FDA approval of the first anti-amyloid antibody to treat Alzheimer’s disease has left clinicians grappling with new questions. How are they to administer aducanumab safely? How will people cope with learning they have amyloid plaques in their brain, a prerequisite for treatment? What type of patient will benefit the most? And will the answers be the same or different for each anti-amyloid antibody? At the Alzheimer’s Association International Conference, held July 31 to August 4 virtually and in San Diego, California, speakers discussed ways to address these issues, sketching a roadmap for integrating anti-amyloid immunotherapy into clinical practice.

  • Aducanumab’s appropriate-use recommendations got tougher.
  • Most research participants handle news of their amyloid status well.
  • ALZ-NET initiative to gather data on real-world safety and effectiveness.

Specific topics included updates to aducanumab's appropriate-use recommendations (AURs), the consequences of disclosing amyloid status, and a new initiative, ALZ-NET, that is now set up to track how treatment works longer-term in the general population. Audiences seemed eager for the information, asking questions until time expired.

And no wonder. Eli Lilly’s anti-amyloid antibody donanemab this month was accepted for priority review under the Food and Drug Administration’s accelerated approval pathway, following Eisai’s lecanemab last month (Fierce Biotech story; Jul 2022 news). Roche’s Phase 3 studies of gantenerumab will read out this fall. This means that three more anti-amyloid antibodies could be approved next year, in an environment where most clinicians still have little experience with this new type of treatment.

Minimizing ARIA Risk
When the FDA granted accelerated approval to aducanumab last year, the terse label raised questions about how to administer the drug and track safety (Jun 2021 news). To fill this gap, six leading clinician-researchers developed AURs, specifying patient selection criteria and an MRI monitoring schedule (Aug 2021 news). Since then, however, concerns about the risk of the brain edema and bleeding known as ARIA have intensified (Oct 2021 news; Dec 2021 news).

These concerns have prompted a revision of the AURs. The original panel—Paul Aisen at the University of Southern California in San Diego, Liana Apostolova at Indiana University School of Medicine in Indianapolis, Alireza Atri at Banner Sun Health Research Institute in Sun City, Arizona, Jeffrey Cummings of the University of Nevada, Las Vegas, Stephen Salloway at Butler Hospital in Providence, Rhode Island, and Michael Weiner at the University of California, San Francisco—has become a working group. It added four members: Suzanne Hendrix of Pentara Corporation, Salt Lake City, Gil Rabinovici of UCSF, Marwan Sabbagh of the Barrow Neurological Institute in Phoenix, and Dennis Selkoe of Brigham and Women’s Hospital, Boston.

Introducing their new AURs in San Diego, Cummings said the main changes involve more stringent exclusion criteria and more frequent MRI scans. Both aim at reducing the risk of ARIA. Specifically, in addition to the previous exclusion of any person who is taking anticoagulants or has a history of bleeding disorders, the new AURs now advise against giving aducanumab to anyone who in the past has had seizures, a stroke, or transient ischemic attacks, as well as anyone who has an autoimmune or inflammatory condition such as lupus or psoriatic arthritis. All of these conditions can make a person more susceptible to ARIA.

Furthermore, the updated AURs recommend APOE genotyping. APOE is the main determinant of ARIA risk, with two-thirds of APOE4 homozygotes having developed ARIA during the aducanumab trials, compared to one-third of E4 heterozygotes and one-fifth of noncarriers. Knowing the genotype of the person before them could help the clinician devise the right management plan for that patient, Sabbagh said. This is the first time APOE genotyping has been recommended as a prerequisite for an AD therapy, and its clinical utility will need to be evaluated, Sabbagh added.

Other anti-amyloid antibodies have different risk profiles. In San Diego, Larisa Reyderman of Eisai reported a 23 percent risk of ARIA in E4 homozygotes treated with lecanemab. Heterozygotes had a 7 percent risk, not statistically different from the 5 percent risk in noncarriers.

For monitoring, the original AURs recommended MRI scans at baseline and prior to the fifth, seventh, and 12th monthly doses, as well as any time symptoms of ARIA appear. The new AURs add a scan before the ninth dose to minimize the risk of dosing through asymptomatic ARIA, and worsening it. The new guidelines also call for having a treatment plan in place to manage severe ARIA. This could include administering steroids or anti-epileptics. “The goal is to create a standard of care that will reduce the likelihood of serious outcomes,” Salloway said.

Audiences peppered the speakers with questions. Among other practical concerns, they wanted to know what factors predict ARIA, what strength scanner to use for MRI, and whether there are long-term effects from ARIA. Cummings noted that the first AURs have been downloaded 20,000 times, demonstrating high demand for this information. The working group also regularly discusses its findings with the FDA; the agency’s last update of aducanumab’s label, in April 2022, brought the label into closer concordance with the AUR. The updated AURs were published April 5 in The Journal of Prevention of Alzheimer’s Disease (Cummings et al., 2022). 

Meanwhile, researchers led by Marco Lyons at Roche proposed an algorithm, dubbed Score of ARIA Risk (SoAR), for quantifying risk. The algorithm assesses a patient's number of E4 alleles as well as the presence of any microhemorrhages in the brain before treatment begins. In the gantenerumab Phase 2 studies, these factors seemed to have independent, additive effects, while other characteristics, such as age, sex, race, and education, did not change ARIA risk. The algorithm takes into account the hazard ratio of each contributing factor. People with at least two risk factors, such as E4 homozygotes, or E4 heterozygotes with microhemorrhages, ran the highest risk of ARIA. The SoAR algorithm requires further validation, but potentially could help doctors make decisions about treating with anti-amyloid immunotherapy, Lyons suggested.

Can You Handle the Truth?
Before starting anti-amyloid therapy, physicians need to know their patients have plaques in the brain. Amyloid positivity is a requirement of both the AURs and the updated FDA label. Alas, data on how people will handle knowing their amyloid status are sparse, though two studies that have looked at this reported no signs of increased anxiety or depression after disclosure (Grill et al., 2020; Largent et al., 2020). 

In San Diego, several speakers presented data that strengthened the case for people taking this knowledge in stride. For example, Claire Erickson of the University of Wisconsin-Madison described a study of 101 cognitively healthy people with an average age of 72, many of whom had a family history of AD. They take part in longitudinal cognitive studies at UW and had undergone PiB PET scanning. After receiving training on the meaning of a positive and negative scan, they learned their results. Afterward, 88 percent said learning their status was useful; none expressed regrets.

Lindsay Clark at UW-Madison examined whether the knowledge changed these participants’ behavior. Before disclosure, all had received lifestyle counseling and set goals for making healthy changes, such as exercising more, eating better, improving sleep, and lowering stress. Six months later, 90 percent of participants had made some progress on these goals. The researchers found no difference in this progress between people who learned they had a positive and those who had a negative amyloid scan. The only difference in behavior between these two groups was that those with a positive scan reported slightly less social activity afterward, possibly indicating some withdrawal or fear of stigma.

“This can be empowering information,” Erickson said. However, she noted that this cohort was highly educated, informed, and engaged in research, hence was not representative of a general clinical population.

Other studies found study participants to be eager to learn biomarker results. Sara Feldman of the University of Michigan, Ann Arbor, described a cohort of 57 participant and partner pairs. Their average age was 74, they were racially diverse, and nearly half had amnestic MCI. In interviews, most said they wanted to learn their imaging, fluid, and genetic results, with 82 percent seeing no downside to doing so. Participants cited benefits such as the ability to participate in clinical trials, to make long-term care plans, and to adopt healthier habits. Of those who perceived negatives, most cited lack of treatment.

Likewise, Fred Ketchum of UW reported that in a telephone survey of 145 cognitively healthy African Americans in their mid-60s, 72 percent said they would be willing to tell their partner their amyloid scan results. Six percent expressed concerns about worrying their partner, another 6 percent feared social stigma (Ketchum et al., 2022). 

“People want this information,” said Annalise Rahman-Filipiak of UMich. She said it will be important to develop educational materials that explain what biomarker results mean, and to assess whether people with MCI and dementia are able to understand and make decisions based on those results. Many researchers in this field participate in the AGREEDementia working group, which develops best practices for risk disclosure. It remains to be seen how well these findings translate to general clinical use, where people are less familiar with medical research.

Gathering Real-World Data
Because many questions remain unanswered about how anti-amyloid immunotherapy will work in practice, the Alzheimer’s Association has brought together a collective to track the benefits and harms of these drugs, as well as those of future disease-modifying AD therapies. Dubbed ALZ-NET, the registry is hosted by the American College of Radiology, with the American Society of Neuroradiology and Brown University’s School of Public Health providing additional support and data analytics, respectively, and the Critical Path Institute helping ensure the registry's data pass regulatory muster (Nov 2021 conference news). ALZ-NET has three co-primary investigators: Rabinovici, Michael Rafii of USC, and Maria Carrillo of the Alzheimer’s Association.

In San Diego, Rafii said that the study’s protocol has been finished and approved, and the IT infrastructure, including electronic case report forms, is in place. The first seven clinics have signed on and are ready to start enrolling. They are Butler Hospital in Providence, Rhode Island; the Neurology Center of New England in Foxboro, Massachusetts; Abington Neurological Associates, Pennsylvania; Coastal Neurology in Port Royal, South Carolina; First Choice Neurology in Aventura, Florida; Neurostudies Inc. in Port Charlotte, Florida; and Genesis Neuroscience Clinic in Knoxville, Tennessee. These sites represent a range of different types of practice, including psychiatric, neurology, and geriatric, Rafii said. Most of this first group are private practices, but hospital and academic clinics are joining, as well. More sites are needed, and interested clinicians can apply online to sign up. ALZ-NET plans to expand internationally in time.

How will it work? Patients will enter the study when they agree to receive anti-amyloid immunotherapy at a participating clinic. Physicians will collect a slew of baseline data, including demographics, medical history, APOE genotype, lifestyle factors, AD symptoms and diagnostics, and brain imaging and fluid biomarkers. In order to compare data between participants, the study requires either the MMSE or MoCA for a cognitive, and the FAQ for a functional assessment; other tests, including the AD8 and NPI-Q, are optional.

Sites will enter follow-up data on each participant every six months for the first two years, and annually thereafter. Safety will be a major focus, including MRI findings, adverse events, and hospitalizations. Participants will also be followed with amyloid and tau PET and FDG-PET. Clinics will partner with imaging sites, which can offer recommendations on detecting and managing ARIA. Patients will stay in the study until they choose to withdraw, or die. Even if they stop immunotherapy, study personnel will continue to track their long-term health.

ALZ-NET aims to answer questions such as how the effects of immunotherapy change over years, who responds best, and how well the treatment works in a diverse real-world population. In the future, as more disease-modifying AD treatments are approved, the data will help compare effectiveness of different drug classes, Rabinovici said. Data will be shared with the research community through USC’s Laboratory of Neuro Imaging (LONI) and the Global Alzheimer’s Association Interactive Network (GAAIN). The registry will work with drug sponsors to gather data they need, for example for Coverage with Evidence Development studies required by the Centers for Medicare and Medicaid Services.

“This is a paradigm shift. ALZ-NET will bring AD care into the modern era,” Rabinovici said.—Madolyn Bowman Rogers

Comments

  1. While initially hailed as a breakthrough, the rocky road that Biogen’s Aduhelm has travelled echoes the political-like divide in our field between the adherents to amyloid-targeted therapies and those calling for a re-evaluation of the posited role Aβ plays in the Alzheimer’s disease pathogenesis story.

    As the first such agent to receive FDA approval, even if only “accelerated,” Aduhelm has greatly sharpened our collective wisdom regarding appropriate use, precautions, monitoring, and has raised critical questions such as duration of therapy (especially when we have biomarker confirmation of plaque elimination), clinically significant versus statistically significant effects, and so on.

    Having “facilitated the approval synapse,” we can expect more such agents to receive similar treatment by the FDA. In expectation of such, the Center for Medicare and Medicaid Services has spoken, and their conclusions were not agent-specific but class-specific. The recommended tests for patients intended to receive such therapies include biomarker confirmation to assure patients harbor the target of such therapy, and now APOE genotyping to more accurately assess individual risk of ARIA.

    Thankfully, there is sufficient data to suggest disclosure of such information to treatment-prospective patients can be done safely, although the wider effects on relatives and those ultimately deemed to not be treatment candidates (or those who begin and fail treatment) are less clear.

    While many advocate for new therapeutic strategies, amyloid-targeted monoclonal antibody therapies have reached a milestone and will be with us, so it is important for clinicians to understand their appropriate use and precautions. While my own hope lies in the search for other strategies, I agree with Ron Petersen’s advocacy for shared decision making with patients and families (Petersen, 2021). If a treatment has received FDA approval, we owe it to our patients to be responsible stewards of such treatment.

    References:

    . Aducanumab: What about the Patient?. Ann Neurol. 2021 Sep;90(3):334-335. Epub 2021 Aug 7 PubMed.

  2. It is ironic that while we hope antibodies will protect against Alzheimer’s disease, we are rejecting a logical alternative: preventive vaccines against AD. This denial is based on the predictably bad results obtained with poorly designed vaccines, the result of a questionable technology transfer from infectious and cancer vaccines to AD, which failed as expected. Vaccines for infectious diseases and cancer induce a strongly pro-inflammatory immunity that is damaging in the case of AD. Since all of the available adjuvants elicit only pro-inflammatory immunity, including alum, all of the AD vaccines are pro-inflammatory. Regardless of the claims. A proof was the AN1792 vaccine with QS-21, a compound I was responsible for developing. The problem with AN1792 was that it induced a highly damaging inflammatory response, which in some cases caused permanent brain damage.

    A hallmark of effectiveness in AD has been the reduction of plaque, which most vaccines did. But plaque is now accepted to be a protection mechanism, rather than AD’s cause. In fact, many cognitively normal elderly people have plaque without dementia. Studies have shown in animal models that human immunoglobulins avert the onset of AD. In fact, the first proof that antibodies protect against cytotoxic aberrant amyloid oligomers was obtained using antibodies from rabbits immunized with those oligomers. Hence, a critical requirement of AD vaccines is that the immunogen must be the toxic oligomers, to elicit production of antibodies against toxic conformational epitope(s). A response that peptides cannot deliver. Ironically, the AN1792 vaccine had the nearly correct immunogen, but with the wrong pro-inflammatory adjuvant. That is the main reason for its failure.

    That Aduhelm was obtained from the lymphocytes of a cognitively normal elderly person shows that people produce protective antibodies. These are lost due to the immune decline associated with aging, an adverse effect that may be resolved by using vaccines to boost immunity. A rational approach to this problem will be to correct past mistakes, rather than using them as arguments against well-designed new vaccines.

    Due to the cost of antibody therapy, and that only a few may afford it, we must contemplate the unpleasant possibility of a two-tier society, where those who can afford the cost will have a normal life, while the unlucky ones face the bleak possibility of in the future losing their minds. Hence, a rationally designed vaccine for AD may prevent/delay the onset of this disease. A cost-effective solution that will benefit the U.S. and the rest of the world.

    Moreover, vaccination will complement AD antibody therapy. As age progresses, vaccines loose some of their efficacy due to immuno-senescence. This drawback may be resolved by using passive immunotherapy with antibodies. Hence, the challenge is how, in an intelligent manner, can we reproduce our body’s immune surveillance mechanism to prevent/delay AD? The resources are there, the question is, are we willing to do it?

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References

Therapeutics Citations

  1. Aduhelm
  2. Donanemab
  3. Gantenerumab

News Citations

  1. Lecanemab: FDA Set Accelerated Approval Decision for January 2023
  2. Aducanumab Approved to Treat Alzheimer’s Disease
  3. Aducanumab: Will Appropriate-Use Recommendations Speed Uptake?
  4. Aduhelm Administration Remains a Trickle, ARIA a Concern
  5. Aduhelm Phase 3 Data: ARIA Is Common, Sometimes Serious
  6. Aduhelm Lowers Tau; Registry to Track Real-World Performance

Paper Citations

  1. . Aducanumab: Appropriate Use Recommendations Update. J Prev Alzheimers Dis. 2022;9(2):221-230. PubMed.
  2. . Short-term Psychological Outcomes of Disclosing Amyloid Imaging Results to Research Participants Who Do Not Have Cognitive Impairment. JAMA Neurol. 2020 Aug 10; PubMed.
  3. . Cognitively unimpaired adults' reactions to disclosure of amyloid PET scan results. PLoS One. 2020;15(2):e0229137. Epub 2020 Feb 13 PubMed.
  4. . What Influences the Willingness of Blacks and African Americans to Enroll in Preclinical Alzheimer's Disease Biomarker Research? A Qualitative Vignette Analysis. J Alzheimers Dis. 2022;87(3):1167-1179. PubMed.

Other Citations

  1. lecanemab

External Citations

  1. Fierce Biotech story
  2. AGREEDementia 
  3. ALZ-NET

Further Reading