Effect of Dietary Hemp Seed on Oxidative Status in Sows during Late Gestation and Lactation and Their Offspring

animals Article Effect of Dietary Hemp Seed on Oxidative Status in Sows during Late Gestation and Lactation and Their Offspring Laurentiu Mihai Palade * , Mihaela Habeanu, Daniela Eliza Marin, Veronica Sanda Chedea , Gina Cecilia Pistol , Iulian Alexandru Grosu, Anca Gheorghe, Mariana Ropota and Ionelia Taranu National Research Development Institute for Animal Biology and Nutrition, IBNA Balotesti, Calea Bucuresti nr. 1, Balotesti, 077015 Ilfov, Romania; (M.H.); (D.E.M.); (V.S.C.); (G.C.P.); (I.A.G.); (A.G.); (M.R.); (I.T.) * Correspondence: ; Tel.: +40-21-351-2081



 Received: 4 March 2019; Accepted: 15 April 2019; Published: 25 April 2019 Simple Summary: Hemp seeds are rich in polyunsaturated fatty acids as well as other bioactive compounds. Using dietary hemp seeds as late gestation and lactation supplementation for sows and early life supplementation for piglets, we found that the indicators of oxidative status were improved in both sows and offspring. Besides the significant improvement in the antioxidant defense system of the sows, our assessment of dietary intervention resulted in an array of increased antioxidative status markers for their progeny. In addition, this could be translated into increased adaptability to the upcoming weaning stage. Abstract: This study shows the antioxidant effect of a dietary hemp seed diet rich in ω-6 polyunsaturated fatty acid (PUFA) on oxidative status in sows during late gestation and lactation and their offspring. Ten pregnant sows were divided into two groups and fed either a control diet (CD) or a hemp diet (HD) containing 2% hemp seed meal for a period of 10 days before farrowing and 5% throughout the lactation period (21 d). After farrowing, 16 of their resulting piglets were divided into two groups: control group CD (eight piglets derived from control sows) and HD group (eight piglets derived from HD sows), respectively. Blood collected from sows and piglets at day 1, 7 and 21 was used for the measurement of antioxidant enzymes (catalase (CAT), superoxide dismutase (SOD), glutathione (GPx)), nitric oxide production (NO), lipid peroxidation (thiobarbituric acid reactive substances—TBARS), reactive oxygen species (ROS) generation and total antioxidant capacity (TAC) in plasma. The results showed a significant improvement in the oxidative status of sows fed HD throughout lactation compared with CD. Similarly, in piglets, HD positively influenced the activities of antioxidant enzymes, TAC and NO levels and significantly decreased lipid peroxidation in plasma until weaning, in comparison with the CD group. This study suggests the potential of hemp seed diet to improve the overall antioxidant status of the lactating sows and their progeny. Keywords: hemp seeds; diet; PUFA; oxidative status; antioxidant enzymes 1. Introduction At weaning, the changes in the piglets’ environment (separation from the sow), nutrition (switch from milk to solid feed) and regrouping (mixing with piglets from other litters) are significant and stressful [1]. Weaning induces a transient oxidative status, usually associated with low feed intake and diarrhea [2], which results in physiological and immunological disturbances, such as an Animals 2019, 9, 194; doi:10.3390/ani9040194 www.mdpi.com/journal/animals Animals 2019, 9, 194 2 of 19 increase in pro-inflammatory cytokines [1,3,4], higher concentrations of hydroperoxides (HPO) and oxidative stress index, HPO/BAP (hydroperoxide/blood antioxidant potential) [2]. Antibiotics have been widely used to control weaning-related infectious diarrhea caused primarily by an increase in Escherichia coli [5]. Alternative approaches, such as nutritional interventions based on bioactive compounds able to replace antibiotics, have been investigated [6,7] in pigs after the ban on antibiotics (2006). Various bioactive compounds could pass through the milk to the offspring, contributing to the development of their immune systems in early life [8–10]. Such interventions positively influence the health status of sows and piglets and the capacity of their offspring to better resist the stress of weaning [11]. For instance, oral administration of Nigela sativa (black cumin, a plant rich in bioactive constituents with antimicrobial activity) extracts, in doses equivalent to 0.0, 1.5 and 4.5 g extract kg−1 to weanling piglets, reduced the levels of naturally occurring E. coli in the jejunal and rectal contents [12]. The addition of Macleaya cordata (Wild) R. Br. extracts to feed for nursery and growing pigs decreased diarrhea occurrence and increased their weight gain [13,14]. Devi et al. (2015) showed that feeding a phytogenic additive (combination of clove, cinnamon, and fenugreek) to piglets challenged with F4+ enterotoxigenic E. coli (ETEC) improved their average daily gain [15]. Also, research conducted by Namkung et al. (2004), Newton et al. (2002) and Liu et al. (2016) showed that bioactive compounds from extracts of cinnamon, thyme, oregano [16] and Sanguinaria canadensis [14,17] inhibited gastrointestinal tract (GIT) colonization by pathogenic bacteria. The consumption of dietary linseed oil during gestation and lactation modifed the fatty acid composition of ileum, its structure and physiology, decreasing the sensitivity of the ileal epithelial barrier to mast cell degranulation in the offspring [18,19]. Increasing antioxidant nutrients in the sow diet could prevent oxidative stress by increasing antioxidant capacity [20]. These authors observed that supplementation of the diet of sows with resveratrol, a powerful antioxidant from grape, during gestation and lactation increased antioxidant enzyme levels in colostrum and milk [20]. This was benefical for piglets by increasing their antioxidant status and weight gain from birth to weaning [20]. Similarly, other bioactive compounds from soy, ginger, grape, etc., alleviate oxidative stress (increasing plasma antioxidants, decreasing pro-inflammatory response) and improve the performance of sows and piglets [21–23]. Both the in vivo and in vitro evidence showed the effect of such compounds in preventing inflammation and oxidative stess. The study of Lin et al. (2016) reported that docosahexaenoic acid (DHA), an ω-3 polyunsaturated fatty acid (PUFA), attenuated LPS-induced inflammatory responses in porcine mammary epithelial cells through modulation of the TLR4 pathway [24]. Also, Horn et al. (2017) showed that garlic compounds mitigate oxidant-induced cellular dysfunction, modulate innate immune function, and stimulate the proliferation of lymphocytes [6]. Hemp (Cannabis sativa L.) is one of the many plants rich in bioactive compounds that have been exploited for health food and medicinal purposes [25–27]. Recently, interest in hemp has been largely focused on seeds, which are nutritionally beneficial for both humans and animals [28]. Hemp seeds (HS) are a great source of phytochemicals, containing around 30% fats and 25% proteins as well (...truncated)