Large Table 2. Salmonella-positive samples found in 440 laying hens from 22 flocks over 76 wk of age and in their final production cycle. Samples  Positive flocks  Positive samples/N1  Liver  7  9/88 (10.2%)  Spleen  6  10/88 (11.4%)  Heart  5  5/88 (5.7%)  Oviducts swab  4  4/88 (4.5%)  Colon content  3  3/88 (3.4%)  Ovarian follicles  2  2/88 (2.3%)  Samples  Positive flocks  Positive samples/N1  Liver  7  9/88 (10.2%)  Spleen  6  10/88 (11.4%)  Heart  5  5/88 (5.7%)  Oviducts swab  4  4/88 (4.5%)  Colon content  3  3/88 (3.4%)  Ovarian follicles  2  2/88 (2.3%)  1Total analized sample. View Large Table 3. Salmonella serovars and their numbers isolated from organs collected from 22 flocks (440 birds) of laying hens in the final production cycle. Serovars  Liver  Spleen  Heart  Oviduct  Colon  Follicle  Total isolates N (%)  Flocks (+)  Gallinarum  2  3  2  1  –1  1  9 (29.1)  2  Heidelberg  1  2  –  1  –  2  6 (19.3)  2  Enteritidis  1  1  1  1  1  –  5 (16.1)  1  Schwarzengrund  2  1  –  –  1  –  4 (12.9)  2  Cerro  1  1  –  –  1  –  3 (9.7)  1  Typhimurium  –  2  –  –  –  –  2 (6.5)  2  Johannesburg  –  –  –  1  –  –  1 (3.2)  1  Montevideo  –  –  1  –  –  –  1 (3.2)  1  Total  7  10  4  4  3  3  31 (100)    Serovars  Liver  Spleen  Heart  Oviduct  Colon  Follicle  Total isolates N (%)  Flocks (+)  Gallinarum  2  3  2  1  –1  1  9 (29.1)  2  Heidelberg  1  2  –  1  –  2  6 (19.3)  2  Enteritidis  1  1  1  1  1  –  5 (16.1)  1  Schwarzengrund  2  1  –  –  1  –  4 (12.9)  2  Cerro  1  1  –  –  1  –  3 (9.7)  1  Typhimurium  –  2  –  –  –  –  2 (6.5)  2  Johannesburg  –  –  –  1  –  –  1 (3.2)  1  Montevideo  –  –  1  –  –  –  1 (3.2)  1  Total  7  10  4  4  3  3  31 (100)    1Not detected. View Large Table 3. Salmonella serovars and their numbers isolated from organs collected from 22 flocks (440 birds) of laying hens in the final production cycle. Serovars  Liver  Spleen  Heart  Oviduct  Colon  Follicle  Total isolates N (%)  Flocks (+)  Gallinarum  2  3  2  1  –1  1  9 (29.1)  2  Heidelberg  1  2  –  1  –  2  6 (19.3)  2  Enteritidis  1  1  1  1  1  –  5 (16.1)  1  Schwarzengrund  2  1  –  –  1  –  4 (12.9)  2  Cerro  1  1  –  –  1  –  3 (9.7)  1  Typhimurium  –  2  –  –  –  –  2 (6.5)  2  Johannesburg  –  –  –  1  –  –  1 (3.2)  1  Montevideo  –  –  1  –  –  –  1 (3.2)  1  Total  7  10  4  4  3  3  31 (100)    Serovars  Liver  Spleen  Heart  Oviduct  Colon  Follicle  Total isolates N (%)  Flocks (+)  Gallinarum  2  3  2  1  –1  1  9 (29.1)  2  Heidelberg  1  2  –  1  –  2  6 (19.3)  2  Enteritidis  1  1  1  1  1  –  5 (16.1)  1  Schwarzengrund  2  1  –  –  1  –  4 (12.9)  2  Cerro  1  1  –  –  1  –  3 (9.7)  1  Typhimurium  –  2  –  –  –  –  2 (6.5)  2  Johannesburg  –  –  –  1  –  –  1 (3.2)  1  Montevideo  –  –  1  –  –  –  1 (3.2)  1  Total  7  10  4  4  3  3  31 (100)    1Not detected. View Large In the current study, Salmonella Enteritidis was detected in the all organ samples processed, except in a single batch of ovarian follicles. These findings are consistent with Gast et al. [15], who isolated the pathogen from the gastrointestinal tract, liver, spleen, ovary, and oviduct of apparently healthy laying hens that were inoculated experimentally with Salmonella Enteritidis. Salmonella Schwarzengrund, Salmonella Cerro, and Salmonella Johannesburg serovars were detected in the colon and reproductive organs (Table 3), indicating that chickens may produce eggs that can be contaminated by infection of the reproductive tract or by feces in the passage through the sewer [16]. The presence of Salmonella serovars isolated from apparently healthy birds in viscera such as the heart (18.2% (4/22)), liver (27.3% (6/22)), and ovarian follicles (9.1% (2/22)) (Table 2) demonstrates the possibility that poultry may be carriers of Salmonella, which points to the need for implementation of control measures that minimize the potential risk to food animals and human health. Hygienic sanitary measures in the handling of poultry are necessary or their products may promote cross-contamination and contaminate edible products of both animal and plant origin [11]. Sterzo et al. [17] identified Salmonella in the follicles’ ovaries, oviduct, and colon, and, therefore, the pathogen potentially can be incorporated into the yolk and white during the formation of the egg, or even on the shell during its passage through the cloaca, or in the nest contaminated with the feces. Although the hosts do not present clinical signs, they are asymptomatic carriers and potential disseminators of the agent, which confirms the importance of adult birds in the spreading of the agent [18, 19]. The following serovars were identified in the colon content: Salmonella Enteritidis, Salmonella Schwarzengrund, and Salmonella Cerro. These serovars are different from those found in the United Kingdom, which identified Salmonella Enteritidis, and Salmonella Typhimurium, Salmonella Mbandaka, Salmonella Havana, and Salmonella Enterica in the stool [20]. In comparison with other studies carried out in Brazil, Salmonella Enteritidis, Salmonella Javiana, and Salmonella Mbandaka, Salmonella Infantis were identified by Gama et al. [10] and Salmonella Enterica, Salmonella Mbandaka, Salmonella Infantis, and Salmonella Newport have also been identified [10, 11]. The results obtained here are similar to those obtained by Poppe [14] and Snow et al. [20], who reported that differences in geography, climate, egg production practices, and laying hens management in a given region reflect the presence of different serovars. Salmonella Heidelberg serovars were identified in the liver, spleen, oviduct, and ovarian follicles in 2 lots of the 22 studied, with a frequency of 19.3% (6/31) among the different serovars identified (Table 3). The Salmonella Heidelberg serovar is cited as the third most frequently isolated in poultry in Canada and the fourth in foodborne diseases in the United States [21]. In Brazil, since 1962, Salmonella Heidelberg has been identified in poultry and by-products [22]. Among the Salmonella that cause infections in humans, Salmonella Heidelberg seems to be more invasive and causes diseases with greater severity than other paratyphoid serovars [23]. It is considered an agent with a high invasive capacity, which constitutes a risk to public health and compromises food safety. Results reinforce the idea that the commercialization of old laying hens may promote an unsafe strategy. Salmonella Gallinarum serovar, agent of fowl typhoid, was detected in 2 lots with a frequency of 29.1% (9/31) in this study (Table 3). Salmonella Gallinarum mainly affects birds, being considered one of the main pathogens of the commercial poultry industry in the infection of chickens (Gallus gallus) [24]. This agent has caused serious animal health problems for the Brazilian poultry industry due to the occurrence of mortality during the rearing and production phase, loss of productive performance of chickens, increased mortality, and decrease in egg production. However, in this study the samples were collected at random and the birds had no clinical signs. Knowledge of the prevalence Salmonella serovars in a likely source of infection, such as discarded chickens, is important for the success of a control program. CONCLUSION It is concluded that individual phenotypic evaluations can be used before the birds are discarded because phenotypic changes are related to the final production. Laying hens over 76 wk of age should not be marketed to small breeders since, in asymptomatic birds, Salmonella serovars have been identified, which are important both for public health and for animal health. A relation was not found between asymptomatic birds for Salmonella and phenotypic evaluations, indicating that the changes were due to age. Footnotes Primary Audience: Production hen REFERENCES 1. Yasmeen F., Mahmood S., Hassan M., Akhtar N., Yaseen M.. 2008. Comparative productive performance and egg characteristics of pullets and spent layers. Pak. Vet. J.  28: 5– 8. 2. Rosa P. S., Albino J. J., Bassi L. J., Saatkamp M. G.. 2007. Identificação e descarte de poedeiras improdutivas. Pages 1– 2 in Instrução técnica para o produtor , Embrapa Suínos e Aves, Santa Catarina, BR. 3. Namata H., Méroc E., Aerts M., Faes C., Abrahantes J. C., Imberechts H., Mintiens K.. 2008. Salmonella in Belgian laying hens: an identification of risk factors. Prev. Vet. Med.  83: 323– 336. Google Scholar CrossRef Search ADS PubMed  4. Tahergorabi R., Matak K. E., Jaczynski J.. 2012. Application of electron beam to inactivate Salmonella in food: recent developments. Food Res. Int.  45: 685– 694. Google Scholar CrossRef Search ADS   5. Merck KGaA, Darmstadt, Germany. http://www.merckmillipore.com/BR/pt/products/industrial-microbiology/culture-media/dLWb.qB.5kgAAAFAX8JkiQpx,nav. 6. Anonymous. 1997. Monitoring and detection of Salmonella. Pages 256 in Poultry and Poultry Environments . Georgia Poultry Laboratory, Oakwood, GA. 7. Probac do Brasil - Produtos bacteriológicos Ltda. Soro Salmonella polivalente, São Paulo, BR. http://probac.com.br/Produto/Detalhe/pt-BR/457. 8. Castellan D. M., Kinde H., Kass P. H., Cutler G., Breitmeyer R. E., Bell D. D., Ernst R. A., Kerr D. C., Little H. E., Willoughby D., Riemann H. P., Ardans A., Snowdon J. A., Kuney D. R.. 2004. Descriptive study of California egg layer premises and analysis of risk factors for salmonella enterica serotype Enteritidis as characterized by manure drag swabs. Avian Dis.  48: 550– 561. Google Scholar CrossRef Search ADS PubMed  9. EFSA 2007. Report of the task force on zoonoses data collection on the analysis of the baseline survey on the prevalence of Salmonella in broiler flocks of Gallus gallus in the EU 2005 - 2006. Pages 1– 85, in European Food Safety Authority . EFSA J. Publishing, Parma, IT. 10. Gama N. M. S. Q., Berchieri A. Jr, Fernandes S. A.. 2003. Occurrence of Salmonella sp in laying hens. Rev. Bras. Cienc. Avic.  5: 15– 21. Google Scholar CrossRef Search ADS   11. Kottwitz L. B. M., Oliveira T. C. R. M., Alcocer I., Farah S. M. S. S., Abrahão W. S. M., Rodrigues D. P.. 2010. Avaliação epidemiológica de surtos de salmonelose ocorridos no período de 1999 a 2008 no Estado do Paraná, Brasil. Acta Sci. Health Sci.  32: 9– 15. 12. Salles R. P. R., Teixeira R. S. C., Siqueira A. A., Silva E. E., Castro S. B., Cardoso W. M.. 2008. Monitoramento bacteriológico para Salmonella spp. em poedeira comercial na recria e produção de empresas avícolas da região metropolitana de Fortaleza, CE, Brasil. Ci. An. Bras.  9: 427– 432. 13. Forshell L. P., Wierup M.. 2006. Salmonella contamination: a significant challenge to the global marketing of animal foods products. Rev. Sci. Tech. Office Int. Epizoot.  25: 541– 554. Google Scholar CrossRef Search ADS   14. Poppe C. 2000. Salmonella infections in the domestic fowl. Pages 107– 132 in Book Salmonella in Domestic Animals . CABI Publishing, UK. Google Scholar CrossRef Search ADS   15. Gast R. K., Guraya R., Guard-Bouldin J., Holt P. S., Moore R. W.. 2007. Colonization of specific regions of the reproductive tract and deposition at different locations inside eggs laid by hens infected with Salmonella Enteritidis or Salmonella Heidelberg. Avian Dis.  51: 40– 44. Google Scholar CrossRef Search ADS PubMed  16. Gast R. K. 1993. Detection of Salmonella enteritidis in experimentally infected laying hens by culturing pools of egg contents. Poult. Sci.  72: 267– 274. Google Scholar CrossRef Search ADS PubMed  17. Sterzo E. V., Varzone J. R. M., Ferrari R.. 2008. Salmoneloses aviárias. Ensaios e Ciência. Ci. Biol. Ag. Saúde.  12: 129– 138. 18. Chappell L., Kaiser P., Barrow P., Jones M. A., Johnston C., Wigley P.. 2009. The immunobiology of avian systemic salmonellosis. Vet. Immunol. Immunopathol.  128: 53– 59. Google Scholar CrossRef Search ADS PubMed  19. Sadeyen J. J., Trotereau P., Velge J., Marly C., Beaumont P. A., Barrow N., Bumstead A., Lalmanach A. C.. 2004. Salmonella carrier state in chicken: comparison of expression of immune response genes between susceptible and resistant animals. Microbes Infect.  6: 1278– 1286. Google Scholar CrossRef Search ADS PubMed  20. Snow L. C., Davies R. H., Christiansen K. C., Carrique-Mas J. J., Wales A. D., O’connor J. L., Cook A. J. C., Evans S. J.. 2007. Survey of the prevalence of Salmonella species on commercial laying farms in the United Kingdom. Vet. Rec.  161: 471– 476. Google Scholar CrossRef Search ADS PubMed  21. Chittick P., Sulka A., Tauxe R. V., Fry A. M.. 2006. A summary of national reports of foodborne outbreaks of Salmonella Heidelberg infections in the United States: clues for disease prevention. J. Food Prot.  69: 1150– 1153. Google Scholar CrossRef Search ADS PubMed  22. Hofer E., Silva Filho S. J., E.M.F. R.. 1997. Prevalência de sorovares de Salmonella isolados de aves no Brasil. Braz. J. Vet. Res . 17: 55– 62. 23. PHAC 2007. Salmonella Heidelberg Ceftiofur-Related Resistance in Human and Retail Chicken Isolates . Public Health Agency of Canada. http://www.phac-aspc.gc.ca/cipars-picra/heidelberg/pdf/heidelberg_e.pdf. 24. Jeong J. H., Song M., Park S. I., Cho K. O., Rhee J. H., Choy H. E.. 2008. Salmonella enterica serovar Gallinarum requires ppGpp for internalization and survival in animal cells. J. Bacteriol.  190: 6340– 6350. Google Scholar CrossRef Search ADS PubMed  © 2018 Poultry Science Association Inc. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

Journal

Journal of Applied Poultry ResearchOxford University Press

Published: May 16, 2018

There are no references for this article.

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off