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Italian Team Developing Nanopore Sequencing, Droplet Digital PCR Test to Monitor Residual Disease

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SAN FRANCISCO (GenomeWeb) – Nanopore sequencing in combination with droplet digital PCR can be used to identify minimal residual disease in some leukemia patients, according to researchers at the University of Bari in Italy.

The researchers developed two pipelines to identify and quantify the genomic rearrangement BCR-ABL1 that is characteristic of chronic myeloid leukemia — one based on fluorescence in situ hybridization followed by droplet digital PCR and another based on Oxford Nanopore Technologies' MinIon followed by ddPCR. In a study published this month in Oncotarget, the team demonstrated that in 10 patients who had been recently diagnosed with CML, they could identify the breakpoint sequence in the BCR-ABL1 rearrangement using either FISH or amplicon sequencing on the MinIon, and then quantify the number of cells containing that rearrangement using ddPCR.

Francesco Albano, senior author of the study and an assistant professor of hematology at the University of Bari, said that his group is now working on developing the MinIon/ddPCR pipeline into a clinical test to monitor for disease recurrence in CML patients who are in remission.

Currently, minimal residual disease for CML patients is typically monitored using real-time quantitative PCR, but often leukemic stem cells with the BCR-ABL1 rearrangement are present below the limit of detect of RT-qPCR, according to the researchers. So, the group wanted to develop a more sensitive approach for monitoring patients.

While DNA-based approaches have previously been shown to be more sensitive, the researchers noted that identifying the breakpoint of the BCR-ABL1 rearrangement can be challenging because it is highly repetitive. In addition, many diagnostic laboratories do not have next-generation sequencing capabilities.

Albano said that the team wanted to design assays "exploiting new, cheap, fast, and innovative strategies, such as the MinIon and ddPCR." In addition, he said, since many labs already have experience using FISH, the group included a second pipeline that relied on FISH, rather than MinIon. That pipeline is "more laborious," he said, "but generally already adopted in laboratories specialized in CML patient monitoring."

In the study, the researchers designed amplicons to span the BCR-ABL1 junction for 10 patients and then barcoded and sequenced them on the MinIon. Sequencing took around 24 hours and generated more than 21,000 reads. Average sequencing depth was 400x and the error rate around 8 percent. For all 10 patients, MinIon sequencing was able to identify the breakpoint and was concordant with Sanger sequencing.

Next, the team used ddPCR to quantify the number of cells that contained the rearrangement. For each patient, they designed a personalized assay based on the sequence of the BCR-ABL1 region. At diagnosis, a median of 87 percent of the patients' cells contained the rearrangement. The researchers also evaluated sixteen samples at 6, 12, and 15 months from diagnosis. Results from the ddPCR assay were consistent with RT-qPCR in all but one case, and the authors noted that the ddPCR assay was "was more sensitive" for "detecting residual disease" than RT-qPCR.

Chia-Lin Wei, director of genome technologies at the Jackson Laboratory who was not involved with the study but who has been using the MinIon to characterize structural variants in cancer genomes, said that the study demonstrated a "very suitable application for nanopore sequencing." She noted that although the MinIon does not yet have the accuracy to evaluate somatic point mutations in a diagnostic setting, sequencing through translocations "is a very ideal type of data" for the system. She added that the MinIon's long reads are particularly valuable since they enable the entire region to be sequenced through in one read, which is important because "breakpoint location can vary patient to patient."

Wei added that combining the MinIon analysis with ddPCR was also a good use of both technologies, since the MinIon could provide a qualitative measurement —yes, the rearrangement is there, or no, it is not — while ddPCR could provide a quantitative measurement of how many cells contained the alteration.

In theory, sequencing on the MinIon could also provide the quantitative information. However, for clinical use, she said that it may not yet have the technical robustness to do so, while ddPCR is "probably one of the best quantitative methods," she said.

Another important factor, Wei added, is that the MinIon has a small footprint and using it is not as technically challenging compared to other NGS instruments

"For a clinician who's never done sequencing, there will still be a learning curve," she said, but, "relatively, it's pretty easy to use."

Albano said the lab's next step is to use the MinIon/ddPCR assay to monitor CML patients who have stopped therapy because their disease is no longer detectable. Such an assay would cost around $400, he estimated, including around $100 to detect the breakpoint sequence using the MinIon and then $300 to monitor the patient via ddPCR.

His group has also published two other studies using the MinIon in a clinical setting for hematological malignancies, including one in which the group used the MinIon to look at mutations in the TP53 gene of chronic lymphocytic leukemia patients and another in which they evaluated BCR-ABL1 rearrangements in CML patients who had developed treatment resistance.

Albano said that these other applications are currently in an "experimental phase," and the group is "comparing MinIon results to standardized NGS platform data." He added that the technology is quickly improving with new sequencing chemistries, which he anticipated would lead to "the improvement and implementation of nanopore-based technology in routine laboratory procedures."