JIAP April 2017 - Probiotics and Periodontitis - A Literature Review

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Journal of the International Academy of Periodontology 2017 19/2: 42–50

Probiotics and Periodontitis – A Literature review


Simona Gatej1, Neville Gully1, Rachel Gibson2,3 and P. Mark Bartold1

1
School of Dentistry, 2Division of Health Sciences, 3School of Med-
icine, The University of South Australia, Adelaide, SA, Australia

Abstract
Objective: This review was designed to explore the use of probiotics in prevention or
treatment of periodontitis.
Methods: A search was performed using MEDLINE and bibliographies from previous
reviews in order to identify any randomised controlled animal and human probiotic
interventions in periodontitis.
Results: Five studies using probiotics in animal models of periodontitis and eight clini-
cal studies using probiotics in patients with chronic periodontitis were analysed. The
analysis of the animal models showed reduction in periodontal pathogens and bleeding
on probing when probiotics were used in adjunction to mechanical debridement and
significant increase in alveolar bone levels and bone density in the probiotic groups
when compared with placebo. Some of the results of the clinical studies indicated de-
creased clinical parameters (gingival inflammation, bleeding on probing, plaque index)
and decreased pro-inflammatory markers levels in saliva or gingival crevicular fluid in
treated periodontitis patients when compared with controls or placebo. Other results
included decreased periodontal pocket depth and clinical attachment loss for scaling and
root planing plus probiotic treatment versus scaling and root planing alone or placebo
and also reduction in Porphyromonas gingivalis numbers and the total viable count and
proportion of obligate anaerobic bacteria.
Conclusions: Within the limitations of this review, the results are encouraging, support-
ing the notion that there is a place for probiotics in the treatment of periodontitis. Future
independent studies are needed to investigate specific probiotic strains, doses, delivery
methods, treatment schedules, mechanisms of action, safety and how to maintain the
results of the probiotic interventions.

Keywords: probiotics, periodontitis, alveolar bone loss, lactobacilli, bifido-


bacteria, Lactobacillus rhamnosus GG

Introduction Whilst these treatments result in a temporary reduction


of the bacterial load and associated inflammation, they
Periodontitis is a common chronic inflammatory con- are often not sufficient to control the disease (Quirynen et
dition affecting the dentition of the adult population al., 2002; Teughels et al., 2007a). Therefore, other adjunc-
(Petersen, 2003). A key factor in the development of tive strategies need to be investigated. The administration
this disease is an increased bacterial challenge, specifically of beneficial bacteria – probiotics – with antimicrobial
the presence of elevated numbers of certain potentially and anti-inflammatory properties is one of several novel
pathogenic commensal bacterial species resulting from approaches being considered as an adjunct treatment for
altered environmental conditions arising from the host’s the management of periodontitis and may offer a low risk,
inflammatory response (Bartold and Van Dyke, 2013). inexpensive and easy-to-use treatment option.
Subgingival debridement, surgical interventions and in
some cases selective use of antibiotics and antiseptics are
Periodontitis
current approaches used to reduce the pathogenic bacteria.
Periodontitis is a chronic inflammatory condition af-
fecting both the hard and soft tissues surrounding the
teeth, caused by a combination of specific bacteria and
inflammatory host responses and resulting in the destruc-
Correspondence to: PM Bartold, Colgate Australian Clinical
tion of the connective tissue of the gingivae, periodontal
Dental Research Centre, 2nd Floor Adelaide Dental Hospital, ligament and alveolar bone (Petersen, 2003). It is one of
Frome Rd, Adelaide SA, Australia, 5000. Phone: +61 8 8313 the two most prevalent oral health burdens world-wide.
3437, Fax: +61 8 8313 6429.

© International Academy of Periodontology


Gatej et al.: Probiotics and periodontitis 43

A World Health Organization report from 2012 found yogurt and cheese. The preservation process called ‘lacto-
15-20% of middle-aged adults suffered from severe fermentation’ is an anaerobic process in which lactic acid
periodontal disease resulting in tooth loss (World Health bacteria, predominantly lactobacilli, convert carbohydrates
Organization, 2012). Periodontitis is also considered a risk into lactic acid, which acts as a preservative (Turpin et al.,
factor for cardiovascular disease, pulmonary disease, type 2010). Consuming fermented foods is an ancient practice
II diabetes, rheumatoid arthritis and adverse pregnancy dating back as far as 5400 BC, whilst recommendations
outcomes (López et al., 2002; Bartold et al., 2005; Blaizot for gastrointestinal illness date back to 76 AD (Rawlings,
et al., 2009; Chee et al., 2013). 2013). The first scientist to lay down the foundations for
The precise etiology of periodontitis is complex, mul- the concept of beneficial bacteria was the Ukrainian born
tifactorial and not completely understood. Generally, it is Nobel laureate bacteriologist Ilya Ilyich Mechnikov, known
believed to be a biofilm-induced disease with the host’s as “the father of modern immunology.” He proposed a
immune system playing a central role (Flemmig, 1999; theory that aging is caused by toxic bacteria in the gut and
Darveau, 2010; Bartold and Van Dyke, 2013; Hajishen- attributed the longevity of peasants from the Balkan area
gallis, 2014a; 2014b). The disease is associated with an to their consumption of large quantities of sour milk that
imbalance in the host’s local microbiome with elevated contained lactobacilli (Mackowiak, 2013).
numbers and proportions of bacterial species designed as Other scientists continued Metchnikov’s work and in
‘pathogens’ and reduced proportions of bacteria associ- 1965 the term “probiotics,” meaning “for life,” was in-
ated with health (Socransky and Haffajee, 1992; Wade, troduced (Lilly and Stillwell, 1965). The current definition
2011; Abusleme et al., 2013). for probiotics is given by the World Health Organization,
Current treatments for periodontal disease, including which defines probiotics as live microorganisms, most
subgingival debridement, surgical interventions and selec- often bacteria (sometimes fungi), which, when consumed,
tive use of antibiotics and antiseptics, aim to reduce the confer beneficial effects to the host (World Health Or-
pathogenic load (Quirynen et al., 2002). Although these ganization, 2002).
numbers of pathogens are reduced considerably, the shift Probiotics are bacterial strains usually isolated from
is only temporary as re-colonization occurs within months human commensal microbiota and adequately character-
(Magnusson et al., 1984; Rhemrev et al., 2006). The use ized for strain identity, content, stability, and proven health
of antibiotics as part of the treatment brings with it the effects. The most commonly used species of probiotics
important global issue of antibiotics resistance that has belong to the Lactobacillus, Bifidobacterium, Escherichia, En-
the potential to render many antibiotics useless. It also terococcus and Bacillus genera and are all ubiquitous residents
brings along a long list of possible side-effects, notably, of the human skin, gastrointestinal tract, respiratory tract
antibiotic-associated diarrhea (Lynne, 2006). and vagina (Floch, 2014).
Considering all of these factors, increasing the propor- Lactobacilli are Gram-positive, rod-shaped, facultative
tion of beneficial bacteria with inflammation modulating anaerobes. Some of the most commonly known mem-
properties presents as an option to address the bacterial bers that have been isolated and studied are Lactobacillus
imbalance and may be considered as a preventive or treat- acidophilus, L. reuteri, L. bulgaricus, L. rhamnosus, L. salivarius,
ment option in achieving periodontal health. and L. casei. Bifidobacteria are Gram-positive, anaerobic
bacteria, with some of the most commonly known mem-
Probiotics bers being Bifidobacterium bifidum, B. breve, B. longum, and
History, sources, definition B. infantis (Turroni et al., 2014).
The microorganisms that live inside and on humans out- Functions and mechanisms
number the body’s cells tenfold with the majority of them
Probiotics fulfil many useful functions, thus having a
being bacteria, with some archaea and eukaryotes also
major heath impact. They produce lactic acid with anti-
being present (Saier and Mansour, 2005). In periodontal
bacterial effect, hydrogen peroxide with antiseptic effect,
health, communities of bacteria live in symbiosis with
and anti-viral and anti-fungal agents that suppress patho-
the host, playing a role in its immune function and health
gens. Probiotics are important for immune system devel-
status. A disturbance in the microbial balance (a process
opment and regulation, maintenance of a healthy lining
labelled as ‘dysbiosis’) has been associated with several
of the gastrointestinal tract, food digestion, synthesis of
medical conditions (Goulet, 2015). Obesity, metabolic
amino acids, proteins and different vitamins, absorption
diseases, gastrointestinal diseases, autoimmune diseases,
of calcium, iron and vitamin D (Ciorba, 2012; LeBlanc
allergies and cancer have all been partly associated with
et al., 2012; Jonathan and David, 2013). In order to exert
an increased number of harmful bacteria and a decreased
all these effects, probiotics need to be able to survive
number of beneficial bacteria (Logan et al., 2003).
the gastrointestinal passage resisting acid and bile and to
Beneficial bacteria are present in preserved food and
preserve their stability during manufacturing and storage
beverages around the world: Korean kimchi, Indonesian
(Meurman, 2005).
tempeh, Indian chutney, Japanese miso, sauerkraut, kefir,
44 Journal of the International Academy of Periodontology (2017) 19/2

Additional studies have shown that a combination of properties, LGG may prove to be a good candidate for
different probiotic species and/or strains (e.g. Lactobacillus future probiotic-periodontitis studies.
rhamnosus GG and Bifidobacterium lactis Bb12) can enhance
their effects in a synergetic manner (Juntunen et al., 2001; Probiotics in other fields of medicine
Toiviainen et al., 2015). Traditionally, probiotics have been used in gastroenterol-
The precise mechanisms of how probiotics exert their ogy. Evidence-based reviews indicate that certain strains
effects are not known yet and may depend on a variety of of probiotics contribute to the microbial balance of the
factors: the condition being treated, the strain and the con- gastrointestinal tract – supporting the immune system and
centration of the probiotics used and the stage when they reducing inflammation (Ciorba, 2012). Clinical trials have
are introduced, the presence of prebiotics or enteric bacteria assessed the effects of probiotics in antibiotic-associated
(Geier et al., 2007). diarrhoea, gastroenteritis, irritable bowel syndrome, inflam-
The effects of probiotics can originate from three local or matory bowel disease, Crohn’s disease, obesity, rheumatoid
systemic main modes of action (Gueimonde and Salminen, arthritis and allergies (Meurman, 2005; Vaghef-Mehrabany et
2006; Shira and Gorbach, 2006; Devine and Marsh, 2009): al., 2014). There are also laboratory studies that have shown
1. Indirectly, probiotics compete with pathogens promising results in treatment of childhood autism and
for essential nutrients; they can also restrict the colon cancer (Rafter, 2003; Critchfield et al., 2011).
pathogens’ adhesion capabilities by changing the
environmental pH. Probiotics and oral health
2. Directly, probiotics are involved in the production There have been many studies published investigating the
of antimicrobial substances (lactic acid, hydrogen potential health benefits of probiotics on systemic health,
peroxide, bacteriocins) that can kill or inhibit the but investigations regarding their use in oral health are lim-
growth of periodontal pathogens. ited by comparison. These vary a lot in terms of probiotics
3. Probiotics can act on the host by modulating the strains used, concentrations, and vehicles for the application
host’s innate and adaptive immune response (reduc- (cheese, lozenges, milk, kefir, ice cream, gum, drops, powder,
ing the production of pro-inflammatory cytokines: and mouthwash; Teughels et al., 2011).
IL-6, IL-1β, TNFα and increasing production of Probiotics have been evaluated in caries control and
anti-inflammatory cytokines: IL-10) and by im- have demonstrated the capacity to reduce Streptococcus mutans
proving the intestinal barrier integrity (Ciorba and levels in saliva (Näse et al., 2001). A recent meta-analysis in-
Stenson, 2009). dicated that probiotics could have a positive effect in caries
prevention (Laleman et al., 2014). There are also probiotic
It has not been established yet if colonization of the oral evaluations in oral conditions, e.g., candidiasis, chemotherapy-
cavity by probiotics is necessary in order for them to exert induced mucositis or halitosis (Stamatova and Meurman,
their effects in the mouth, and the process of colonization 2009; Laleman and Teughels, 2015).
of the oral cavity itself remains unclear, with studies using
biased methods of detecting bacteria (Ravn et al., 2012). Probiotics and periodontitis
In periodontal disease, some studies investigated the role of
Lactobacillus rhamnosus GG probiotics in gingivitis and reported a significant decrease in
One of the most studied probiotic microorganisms is terms of plaque and gingival indices, bleeding on probing
Lactobacillus rhamnosus GG (LGG). It was originally isolated and gingival inflammation in the probiotic groups (Laleman
from healthy human intestines in 1983 (Gorbach, 1996). and Teughels, 2015).
LGG survives the low pH of the stomach and the bile A search was performed using MEDLINE in order
acids of the duodenum. It has pili facilitating adherence to to identify any randomised controlled animal and human
the inner lining of the digestive system, thus colonizing the probiotic intervention studies in periodontitis. The search
intestine (Tripathi et al., 2012). One study investigating the considered those works published between 1980 and Au-
colonisation of LGG in the oral cavity concluded that this gust 2015 and aimed at evaluating the effects of probiotics
is improbable in the majority of cases but possible in some in periodontitis using the words “periodontal disease.”
(Yli-knuuttila et al., 2006). “periodontitis” and “probiotics.” Additional hand searches
Lactobacillus rhamnosus GG has been extensively investi- were performed and included bibliographies from previ-
gated in gastrointestinal studies and it is now used in dairy ous reviews on the topic of oral probiotics (Stamatova and
products in many countries. This probiotic does not ferment Meurman, 2009; Teughles et al., 2011; Raff and Hunt, 2012;
sucrose or lactose and has been shown to significantly reduce Dhingra, 2012; Laleman and Teughels, 2015). Only articles
the risk of caries (Meurman et al., 1995; Näse et al., 2001). published in English were selected. Five studies using pro-
It has also been demonstrated to have anti-inflammatory biotics in animal models of periodontitis and eight clinical
properties in vivo (Lin et al., 2009). studies using probiotics in patients with chronic periodontitis
Considering its non-cariogenic and anti-inflammatory were identified.
Gatej et al.: Probiotics and periodontitis 45

Probiotics in animal models of periodontitis apply, together with the use of conventional radiographic
Table 1 highlights four animal studies where periodontal films that introduces potential measurement accuracy
pockets were artificially created or a ligature-induced peri- errors.
odontitis model was used in either rats or beagle dogs. In a randomised controlled study, 32 rats with ligature-
Five millimetre periodontal bony defects were surgi- induced experimental periodontal disease were adminis-
cally created four months prior to the experiment in a tered Bacillus subtilis for 44 days (Messora et al., 2013). The
split-mouth, double-blind, randomised trial in beagle dogs, probiotic intervention generated reduced attachment loss
(Teughels et al., 2007b). Pellets containing a mixture of and alveolar bone loss and protected the small intestine
Streptococcus salivarius, S. sanguinis and S. mitis were applied from reactive changes induced by ligature-induced peri-
to the root surface after scaling and root planing (i.e., to a odontitis. There are a few shortcomings to this study. Like
suppressed oral microbiota). The authors concluded that all ligature-induced periodontitis models, the mechanical
the use of probiotics significantly delayed and reduced lesions could aggravate the periodontal destruction (Molon
inflammation (bleeding on probing) in the probiotic group et al., 2013). In addition, the mode of probiotic administra-
when compared with scaled and root planed pockets tion, via drinking water, makes it difficult to quantify the
alone. There was also reduction in total anaerobic bacteria amount ingested by each animal.
and delay in recolonization of pockets by the pathogens In another ligature-induced periodontitis study, a 44-
when compared with the control group, and the reduced day experiment using the probiotic B. subtilis and restraint
levels were maintained 12 weeks after the treatment in the stress concluded that probiotics supplementation may
probiotic group but not the control group (Teughels et al., reduce tissue breakdown in unstressed rats and that im-
2007b; Teughels et al., 2011). The limitations of the study munomodulatory effects of probiotics in intestinal and
were the absence of a placebo control group, the inter- periodontal tissues were influenced by stress (Foureaux et
subject variation, the small sample size (eight dogs) and al., 2014). All the limitations of the Messora et al. (2013)
the intra-oral translocation. study apply here as well.
Another study using the same model in eight beagle The animal studies showed an effect of probiotics on
dogs found there was a significant increase in bone levels oral microbiota and a limited effect on periodontal param-
for the periodontal pockets treated with probiotics for 12 eters. Due to the limited data available and all the limitations
weeks in comparison with the control group (Nackaerts discussed above, it is premature to draw a conclusion on the
et al., 2008). Bone density in the probiotic group also im- recommended methodology (probiotic strain, concentra-
proved significantly. The previously mentioned limitations tion, duration of treatment and mode of administration).

Table 1. Animal probiotics studies included in this review


Study Type of participants, Condition Probiotic strains, ve- Results
number hicle, time
Teughles et al., 2007 Beagle dogs, 8 Artificially created Streptococcus salivarius, Reduction in periodon-
(Teughels et al., 2007b) periodontal pockets S. sanguinis, S. mitis, tal pathogens and BOP
pellets, 12 weeks when probiotics were
used in adjunction to
mechanical debridement
Nackaerts et al., 2008 Beagle dogs, 8 Artificially created S. salivarius, S. sangui- Significant increase in
periodontal pockets nis, S. mitis, pellets, 12 bone levels and bone
weeks density in probiotic
group when compared
with placebo
Messora et al., 2013 Wistar rats, 32 Ligature-induced Product based on Bacil- Mean values of AL and
periodontitis lus subtilis, in water, 44 ABL were significantly
days higher in the induced
periodontitis group com-
pared with the treatment
group
Foureaux et al., 2014 Wistar rats, 64 Ligature-induced Product based on B. Bone loss was prevented
periodontitis subtilis, in water, 44 in the probiotic treated
associated with days induced periodontitis
restraint stress unstressed group

BOP, bleeding on probing; AL, attachment loss; ABL, alveolar bone level
46 Journal of the International Academy of Periodontology (2017) 19/2

Probiotics in clinical studies in patients with L. brevis lozenges were used in a 2007 double-blind
chronic periodontitis 4-day study in 21 male and female adults with no systemic
diseases and with moderate to severe chronic periodontitis
Studies using probiotics in patients with chronic peri-
to assess anti-inflammatory effects of this probiotic (Riccia
odontitis present a high degree of heterogeneity in the
et al., 2007). The authors concluded that all clinical param-
probiotic strains, dosages, vehicles of administration,
eters (gingival index (GI), plaque index (PI), calculus and
modes of administration and duration. Table 2 presents
temperature sensitivity) decreased in the probiotic group, in
eight clinical studies with variations in terms of the
association with salivary levels of prostaglandin E2 (PGE2),
severity of disease, sample size and administration of
matrix metalloproteinase (MMP) and interferon γ (INF-γ).
oral hygiene instructions.

Table 2. Clinical probiotics-chronic periodontitis studies included in this review


Study Type of participants, Probiotic strains, Results
number, age vehicle, time
Riccia et al., 2007 Adults, 29, 24-51 Lactobacillus brevis, Decreased clinical parameters in treated peri-
lozenges, 4 days odontitis patients when compared with controls
(gingival inflammation, BOP, plaque, calculus,
temperature sensitivity)
Decreased levels of PGE2, MMP and INF-γ in
saliva samples of treated periodontitis patients
Shimauchi et al., 2008 Adults, 66, 32-61 L. salivarius, tablets, 8 Current smokers in the probiotic group showed a
weeks significantly greater improvement of plaque index
and probing pocket depth from baseline when
compared with those in the placebo group
Vivekananda et al., 2010Adults, 30, 34-50 L. reuteri, lozenges, 42 PPD, CAL, GI, GBI and PPD significantly reduced
days in the SRP plus probiotic group compared with
SRP alone or placebo
Teughles et al., 2013 Adults, 30, older than L. reuteri, lozenges, 12 Significantly more pocket depth reduction and at-
35 weeks tachment gain in the moderate and deep pockets
and also reduction in P. gingivalis numbers in the
test group when compared with controls
Vicario et al., 2013 Adults, 20, 44-65 L. reuteri, tablets, 30 Improved short-term clinical outcomes (PI, BOP,
days and PPD) in non-smoking patients with initial-to-
moderate chronic periodontitis

Szkaradkiewicz et al., Adults, 38, 31-46 L. reuteri, tablets, 2 Significant improvement in SBI, periodontal prob-
2014 weeks ing depth and clinical attachment level and also
decreased levels of pro-inflammatory cytokines
TNF- α, IL-1β, IL-17 in treated patients when
compared with the control group
Ince et al., 2015 Adults, 30, 35-50 L. reuteri, lozenges, 3 Significant differences in PI, GI, BOP and PPD
weeks and significant mean values of attachment gain in
favour of the test group compared with con-
trols. Significant decreased levels of MMP-8 and
increased levels of TIMP-1 were found in GCF for
the test group up to day 180
Tekce et al., 2015 Adults, 30, 35-50 L. reuteri, lozenges, 3 1 year follow-up study from the previous Ince
weeks et al.; 2015. PI, GI and BOP significantly lower
in the test group compared with controls; differ-
ence in the total viable count and the proportion
of obligate anaerobes were decreased in the test
group up to day 180

PGE2, prostaglandin E2; MMP, metalloproteinase; TIMP-1, tissue inhibitor of metalloproteinase; INF-γ, interferon
γ; PI, plaque index; BOP, bleeding on probing; PPD, pocket probing depth; CAL, clinical attachment loss; GI,
gingival index; GBI, gingival bleeding index; SRP, scaling and root planing; SBI, sulcus bleeding index
Gatej et al.: Probiotics and periodontitis 47

The inflammatory effects of L. brevis were attributed to its formed. The subject size used in this study was quite small
capacity to prevent the production of nitric oxide and hence (20 patients) and the study period short. No statistically
the release of PGE2 and the activation of MMPs (Riccia significant changes could be shown in the control group
et al., 2007). No placebo group was used in this study, no (Vicario et al., 2013).
data were provided on the periodontal disease, and data In 2014, an experiment using L. reuteri tablets for
for bleeding on probing (BOP) were unclear. two weeks in 38 adult patients with moderate chronic
L. salivarius tablets were administered three times periodontitis found significant improvement (p < 0.05)
daily for eight weeks in a double-blind, placebo-controlled, in sulcus bleeding index (SBI), PPD and CAL in treated
randomised clinical study that included 66 adult patients patients when compared with controls (Szkaradkiewicz
with mild to moderate chronic periodontitis (Shimauchi et et al., 2014). The gingival crevicular fluid (GCF) levels of
al., 2008). The authors found significantly decreased PI, pro-inflammatory cytokines TNF-α, IL-1β and IL-17 were
GI and pocket depth in probiotic treated smokers when decreased in the treated group (Szkaradkiewicz et al., 2014).
compared with placebo. No significant difference was The effects of L. reuteri on clinical and biochemical
detected in BOP between the probiotic and the placebo parameters, adjunctive to initial periodontal therapy, were
groups. The study also looked at salivary lactoferrin levels evaluated in a randomised, parallel, controlled, double-
as a measure for the host’s immune response and found masked clinical trial of 30 adult patients with initial to
that these were decreased significantly in the test group moderate chronic periodontitis over a one-year period
smokers. The study does not report on the lactoferrin levels (İnce et al., 2015; Tekce et al., 2015). Significant differ-
of the non-smokers group alone. The Hawthorne effect ences were found in PI, GI, BOP and PPD in favour of
regarding altered oral hygiene regimens due to observation the test group, together with significant mean values of
was taken into account. The patients who volunteered were attachment gain. The GCF levels of proteolytic enzyme
workers at the company that manufactured the probiotic metalloproteinase MMP-8 and the tissue inhibitor of me-
tablets and funded the study (Shimauchi et al., 2008). talloproteinase TIMP-1 were measured and followed for
The use of L. reuteri lozenges in 30 adult patients with 360 days, with significantly decreased levels of MMP-8 and
mild to moderate chronic periodontitis combined with increased levels of TIMP-1 detected up to day 180. Both
scaling and root planing (SRP) significantly reduced GI, forms of MMPs (active and latent) were measured and the
clinical attachment loss (CAL), gingival bleeding index active forms seemed to be found at sites with progressive
(GBI) and periodontal pocket depth (PPD) and was more periodontitis. The total viable count and the proportion
effective than either treatment alone (Vivekananda et al., of obligates anaerobes were also decreased up to day 180.
2010). Patients receiving only probiotics without SRP also The study was supported by a private laboratory. However,
showed significant clinical improvement when compared the authors of the study declared that the company was
with placebo. The administration of probiotics started 21 not involved in the data management (İnce et al., 2015;
days after SRP, twice a day for three weeks. The authors of Tekce et al., 2015).
this double-blind, randomised, placebo-controlled clinical The high degree of heterogeneity of the human studies
trial presented probiotics as an adjunct or alternative to (different strains and concentrations, small sample size, dif-
periodontal treatment when SRP might be contraindicated. ferent duration of treatment, durability of response, mode
The private laboratory making the probiotic funded the test of administration and the role of environmental factors
products and the publication of the study (Vivekananda such as the pH of the delivery area) makes it difficult to
et al., 2010). draw a robust conclusion. Despite all these limitations, it
L. reuteri lozenges were also used for 12 weeks in a seems that probiotics can still have an impact on the oral
randomised, placebo-controlled clinical trial in 30 adults microbiota and a limited effect on periodontal parameters.
with moderate to severe previously untreated chronic peri- This now needs to be investigated further.
odontitis (Teughels et al., 2013). The group found that there Probiotic therapy is generally considered to be safe and
was more pocket depth reduction and attachment gain, complications rare (Ciorba, 2012) with a closer exploration
together with reduction in Porphyromonas gingivalis numbers needed in critically ill or immunocompromised patients
in the probiotic group when compared with controls, con- (Verna and Lucak, 2010).
cluding that L. reuteri can be a useful adjunct to SRP. The
private laboratory that manufactured the probiotic partially Conclusions and recommendations for future
supported this study (Teughels et al., 2013). research
Two strains of L. reuteri tablets were used for 30 days
Periodontitis is an inflammatory disease that has proven
in a double-blind, placebo-controlled, randomised clini-
very difficult to treat. The results of the animal and clini-
cal trial in non-smoking patients with initial to moderate
cal periodontitis studies included in this short literature
chronic periodontitis (Vicario et al., 2013). The probiotics
review support the notion that there is a place for probiot-
used significantly improved short-term clinical outcomes
ics in the treatment of periodontitis and that probiotics
(BOP, PI and PPD). No mechanical intervention was per-
may offer a low-risk, inexpensive, easy to use prevention
48 Journal of the International Academy of Periodontology (2017) 19/2

or treatment option for the management of periodontal Floch MH. Recommendations for probiotic use in
disease. In the future, more independent studies are humans-a 2014 update. Pharmaceuticals (Basel, Swit-
needed to look into specific probiotic strains, doses, zerland) 2014; 7:999-1007.
delivery methods, treatment schedule, mechanisms of Foureaux RC, Messora MR, de Oliveira LFF, et al. Ef-
action, safety and how to maintain the results of the fects of probiotic therapy on metabolic and inflam-
probiotic interventions. matory parameters of rats with ligature-induced
periodontitis associated with restraint stress. Journal
Acknowledgments of Periodontology 2014; 85:975-983.
Geier MS, Butler RN and Howarth GS. Inflammatory
None of the authors of this review declares a conflict
bowel disease: Current insights into pathogenesis
of interest or obtained any kind of financing or sup-
and new therapeutic options; probiotics, prebiotics
port from any company related to the production of
and synbiotics. International Journal of Food Microbiology
probiotics.
2007; 115:1-11.
Gorbach SL. The discovery of Lactobacillus GG. Nutrition
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