Potential of plant essential oils and their components in animal agriculture – in vitro studies on antibacterial mode of action

Review ARTICLE

Front. Vet. Sci., 14 September 2015 | http://dx.doi.org/10.3389/fvets.2015.00035

Corliss A. O’Bryan, Sean J. Pendleton^†, Philip G. Crandall and Steven C. Ricke*

• Department of Food Science, Center for Food Safety, University of Arkansas, Fayetteville, AR, USA

The antimicrobial activity of essential oils and their components has been recognized for several years. Essential oils are produced as secondary metabolites by many plants and can be distilled from all different portions of plants. The recent emergence of bacteria resistant to multiple antibiotics has spurred research into the use of essential oils as alternatives. Recent research has demonstrated that many of these essential oils have beneficial effects for livestock, including reduction of foodborne pathogens in these animals. Numerous studies have been made into the mode of action of essential oils, and the resulting elucidation of bacterial cell targets has contributed to new perspectives on countering antimicrobial resistance and pathogenicity of these bacteria. In this review, an overview of the current knowledge about the antibacterial mode of action of essential oils and their constituents is provided.

Introduction

Plant materials including flowers, roots, bark, leaves, seeds, peel, fruits, and wood can be used to extract aromatic and volatile liquids known as essential oils (EOs) (1–3). These EOs have a long history of use for medical purposes, in perfumes and cosmetics, and as herbs and spices for foods. EOs are considered to be secondary metabolites in plants; secondary metabolites are organic compounds that are not directly involved in the normal growth, development, or reproduction of the plant (4). These secondary metabolites are often involved in plant defense and thus may possess antimicrobial properties (4, 5). The first experiment to determine the bactericidal properties of EOs is said to have been carried out by de la Croix in 1881 (6). In more recent years, many EOs, or their components, have been shown to possess broad-range antibacterial properties (7).

Increased resistance to infectious diseases, including parasitic infections such as coccidiosis, has been noted when plant phytonutrients were fed to animals. For instance, Lee et al. (8) found that feeding plum powder to laying hens increased their immune response as well as conferring immunity to coccidiosis. Lillehoj et al. (9) determined the effects of feeding capsicum oleoresin or cinnamaldehyde on the global gene expression profiles of broilers. Capsicum oleoresin induced gene changes in genes associated with metabolism and immunity, whereas cinnamaldehyde affected genes related to antigen presentation, humoral immune response, and inflammatory disease. Feeding of these compounds also protected the birds against infection with live coccidiosis parasites. Mathlouthi et al. (10) found that oregano or rosemary EOs had different antimicrobial effects in vitro against pathogenic and non-pathogenic bacteria but had the same growth promoting effects as avilamycin when added to broiler diets. Authors speculated that the in vivo growth promotion effects were due to ecological changes in the bacterial gut flora rather than antibacterial effects against a single bacterial genus and species. Betancourt et al. (11) confirmed a shift in gut flora in the foregut but not ceca and colon in broilers fed oregano EOs during a 42-day grow out period.

Alali et al. (12) tested a mixture of carvacrol, thymol, eucalyptol, and lemon for the ability to prevent colonization and shedding in broilers intentionally fed Salmonella Heidelberg. They determined that feeding 0.05% (v/v) of the EO mixture significantly reduced the colonization of the crops of challenged birds as well as lowering feed conversion and improving weight gain in the birds. However, cecal colonization and shedding were not significantly decreased. Cerisuelo et al. (13) fed an EO mixture composed of cinnamaldehyde and thymol to broilers, either with or without butyric acid. They determined that the EO blend reduced cecal numbers of Salmonella, especially when combined with butyric acid, as compared to control feed. Ricke et al. (14) provide an overview of the anti-Salmonella effects of EOs in agriculture.

Benchaar et al. (15) investigated the effects of EOs in vitro rumen microbial fermentation. They determined that only the phenolic compounds, carvacrol, thymol, and eugenol affected ruminal fermentation, relative to the control, increasing pH and butyrate and decreasing propionate, indicating antibacterial activity which was not nutritionally beneficial. Callaway et al. (16) studied the in vitro effects of orange peel and orange pulp, both sources of EOs, against Escherichia coli O157:H7 and Salmonella typhimurium in rumen fluid. Growth of both pathogens was reduced by addition of 0.002 g/ml of orange pulp or orange peel. Callaway et al. (17) were able to demonstrate that the orange peel products when fed to experimentally inoculated sheep reduced S. typhimurium populations in the gut, with a significant reduction reached in the ceca.

The antimicrobial properties of EOs are a recent focus for agricultural applications because of a desire on the part of many consumers to reduce the use of “hazardous or unnatural chemicals” in their food (18–20). Although there are many studies on the antimicrobial activities of EOs, few take the next step and determine the mode of action of these compounds. However, application of EOs as antibacterial substances for food animals or as food preservatives requires detailed knowledge about their properties, including the mode of action. The purpose of this review is to provide an overview of current knowledge about the antimicrobial mode of action of EOs and their constituents.