# Assessing Agreement between miRNA Microarray Platforms

^{*}

## Abstract

**:**

## 1. Introduction

## 2. Experimental Section

#### 2.1. Samples

^{©}Human Total RNA Survey Panel, (Ambion Inc, Austin, TX, USA). RNA material was analyzed in different laboratories, as follows: Affymetrix processing took place at the Biomedical Technologies Institute of the University of Milan (Segrate, Italy); Illumina and Agilent processing were performed at the Department of Experimental Oncology of the National Cancer Institute (Milan, Italy). For both samples, three technical replicates for each platform were performed, leading to a total of 18 arrays, six for each different microarray platform.

#### 2.2. Sample Preparation and Hybridization

^{©}Scanner 3000 7G to acquire fluorescent images of each array and analyzed by use of GeneChip Operating Software (GCOS, version 1.2).

#### 2.3. Data Pre-Processing

#### 2.3.1. Affymetrix GeneChip^{©} miRNA Array

^{©}miRNA QC Tool software (Version 1.0.33.0) to quantify the signal value. Quality control (QC) was assessed by plotting the average intensity of the oligo spike-in and background probe sets (included in the control target content) across all of the arrays. According to Genisphere, oligo spike-in 2, 23, 29, 31 and 36 probe sets should present a value of more than 1000 intensity units to accept array quality. The miRNA arrays were detected using the Affymetrix detection algorithm, based on the non-parametric Wilcoxon rank-sum test, applied independently on each array and probe/probe set; a p-value greater than 0.06 stands for “not detected above background” [19]. For data normalization, the “default” method was used, obtaining log2 expression values (expression values data matrix) from the raw data (intensity values data matrix). Briefly, this method involved the following three steps: grouping the background probes intensities based on GCcontent, where the median intensity of each bin was the correction value for each probe with the same GC content; a quantile normalization and, finally, a median polish summarization. To obtain a single intensity value for each miRNA mapped on the log2 array, intensity measures for replicated spots were averaged.

#### 2.3.2. Agilent Human miRNA Microarray (V1)

#### 2.3.3. Illumina HumanMI_V2

#### 2.3.4. miRNA Selection and Normalization

#### 2.4. Statistical Analysis

#### 2.4.1. Intra-Platform Reliability

#### 2.4.2. Between-Platform Agreement

**(a)****No bias:**(${a}_{0}$ = 0, ${b}_{0}$ = 1)$$\Delta =\left(-{t}_{1-\alpha /2,n-1}\sqrt{1+\lambda}{\widehat{\sigma}}_{\delta},+{t}_{1-\alpha /2,n-1}\sqrt{1+\lambda}{\widehat{\sigma}}_{\delta}\right)$$**(b)****Fixed bias:**(${a}_{0}$≠ 0, ${b}_{0}$ = 1)$$\Delta =\left({a}_{0}-{t}_{1-\alpha /2,n-1}\sqrt{1+\lambda}{\widehat{\sigma}}_{\delta},{a}_{0}+{t}_{1-\alpha /2,n-1}\sqrt{1+\lambda}{\widehat{\sigma}}_{\delta}\right)$$**(c)****Proportional bias:**(${a}_{0}$ = 0, ${b}_{0}\ne $ 1)$$\Delta =\left(\left({b}_{0}-1\right){X}_{i}-{t}_{1-\alpha /2,n-1}\sqrt{1+\lambda}{\widehat{\sigma}}_{\delta},\left({b}_{0}-1\right){X}_{i}+{t}_{1-\alpha /2,n-1}\sqrt{1+\lambda}{\widehat{\sigma}}_{\delta}\right)$$**(d)****Fixed and Proportional bias:**( ${a}_{0}\ne $ 0, ${b}_{0}\ne $ 1)$$\Delta =\left({a}_{0}+\left({b}_{0}-1\right){X}_{i}-{t}_{1-\alpha /2,n-1}\sqrt{1+\lambda}{\widehat{\sigma}}_{\delta},{a}_{0}+\left({b}_{0}-1\right){X}_{i}+{t}_{1-\alpha /2,n-1}\sqrt{1+\lambda}{\widehat{\sigma}}_{\delta}\right)$$

## 3. Results and Discussion

#### 3.1. Data Description

^{©}miRNA Array, Agilent Human miRNA Microarray (V1) and Illumina humanMI_V2). MiRNA selection described in the Experimental Section, resulted in a total of 813 human miRNAs considered for analysis, which account for 95.99% of human miRNAs on Affymetrix platforms, 95.53% on Agilent and 94.76% on Illumina (see Figure 1). Pairwise intersections of human miRNA lists revealed that the larger overlap occurred when Affymetrix and Agilent were considered (830 miRNAs, 97.99% of Affymetrix hsaand 97.53% of Agilent hsa), whereas Illumina showed a slightly poorer degree of overlap with both Affymetrix (817 miRNAs, 96.46% of Affymetrix and 95.22% of Illumina) and Agilent (815 miRNAs, 95.77% of Agilent and 94.99% of Illumina).

Affymetrix | Agilent | Illumina | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|

Sample | Array | 25th | 50th | 75th | IQR | 25th | 50th | 75th | IQR | 25th | 50th | 75th | IQR |

1 | 4.907 | 5.044 | 5.592 | 0.685 | 3.415 | 3.911 | 5.804 | 2.389 | 6.821 | 8.830 | 10.772 | 3.951 | |

hREF | 2 | 4.943 | 5.066 | 5.570 | 0.627 | 3.366 | 3.955 | 5.998 | 2.632 | 7.168 | 9.150 | 11.015 | 3.847 |

3 | 4.943 | 5.087 | 5.615 | 0.672 | 3.449 | 4.065 | 6.242 | 2.793 | 7.103 | 9.117 | 10.907 | 3.804 | |

1 | 5.160 | 5.285 | 5.508 | 0.348 | 3.139 | 3.432 | 4.065 | 0.926 | 5.492 | 6.863 | 8.782 | 3.290 | |

A498 | 2 | 5.375 | 5.524 | 5.827 | 0.452 | 3.066 | 3.448 | 4.287 | 1.221 | 5.606 | 6.973 | 8.942 | 3.336 |

3 | 5.468 | 5.651 | 5.983 | 0.515 | 2.690 | 3.175 | 3.988 | 1.298 | 5.812 | 7.294 | 9.246 | 3.433 |

**Figure 2.**Box and density plots for both samples. The left column refers to hREF and the right column to A498. Plots refer to non-normalized log2-transformed data. (

**Lower panels**) Solid lines represent the technical replicate labeled as 1 in the datasets, whereas dashed lines and dotted lines represent technical Replicate 2 and 3, respectively.

#### 3.2. Intra-Platform Reliability

**Table 2.**CCC and Overall CCC with bootstrap 95%CI (common miRNAs) CCCs and the OCCC were computed on the 813 miRNAs common across all platforms considered for the study, and bootstrap 95%CI for the Overall Concordance Correlation Coefficient were computed using 1000 bootstrap samples and the percentile method [32].

Affymetrix | Agilent | Illumina | ||||||||
---|---|---|---|---|---|---|---|---|---|---|

Sample | Pair | CCC | OCCC | CI 95% | CCC | OCCC | CI 95% | CCC | OCCC | CI 95% |

1-2 | 0.988 | 0.997 | 0.991 | |||||||

hREF | 1-3 | 0.993 | 0.992 | (0.990–0.993) | 0.989 | 0.994 | (0.993–0.995) | 0.993 | 0.994 | (0.994–0.995) |

2-3 | 0.994 | 0.995 | 0.999 | |||||||

1-2 | 0.935 | 0.975 | 0.996 | |||||||

A498 | 1-3 | 0.888 | 0.927 | (0.906–0.941) | 0.970 | 0.975 | (0.969–0.979) | 0.981 | 0.989 | (0.987–0.991) |

2-3 | 0.961 | 0.978 | 0.989 |

**Table 3.**Concordance correlation coefficient (CCC) and overall CCC with bootstrap 95% CI (detection call filtering). CCCs and the OCCC were computed on the 347 miRNAs common across Illumina and Agilent platforms after detection call filtering (present on at least three samples), and bootstrap 95% CI for the overall CCC were computed using 1000 bootstrap samples and the percentile method [32].

Agilent | Illumina | ||||||
---|---|---|---|---|---|---|---|

Sample | Pair | CCC | OCCC | CI 95% | CCC | OCCC | CI 95% |

1-2 | 0.996 | 0.988 | |||||

hREF | 1-3 | 0.978 | 0.989 | (0.987–0.990) | 0.994 | 0.993 | (0.992–0.994) |

2-3 | 0.992 | 0.998 | |||||

1-2 | 0.974 | 0.997 | |||||

A498 | 1-3 | 0.988 | 0.983 | (0.979–0.986) | 0.987 | 0.992 | (0.990–0.994) |

2-3 | 0.986 | 0.992 |

#### 3.3. Between-Platform Agreement

${a}_{0}$ | ${b}_{0}$ | ||||
---|---|---|---|---|---|

Sample | Pair | Estimate | CI 95% | Estimate | CI 95% |

Agilent vs. Affymetrix | −6.1037 | (−6.4471, −5.7603) | 1.9610 | (1.8964, 2.0255) | |

hREF | Illumina vs. Affymetrix | −4.7630 | (−5.5006, −4.0254) | 2.4418 | (2.3472, 2.5363) |

Illumina vs. Agilent | 3.6033 | (3.3791, 3.8274) | 1.0925 | (1.0371, 1.1479) | |

Agilent vs. Affymetrix | −14.2358 | (−16.3792, −12.0923) | 3.1409 | (2.9815, 3.3004) | |

A498 | Illumina vs. Affymetrix | −17.4064 | (−18.6406, −16.1722) | 4.2889 | (4.1679, 4.4098) |

Illumina vs. Agilent | 2.1916 | (1.7773, 2.6058) | 1.3254 | (1.2407, 1.4100) |

**Figure 3.**Agreement intervals for line hREF, $\lambda =1$. (

**A**) The comparison Agilent-Affymetrix; (

**B**) the comparison Illumina-Affymetrix; and (

**C**) Illumina-Agilent. The samples/miRNAS have been plotted in ascending order according to their value on the second platform in the y-axis label, so that the x-axis only contains a progressive value from one to 813 according to such ordering.

**Figure 4.**Agreement intervals for line A498, $\lambda =1$. (

**A**) The comparison Agilent-Affymetrix; (

**B**) the comparison Illumina-Affymetrix; and (

**C**) Illumina-Agilent. The samples/miRNAs have been plotted in ascending order according to their value on the second platform in the y-axis label, so that the x-axis only contains a progressive value from one to 813 according to such ordering.

**Table 5.**Estimates of λ and CI 95%. Values were obtained as the ratio of ${\sigma}_{\u03f5}^{2}$ (error variance of Y) and ${\sigma}_{\delta}^{2}$ (error variance of X), estimated via random effects models.

Sample | Pair | λ | CI 95% |
---|---|---|---|

Agilent-Affymetrix | 2.608 | 2.409–2.824 | |

hREF | Illumina-Affymetrix | 2.935 | 2.711–3.178 |

Illumina Agilent | 1.125 | 1.039–1.218 | |

Agilent-Affymetrix | 4.125 | 3.810–4.466 | |

A498 | Illumina-Affymetrix | 5.576 | 5.150–6.037 |

Illumina-Agilent | 1.352 | 1.248–1.463 |

${a}_{0}$ | ${b}_{0}$ | ||||
---|---|---|---|---|---|

Sample | Pair | Estimate | CI 95% | Estimate | CI 95% |

Agilent vs. Affymetrix | −7.3495 | (−8.1460, −6.5529) | 2.1806 | (2.0824, 2.2789) | |

hREF | Illumina vs. Affymetrix | −7.0221 | (−9.3909, −4.6533) | 2.8402 | (2.6707, 3.0096) |

Illumina vs. Agilent | 3.4477 | (3.2018, 3.6936) | 1.1235 | (1.0655, 1.1816) | |

Agilent vs. Affymetrix | −12.4128 | (−12.9575, −11.8681) | 2.8265 | (2.7461, 2.9068) | |

A498 | Illumina vs. Affymetrix | −20.3938 | (−29.7127, −11.0749) | 4.8042 | (4.4718, 5.1366) |

Illumina vs. Agilent | 1.5756 | (0.9998, 2.1514) | 1.4804 | (1.3806, 1.5802) |

**Figure 5.**Agreement intervals for line hREF, λ estimated. (

**A**) The comparison Agilent-Affymetrix; (

**B**) the comparison Illumina-Affymetrix; and (

**C**) Illumina-Agilent. The samples/miRNAs have been plotted in ascending order according to their value on the second platform in the y-axis label, so that the x-axis only contains a progressive value from one to 813 according to such ordering.

**Figure 6.**Agreement intervals for line A498, λ estimated. (

**A**) The comparison Agilent-Affymetrix; (

**B**) the comparison Illumina-Affymetrix; and (

**C**) Illumina-Agilent. The samples/miRNAs have been plotted in ascending order according to their value on the second platform in the y-axis label, so that the x-axis only contains a progressive value from one to 813 according to such ordering.

**Table 7.**miRNA in agreement between arrays. Number (n) and proportion (%) of miRNAs lying in the different agreement intervals, estimated according to the measurement error model parameters estimated by setting λ = 1 and by estimating it via random effects models. Confidence intervals for the proportions were computed using the Clopper–Pearson exact method [39].

$\lambda =1$ | λ Estimated | ||||
---|---|---|---|---|---|

Sample | Comparison | $\%\phantom{\rule{0.277778em}{0ex}}(CI95\%)$ | n | $\%\phantom{\rule{0.277778em}{0ex}}(CI95\%)$ | n |

Agilent-Affymetrix | 82.53 (79.75–85.08) | 671 | 84.26 (81.57–86.70) | 685 | |

hREF | Illumina–Affymetrix | 82.78 (80.01–85.31) | 673 | 89.91 (87.64–91.90) | 731 |

Illumina-Agilent | 97.79 (96.52–98.68) ^{†} | 795 | 97.54(96.23–98.49) ^{†} | 793 | |

Agilent-Affymetrix | 74.17 (71.02–77.15) | 603 | 78.84 (75.87–81.60) | 641 | |

A498 | Illumina-Affymetrix | 56.46 (52.97–59.90) | 459 | 73.43 (70.25–76.44) | 597 |

Illumina-Agilent | 95.45 (93.78–96.78) | 776 | 96.31 (94.77–97.50) | 783 |

^{†}: the platform pair is in agreement.

## 4. Conclusions

**Figure 7.**Measurement error model fit. The red line represents fitted values of the measurement error model and green crosses represent miRNAs not in agreement after bias correction. For simplicity, we represent the model fit for $\lambda =1$ separately for line A498 (

**A**) and hREF (

**B**).

## Supplementary Files

Supplementary File 1## Acknowledgments

## Author Contributions

## Conflicts of Interest

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Bassani, N.P.; Ambrogi, F.; Biganzoli, E.M.
Assessing Agreement between miRNA Microarray Platforms. *Microarrays* **2014**, *3*, 302-321.
https://doi.org/10.3390/microarrays3040302

**AMA Style**

Bassani NP, Ambrogi F, Biganzoli EM.
Assessing Agreement between miRNA Microarray Platforms. *Microarrays*. 2014; 3(4):302-321.
https://doi.org/10.3390/microarrays3040302

**Chicago/Turabian Style**

Bassani, Niccolò P., Federico Ambrogi, and Elia M. Biganzoli.
2014. "Assessing Agreement between miRNA Microarray Platforms" *Microarrays* 3, no. 4: 302-321.
https://doi.org/10.3390/microarrays3040302