A selection of assays published since 2013 of successful antimicrobial activity of chosen probiotics using the spot‐on lawn/agar spot assay on chosen pathogenic microorganisms.
Abstract
The antimicrobial or antagonistic activity of probiotics is an important property that includes the production of antimicrobial compounds, competitive exclusion of pathogens, enhancement of the intestinal barrier function and others. There are many methods to ascertain probiotic properties, including various in vitro and in vivo methods. The in vivo methods include various modifications of the spot‐on lawn assay, agar well diffusion assay (AWDA), co‐culturing methods, usage of cell lines and others. In many cases in vitro antagonist activity is observed, but in real settings it is not observed. The in vivo methods mainly used are animal models; however, their use is being restricted according to the European legislation OJ L136. The justification of animal models is also questionable as the results of studies on animals do not predict the same results for humans. The use of replacement alternative methods, for example incorporating human cells and tissues, avoids such confounding variables. Most important studies are double‐blinded randomized clinical trials; however, these studies are difficult to perform as it is not easy to achieve uniform conditions. There is a clear need for more elaborate assays that would better represent the complex interactions between the probiotics and the final host. This complex situation is a challenge for scientists.
Keywords
- antimicrobial effect
- in vitro methods
- in vivo methods
- pathogens
- probiotics
1. Introduction
Throughout the history of microbiology, most human studies have been focused on the disease‐causing organisms found on or in people; whilst fewer studies have examined the benefits of the resident bacteria. However, we are surrounded by beneficial microorganisms that live in or on the human body. The intestinal microbiota is very well adapted, exceptionally stable and very specific for each individual. In normal conditions of stable functioning of the digestive system, neutral and beneficial microorganisms dominate. It is estimated that there are 100 trillion microorganisms in the intestine of a human adult and this is 10 times larger than the number of cells in the human body [1, 2]. However, the balance of the intestinal microbiota is negatively influenced by modern lifestyle, leading to increased numbers of pathogenic microorganisms that disrupt microbial balance and cause a reverse from beneficial to harmful functioning. In such cases, the external support with probiotics is very welcome and supported by several scientific studies [3].
According to the Food and Agriculture Organisation of the United Nations (FAO) and the World Health Organisation (WHO), probiotics are defined as live microorganisms, which when administered in adequate amounts confer a health benefit on the host [4, 5]. The most common probiotic bacteria are certain strains from the genera
Probiotics together with other beneficial microbes are commensals of the gut and differ from pathogenic bacteria in the terms of their actions on immune cells in the gut as they do not stimulate the proliferation of mononuclear cells or trigger an inflammatory action [8]. Regardless of whether the probiotics are used for human or animal consumption, there are several characteristics that a probiotic must achieve. Some of the important characteristics of probiotics include the following: a probiotic must be generally required as safe (GRAS); a probiotic should exhibit bile and acid tolerance in order to survive the path from the oral cavity to the small intestine where it lives, multiplies and excretes beneficial nutrients and molecules; a probiotic should have the ability to adhere to mucus and/or epithelial cells, and/or other surfaces; a probiotic should be susceptible to antibiotics; a probiotic should exhibit antimicrobial activity against pathogens [3, 5, 9, 10]. Although it is accepted that probiotics must be of human origin [4, 5], many authors have found that some strains that are not normally isolated from human have shown to be effective [11, 12], which negates this requirement. As noted above, one of the important attributes of probiotics is their antimicrobial effect against pathogens by maintaining the homeostasis of the intestinal flora. Assessing the antimicrobial effect of various probiotics against pathogenic microorganisms is the guiding concept of this chapter. This chapter reviews the principles and results from various authors of different methods for determining the antimicrobial or antagonistic effect of probiotics against potential pathogens.
2. Antimicrobial or antagonistic properties of probiotics
In literature both the terms “antimicrobial” and “antagonistic” are found to determine the ability of one species to inhibit the growth of another species. According to the online Encyclopaedia Britannica, “antagonism” refers to an “association between organisms in which one benefits at the expense of the other,.” However, this encyclopaedia does not include the adverb “antimicrobial.” On the other hand, it contains “antimicrobial agent” that refers to “a large variety of chemical compounds that are used to destroy microorganisms or to prevent their development..” The online Merriam Webster dictionary defines “antimicrobial” as “destroying or inhibiting the growth of microorganisms and especially pathogenic microorganisms” and “antagonistic” as “showing dislike or opposition: showing antagonism.”
This antimicrobial/antagonistic ability is especially important for probiotics as one of the functional beneficial requirements of probiotics is a broad antimicrobial spectrum as well as antagonism against pathogenic bacteria with strong antimicrobial activity. The antagonistic activity of one microorganism against another can be caused by competitive exclusion, immune modulation, stimulation of host defence systems, production of organic acids or hydrogen peroxide that lower pH, production of antimicrobials such as bacteriocins, antioxidants, production of signalling molecules that trigger changes in gene expression [13–15]. Antimicrobial substances produced by beneficial microorganisms are known to include lactic acid, acetic acid, formic acid, phenyllactic acid, benzoic acid as well as other organic acids, short chain fatty acids, hydrogen peroxide, carbon dioxide, acetaldehyde, acetoin, diacetyl, bacteriocins and bacteriocins‐like inhibitory substances and others [10, 16, 17]. The most common bacteriocins include lacticin, lactocin, pediocin, pisciolin, enterocin, reuterin, plantaricin, enterolysin and nisin [18, 19].
3. Methods
3.1. Methods of literature research
A literature overview of three databases was conducted using the two following keywords: “probiotic” and “antimicrobial” between the years 1980 and 2016. The search yielded 2882, 1017, and 6200 publications in PubMed, Web of Science, and Science Direct databases, respectively (Figure 1).
All three databases showed great increase in the number of publications in the past 10 years. The highest results were obtained via Science Direct due to the fact that this database includes various journals and books from the area of food and dairy sciences, the area of probiotics for animals as well as the area of human probiotics. PubMed on the other hand contains only research of probiotics for humans. Also, the programs for keyword searching for each chosen database seem to differ among each other thus yielding very different numbers of publications in journals, chapters and conference proceedings. The research on the methods for determining the antimicrobial effect of strain‐specific probiotics was conducted by adding an additional keyword aside “probiotic.” This keyword described the various investigated methods for determining the antimicrobial/antagonistic activity of probiotics (i.e., spot‐on lawn, agar spot, agar well diffusion, paper disc, co‐culturing,
3.2. In vitro methods for determining the antimicrobial/antagonistic effect of probiotics against other microorganisms
3.2.1. Spot‐on lawn antimicrobial assay/agar spot antimicrobial assay
The spot‐on lawn antimicrobial assay has been described by several authors. Several modifications of the method have been made. Also various other expressions are used such as agar spot assay, critical dilution assay and deferred antagonism assay [10, 16, 20–22].
One of the simplest published principles of the spot‐on lawn antimicrobial assay (Figure 2a) consists of the following steps: different nutrients, selective or differential media, are prepared and various chosen indicator microorganisms or pathogens at different initial concentrations are either inoculated in a confluent manner after hardening of agar or are mixed with the agar in liquid state and poured into the plate. Different dilutions of aliquots of the investigated probiotic or cell‐free supernatant with bacteriocins are then spotted onto the media already inoculated with chosen indicator microorganisms [20, 23, 24].
After incubation, the antimicrobial activity is expressed either as inhibition zone or as arbitrary units (AU/mL). The zone of inhibition is noted either as the diameter or the area of the inhibition zone. The critical dilution is noted as the last dilution that produces a zone of inhibition larger than 6 mm. Arbitrary units are defined as the reciprocal of the highest dilution at which the growth of the indicator microorganism or pathogen is inhibited and are calculated as (1000/
A modification is the agar spot antimicrobial assay (Figure 2b) and consists of the following steps: MRS agar or other specified agar is prepared and the probiotic bacteria or test cultures (few µL) are spotted on. These agars are then incubated to develop spots. Next, the indicator bacteria (pathogenic species, spoilage species and other probiotic species) are mixed into specific soft agar (0.7%) and poured over a plate. The plates are then incubated aerobically or anaerobically and the inhibition zones are read. A clear zone of more than 1 mm around the spot is considered as positive [25]. A third modification is the spot‐on lawn antimicrobial assay with wells (Figure 2c), which consists of the following steps: chosen nutrients, selective or differential media, are prepared. Wells (6 mL, 7 mm or other dimensions) are bored in each plate and the bottom of the wells is sealed with agar. Aliquots of active cultures at different dilutions are pipetted into the wells. The plates are left at room temperature to allow migration and settling of the test cultures. The samples are then incubated for 3 h at 37°C and the plates are then overlaid with agar seeded with indicator pathogenic microorganisms (or other indicator organisms) and incubated at suitable incubation conditions. After incubation, the antimicrobial activity is expressed either as inhibition zone or as arbitrary units (AU/mL) [16].
The fourth modification is the cross streak assay [26] where each probiotic strain is streaked in three parallel lines onto agar using a 1‐mL loop. Once these lines have dried, test pathogenic strains are streaked perpendicular to these initial strains in the same fashion, giving three possible zones of inhibition for each combination of strains. It was assumed that when there is inhibition, it is caused by the tester probiotic strain hindering the growth of the second‐streaked (indicator) strain.
3.2.2. Agar well diffusion assay/paper disc assay
The agar well diffusion assay (AWDA) (Figure 3a) is used for determining the antagonistic effects of cell‐free supernatants. The general principle of agar well diffusion assay consists of the following steps: different nutrients, selective or differential media, are prepared. The plates are inoculated with the chosen indicator microorganism. The 6‐mm or 7‐mm wells are bored in each plate. Aliquots of different dilutions of cell‐free supernatants are pipetted into the wells. After incubation, the antimicrobial activity is expressed either as inhibition zone or as arbitrary units (AU/mL) [20, 22]. The paper disc assay (Figure 3b) is a modification where instead of making wells, discs measuring 6 mm are absorbed with aliquots of cell‐free supernatant and placed on the agar inoculated with indicator strains. After incubation, the inhibition zone is evaluated based on the clear zone around the paper disc [23].
3.2.3. Co‐culturing assays for determining the antimicrobial activity
Determining the antimicrobial activity of probiotics against common pathogens is also possible with the co‐culturing assay. This method includes the following steps: preparation of incubation media (i.e., nutrient broth, reconstituted skim milk, sterilized milk, yogurt, whey, etc.). Aliquots of pathogenic and probiotics microorganisms are inoculated into the incubation media. The samples are mixed well and incubated. After incubation, the population of pathogenic bacteria are counted on appropriate agars. Values are usually expressed as log cfu/mL [14–16, 27, 28].
The microtitre plate assay is a version of the co‐culturing assay that includes the following steps: cell‐free supernatant of active probiotic or other investigated microorganism is prepared and divided into several parts that undergo different conditions (i.e., NaOH added to neutralize pH, left acidic, heated, etc.). Pathogenic microorganisms are cultured and added to appropriate broth. The microtitre plate is used to prepare mixes of probiotics/cell‐free supernatants and pathogenic microorganisms and incubated at suitable incubation conditions. Before and after incubation, the optical density at 620 nm is measured and the suppressive activity is calculated as a percentage of inhibition of pathogen growth [15].
Another important type of co‐culturing assay is using cell lines. As several important mechanisms underlying the beneficial effects of probiotics include the effects of probiotic properties on specific tissues, particularly on the intestine, the evaluation of probiotic effects on human intestinal cell lines
3.3. In vivo methods for determining the antimicrobial/antagonistic effect of probiotics against other microorganisms
For
However, many scientists have reverted to
The European legislation OJ L136 of 08.06.2000 includes the 3Rs regulation that results in important reduction of studies on animal models and consists of the following.
The
4. Recent results of in vitro antimicrobial/antagonistic assays for various probiotic strains
The following section contains results of the antimicrobial/antagonistic assays for various probiotic strains or strains with probiotic‐like properties against various potential pathogens, spoilage microorganisms, or other probiotic microorganisms. The results reported using different assays (spot‐on lawn/agar spot, agar well diffusion/paper disc, co‐culturing, microtitre plate and cell line assays) are published by various authors stated in the text and some of the individual procedures are briefly explained.
4.1. Recent results of selected spot‐on lawn/agar spot antimicrobial assays
The antimicrobial activity of
In another research [24], screening for bacteriocins using the spot‐on lawn method was used. One hundred and fifty lactic acid bacteria were isolated from samples of traditional fermented Vietnamese pork. The isolate named
Tharmaraj and Shah [16] used the spot‐on‐lawn technique with wells to test the inhibition of chosen pathogenic bacteria (
Soomro et al. [23] also used the spot‐on lawn method to determine antimicrobial activity of various
Probiotic strains or strains with probiotic potential with efficient antimicrobial activity |
Indicator pathogenic microorganisms | Reference |
---|---|---|
[35] | ||
[38] | ||
[39] | ||
[40] | ||
[41] | ||
[42] | ||
[43] | ||
[44] | ||
[45] | ||
[46] | ||
[47] | ||
[48] | ||
[49] | ||
[50] |
Assays published since 2013 of antimicrobial activity of chosen probiotics using the spot‐on lawn/agar spot assay on chosen pathogenic microorganisms are noted in Table 1.
As noted in Table 1, the most common investigated probiotic strains or strains with probiotic potential were from the genus
4.2. Recent results of selected agar well diffusion assays/paper disc methods
The agar well diffusion assay was conducted in the research by Ali et al. [51], where 14 isolates with probiotic potential were screened for antimicrobial activity against
In the previously mentioned research by Soomro et al. [23], the paper disc method was also used. Sterile filter discs measuring 6‐mm diameter with an absorbed aliquot of 20 µL of cell‐free supernatant of
Assays published since 2013 of antimicrobial activity of chosen probiotics using the agar well diffusion assay or the paper disc assay on chosen pathogenic microorganisms are noted in Table 2. The results show that the agar well diffusion assay or the paper disc assay is the most common method used for determining the antimicrobial or antagonistic effect. The most common investigated probiotic strains or strains with probiotic potential were again from the genus
Probiotic strains or strains with probiotic potential with efficient antimicrobial activity |
Indicator pathogenic microorganisms | Reference |
---|---|---|
[29] | ||
[34] | ||
C1, |
[35] | |
[38] | ||
[41] | ||
[52] | ||
[53] | ||
[54] | ||
[55] | ||
[56] | ||
[57] | ||
[58] | ||
[59] | ||
[60] | ||
[61] | ||
[62] | ||
[63] | ||
[64] | ||
[65] | ||
[66] | ||
[67] | ||
[68] | ||
[69] | ||
[70] | ||
Typhimurium MTCC733, |
[71] | |
[72] | ||
[73] | ||
[74] |
4.3. Recent results of selected co‐culturing assays
The influence of the potential pathogenic bacteria
Tharmaraj and Shah [16], as already mentioned in the previous section, also investigated the inhibition effect of various probiotics against chosen pathogenic and spoilage bacteria with the co‐culturing method. Briefly, 9 mL of reconstituted skim milk was inoculated with 1 mL of overnight culture of probiotic bacteria and 0.1 mL of pathogenic or spoilage bacteria. The medium was mixed well and incubated at 37°C for 24 h. / were counted on nutrient agar and the log population calculated (Table 6). All four pathogenic bacteria were inhibited by all probiotic strains tested to varying degrees. On average, the probiotic bacteria reduced the population of pathogenic bacteria by 2.8 log units.
Ratsep et al. [15] published their research of a microtitre plate assay on the antimicrobial effect of
Another important co‐culturing method is the use of cell lines as noted in the research by Abdel et al. [31] of 12 lactobacilli isolates interfering with the adherence and invasion of
Assays published since 2013 of antimicrobial activity of chosen probiotics using various co‐culturing assays on chosen pathogenic microorganisms are noted in Table 3. The results were similar to the results of spot‐on lawn and agar well diffuse assays.
Probiotic strains or strains with probiotic potential with efficient antimicrobial activity |
Indicator pathogenic microorganisms | Reference |
---|---|---|
[9] | ||
[41] | ||
[69] | ||
[75] | ||
[76] | ||
[77] | ||
[78] | ||
[79] | ||
I‐4036, |
443 |
[80] |
[81] |
5. Recent results of in vivo antimicrobial/antagonistic assays for various probiotic strains
5.1. Recent results of determining the in vivo antimicrobial assays using animal models
In the research by Mazaya et al. [36], both
Lazarenko et al. [82] conducted an
In the study by Bujalance et al. [35], a lack of correlation between
Probiotic strains or strains with probiotic potential with efficient antimicrobial activity |
Indicator pathogenic microorganisms | Reference |
---|---|---|
[30] | ||
[34] | ||
[36] | ||
[54] | ||
[78] | ||
[82] | ||
[84] | ||
[85] | ||
[86] |
The most recent
5.2. Recent results of determining the in vivo antimicrobial assays using clinical trials
Most important research on the antagonistic effect of probiotics are clinical trials, however only a few well conducted clinical studies have been reported. Most clinical studies include the comparison of antibiotic therapy with adjuvant probiotic therapy. In the study by Dore et al. [87], in this prospective, single centre, open label pilot study, patients scheduled for upper endoscopy for any reason and found to be positive for
In the study by Pendharkar et al. [88] the clinical outcome for women conventionally treated for bacterial vaginosis and yeast infection with probiotics bacilli was investigated. This study is an example of the antibiotic therapy with adjuvant probiotic therapy. In the clinical trial, women were recruited in three groups as follows: women with bacterial vaginosis receiving clindamycin and metronidazole treatment together with a prolonged administration of EcoVag® (containing
Some of the most recent
Probiotic strains with efficient antimicrobial activity using |
Pathogenic microorganisms or treated disease |
Basic therapy | Type of trial | Reference |
---|---|---|---|---|
Proton pump inhibitor: pantoprazole | CT | [87] | ||
Antibiotics: Clindamycin, metronidazole, fluconazole | CT | [88] | ||
Standard triple |
DBRCT | [89] | ||
Antibiotics: broad spectrum oral antibiotics | DBRCT | [90] | ||
Antibiotics: broad spectrum oral antibiotics: lansoprazole, amoxicillin, clarithromycin | BDRCT | [91] | ||
Antibiotics: broad spectrum oral antibiotics | CT | [92] | ||
Antibiotic: metronidazole | CT | [93] |
6. Discussion and conclusions
The antimicrobial ability of probiotics is a very important trait and includes the production of antimicrobial compounds, competitive exclusion of pathogens, enhancement of the intestinal barrier function and others. Usually, probiotic strains produce more than one antimicrobial substance that may act synergistically, increasing the spectrum of targeted microorganisms. This property may be desirable as long as this antimicrobial spectrum is restricted to pathogenic microorganisms but it cannot be excluded that it will not affect the normal microbiota of the gut or other microbiotas as well [94]. The results show that probiotic properties are strain dependent and that strain identification is imperative [3].
Probiotic candidates have been accessed from very diverse habitats including faeces of breast‐fed human infants [65, 69, 80, 85, 95], faeces of healthy adults [9, 15, 65, 70], faeces of elderly [81], faeces of children [25, 96], breast milk [42], human saliva [52], vaginal isolates of healthy women [66, 75], various fermented foods or beverages including raw or fermented milk [23, 35, 44], kefir [97], cheese [51, 56, 98], whey [99], yogurt [16, 41], dahi [100, 101], other dairy products [25, 36, 61], sourdough [102], sausages [17], fermented meat [24], kimchi [10, 62], maize [25, 59], fermented olives [103], Yerba mate [79], ragi [64], soy sauce [86], soil [104], as well as animal origin including rat faeces [71], geese [68], calves [105], pigs [45], fish [39, 60, 63, 78] and other seafood [40, 43, 46] and many others.
By far, the most commonly investigated probiotic were bacteria of the genus
The antimicrobial activity of probiotic microorganisms has a very wide area application including adjuvant therapy to antibiotic consumption or for correcting dysbiosis of the gastrointestinal tract microbiome due to diarrhoea [37, 38, 106], antagonistic activity in humans against urinary tract infections [26, 66, 75], eradicating
The process of determining antimicrobial properties of probiotic is complex and includes
There is a clear need for more elaborate assays that would better represent the complex interactions between the probiotics and the host microbiome to understand the consequences of the
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