INTRODUCTION — Allergen immunotherapy for the treatment of allergic respiratory diseases has traditionally been administered by subcutaneous injections. Subcutaneous immunotherapy (SCIT) has proven efficacy in allergic rhinitis and asthma, but it requires regular injections at a clinician's office (typically over a period of three to five years) and carries the risk of potentially serious systemic allergic reactions in response to the treatment itself.
Oral immunotherapy (OIT) has been of clinical interest because it offers specific advantages over injection immunotherapy. OIT is more easily administered, avoids cumbersome injections regimens, and carries a much lower risk of anaphylaxis compared with SCIT.
The techniques, mechanisms of action, advantages, and limitations of OIT for allergic rhinitis will be reviewed here. SCIT is discussed separately. (See "Subcutaneous immunotherapy for allergic disease: Indications and efficacy" and "Subcutaneous immunotherapy for allergic disease: Therapeutic mechanisms".)
OIT for the treatment of other allergic diseases is reviewed separately. (See "Future therapies for food allergy" and "Latex allergy: Management", section on 'Immunotherapy'.)
Background — Oral immunotherapy (OIT) was first proposed as a method of treatment for allergic disease in the early 1900s. In the 1980s, properly designed clinical trials first demonstrated a dose-dependent therapeutic response with specific and well-characterized aeroallergens. In 2006, the World Health Organization recognized the cumulative evidence that OIT represented a viable alternative to SCIT and encouraged continued clinical investigation to characterize optimal techniques [1].
Availability — Sublingual tablet immunotherapy (STIT) has been approved by the European regulatory authorities and is in use throughout the European Union (EU). In the United States, OIT has not been approved by the Food and Drug Administration at the time of this writing. In addition, there are no commercially available products specifically intended for OIT in the US, and no standardized information on how to prepare an oral extract from the available extracts intended for use in SCIT.
MECHANISMS OF ACTION — The gut is the largest mucosal organ of the body and is exposed to numerous foreign proteins on a constant basis. The normal response of the gut immune system to nonpathogenic proteins is tolerance, a fact which forms the basis for the concept of oral immunization.
The gut immune system is comprised of various physical barriers, secretory IgA, the gut associated lymphoid tissue (GALT), and lymphoid organs (mesenteric lymph nodes, spleen, and liver). Within the GALT, two areas of importance for antigen processing are the tonsils and adjacent ring of lymphoid tissue in the posterior pharynx, and the Peyer's patches of the duodenum, jejunum, and small intestine. The GALT is essential for normal tolerance to most foreign proteins, as well as in the immunologic response to OIT. The role of the GALT in the pathogenesis of food allergy is reviewed elsewhere. (See "Pathogenesis of food allergy".)
Allergens used in OIT are usually intended for absorption either in the mouth or within the small intestine, as the conditions of the gastric environment (pH and other factors) destroy many allergenic proteins. Whether the immunologic response to allergens absorbed through the oral mucosa is different from that to allergens absorbed through the intestine is an area of ongoing investigation.
Immunologic changes following OIT — Oral immunotherapy (OIT) is less well-studied than subcutaneous immunotherapy (SCIT), although similar immunologic mechanisms appear to be involved [5]. The immunologic changes observed with SCIT are discussed in more detail elsewhere. (See "Subcutaneous immunotherapy for allergic disease: Therapeutic mechanisms".)
The following changes in the humoral responses to allergens are seen with OIT [6-13]:
OIT also results in changes in the cellular response to allergens, including [14-18]:
METHODS — Oral immunotherapy can be administered in several ways. Technical variations include preparation of allergen, the types of allergens used, the doses involved, and schedules of administration.
Forms of oral allergen immunotherapy — Several allergen preparations have been studied in oral immunotherapy. The following forms are most promising:
Types of allergens — The majority of studies of oral immunotherapy have been performed with pollen allergens in patients with allergic rhinitis. The use of food allergens or latex allergens in oral immunotherapy is discussed separately. (See "Future therapies for food allergy" and "Latex allergy: Management", section on 'Immunotherapy'.)
Doses — The cumulative amount of allergen administered in the course of a year is generally 20 to 200 times greater with oral forms of immunotherapy compared with SCIT. In some studies, the daily dose of allergenic protein in micrograms is equivalent to the dose given every two to four weeks in SCIT.
The reason(s) that higher doses are needed have not been fully defined, although they may include loss of allergen through digestion, as well as the immunologic effects of high versus low levels of allergen exposure in the gut.
Schedules — Escalating doses are administered once daily, usually beginning a few months before the pollen season. As an example, STIT treatment for seasonal allergens is generally started two to three months prior to the start of the relevant pollen season. Continuous year-round OIT is another option, although this did not appear to be superior to preseasonal treatment after the first year, in one open label study of grass pollen SLIT [22]. However, the best approach is not clear, since the studies that showed persistent benefit two years after completion of a three year course of STIT used continuous year-round treatment, as described below [23]. (See 'Persistence of therapeutic benefit' below.)
Maintenance doses are reached by 3 to 12 weeks of treatment. During the maintenance phase, OIT is administered daily to weekly through the pollen season.
Duration of therapy — The optimal duration of a course of oral immunotherapy has not been defined. However, one controlled but nonrandomized study of 78 patients undergoing dust mite SLIT for three, four or five years found that patients experienced persistent reduction in symptoms lasting seven, eight and eight years, respectively [24]. Based on this, the authors suggested four years of therapy was a reasonable goal until more data are available. Other studies evaluating the persistence of benefit after stopping therapy are reviewed below. (See 'Persistence of therapeutic benefit' below.)
EFFICACY AND SAFETY — A 2011 systematic review of 60 randomized trials (published through 2009) included approximately 2300 adults and children receiving active SLIT treatment and equivalent numbers receiving placebo [25]. Most studies involved treatment with single pollens (most commonly grass) or house dust mite preparations, at a range of doses. Treatment resulted in a statistically significant reduction in symptoms [standardized mean difference of -0.42 (95% CI -0.69 to -0.15)] and in medication requirements [standardized mean difference of -0.43 (95% CI -0.63 to -0.23)]. Fifteen studies included only children, with results that were similar to those in adults. There was a trend for greater improvement with treatments lasting longer than one year. Local side effects (oral pruritus and swelling, throat irritation) and nausea were more common with active treatment, although systemic adverse effects (rhinitis or rhinoconjunctivitis) were equal in active treatment and placebo groups. No trial reported anaphylaxis or the need to administer epinephrine. Effects on quality of life could not be assessed because a variety of different measurements were used. Publication bias could not be excluded, as with any systematic review.
STIT (sublingual tablets) — Among the different approaches to oral immunotherapy, studies using sublingual tablets (STIT) of grass pollen have yielded some of the best results. The following series of studies illustrates the steps required to define an effective approach for each type of oral immunotherapy.
Single grass allergen — European studies with Timothy grass STIT have demonstrated clinical benefit in grass allergic subjects [11,26].
Multiple grass allergens — There are a limited number of high-quality studies in which multiple allergens were given simultaneously in OIT.
A standardized sublingual tablet has been produced (Oralair®, Stallergenes) that contains allergens from five grass species that are prevalent in Europe: Timothy (Phleum), Rye (Lolium), June (Poa), Orchard (Dactylis), and Sweet Vernal (Anthoxanthum). A study to establish dosing of the 5-grass product randomized 628 grass allergic adults with rhinoconjunctivity to three different doses: 100 Index of reactivity units (IR) (equivalent to 8.3 mcg or allergen, 300 IR (25 mcg), or 500 IR (42 mcg)) [30]. Treatment was initiated 16 weeks prior to the grass season, with an incremental step-up dosing of 100 IR over the first 5 days until the final dose was achieved, and continued through the grass season.
Therapy was well-tolerated. Adverse effects included mild to moderate oral pruritis and/or throat irritation. No serious or life-threatening adverse events attributable to active study medication were reported. The highest two doses yielded significant improvement in rhinoconjunctivitis total symptom scores, and in secondary endpoints of clinical efficacy, compared with placebo or the lowest dose [30].
Another similar study of 278 children and adolescents with rhinoconjunctivitis found that the 300 IR dose was well-tolerated and effective in this age group as well [31]. Dosing two and four months preseason, in addition to during the grass season, were similarly effective in a randomized trial of 633 adults [32].
Persistence of therapeutic benefit — Some preliminary data are available about the persistence of benefit with several years of therapy, as well as after treatment is stopped. OIT appears to be similar to subcutaneous immunotherapy in these respects.
The Timothy grass STIT trial discussed above [26] was extended in its double-blind, randomized, placebo-controlled fashion for an additional two years with a subsequent two-year follow-up [33]. Three-hundred-fifty-five (355) of the original 634 participants volunteered to participate in the double-blind, placebo-controlled extension arm of this long-term treatment phase of the study. Clinically, the significant improvements in mean rhinoconjunctivitis symptom scores and QOL persisted in the extension phase. In addition, there was a continued increase in IgG4 levels through the course of the two years of treatment in the grass allergen tablet-treated group, while the antibody levels did not change in the placebo-treated group.
The grass immunotherapy treatment was well-tolerated and <1 percent of participants dropped out due to a serious adverse event. In contrast to the first year of study, during which 46 percent of grass-treated subjects (versus 4 percent of placebo) reported oral pruritus, only four events of oral pruritus were reported. Thus, the therapy was better tolerated over time.
Subsequent reports provided information about the same group of patients, who had received three years of active therapy (or placebo), and were reevaluated one and two years after discontinuing treatment [23,34]. The grass allergen-treated group demonstrated sustained reductions in rhinoconjunctivitis symptom scores and medication scores and improvements in quality of life at the end of the second year following treatment [23,35]. This is the first controlled study demonstrating that oral immunotherapy, like subcutaneous injection immunotherapy, can provide benefit that persists after treatment is discontinued.
SLIT (sublingual aqueous extracts) — Another approach to the delivery of OIT involves glycerinated aqueous allergen extracts that are initially held under the tongue for two to three minutes and then swallowed. This construct has gained acceptance in Europe and is being studied in US clinical trials. In the United States, phase I studies on safety and tolerability have been carried out with ragweed, grass, house dust mite, and cat glycerinated extracts [36]. These clinical studies used the commercially available standardized glycerinated extracts currently licensed for subcutaneous immunotherapy.
Ragweed — The most advanced clinical trials have been performed with ragweed in a series of studies conducted by Greer Laboratories Inc (Lenoir, NC) [37,38]. These clinical studies used the commercially available standardized glycerinated ragweed extract currently licensed for subcutaneous immunotherapy.
House dust mite — SLIT with house dust mite allergen can induce the immunologic changes associated with clinical improvement. However, significant reductions in clinical symptom scores and medication use have not been clearly demonstrated:
Multiple different pollen allergens — It is not yet certain that multiple different allergens can be given simultaneously in OIT without impacting efficacy. In one study, 54 grass-allergic patients were randomized to placebo, monotherapy with timothy extract (19 mcg Phleum p 5 daily), or timothy extract plus nine additional unstandardized pollen extracts [41]. Threshold for titrated nasal challenge, skin prick tests, and serum-specific IgG4 levels were statistically-shifted in favor of active treatment with timothy extract. A modest positive trend was observed in clinical parameters in the multiple pollens group, which did not reach clinical significance. Thus, further studies are needed to determine whether multiple different types of allergens can be combined. (See 'Issues requiring further study' below.)
Microencapsulated OIT with ragweed — Microencapsulated preparations of allergens have also been studied, although results have been somewhat more mixed.
In a unpublished precursor trial, microencapsulated (ragweed) pollen extract (MRPE, standardized for units of Amb a 1) was studied in 607 ragweed-allergic patients [42]. Patients received 40 units Amb a 1 per day, 40 units Amb a 1 per week, or placebo. Treatment started 8 to 12 weeks prior to ragweed season and continued up to 24 weeks. Subjects receiving the once-daily regimen for 10 weeks experienced a 36 percent improvement in the primary endpoint. The therapy was generally safe and well-tolerated, though the number and severity of gastrointestinal side effects was higher with the once-daily regimen.
A 2007 clinical trial was designed to establish an effective and safe dose for oral microencapsulated immunotherapy [42,43]. Active treatment (40 mcg Amb a 1 per day; started 10 to 24 weeks pre-ragweed season) resulted in a significant increase in ragweed-specific antibody, but no clinical improvement in allergy symptoms compared with placebo. Thus, microencapsulated products require further study before they can be applied clinically.
Use in pregnancy — Published data addressing the safety of OIT or SLIT in pregnancy is lacking. However, reports of adverse outcomes or fetal harm have not emerged despite decades of use in various countries. European manufacturers suggest an approach similar to the one used for injection immunotherapy, ie, that treatment not be initiated in a pregnant patient, but if a woman becomes pregnant during treatment, therapy could be continued provided the patient has not had significant allergic reactions to therapy in the past.
PATIENTS WITH CONCOMITANT ASTHMA — A small number of trials have examined the safety and efficacy of OIT in patients with rhinoconjunctivitis and concomitant asthma [44,45]. These studies suggest that OIT can be safely administered to most patients with asthma, although it may not significantly improve asthma control.
Adults — A randomized trial of 114 adult subjects (aged 18 to 65) with mild to moderate grass pollen-induced asthma and rhinoconjunctivitis, assigned subjects to treatment with 75,000 SQ-T (15 mcg Phleum p 5), Timothy grass allergen sublingual tablet (Grazax®), or placebo [44]. The primary endpoints were average asthma symptom and medication scores during the grass pollen season.
During the grass season, asthma symptom and medication scores rose slightly in both active and placebo groups, but no discernible differences were observed between groups. Consistent with other trials with the STIT construct, significant improvement in mean rhinoconjunctivitis symptom scores, medication scores, and well days (37, 41, and 54 percent respectively) was observed in the group receiving active STIT. No serious adverse events were reported in the study and the number of adverse events linked to asthma was reported as similar between groups.
This clinical trial provided data on the safety of self-administration of the grass allergen tablet in asthmatic subjects and showed that allergen treatment did not impair asthma control, although there was no significant improvement in asthma symptoms either.
Children — A randomized trial of 253 children (5 to 16 years of age) with seasonal allergic rhinoconjunctivitis with or without asthma, demonstrated that the same Timothy grass sublingual tablet formulation (75,000 SQ-T units (15 mcg Phl p 5)) was safe and effective, and did appear to have a positive impact on asthma symptoms and medication use [45].
Treatment was initiated 8 to 23 weeks prior to the grass season and continued through the season. Ninety-two percent of children completed the trial. No serious adverse events were assessed as being treatment-related [45].
In the grass tablet-treated group, the primary endpoints of median improvement of rhinoconjunctivitis symptom scores and medication scores were met [45]. The active treatment also showed a significantly greater number of "well days" versus placebo treatment. During the study, 105 children (42 percent) reported asthma (5 percent severe, 48 percent moderate). Although only 23 percent used any asthma medications, a relative difference in median asthma symptom score was observed in the active treatment group versus placebo-treated children and use of asthma "relief" medication was nominally lower in the active treatment group.
COMPARISON OF OIT AND SCIT
Advantages and disadvantages of OIT — There are several potential advantages of OIT, compared with SCIT:
The disadvantages of OIT include:
Comparative efficacy — Few trials have directly compared SLIT and SCIT, and a firm conclusion cannot be made based upon these limited data [49-51].
Issues requiring further study — Further research is needed in several areas, in addition to optimizing dosing and delivery systems. Incompletely answered questions include the following [52,53]:
Practical considerations — The optimal way to incorporate OIT into clinical practice remains to be determined. The following types of patients raise specific questions about the best use of OIT.
SUMMARY AND RECOMMENDATIONS
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