At the Faculty of Veterinary Medicine and Animal Science (FMVZ) at USP, research reveals that the gestation environment of female pigs has an influence on the development of the piglet's brain. The study, carried out in partnership with the Universities of Passo Fundo (Rio Grande do Sul) and Uppsala (Sweden), indicates that pregnancy in an uncomfortable environment increases the occurrence of repetitive behaviors, so-called stereotypies. 

The researchers also carried out an epigenetic analysis, that is, the influence of the external environment on the activation or not of genes. Changes were found in areas of the brain linked to emotions both in the offspring of pigs that received environmental enrichment, and in piglets born to females that showed stereotypies, such as chewing without having anything in their mouth.

The results of the work were published in an article in the scientific journal Epigenetics. In Brazil, Normative Instruction 113 of the Ministry of Agriculture and Livestock, promoted on December 16, 2020, establishes for the year 2045 the prohibition of the use of gestation crates, the most widely adopted pig breeding system in the country, in which Animals are confined in cages. 

“The standard mirrors what is already happening in Europe, where the system was banned in 2012, but the most frightening thing is the deadline given for the change”, says FMVZ professor Adroaldo Zanella, research advisor, to Jornal da USP. “The instruction also provides for the enrichment of the environment where the pigs are kept.”

“All experiments were carried out in collective pens, which represent better welfare conditions. The results of the work serve as a warning about the risks of maintaining the old system for so long”, says researcher Patrícia Tatemoto, first author of the article. “This study highlights the consequences of the gestation environment on the organization of the animals’ brain, with lifelong consequences”, adds Zanella.

In the first stage of the study, carried out with 36 female pigs and their piglets, expressions of repetitive behaviors (stereotypies) in mothers were analyzed. “We concluded that manifestations of stereotypy were correlated with changes in the piglets’ emotionality”, reports Patrícia Tatemoto. “The more repetitive behaviors the mothers had, the less the piglets expressed fear.” The data obtained in this phase were published in three studies between 2019 and 2020, in the journals Frontiers in Veterinary Science and Applied Animal Behavior Science.

Repetitive behaviors

During the second phase of the research, pregnant females were divided into two environments, and in one of them, the stalls were lined with hay to verify the influence of environmental enrichment on the generation of repetitive behaviors. “Pigs like to explore their environments, they have a very rich olfactory system, so it made sense to place the hay, which was changed daily”, says the researcher. “In environments without hay, the lack of meeting this animal demand led many females to chew without anything there, which is a stereotypy.”

At this stage, epigenetic changes in the piglets were also analyzed, that is, changes influenced by the environment in the activation of genes (methylation) in the brain. Three regions responsible for activating the limbic system, which modulates emotions, were verified: the amygdala, the frontal cortex and the hippocampus. “An epigenetic change does not alter the genetic code. It determines which genes are activated and deactivated and when these effects occur”, explains the FMVZ professor. “The epigenome is influenced by the external environment, such as diet, lifestyle and environmental factors. Methylation is an epigenetic change that modulates gene activation.”

“The enrichment of the gestation environment affected more the tissue of the frontal cortex, the area responsible for determining the execution of movements, and the hippocampus, responsible for memory processes”, observes Patrícia Tatemoto. “The repetitive behavior demonstrated by female pigs was associated with the methylation of several genes in the amygdala, that is, it altered the activation of genes in the area that is the center of fear in the brain”, observes the researcher. “In the previous stage of the study, when the mother expressed stereotypy, the children showed less fear.”

According to the researcher, new studies will determine exactly the mechanism involved in the process, and its consequences. “However, this is a sign that the well-being of mothers during pregnancy is compromised,” she highlights.

"The occurrence of stereotypies apparently mitigates the impact of the poor environment on the organization of piglets' emotionality.”

“Research has shown that enriching the gestation environment is extremely important for improving the animal welfare of females, and stereotypy changes the fear indicators of the offspring”, highlights Professor Zanella. “The results show the importance of the prenatal period in modulating the central nervous system for adaptive processes, and in this way, improving well-being conditions during pregnancy is providing tools for newborns to face the demands and challenges of the pregnancy environment."

The conclusions of the work were presented in the article An enriched maternal environment and stereotypies of sows differentially affect the neuro-epigenome of brain regions related to emotionality in their piglets, published in the scientific journal Epigenetics on May 16th. The research was financed through a project by the São Paulo State Research Support Foundation (FAPESP), coordinated by professor Zanella, and Patrícia Tatemoto had the support of the Coordination for the Improvement of Higher Education Personnel (CAPES). The experiments were carried out on the USP campus, in Pirassununga, with the collaboration of Granja Topgen, in Jaguaraiva (Paraná).