The tendency of increase observed in the present study (Fig. 1) showed that the COI of poultry carcasses is a useful tool in the identification of historical variations of condemnation. These trends reflect technologies used, sanitary conditions of the batch, and employee training policies [3,4,5]. Therefore, the proper recording and analysis of the occurrences of condemnation in a slaughterhouse are essential for the planning of preventive measures, aiming at economic gains for the meat supply chain [10, 11]. In addition, they may show behavioral changes in condemnation rates and indicate the need for specific investigations, such as the changes observed in COIs from 2017 onwards (Fig. 1).
Concurrent with the increase in slaughterhouse COI, there was a reduction in turkey slaughter, with a subsequent discontinuation and replacement of broiler slaughter by heavy chicken slaughter. Evaluating Groups A and B, it was evidenced that there was a higher rate of condemnation in the period in which only heavy chickens were slaughtered (Table 2). The higher age of these animals at slaughter, compared to griller chickens, and the high stocking rate of the sheds were factors directly linked to the increase in the occurrence of condemnation . Turkeys showed little impact on this COI variation, as they represented only 5% of the total number of animals slaughtered in the period evaluated. Furthermore, changes in Brazilian legislation in 2017 and 2019 impacted carcass disposal standards and increased the number of inspection agents in the slaughter process. Added to this, the greater incentive to train teams, from 2018 onwards, with a focus on ante and post-mortem inspection, may also have contributed to this finding [1, 17, 18].
In agreement with other studies our findings showed that condemnation rates can vary from 0.75 to 13.16%, so the result observed in the present work has an intermediate value, with 7% of condemnations between 2009 and 2019 [4, 6,7,8, 19]. However, the direct comparison between condemnation rates from different countries must be done with caution since there are variations in the legislation and the criteria for the destination of the carcass. In addition, characteristics of climate, altitude, production systems, and even social differences may contribute to the observed variations [9, 10, 20,21,22].
The relative contribution of the causes of condemnation of poultry carcasses highlights the challenges that need to be faced by the poultry industry (Table 1). These challenges impact differently in each region and country as they are influenced by management failures, the slaughter process, or poultry flock health [6, 10, 22, 23]. The latter, as it involves etiological agents, tend to be influenced by management and also by geographic and climatic characteristics of each region and season of the year [5, 7, 11].
In the present study, the four main causes of condemnation were: (i) contamination, (ii) contusion/traumatic injury, (iii) dermatitis and (iv) aersacculitis (Table 1)”. Similar results were found in other studies, with erosacculitis being the only difference observed, since for other studies this was not among the main causes of condemnation [4, 7, 8]. This difference can be explained by the slaughter of broilers and turkeys in the evaluated slaughterhouse, the latter being responsible for contributing with the highest number of condemnations for aerosacculitis. The higher occurrence of aerosacculitis in turkeys may be related to the greater age at slaughter, which implies a longer exposure to variables relevant to the development of the disease: handling failures, poor air quality, high concentrations of dust and ammonia, and the presence of pathogenic microorganisms such as Escherichia coli and Mycoplasma spp. [4, 10, 24].
The high frequency of carcass contamination (37.12%) must be analyzed and prevented by slaughterhouses. According to Brazilian legislation, condemnation by contamination can occur in poultry due to extravasation of gastrointestinal content, bile or any other type of macroscopic contamination identified in the slaughter line . Among the possible causes of contamination, the extravasation of gastrointestinal contents deserves special attention as it is one of the main sources of foodborne pathogens such as Salmonella spp., E. coli, and Campylobacter jejuni [20, 23, 25]. Carcass contamination occurs largely due to difficulties in adjusting equipment during the slaughter of uneven batches, or fasting periods in disagreement with the recommendations [3, 7].
The second main cause of condemnation (injury/traumatic injury), as well as contamination, is also considered a technological failure and is usually related to problems during the catching, transport, or hanging of poultry [22, 26, 27]. Therefore, the integration of the production chain (producers and slaughterhouse) and training focused on good management practices and animal welfare are essential for reducing condemnation [3, 4, 28].
These condemnations resulting from technological failures are part of the daily routine of poultry slaughterhouses. In this way, continuous actions need to be incorporated into the establishments’ practices, such as training and preventive maintenance of equipment, to reduce these problems [3, 29, 30]. It should be noted, however, that specific studies must be adopted in each slaughterhouse to identify the real cause of the problem among all the variables that may be involved.
Dermatitis was identified as the third leading cause of condemnation, being the first when considering those involving pathogenic agents. Dermatitis is the term used by the Brazilian Federal Inspection Service to record skin diseases, with the exception of cellulitis . Its occurrence is related to high stocking rates, bird weight, temperature stress, and litter quality [7, 12].
High and moderate positive correlations between some causes of condemnation were identified in the present study (Fig. 2). Septicemia has already been associated with several bacteria such as Escherichia coli, capable of reaching the bloodstream during a case of aerosacculitis or through the intestinal wall, and Staphylococcus aureus, which are commonly associated with skin lesions (dermatoses and cellulitis) [3, 10]. In cases of cachexia and disgusting aspects, there are several possible causes associated with this finding, such as malnutrition, which is unlikely in industrial production, management problems, environment, or secondary causes of diseases or pathologies [23, 32]. Therefore, by evaluating the diseases’ predisposing factors and the correlation results, we can understand that actions that improve sanitary and management conditions will bring benefits in the simultaneous reduction of several condemnation causes [4, 12].
The relationship between causes of condemnation and annual variations in rainfall, humidity, and temperature have already been studied by other authors [12, 33]. In the present study, the only cause of condemnation for non-technological failures with an ASI difference was ascitic syndrome, with the highest values identified in the months of July to October (P < 0.05) (Fig. 3). A similar result was found by Souza et al.  who, analyzing the states with the highest poultry production in Brazil, identified the highest ASIs from July to September. These variations in ASI values can be explained by the fact that ascitic syndrome is a metabolic syndrome, which is caused by interactions between diet, genetic, and environmental factors (altitude and temperature) [34, 35]. Corroborating this information, July to September correspond to the coldest period of the year in the southeastern region of Brazil . Thus, the findings of this work can help in the planning of adequate management in relation to the temperature and ventilation of the sheds in cold climates, reducing the incidence of this syndrome.
Regarding the evaluation of reductions and increases in the ASIs for condemnations not associated with technological failures (Fig. 4), we can use the results obtained as a way of predicting future condemnation in a stable population [33, 36]. This forecast on the occurrence of condemnation is fundamental in determining preventive management procedures and directing the training of inspection and quality control teams and technicians working in the field . This training can prioritize causes of condemnation that are critical in a certain period of the year, instead of causes in which there is a significant reduction in the occurrence. This rational use of financial and human resources can contribute to obtaining more expressive results in the reduction of diseases in the field and in the ease of their identification during the slaughter process [15, 37].