A case study of development, validation, and acceptance of a non-animal method for assessing human vaccine potency
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1 Available online at Procedia in Vaccinology 5 (2011) NICEATM-ICCVAM # International Workshop on Alternative Methods to Reduce, Refine, and Replace the Use of Animals in Vaccine Potency and Safety Testing: State of the Science and Future Directions Bethesda, Maryland, USA, September 2010 A case study of development, validation, and acceptance of a non-animal method for assessing human vaccine potency Johan Descamps *, Didier Giffroy, Eric Remy, Frederic Mortiaux, Jean-Claude Mareschal, Cecile Ponsar, Michel Duchene GSK Biologicals, Rue de l Institut 89, B-1330 Rixensart, Belgium Abstract Hepatitis B vaccine (Engerix B) is a recombinant vaccine containing hepatitis B surface antigen (HBsAg) produced in Saccharomyces cerevisiae. Initially, this vaccine was released using specifications that required an in vivo potency assay in mice. This paper describes the move from the in vivo potency test toward in vitro potency assays: the in vitro Auszyme test (Abbott Laboratories) and the GSK Biologicals in-house test based upon the inhibition enzyme-linked immunosorbent assay (ELISA) principle. The challenges and difficulties during the development and introduction of this in vitro assay are presented from validation studies performed by GSK Biologicals, through regulatory acceptance, to the implementation of the alternative method by the European Directorate for the Quality of Medicines (EDQM) and HealthCare Control Authorities for Official batch release. Based upon our experience introducing an in vitro model for Engerix B potency assay, we offer suggestions to facilitate future introduction of in vitro assays Published by Elsevier Ltd. Open access under CC BY-NC-ND license. Selection and/or peer-review - under responsibility of the National Toxicology Program Interagency Center for the Evaluation of Alternative Toxicological Methods (NICEATM). Keywords: non-animal methods; in vitro test; potency test; Hepatitis B vaccine 1. Introduction GSK Biologicals hepatitis B vaccine (Engerix B) contains purified recombinant hepatitis B surface antigen (HBsAg) particles produced from Saccharomyces cerevisiae. It has been available since Initially, this vaccine was released onto the markets using specifications requiring an in vivo potency test. This paper describes the progress from in vivo potency tests toward in vitro potency assays for release purposes. The historical background, the different assays developed, and the associated validation work are detailed. The challenges and the difficulties encountered in implementing the alternative to the in vivo test are also discussed. # The National Toxicology Program Interagency Center for the Evaluation of Alternative Toxicological Methods and the Interagency Coordinating Committee on the Validation of Alternative Methods * Corresponding author. address: johan.descamps@gskbio.com X 2011 Published by Elsevier Ltd. Open access under CC BY-NC-ND license. Selection and/or peer-review under responsibility of the National Toxicology Program Interagency Center for the Evaluation of Alternative Toxicological Methods (NICEATM). doi: /j.provac
2 Johan Descamps et al. / Procedia in Vaccinology 5 (2011) Historical background In 1986, SmithKline Biologicals submitted a Product License Application for the hepatitis B vaccine, Engerix B. Engerix B contains 20 µg/ml of HBsAg, produced by recombinant technology in Saccharomyces cerevisiae and adjuvanted with aluminum hydroxide (Al(OH) 3 ). The initial potency release assay for this vaccine was an in vivo vaccination-serology test performed in mice. This test consisted of an immunological extinction procedure in mice using an ED 50 assay (effective dose 50% or the dose needed to induce a protective immune response in 50% of the mice) for vaccine kept at 4 C and at 37 C for 7 days. Because the test parameters duplicated the number of animals required to release a vaccine lot, a first effort was made to develop a simpler method. In 1992, with the product known to be stable, a variation was introduced to reduce the number of mice used by eliminating the duplicate test performed on samples stored at 37 C. A second effort was made to replace the use of animals in the Engerix B potency assay through the development of an in vitro antigen quantification method based upon the commercial Auszyme Sandwich ELISA kit (Abbott Laboratories, Chicago, IL). In 1995, this resulted in the introduction of a variation to the marketing authorization allowing the in vitro potency assay. In 2005, after Abbott Laboratories announced that they were discontinuing commercial production of the Auszyme kit, GSK Biologicals began development of an in-house ELISA test. Since 1995 the European Pharmacopoeia (Ph. Eur.) Monograph has allowed a choice between the in vivo potency assay and an in vitro method [1]. At the World Health Organization (WHO) level, in vivo testing requirements were published in the guidelines in 1987 and were revised in 1997 to include the option of an in vitro potency test [2]. 3. Validation of in vitro methods 3.1. Description of the methods In vivo method for HBsAg potency Immunogenicity of HBsAg-containing vaccines can be measured by the in vivo assay as described in the Ph. Eur. 1/2008 [3]; the WHO Guidelines [2]; and the United States Pharmacopeia (USP), Monograph 88 [4]. Mice are immunized with either a dose range of the test vaccine or reference, and with a dilution buffer. The induced anti- HBsAg antibodies are then measured, and a cut-off value is determined. The number of anti-hbsag-positive mice is determined, and the ED 50 value is calculated by probit analysis [5]. The specification set is ED 50 <1000 ng HBsAg In vitro method for HBsAg content using Auszyme EIA kit This test is described in the Ph. Eur. (Method B) and uses the Abbott Auszyme Sandwich ELISA Kit (Abbott Laboratories, Chicago, IL, USA). HBsAg-containing vaccines are diluted in phosphate-buffered saline (PBS) containing 0.2% bovine serum albumin (BSA). The different dilutions are incubated for three hours at 40 C with plastic beads that are coated with mouse monoclonal IgM anti-hbsag antibodies. The beads are then washed and incubated for 30 minutes at room temperature with mouse monoclonal IgG anti-hbsag antibodies labelled with peroxydase. The beads are washed and the amount of HBsAg is measured by a Colorimeter at 490 nm after adding orthophenylene diamine as the substrate and stopping the reaction by adding H 2 SO 4. The optical density (OD) measured is proportional to the amount of HBsAg present in the vaccine In vitro method for HBsAg content using an in-house-developed method based upon an inhibition ELISA In 2005, when Abbott Laboratories decided to discontinue the commercial production of the Auszyme kit, GSK Biologicals developed an in-house ELISA test. This test is based upon the inhibition ELISA principle. Standard vaccine and vaccine samples are diluted in PBS containing 0.1% BSA and 0.1% Tween 20. One hundred microliters of a fixed amount of human polyclonal anti-hbsag antibody (Nabi-HB, Nabi Pharmaceuticals, Boca Raton, FL, USA; approx. 170mIU/mL) are then allowed to react overnight (25 C, agitation) with 100 µl of the different dilutions in microplates (Greiner Bio-One, plates for cell culture, Frickenhausen, Germany). The microplates are centrifuged (10 minutes at 200 rpm), and the supernatant fluid is transferred to ELISA plates (Nunc, Maxisorp, Roskilde, Denmark) that have been precoated overnight with 1 µg/ml HBsAg and post-coated with PBS-BSA 1%. The plates are incubated for 2 hours at 37 C and then washed. Goat anti-human IgG antibodies coupled to
3 186 Johan Descamps et al. / Procedia in Vaccinology 5 (2011) peroxydase are added under agitation for 1 hour at 37 C. The amount of bound antibodies is then measured colorimetrically by adding tetramethylbenzidine/h 2 O 2 as a substrate. After incubating for 20 minutes at room temperature in the dark, the reaction is stopped by adding H 2 SO 4, and the OD is read at 450 nm. The OD measured is inversely proportional to the amount of HBsAg present in the unknown vaccine samples Validation of Auszyme test Initially, each lot of Engerix B was released on the basis of an immunogenicity test in mice (mouse potency test). After discussions with the regulatory authorities of the European Union and the United States, GSK Biologicals developed an in vitro test based upon the Auszyme Monoclonal Enzyme immunoassay (Abbott Laboratories). The reference vaccine used as a standard in this assay was a commercial lot of Engerix B, representative of the routine production process and released according to the current specifications (in vivo potency test). The Auszyme in vitro method was validated as follows: Linear dose-range response: a dose-range of the reference vaccine containing ng HBsAg/mL was prepared for each test. The vaccine lot to be tested was diluted in order to obtain ng HbsAg /ml. If the validity criteria of the parallel line assay (linearity and parallelism) were met, then the HBsAg content could be calculated [5]. Reproducibility of the method (inter-assay variation): the HBsAg content was calculated from 20 different assays on the same lot. The mean value obtained was 20.4 µg/ml (standard deviation [SD] coefficient of variation [CV] 3.5%). Comparison of in vivo in vitro results: 147 commercial lots were tested in vivo and in vitro over a period spanning 18 months. The mean in vitro result was 23.9 µg/ml (SD 2.1; Lower Confidence Limit (LCL) 99% 18.5; Upper Confidence Limit (UCL) 99% 29.4). For the in vivo test, the mean value was ED ng (SD 136; LCL 99% 55; UCL 99% 758). All lots met the in vivo specifications. Results showed no direct mathematical correlation between the in vitro assay and the in vivo assay: the Pearson correlation coefficient was 0.06 (p value > ). Special attention was focused on the establishment of a reference vaccine. This reference lot was produced under routine production conditions and met all release specifications. In addition, this first reference lot was included in a clinical trial and shown to be safe and efficacious in humans. This same reference lot was also used as a reference vaccine for the in vivo potency assay and was included in a collaborative study organized by the Ph. Eur. to validate two candidate Ph. Eur. Biological Reference Preparations (BRPs). Discriminating power of the in vitro assay: because only consistent Engerix B lots were available, the following approaches were implemented: Data were generated with lots obtained after exposure to elevated temperatures (accelerated stability data after incubation at 37 C and 45 C). Results are shown in Table 1. The Engerix B vaccine does not lose antigenic activity for a period of up to 8 weeks at 37 C. However, after incubation of the vaccine at 45 C, the ELISA content decreased from week 3 onward to reach, at week 8, about 30% of the value found before incubation. It should be noted that vaccine incubated for 12 weeks at 45 C still met the in vivo specifications. This experiment shows that the in vitro assay is a more sensitive tool than the in vivo assay to detect nonconsistent lots under accelerated stability conditions. Data were generated on a range of lots prepared by dilution of more-concentrated lots of Engerix B. A super-potent lot was prepared at 80 µg/ml of HBsAg, and subpotent lots were formulated at 10 and 5 µg/ml. The antigen content of the super-potent lot could not be calculated because the OD values were beyond the range of the calibration curve. For the subpotent lot at 5 µg/ml of HBsAg, the OD values were below the lowest point of the standard curve, so it was not possible to attribute a value. For the 10 µg/ml samples, two OD values fell within the standard curve. The calculated values were 8 µg/ml and 8.5 µg/ml of HBsAg. This shows that the in vitro assay is capable of detecting subpotent lots while the proposed measuring range varies from 10 to 40 µg/ml.
4 Johan Descamps et al. / Procedia in Vaccinology 5 (2011) Table 1. In vitro potency stability studies using Auszyme in vitro test Incubation Time (Weeks) T LOT A Engerix B HBsAg (µg/ml) % Recovery LOT B Engerix B HBsAg (µg/ml) % Recovery C C C C C C C C C C Validation of in-house ELISA assay The inhibition ELISA described above was designed by GSK Biologicals to allow testing of the vaccines without desorbing the antigen from the adjuvant system and to allow the use of the same BRP. The antibodies used in this ELISA were shown to bind to a protective epitope of HBsAg. In a competition assay, RF1 anti-hbs antibodies blocked the infectivity of HB virus in a susceptible chimpanzee model [6, 7]. The Nabi-HB antibodies used in the inhibition ELISA compete directly with a fixed amount of biotinylated RF1 monoclonal antibodies (Mabs) for binding to HBsAg. The results demonstrate that the level of RF1-like protective antibodies in the Nabi-HB preparation is equivalent to that found in the pool of Engerix B vaccine antisera and that they are directly linked to a protective effect against HB. The validation of the inhibition ELISA was performed according to the Guidelines of the International Conference on Harmonisation [8]. The following parameters were investigated. Full details have been published previously [9]. Dose-response range When plotted in a lin/log-transformed format, the dose-response curves showed a sigmoid shape. For the concentrations used in the routine test (60 to 360 ng/ml), the graph was in the linear part of the curve for the standard preparation and the test samples. Limit of quantification Because the OD values must be in the linear range of the standard (60 to 360 ng/ml), the lowest limit for a quantitative test was 60 ng/ml. Limit of detection The limit of detection as determined in six independent experiments was 35 ng/ml. Linearity and parallelism In the six experiments, linearity was demonstrated for the range 60 to 360 ng/ml; the correlation coefficients for the different standard curves were all above Validity criteria were set for parallelism and linearity: P values must be higher than Repeatability (Table 2) The repeatability or intra-assay precision was assessed on three lots of Engerix B. Each lot was tested six times on the same day. The coefficients of variation (CV) for the three lots were 2.7% - 5.0% - 5.9%. Intermediate precision (Table 2) The intermediate precision or the inter-assay precision was tested on three lots of Engerix B. Each lot was tested in six independent experiments. The CVs were 4.0% - 5.6% - 3.2%.
5 188 Johan Descamps et al. / Procedia in Vaccinology 5 (2011) Accuracy Accuracy was measured on an Engerix B lot spiked with 5, 10, or 15 µg of HBsAg. The recovery was 112%, 107%, and 104%, respectively. Specificity A nonspecific binding of the Nabi-HB serum to aluminium at high concentrations was observed. However, at the dilutions used to test the vaccines, nonspecific binding was not observed. Specificity was also controlled by testing other vaccines not containing HBsAg, such as Havrix (hepatitis A), Tritanrix (DTPw), Infanrix and Infanrix IPV (DTPaIPV), and Hiberix (haemophilus influenza type B). No evidence of nonspecific binding or aspecific reactions was found. Bridging with Auszyme method Potency results for 64 Engerix lots using both methods are shown in Table 3. There is a very good correlation between the two methods, and the observed CV was almost identical. In order to verify the reproducibility and the transferability of the ELISA method to different outside laboratories, a study was set up with four different Official Medicines Control Laboratories (OMCL) in Europe. Results are summarized in Table 4. The CV calculated from all the valid results for the different laboratories was 7.3%, which shows that the inhibition ELISA method was reproducible and transferable to the control authorities in charge of releasing vaccine batches on the basis of testing. Table 2. Intra-assay and inter-assay precision of the GSK ELISA assay Engerix B lot Mean HBsAg Content (µg/ml) Standard Deviation Coefficient of Variation (%) Intra-assay Precision Lot Lot Lot Inter-assay Precision Lot Lot Lot Challenges When developing and validating alternatives to in vivo tests, different driving factors must be considered. In addition to ethical considerations and industrial resources (throughput) and motivation, acceptance by authorities is imperative. Regulatory authorities acceptance is one of the most challenging aspects of alternatives implementation. Variations to the marketing authorizations had to be submitted in more than 120 countries before the in vitro potency test could be introduced as an alternative to the in vivo test used for routine release activities. Because variations had to be submitted for all the hepatitis B-containing vaccines, more than 500 variations had to be submitted worldwide. This is a tremendous amount of administrative work without any added value from a technical and quality point of view on the sides of both the manufacturer and the authorities. The variations were submitted in 1995 and took more than four years to gain approval. In Europe, on average, the approval of this variation took between 20 and 35 months.
6 Johan Descamps et al. / Procedia in Vaccinology 5 (2011) Table 3. Bridging Auszyme and GSK in vitro ELISA methods for potency determination of Engerix B vaccines Auszyme Method (µg/ml) New Method (µg/ml) Number of Lots MEAN Standard Deviation CV (%) This hepatitis B case study shows that worldwide introduction of a variation for an alternative to an in vivo test is a long and laborious task. This lengthy approval process had the following consequence: since the approval of the in vitro assay did not occur at the same time in the different countries, both potency tests (in vivo and in vitro) had to be run in parallel over a certain period for routine quality control (QC) release testing, leading to an increased complexity in the supply chain activities without any added value for the public health. This also considerably delayed the elimination of animal use for the hepatitis B potency assay. For the Auszyme replacement test, the method had to be changed because the manufacturer of this commercial kit decided to stop production and sale. This resulted in a need to develop and approve a new test in a very short time frame in order not to interfere with routine release and supply. The decision made by Abbott Laboratories not only affected the pharmaceutical industry but also all the control authorities in charge of releasing hepatitis B- containing vaccines on the basis of testing. Variations for this replacement test were introduced in 2005 in more than 100 countries. Five years later, some countries have not yet approved the change. In this context, in the EU, four different OMCLs agreed to evaluate this test. The joint evaluation greatly facilitated the transfer and further acceptance of this test within the EU. Additionally, a close collaboration was set up with OMCLs in the EU. In the international arena, the transfer of the test methodology faced some hurdles. The alternative test transfer to some National Control Laboratories was problematic due to technical and equipment constraints, e.g., technical issues, equipment issues, calculation issues, and validity criteria, but also due to the lack of reference to this in vitro test in national pharmacopoeia. This highlighted the need for a simplified procedure for introducing alternatives to in vivo testing but also the need for coordination between all interested parties (licensing and control authorities and manufacturers) and for international harmonization. 5. Future directions This article provided a case study on the development, validation, and acceptance of a non-animal method for assessing human vaccine potency. The example of a hepatitis B vaccine (Engerix B) demonstrated that this process is a long and tedious task. A first report on the development of in vitro tests for hepatitis was published as early as 1999 [10]. The in vitro assay has now been in use for more than 15 years, and no reports have been made of any issues with the potency of HBsAg-containing vaccines. This in vitro assay has allowed a very important reduction in the use of mice for routine release testing [10] of HBsAg-containing vaccines. There are several recommendations to facilitate the introduction of alternative in vitro tests in the future. For example, in vitro potency tests for routine release purposes should be considered and evaluated very early in the development of new vaccines. This implies that during the development and characterization phases of a new vaccine both in vivo and in vitro methods will coexist. The in vivo potency method should be seen as a characterization test that demonstrates the induction of an immune response or protection against a challenge. Once consistency of manufacturing has been demonstrated for this parameter, the routine QC release test for potency could then be shifted to a validated in vitro assay. This validated in vitro potency assay is a more precise and more powerful tool to verify the consistency of production than the variable in vivo test. As such, this in vivo test should be limited to the support of significant changes in the manufacturing process.
7 190 Johan Descamps et al. / Procedia in Vaccinology 5 (2011) Table 4. Reproducibility and transferability of the GSK ELISA assay with different OMCLs Laboratory GSK OMCL 1 OMCL 2 OMCL 3 OMCL 4 Test HBsAg Content (µg/ml) Invalid 3 Invalid MEAN 27.1 Standard Deviation 2 CV (%) 7.3 During the early phase of vaccine development, the in vitro test development should be discussed with the different National Control Authorities. Ideally, collaborative studies should be set up at an international platform to evaluate these in vitro alternatives. This implies that there should be a worldwide consensus and harmonization on the development, validation requirements, and regulatory acceptance mechanisms of alternative in vitro tests. In order to introduce in vitro alternative tests more easily and more quickly, there should be some mechanisms to facilitate their introduction and acceptance. For instance, in Europe, a simplified mechanism exists to treat variations on a worksharing basis between the different authorities. Other possibilities that could expedite implementation include global approval of the variation by using a simplified administrative procedure that covers all vaccines implied by the change, the application of a fast-track procedure for variations that defend the 3R principles, and support from WHO to recognize and introduce into the WHO Guidelines in vitro alternatives as soon as they become available. Only when a joint effort is maintained between the different parties will in vitro potency tests be introduced on an international basis for routine QC release testing. The example shown in this article of the introduction of an in vitro potency assay for hepatitis B vaccines demonstrates that it is a long but very feasible process. References [1] Method of Analysis. Biological assays: Assay of hepatitis B vaccine (rdna) [ch ]. In: European Pharmacopoeia, 67th ed. Strasbourg, France: European Department for the Quality of Medicines & HealthCare (EDQM), Council of Europe, 2011 [2] WHO Expert Committee on Biological Standardization. Requirements for hepatitis B vaccines made by recombinant DNA techniques. In: WHO Technical Report Series, No Geneva: World Health Organization, 1989, 28. Available at: [3] European Pharmacopoeia. Monograph Hepatitis B vaccine (rdna), Ph.Eur. 6 th Edition. Strasbourg, France: European Department for the Quality of Medicines within the Council of Europe; 2008.
8 Johan Descamps et al. / Procedia in Vaccinology 5 (2011) [4] United States Pharmacopoeia- National Formulary. Monograph 88 'Biological reactivity tests, in vivo'. United states Pharmacopoeial Convention,Inc Twinbrook Parkway, Rockville, MD 20852,USA. [5] Finney DJ. Parallel line assays. In: Statistical Method in Biological Assay, 3 rd ed. London: Charles Griffin & Company, 1978, [6] Iwarson S, Tabor E, Thomas HC, Goodall A, Waters J, Snoy P, et al. Neutralization of hepatitis B virus infectivity by a murine monoclonal antibody: an experimental study in the chimpanzee. J Med Virol 1985;16(1): [7] Waters JA, Brown SE, Steward MW, Howard CR, Thomas HC. Analysis of the antigenic epitopes of hepatitis B surface antigen involved in the induction of a protective antibody response. Virus Res 1992;22(1):1-12. [8] International Conference on Harmonisation (ICH). Guidance for Industry. Q2B Validation of Analytical Procedures: Methodology, [9] Giffroy D, Mazy C, Duchêne M. Validation of a new ELISA method for in vitro potency assay of hepatitis B-containing vaccines. Pharmeuropa Bio 2006;1:7-14. [10] Descamps J, Mary A, Rommel E, Anhoury ML, De Neys R, Duchêne M. Release potency tests of hepatitis vaccines. In: Sesardic D, Brown F, Hendriksen CFM, editors. Alternatives to Animals in the Development and Control of Biological Products for Human and Veterinary Use. Meeting of the International Association of Biological Standardization. September London. Dev Biol Stand (Basel): Karger, 1999;100:
Project leader: David Wood (1) ; Statisticians: Dawn Sands (1), Alan Heath (1) BRPs for inactivated adsorbed hepatitis A vaccines 1.
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