One more step towards the end of recessive diseases

In the last century infant mortality has declined precipitously in the Western world, thanks in large part to the development of antibiotics and vaccination. Yet as the suffering and death from infectious disease has reduced, the burden from genetic disease has become proportionately greater: currently around 20% of all infant deaths in developed countries are a result of inherited Mendelian (single-gene) disorders.

What can be done to reduce this burden? Increasingly sophisticated methods for detecting disease in embryos during pregnancy will help, and these have recently taken another step forward with the development of accurate, non-invasive methods based on analysing foetal DNA in the blood of pregnant mothers (an article in the BMJ this week demonstrates the feasibility of this approach for a non-Mendelian disease, Down syndrome; and the same group showed late last year that this approach can also be applied to effectively any known disease-causing mutation). Yet these approaches detect disease after pregnancy has already begun.

Disease mutations can also be detected in embryos prior to implantation, for prospective parents undergoing IVF. But IVF remains an expensive, arduous and invasive procedure, and thus a weapon of last resort for most parents-in-waiting; as Armand Leroi notes drily in an exceptional 2006 article in EMBO Reports: "nature has contrived a cheap, easy and enjoyable way to conceive a child; IVF is none of these things." (While Leroi goes on to argue that the challenges of IVF are less severe for young couples with no fertility problems, it still seems fairly implausible that this will become the default mode of reproduction in the near future.)

However, for some classes of Mendelian disease it's possible to move the screening one step back. Recessive diseases are insidious things. The mutations that cause them lurk undetected - each of us carry perhaps 5 to 10 of them - as their carriers are protected by the presence of a healthy second copy of the affected gene. These mutations can thus wait silently for generation after generation, until a carrier is unlucky enough to fall for someone who carries the same mutation, or another mutation in the same gene. The children of such a couple will each have a 25% chance of inheriting one damaged copy of the gene from each parent and thus developing the disease.

The ability of a recessive mutation to pass silently from generation to generation means that many children born with recessive diseases have no family history. And while certain marriage practices (notably serial first-cousin marriage) can dramatically increase the risk of having a child with a recessive disease, these diseases can also explode into appearance in families with no obvious risk factors.

However, the fact that both parents must carry mutations in the same gene to pass a recessive disease to their children raises the possibility of detecting risk before a couple has even conceived children. For instance, one could screen both members of a couple for a panel of known mutations, an approach currently offered by US company Counsyl (disclaimer: my wife and I both accepted free tests from Counsyl in 2009). However, while a panel containing all known Mendelian mutations could detect a substantial fraction of all genetic disease (Leroi again), it can never eliminate the risk, because many Mendelian mutations remain undiscovered. However, one could go one step further: rather than simply look for known mutations, one could examine the entire sequence of all genes known to be associated with Mendelian diseases, and thus identify new mutations lurking in the same gene.

In an article published today in Science Translational Medicine a group of US researchers describe a high-throughput approach for doing precisely that.

Rather than review the technical aspects of the paper in great detail, I'll just hit the main points I took from it:

  • The 448 genes selected for the screening panel are the product of walking a political tightrope. While the authors indicate that the marginal costs of adding extra sequence mean that the optimal cost-benefit ratio comes from including a very broad range of diseases, they have excluded diseases that might trigger controversy (such as deafness and adult-onset disorders).
  • The authors do a commendable job of comparing multiple technologies for capturing disease genes and for sequencing the captured DNA; the final product is a combination of Agilent SureSelect for sequence capture and Illumina HiSeq for sequencing.
  • This approach allowed them to detect ~95% of the genetic variants in their target genes with very high accuracy. In other words, they might miss around 5% of disease-causing mutations in these genes, but the ones they find are probably real.
  • Perhaps the single most important message from the paper, which I hope to expand on in a future post, is that disease mutations reported in the literature are depressingly enriched for false positives. The authors suggest that 27% of mutations in their samples that overlap with entries the largest database, the Human Gene Mutation Database, turned out to be the result of sequencing errors or mistakes in the literature (e.g. common polymorphisms that have been falsely reported to be disease-causing).
  • The researchers found that the 104 sequenced samples contained on average 2.8 known disease-causing mutations in the surveyed genes. This fits with expectations: each of us is likely walking around with 5-10 of these severe disease-causing variants in total, which we will only know about if (1) we get our genomes sequenced, or (2) we're unlucky enough to have children with a partner who carries mutations in the same gene.
  • The authors estimate the cost of their test at $378, which they note is "approximating that expended on treatment of severe recessive childhood disorders per U.S. live birth". In other words, offering this type of screen across the US population as a whole would be roughly cost-neutral from a healthcare stand-point, while simultaneously reducing the number of children dying from genetic diseases.

Given the plummeting costs of sequencing and the economies of scale, the cost-benefit ratio for this type of screening panel will continue to drop. In this context it seems inevitable that some form of sequencing approach will ultimately be implemented as routine for young parents-to-be.

That's not to say there aren't challenges ahead: obviously the current implementation misses ~5% of disease-causing mutations in the targeted genes (although this will improve with better sequence capture technology), and the panel of targeted genes needs to increase. But the largest obstacle that needs to be overcome is predicting the probability of disease causation for novel genetic variants uncovered by these screens: if two potential parents both carry rare protein-altering mutations in the same gene, but those mutations have never been seen in actual disease patients, what advice can we provide? Tools for predicting likely functional impact based on protein structure and evolutionary conservation are a start, but remain in their infancy; this is, I suspect, the challenge that needs to be faced up to by geneticists over the next five years.
Another key road-block is a social one: engineering the systems required to explain the results from these tests to large numbers of people, most of whom have very little understanding of genetics. The medical system is currently entirely unequipped to cope with an influx of this type of genetic data; yet cope it must, as the wave is coming fast.

Finally, the media coverage of this study has predictably stirred up the standard ethical and religious objections; these make for interesting dinner party conversation, but are largely irrelevant in any practical sense. Parents, as a group, will simply do whatever it takes to increase the probability that their children will be born healthy. Armand Leroi conveys this point well in the 2006 article mentioned above:

These abortions are eugenic in both intention and effect--that is, their purpose is to eliminate a genetically defective fetus and thus allow for a genetically superior child in a subsequent pregnancy. This is a harsh way of phrasing it; another way is to say that parents just want to have healthy children. Nevertheless, however it is phrased, the conclusion is starkly unavoidable: terminating the pregnancy of a genetically defective fetus is widespread. Moreover, because none of the countries mentioned above coerce parents into aborting deformed fetuses, these abortions--which number many thousands each year--are carried out at the request of the parents, or at least the mothers. This high number of so-called medical abortions shows that many people, in many parts of the world, consider the elimination of a genetically defective fetus to be morally acceptable.

Protests from ethicists and ministers may lead to some entertaining talk radio discussions, but ultimately the desire of parents for healthy children will sweep aside all objections (just as moral objections to tissue transplants and IVF were swept aside for similarly pragmatic reasons). In the face of this implacable tide I find it difficult to get too engaged in the moral debates on these issues; they just seem like a waste of time.

In closing: this is a commendable study, and offers a taste of what is to come. Carrier screening will be one of the first genomic technologies to really provide medical utility in a population health sense. It's important not to minimise the technical and logistical challenges ahead, but it seems inevitable that this approach will begin to be adopted on a population scale in the near future. And while noise and fury from critics on both the left and the right is similarly inevitable, the bottom line is simple: this technology will mean fewer children dying in pain, and all the moral outrage in the world won't drown that out.

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re: what you point out as depressingly high false positive - in the screening community that's actually considered a good thing - you'd rather have false positives (which you can reconfirm by targeted sequencing/whatever) than false negatives.

Hi Jon,

In the specific "depressingly high" example in my post, the problem is that these are (mostly) artefacts in the literature rather than in your own experiment, so they're harder to untangle.

I can't help but wonder how many kids have been given a false diagnosis based on these artefacts; perhaps it's a small number, but I'm sure it's not zero.

Forgot to say: fair point about FPs vs FNs in screening (although obviously if the FP rate is way too high, or if you need to do an invasive assay for follow-up - as in Down syndrome - you're in trouble).

Yeah, the tolerance for FPs is more in the newborn screening arena rather than carrier screening.

Protests from ethicists and ministers may lead to some entertaining talk radio discussions, but ultimately the desire of parents for healthy children will sweep aside all objections (just as moral objections to tissue transplants and IVF were swept aside for similarly pragmatic reasons). In the face of this implacable tide I find it difficult to get too engaged in the moral debates on these issues; they just seem like a waste of time.

The excellent EMBO paper you cite ends in a much more nuanced way - that the morality of the issue is important, simply a scientist has no privileged contribution to make:

Some readers might find it peculiar that in this discussion of neo-eugenics, I have not considered the ethical or legal implications with which this subject is generally considered to be fraught. Although I do not doubt their importance, I simply have no particular knowledge of them. Peter Medawar put it best 40 years ago: âIf the termination of a pregnancy is now in question, scientific evidence might tell us that the chances of a defective birth are 100 percent, 50 percent, 25 percent, or perhaps unascertainable. The evidence is highly relevant to the decision, but the decision itself is not a scientific one, and I see no reason why scientists as such should be specially well-qualified to make itâ

I would assume that with so much allelic heterogeneity and the difficulty in separating pathogenic variants from benign variants at many loci, this approach is going to be a bit dicey for some time. In time, most of these ambiguities will be clarified and this analysis will be very useful.

Another key road-block is a social one: engineering the systems required to explain the results from these tests to large numbers of people, most of whom have very little understanding of genetics. The medical system is currently entirely unequipped to cope with an influx of this type of genetic data; yet cope it must, as the wave is coming fast.

You're right, but on the bright side I think that interpreting results for common multigenic diseases would be much more difficult for medical doctors. I believe this is a great step towards the end of recessive diseases, as you say. Regarding eugenics, the word frightens more than its meaning.

Hi Neil,

The excellent EMBO paper you cite ends in a much more nuanced way - that the morality of the issue is important, simply a scientist has no privileged contribution to make

I'm not saying the moral issues here aren't important in a metaphysical sense (although, like Leroi, I don't have the background to contribute usefully to that discussion), just that they'll have very little practical impact on whether or not these technologies are adopted. If you think that there are moral objections that will be sufficient to overcome the parental desire to have healthy children and thus halt adoption of carrier testing, however, I'd be very interested to hear your argument.

Hi Daniel

I suppose I see morality as a practical subject for all, rather than a topic just for the philosophers. However, I agree that there is no requirement to engage with any and everybody on a topic, especially if you can see that the answer is pre-judged.

As it is in this case.

In the UK, there is already a national antenatal screening programme looking at fetal abnormalities, and a newborn programme looking at "phenylketonuria (PKU), congenital hypothyroidism (CHT), sickle cell disease (SCD), cystic fibrosis (CF) and medium-chain acyl-CoA dehydrogenase deficiency (MCADD)" i.e. already including some recessive disorders for which from-birth treatments are indicated - see http://www.screening.nhs.uk/policydb.php for a full list of all programmes considered.

Extension to carrier testing "merely" requires it to pass the usual screening criteria - http://www.screening.nhs.uk/criteria - the most relevant of which are:

  • 4. If the carriers of a mutation are identified as a result of screening the natural history of people with this status should be understood, including the psychological implications.
  • 9. If the test is for mutations the criteria used to select the subset of mutations to be covered by screening, if all possible mutations are not being tested, should be clearly set out.
  • 14. There should be evidence that the complete screening programme (test, diagnostic procedures, treatment/ intervention) is clinically, socially and ethically acceptable to health professionals and the public.
  • 15. The benefit from the screening programme should outweigh the physical and psychological harm (caused by the test, diagnostic procedures and treatment).
  • 19. Adequate staffing and facilities for testing, diagnosis, treatment and programme management should be available prior to the commencement of the screening programme.
  • 22. If screening is for a mutation the programme should be acceptable to people identified as carriers and to other family members.

I'm sure somewhere this is being put together as a proposal right now.

Hi Neil,

That last criterion is extremely interesting, as it could allow current disease patients to block the widespread adoption of testing to eliminate that disease. This seems like a pretty good example of a case where the desires of parents will clash with the suggestions of ethicists: from a parent's perspective, why should a current sufferer of a disease be able to prevent me from doing my best to have healthy children?

In addition, it's unclear to me whether you're suggesting that these criteria for providing an NHS-funded screening programme should also be extended to decisions about whether or not to permit a commercial entity from offering carrier screening to UK citizens. And if so, if the data aren't yet available to satisfy all of the criteria, should these tests be banned?

Daniel @10

That last criterion is extremely interesting, as it could allow current disease patients to block the widespread adoption of testing to eliminate that disease.

You mean for things that some think of as a disease and many do not? - like:

"Deaf demand right to designer deaf children"
http://www.timesonline.co.uk/tol/news/uk/health/article3087367.ece

I think the section may have arisen from the early history of compulsory sickle cell testing in the US - this from http://www.scienceprogress.org/2008/05/a-brief-history-of-genetic-testi…

Sickle cell testing between 1970 and 1972 was mandatory in 12 states and targeted African-Americans. Misunderstanding was rampant, perhaps because the term âsickle cell traitâ for carriers suggested that their condition was somehow visible. What they carried was stigma. At the time, the disease could not be prevented, tested for before birth, or treated. So why identify carriers?

This seems like a pretty good example of a case where the desires of parents will clash with the suggestions of ethicists: from a parent's perspective, why should a current sufferer of a disease be able to prevent me from doing my best to have healthy children?

I think this is saying no such thing - merely that the NHS will not attempt to roll out a national program if there is serious opposition to it.

In addition, it's unclear to me whether you're suggesting that these criteria for providing an NHS-funded screening programme should also be extended to decisions about whether or not to permit a commercial entity from offering carrier screening to UK citizens.

No. Like many here, I believe that genetic testing should be registered and regulated to keep the bottom-feeders out of the market, but I was mainly responding to your suggestion that carrier testing would become "routine" once the price came down and the utility goes up - it needs more than that.

And if so, if the data aren't yet available to satisfy all of the criteria, should these tests be banned?

In my view, no. What we're facing is a lack of data, not ethical roadblocks.