Protocols of sensitizations in food allergy
1. Introduction
The prevalence of allergies has dramatically and rapidly increased over the past decades in areas with a “westernized” or “industrialized” lifestyle. This increase and the dichotomy in the rate of allergic disease between industrialized and developing countries are two lines of evidence suggesting that environmental changes are a major factor in the development of allergies. There is mounting evidence that the microbiota is a key environmental factor that influences oral tolerance. Alterations in the sequential establishment of gut microbiota observed in western countries could therefore be responsible for a T-helper balance deviation toward a Th2 profile, a major factor in the rise of allergic diseases. Likewise treatment with broad spectrum antibiotics in infancy leading to microbiota alterations and dysbiosis, is associated with increased susceptibility to allergy [1]. Indeed recent epidemiological studies have linked factors influencing microbiota establishment and risk of allergy [2,3]. Hence, increasing evidences suggest that the composition of the microbiota influences intestinal barrier functions [4,5] and both local [6] and systemic immune responses [7]. A specific signature of the microbiota has been associated with allergy sensitivity [8-10]. This hypothesis has been confirmed by studies using mice models which have shown that the gut microbiota is likely to play a role in the development of oral tolerance. We and other have shown that the lack of gut microbiota in germ free mice is associated with the development of Th2 and IgE responses to dietary antigens [11,12]. The specific gut microbiota observed in mice with food allergy by Noval-Rivas
If present results of clinical trials do not allow concluding unambiguously in favor of probiotics, studies have shown the benefits of this approach, justifying further research in this direction [13,19-21]. Recent reviews reported studies showing the beneficial effects in the prevention of atopic dermatitis [19-21]. Prevention of respiratory allergies also seems possible [21]. Differences between studies are most likely due to differences in the populations studied - in terms of type of allergy, evolutionary stage of the disease, environment, genetic background - but also to the various probiotic used in terms of strain, dose, duration and time of administration in relation to the development of allergy, and finally the follow-up period [13,19]. The combined prenatal and postnatal administration of probiotics appears more effective [21]. However, the conflicting results reported today do not allow the recommendation of the use of probiotics in prevention of allergy by expert committees. Despite the promising results on prevention and treatment of allergic diseases by various strains, EFSA did not delivered favorable opinions on requests. Progress in our basic knowledge of probiotic strains, in strain selection, and in understanding their mechanisms of action is needed to give credibility to the health claims made for probiotics and especially for the design of efficacious therapeutic agents. For these reasons, animal models constitute unavoidable tools for biomedical research. They are used for their potential to mimic the human disease process, and allow better understanding of key events of allergic disease development.
2. Animal models of food allergy, asthma and atopic dermatitis
In this chapter, only animal models that have been used to characterize the impact of probiotics on allergy will be described.
The impact of probiotics on allergy – including food allergy, asthma and atopic dermatitis – was mainly studied on small laboratory animals (mice and rats), but domestic animals, as dogs and piglets, were also used. It is important to carefully choose animal model because it can deeply affect the study. Indeed, genetic predispositions condition IgE responsiveness [22].
2.1. Rodent models
2.1.1. Mice model
Mice are the first model organism because of its easy reproduction and its low cost of maintenance. This model does not completely mirror the human but it shares with him similar mechanisms of immune regulation, notably in T cell polarization [23]. These animals have the capacity to produce IgE and IgG1 antibodies, and, depending on their genetic background, strains can be divided into high or low IgE responders [22]. There are also differences in their ability to produce Th1 and Th2 cytokines.
Murine models of food allergy and asthma have been investigated in several strains, including BALB/c, C57BL/6 and C3H/HeJ. BALB/c strain is the most commonly used in models of experimental induced allergy. Indeed, BALB/c mice develop a strong Th2 response following sensitization and challenge with an allergen, with higher levels of allergen-specific IgE. It can be explained by a genetic predisposition towards the development of Th2 cells, implicate in allergy process [24]. This bias is caused by the loss of functional IL-12 receptor which leads to promote the generation of IL-4-producing cells. Indeed, IL-12 favors the generation of Th1 effector cells which antagonize the effects of IL-4 [25]. Many authors have succeeded to sensitize BALB/c mice with different allergens, such as ovalbumin (OVA) [26,27], ovomucoid [27] and β-lactoglobulin [28]. However, according to protocols, teams have obtained conflicting results. For instance, Morafo
C57BL/6 mice are intermediate IgE responders [22] and have been used successfully in allergen challenge studies [30-32]. C57BL/6 strain has the advantage of being stable and having its genome entirely sequenced. Moreover, the most available knock-out strains mice are created on C57BL/6 genetic background.
C3H/HeJ strain is also used [33-35]. It has a mutation in the gene
One study has compared these three mice strains in a model of asthma [38]. After immunizations to OVA/alum, BALB/c strain develops an α-actin smooth muscle hyperplasia and an airway responsiveness which was more important than in C57BL/6 and C3H/HeJ. These results have been confirmed by Van Hove
Strain NC/Nga, firstly developed by Matsuda
2.1.2. Rat model
The rat is another small animal model to examine food allergy, but it is few implemented [43-45]. Due to the size of this species, it is possible to monitor within individual animals the kinetics of specific serum antibody responses. They have the capacity to produce IgE and IgG2a antibodies [46]. The Brown Norway strain is a suitable model with a high-IgE response after oral sensitization [47,48]. However, Dearman
2.2. Large animal models
Swine and dogs are an example of large animal models that have been investigated for allergy. They are less commonly used because they are most expensive than rodents and their housing is uneasy. However, in many aspects, closer similarities exist between these large animal species and humans. First, dog’s gut anatomy and physiology and nutritional requirements are similar to humans [50]. Second, atopic dogs share many allergies with human. Indeed, it develops spontaneously allergic reaction to dust mites and foods for example, with an incidence of 10% [51]. In this way, dogs present frequently IgE-mediated food hypersensitivity, with clinical symptoms comparable to those of human including gastrointestinal and dermatologic reactions. Of this fact, this model can be utilized for mimicking and characterizing mechanisms involved in the development of food allergies in children. To the best of our knowledge, up to now, the impact of probiotics has been only study on atopic dermatitis [52,53].
Only two teams used swine model within the framework of food allergy [54] and asthma [55]. Swine presents a number of important advantages for study allergy. Indeed, they have a similarity with young children in terms of size, organ development, intestinal physiology, whether anatomically or histologically, mucosal immunity and disease progression [56]. They are able to produce IgG and IgE [51].
3. Protocols of allergic sensitization
Multiple methods are used to induce allergy in animal models. Differences between protocols consist of the nature and dose of the allergen, and the strategy used to sensitize the animal prior to challenge (route of exposure and use or not of an adjuvant). The number of sensitizations is also extremely variable from one study to another, between 1 and 4 per week, during 1 from 8 weeks, according to the model, the use or not of an adjuvant, and the route of exposure (Tables 1 to 3).
3.1. Allergens
Many allergens are used to sensitize the different animal species. Ovalbumin (OVA), the main protein found in egg white, is used in more than 50% of publications on probiotic and allergy. Other major allergens are peanut extract in food allergy [30,35,43,57], birch pollen from
The dose of allergen and its frequency of administration are also important parameters in the magnitude of the immune response. Kroghsbo
3.2. Route of exposure
The route by which antigen is administered has its advantages and disadvantages, and affects both the magnitude and the type of response obtained. It must be chosen depending on the purpose of the study. The route of delivery to animals should closely look like about the projected route of administration to humans. The most common routes for allergen administration are oral, IP and epicutaneous (EC) routes. Intra-nasal (IN) - for administration of pneumallergen in model of asthma [69], intra-tracheal (IT) [55], and subcutaneous routes (SC) [55,59,60,62,70,71] are more rarely employed.
3.2.1. Oral route
To model food allergy, antigen administration via the gastrointestinal tract – in other words, by gavage (IG) – provides clear ties to the human condition, and it is thus very relevant for exposure to food antigens. Additionally, it has the advantage of being economical, convenient, and relatively safe. Oral route also allows testing different allergens to evaluate their allergenic potential [64]. Oral immunization does not discriminate between males versus females, with no differences in their level of Th1 (i.e. IgG2a) or Th2 -associated (i.e. IgE and IgG1) antibodies [65]. This route can be used for sensitization studies [30,33-35,43-45,72-75] but also for tolerance studies [76-78]. Consequently, this route is principally used to study the impact of probiotics on food allergy.
3.2.2. Intraperitoneal route
The intraperitoneal administration is a common technique in laboratory rodents. It can be used to administer large volumes of fluid safely, unlike oral route which only tolerate low volumes [79]. The pharmacokinetic of substances administered by this route is closed to those seen after oral administration, with a passage by the liver. Special care must be taken regarding the injected substances which should be sterile, isotonic and nonirritating. There are differences in sensitization according to the gender when this route is applied. Bonnegarde-Bernard
3.2.3. Epicutaneous route
Some substances can also be administered directly to the skin surface (epicutaneous administration) for a topical affect. The allergen is captured by skin dendritic cells that migrate to the afferent lymph nodes and activate immune responses and allergen-specific cytokine production [84]. Several studies have demonstrated that this route allows to sensitize to various antigens, in the absence of adjuvant [85], with a strong Th2 response [86,87]. For that, they utilized occlusive dressings and/or prolonged exposure to the antigen. The extent of absorption of substances through the skin and into the systemic circulation depends on many parameters, as for example the surface area of application, the integrity of the skin and the contact time [79]. Contrary to the oral route, the epicutaneous administration is inadequate to discriminate the allergenic potential of proteins [64]. This route is very employed in atopic dermatitis model [52,53,66,88-95].
3.2.4. Comparison of routes of exposure
Several publications have compared the impact of these different routes of administration on sensitization. Animals can be sensitized to many allergens, but in an adjuvant-dependent manner, whatever the route practiced (IP, SC, IG, EC, and IN), with a significant production of allergen-specific IgE, IgG1 and IgG2a [49,64,85]. The maximal level of these immunologic markers is attained via the cutaneous route [85]. A mucosal administration (i.e. IG, SC or IN administrations) was shown to develop a robust allergen-specific IgA response by contrast with a cutaneous exposure [85]. The intraperitoneal route allowed a stronger IgE and IgG response compared with that obtained by oral route [49], but this response was weaker than the one observed with intranasal and epicutaneous allergen application [68]. Contrary to the oral route, intraperitoneal and epicutaneous administrations did not allow the induction of oral tolerance [87].
3.3. The use of adjuvant
Most proteins are poorly immunogenic or non-immunogenic when administered on their own. To increase the immune response and thus sensitize animals, the majority of experimental studies utilize an adjuvant. The latter leads to a Th2 skewing, and abrogates the establishment of oral tolerance [96, 97]. There are exogenous Th2 adjuvants as glycans, endogenous adjuvants as thymic stromal lymphopoietin (TSLP) and experimental adjuvants as cholera toxin, aluminum hydroxide and enterotoxin B from
3.3.1. Cholera toxin
Cholera toxin (CT) is secreted by the bacterium
3.3.2. Aluminum hydroxide
Aluminum hydroxide (alum) rarely induces cellular immune responses. However, it slows down the rate of release of the antigen and in this way increases the duration of antigen interaction with the immune system. It also promotes macrophage uptake. Therefore, it enhances the immune response against the antigen [97,99].
3.3.3. Enterotoxin B from Staphylococcus aureus
The enterotoxin B (SEB) is produced by
3.3.4. Impact of dose of adjuvant
Few studies have focused on the impact of dose adjuvant on sensitization. Kroghsbo
4. Probiotic administration
Animal models can be used to select probiotic strains which can prevent or manage allergy, and to study their mechanism of action. Indeed, these animal models can be discriminant. For instance, if number of studies showed a positive impact of probiotic supplementation in their models of allergy (Tables 4 to 6), Meijerink
4.1. Evaluation of beneficial effect of probiotic
The beneficial effect of probiotic supplementation is evaluated according to the model used.
4.1.1. Models of anaphylaxis
In models of anaphylaxis, clinical markers are analyzed after challenge by allergen, according to a scale score based on observed clinical symptoms (number of itches, mobility during the experiment, swelling of eyes and/or noise, aspect of hair, and body temperature). Thang
4.1.2. Models of asthma
In models of asthma, there is no scale of scores. The impact of probiotic is estimated by the determination of the cellular composition of bronchoalveolar fluid (total cell count and proportion of each cell type – lymphocytes, neutrophils, eosinophils and monocytes), the evaluation of number of infiltrated inflammatory cells in lung, and by the measurement of bronchial hyperresponsiveness [70,81,104].
4.1.3. Models of atopic dermatitis
As in models of food allergy, a scale of scores can be used in models of atopic dermatitis. Matsuda
The limit of all these evaluations lies in its subjectivity despite a blind evaluation system. This subjectivity results in a problem of reproducibility of the method. An analysis of biological markers of allergic reaction, i.e. the dosage in plasma of mast cell protease-1 (MCP-1) and/or histamine release during mast cell degranulation, provides less subjective data than clinical score [30,34,35]. These models also allow evaluating sensitization through dosage of allergen-specific and total IgE, IgG1 and IgG2a [60,92,100].
4.2. Route and dose of probiotic supplementation
The dose of probiotic is often comprised between 106 and 109 CFU. When the dose of probiotic is tested, the highest dose shows, most of the time, better results [35,62,89,94,106]. Jan
In oral administration, we distinguish the intra-gastric (IG) administration, in other words the gavage (with a needle), from oral administration (PO) (probiotic mixed in water or food). These two routes of exposure are principally used for the probiotic supplementation and whatever the types of allergy study. Gavage allows giving a precise dose of bacteria, but it is constraining because each animal must be handled individually leading to an additional stress in animals. Administration of the probiotic strains in drinking water or food avoids these problems of stress, but it raises the problem of their stability. Moreover, it does not allow knowing precisely the amount of bacteria received per day per animal. Probiotic can also be given by intranasal administration in models of asthma, or by epicutaneous exposure in models of atopic dermatitis. Intranasal administration allows a contact more extended with the probiotic, and therefore a longer action. However, according to the protocols, an anesthesia is necessary [107,108]. It could affect the lung antigen deposition by changing the breathing pattern and airway reflexes in animal [109]. Pellaton
4.3. Window and frequency of probiotic administration
In the window of administration, we will consider the number of weeks of supplementation as well as the number of administration per week. According to studies, the probiotic is administered between 1 to 15 weeks, during 3 to 7 days per week.
The term “prevention” refers to an administration of the probiotic that starts prior to sensitizations and continues throughout the experiment. On the contrary, the term “management/treatment” refers to an administration of the probiotic that starts after sensitizations until the end of protocol.
In studies, probiotic is mainly tested for prevention and therefore administrated until two weeks before the start of sensitizations. Meijerink
This high heterogeneity in the different protocols of probiotic administration make difficult, even impossible, comparisons between studies, and prevents establishment of an optimal administration scheme of probiotic. Comparison between prevention and management protocols shows that the window of administration plays a key role in the efficiency of probiotic, with a better effect in prevention. Indeed, in a model of food allergy, Kim
4.4. Age and sanitary status of animals
The age and the sanitary status of animals have also an influence. In study of Lyons
5. Concluding remarks
At a time when probiotics seem promising products for the prevention and treatment of allergy, fundamental and clinical studies failed the issuance of health claims and the implementation of recommendations by expert committees. The use of animal models is an essential step in the selection of strains of interest. However, such a use must be part of a rationalization process taking into account the 3Rs (Reduce, Reuse and Recycle) and ethical rules.
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BALB/c | 6 wks | BLG | IP | alum | 1/wk, x1 wk | [80] |
BALB/c male |
3 wks | BLG | IP | alum | 1/wk, x3 wks | [28] |
BALB/c female |
6 wks | OVA | IP | alum | 1/2wks, x2 | [100] |
OVA-TCR female |
8 wks | OVA | IG | / | 4/wk, x2 wks | [73] |
C3H/HeOuJ female |
6 wks | peanut extract | IG | CT | 3/wk then 1/wk, x3 wks | [57] |
BALB/c | 6 wks | OVA | IG | CT | 4/wk then 1/wk | [75] |
Swiss Albino | 6-8 wks | OVA | IP | alum | 1/wk, x2 wks | [116] |
C3H/HeJ female |
8 wks | shrimp tropomyosin | IG | CT | 1/wk, x4 wks | [34] |
BALB/c female |
18-22g | OVA | IP | SEB | 3/wk, x1 wk | [115] |
C3H/HeJ female |
5 wks | peanut extract | IG | CT | 1/wk, x8 wks | [35] |
BALB/c male | 7 wks | OVA | IP | alum | 1/wk, x2 wks | [83] |
C3H/HeJ female |
5 wks | OVA | IG | CT | 3/wk then 1/2wks, x2 | [72] |
C3H/HeOuJ female |
3 wks | whey protein | IG | CT | 1/wk, x6 wks | [74] |
BALB/c | 8 wks | OVA | IP | CT | 1/wk, x3 wks | [112] |
C57BL/6 female |
8 wks | peanut extract | IG | CT | 1/wk, x4 wks | [30] |
C3H/HeJ female |
3 wks | OVA | IG | CT | 3/wk then 1/2wks, x2 | [33] |
Sprague-Dawley male | 150-180g | OVA | IG and IP | Freund | 4/wk then 1/wk | [44] |
Brown-Norway female | 3 wks | OVA | IG | / | 7/wk, x6 wks | [45] |
Brown-Norway female | 3-4 wks | peanut extract | IG | / | 7/wk, x6 wks | [43] |
Yorkshire | birth | ovomucoid | IP | CT | 1/wk, x3 wks | [54] |
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GF BALB/c female |
8 wks | Bet v 1 | SC | alum | 1/2wks, x3 | [60] |
BALB/c female | 5 wks | cedar pollen | SC | / | 5/2wks | [70] |
GF BALB/c | birth | Bet v 1 | SC | alum | 1/2wks, x3 | [59] |
BALB/c female |
6 wks | OVA | IP | alum | 1/wk, x2 wks | [91] |
BALB/c male |
20-25g | OVA | IP | alum | 1/wk, x2 wks | [104] |
BALB/c female |
6-8 wks | Der p | SC | Freund | 1/wk, x2 wks | [62] |
BALB/c female |
6-10 wks | Bet v 1 + |
IP | alum | 1/2wks, x3 | [58] |
BALB/c male |
5 wks | OVA | IP and IN | alum | 1/2wks (IP) then 3/wk, x4 wks (IN) | [69] |
BALB/c female |
3 wks | cedar pollen | SC | / | 4/wk then 1/wk | [71] |
BALB/c female |
6-8 wks | OVA | IP | alum | 1/2wks, x4 | [82] |
BALB/c male |
5-8 wks | OVA | IP | alum | 1/wk, x2 wks | [81] |
C57BL/6 female | 6-8 wks | OVA | IP | alum | 1/2wks, x2 | [31] |
BALB/c male |
20-25g | OVA | IP | alum | 2/wk, x1 wk | [111,117] |
C57BL/6 female | 3-4 wks | Der p2 | EC | / | 1/2wks, x3 | [32] |
BALB/c | 20-25g | OVA | IP | CT | 2/wk, x1 wk | [112] |
BALB/c | - | Der p1 | IP | alum | 1/wk, x3 wks | [61] |
BALB/c female |
6 wks | OVA | IP | alum | 1/wk, x2 wks | [110] |
BALB/c female |
4 wks | OVA | IP | alum | 1/2wks, x2 | [106] |
BALB/c female |
8 wks | OVA | IP | / | 3/wk, x2 wks | [118] |
BALB/c female |
6-8 wks | OVA | IP | alum | 1/2wks, x2 | [119] |
BALB/c female |
8 wks | Par j 1 | IP | alum | 1/3wks, x2 | [101] |
Duroc x Landrace | 3 wks |
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SC et IT | alum | 1/2wks, x3 (SC) then 1/2wks, x2 (IT) | [55] |
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NC/Nga | - | FITC | EC | dibutyl phtalate | 1/wk, x3 wks | [92] |
NC/Nga male | 6 wks | DNCB | EC | / | 2/wk, x2 wks | [120] |
NC/NgaTnd | 8 wks | / | / | / | / | [105] |
SKH-1/fr female |
4 wks | OVA | EC | / | 1/3wks, x3 | [90] |
NC/Nga | 6 wks | Df | EC | SDS | 1/wk, x5 wks | [95] |
NC/NgaTndCrlj female | 10 wks | Df | EC | SDS | 2/wk, x4 wks | [88] |
BALB/c female | 8-10 wks | OVA | IP and EC | alum | 1/2wks, x2 then 7/2wk, x3 | [94] |
NC/NgaTnd | 5 wks | / | / | / | / | [42] |
NC/Nga male | 4 wks | DF | IP | / | 1/wk, x14 wks | [121] |
NC/Nga female | 6 wks | DNCB | EC | / | 2/wk, x3 wks | [89] |
NC/Nga female | birth | / | / | / | / | [122] |
NC/Nga | 6 wks | Df | EC | / | 3/wk, x5 wks | [66] |
NC/Nga male | 6 wks | PCl | EC | / | 1x | [93] |
Beagle | birth | Df | EC | / | 3/wk, x1 wk | [53] |
Beagle | birth | Df | EC | / | 2/wk, x12 wks | [52] |
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IG | 3/wk, x4 wks | 200µg or 2mg | sensitization | ↘ | [80] |
VSL#3 | IG | 7/wk, x5 wks | 15.109 CFU | clinic sensitization |
↘ ↘ |
[28] |
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IG | 7/wk, x3 wks | 2mg | sensitization | L1, L3, L4, ↗ L2 | [100] |
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IG | 4/wk, x2 wks | 2mg | clinic sensitization |
↘ LB, LC, BL ↘ LB, LC, BL |
[73] |
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IG | 3/wk, x6 wks | 109 CFU | sensitization | ↗ LP, ↘ LS, LC | [57] |
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PO | 7/wk, x1 (M) or 8 (P) wks | 5.108 CFU/mL | clinic sensitization |
P, ↘ M P, M |
[75] |
Dahi | PO | 7/wk, x1,2 or 3 wk(s) | - | sensitization | ↘ | [116] |
VSL#3 | IG | 7/wk, x3 wks | 7,5.108 CFU | clinic sensitization |
↘ ↘ |
[34] |
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IG | 7/wk, x1 wk | 108 CFU/mL | sensitization | ↘ | [115] |
ImmuBalance™ | PO | 7/wk, x4 wks | 0,5 or 1% | clinic sensitization |
↘ ↘ |
[35] |
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PO | 7/wk, x5 wks | 0,075% | sensitization | ↘ | [83] |
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PO | 7/wk, x7 wks (P) or 7/wk, x2 wks (M) | 0,2% | clinic sensitization |
↘ P, M ↘ P, M P > M |
[72] |
Immunofortis (IF) symbiotic (SY) |
PO | 7/wk, x10 wks | 2% | clinic sensitization |
↘ IF, BB, SY ↘ SY, IF, BB |
[74] |
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IG | 7/wk, x5 wks | 2.109 CFU | sensitization | ↘ BL, BB, LS | [112] |
VSL#3 | IG | 7/wk, x3 wks | 7,5.108 CFU | clinic | ↘ | [30] |
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PO | 7/wk, x7 wks | 0,2% | sensitization |
↘ BB, LC, EC BB, LC > EC |
[33] |
LGG |
IG | 7/wk, x4 wks | 109 CFU | - | [44] | |
LGG + |
IG | 7/wk, x2, 3 or 10 wks | 0,5.109 CFU | sensitization | ↘ | [45] |
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IG | 7/wk, x8 wks | 109 CFU | sensitization | [43] | |
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IG | 7/wk, then 3/wk then 1/wk, x3 wks | 109 CFU | clinic sensitization |
↘ |
[54] |
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IG | 1x (parents before coupling) | 2.108 CFU | sensitization | ↘ | [60] |
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IG | 7/wk, x3 wks | 60mg | infiltration sensitization |
[70] | |
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PO | 7/wk, x4 wks | 2.109 CFU/mL | clinic sensitization |
↘ |
[59] |
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IG | 7/wk, x3 wks | 109 CFU/600µL | infiltration | ↘ | [91] |
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IG | 7/wk, x4 wks | 60mg | infiltration | ↘ | [104] |
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IG | 7/wk, x4 wks | 1,2 or 4.106 CFU | sensitization | [62] | |
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IN | day of sensiti-zation (M) or 3/wk, x2 wks (P) | 5.108 CFU | sensitization | ↘ M, P NCC3010 > NCC2461 |
[58] |
LGG (LG) |
PO | 7/wk, x8 wks | 5.107 CFU/g | clinic sensitization |
↘ LC, LG ↘ LC, LG |
[69] |
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IG | 7/wk, x3 wks | 30mg | sensitization | [71] | |
|
IG | 7/wk, x8 wks | 2,6 or 5,5.106 CFU, or 3,6.107 CFU | infiltration sensitization |
↘ ↘ |
[82] |
|
IG | 7/wk, x2 wks | 109 CFU | infiltration sensitization |
↘ ↘ |
[81] |
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IG | day of sensiti-zation (M) or 7/wk, x4 wks (P) | 108 CFU | infiltration sensitization |
↘ M, P ↘ M, P |
[31] |
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IG | 7/wk, x1 wk | 109 CFU | infiltration sensitization |
↘ ↘ |
[111,117] |
|
IG | 3/wk, x4 wks | 109 CFU | sensitization | ↘ | [32] |
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IG | 7/wk, x2 wks | 2.109 CFU | infiltration | ↘ BL, BB, LS | [112] |
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IN | 3/wk, x2 wks | 109 CFU | sensitization | ↘ | [61] |
|
IG | 7/wk, x3 wks (P) or 1 wk (M) | 109 CFU | infiltration sensitization |
↘ P, M ↘ P, M |
[110] |
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IN or IG | 7/wk, x1 wk | 109 CFU | infiltration | ↘ A, B IN > IG |
[106] |
LGG (LG) |
IG | 4/wk, x8 wks | 109 CFU | infiltration sensitization |
↘ LG, BB ↘ LG, BB |
[118] |
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PO | 7/wk, x7 wks | 10.1010 CFU | clinic | ↘ | [55] |
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CUT | 1/wk, x4 wks | 20% v/v | clinic sensitization |
↘ |
[92] |
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IG | 7/wk, x2 wks | 5.109 CFU/mL | clinic sensitization |
↘ ↘ |
[120] |
ImmuBalance™ | PO | 7/wk, x2 wks | 1,8.108/g | clinic infiltration sensitization |
↘ ↘ ↘ |
[105] |
|
IG | 7/wk, x8 wks | 109 CFU/600µL | clinic infiltration sensitization |
↘ ↘ ↘ |
[90] |
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PO | 7/wk, x8 wks | 1010 CFU | clinic infiltration sensitization |
↘ A, B, C ↘ A, B, C ↘ A, B, C |
[95] |
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IG | 6/wk, x4 wks | 1,2.1017 CFU | clinic infiltration |
↘ ↘ |
[88] |
|
PO | 7/wk, x4 wks | 107 or 108 CFU | clinic infiltration sensitization |
↘ ↘ |
[94] |
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PO | 7/wk, x12 wks (P) or 7/wk, x7 wks (M) | 5.108 CFU/mL | clinic sensitization |
↘ P, M ↘ P, M |
[42] |
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PO | 7/wk, x15 wks | 1mg | clinic sensitization |
↘ A, B, C ↘ A, B, C |
[121] |
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PO | 7/wk, x3 wks | 1 or 2% | clinic sensitization |
↘ 2% > 1% |
[89] |
LGG | PO | 7/wk, x10 wks | 4.104 CFU/g | clinic infiltration sensitization |
↘ ↘ |
[122] |
|
IG | 2 days | 1,5.1011 CFU/mL | clinic sensitization |
↘ |
[66] |
|
PO | 7/wk, x11 wks | 0,03% or 0,3% | clinic sensitization |
↘ 0,3% > 0,03% |
[93] |
LGG Culturelle® | IG | 7/wk, x6 months | 20.109 CFU | - | [53] | |
LGG | IG | 7/wk, x6 months | clinic | ↘ | [52] |
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