Iodinated contrast dye–diluent combination exhibits longer time to full dye saturation compared to lidocaine, bupivacaine, and water in porcine cadaveric nervous tissue

Victoria Albano Department of Clinical Sciences, Cornell University, Ithaca, NY

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Stephanie Hon Department of Clinical Sciences, Cornell University, Ithaca, NY

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Stephen Parry Cornell Statistical Consulting Unit, Cornell University, Ithaca, NY

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Cristina de Miguel Garcia Department of Clinical Sciences, Cornell University, Ithaca, NY

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 DVM, MSc, DECVAA

Abstract

OBJECTIVE

Dye-diluent combinations have different nerve-staining behavior, making locoregional cadaveric dye study findings difficult to compare. The objective of this study was to quantify the effect of 4 diluents on nerve color saturation when used in combination with commercial food dye.

METHODS

48 unpreserved brachial plexus nerves were randomized into 4 diluent groups. Lidocaine, bupivacaine, iodinated contrast, and sterile water were combined with commercial food dye (10:1), and prosected nerves were immersed in one of these groups for 1, 15, 30, or 60 minutes. Images at baseline and at each timepoint were processed using ImageJ. Color saturation was divided into quartiles (dark, medium dark, medium light, or light). The percentage of nerve area stained in each quartile was compared using a 2-way ANOVA and post hoc Tukey test.

RESULTS

At 1 minute, water and bupivacaine had a higher percentage of area of dark saturation compared to contrast. At 15 and 30 minutes, dark and medium-dark saturation percentages of area were also larger in lidocaine, bupivacaine, and water compared to contrast. There were no differences in saturation percentages of areas between groups at 60 minutes. Within groups, all diluents had darker percentages of area saturation at 15, 30, and 60 minutes compared to minute 1.

CONCLUSIONS

In porcine nerves, the staining profiles of 2% lidocaine, 0.5% bupivacaine, and sterile water combined withcommercial food dye appear similar and may be used interchangeably after 15 minutes of exposure. When using iodinated contrast, exposures over 60 minutes yield comparable results to other diluents.

CLINICAL RELEVANCE

Diluents contribute to heterogeneous nerve-staining behavior and should be considered when comparing study outcomes. If contrast is used as the diluent in cadaveric studies with postoperative imaging, researchers should be aware of the significant delay to reach a saturation level comparable to other diluent combinations.

Abstract

OBJECTIVE

Dye-diluent combinations have different nerve-staining behavior, making locoregional cadaveric dye study findings difficult to compare. The objective of this study was to quantify the effect of 4 diluents on nerve color saturation when used in combination with commercial food dye.

METHODS

48 unpreserved brachial plexus nerves were randomized into 4 diluent groups. Lidocaine, bupivacaine, iodinated contrast, and sterile water were combined with commercial food dye (10:1), and prosected nerves were immersed in one of these groups for 1, 15, 30, or 60 minutes. Images at baseline and at each timepoint were processed using ImageJ. Color saturation was divided into quartiles (dark, medium dark, medium light, or light). The percentage of nerve area stained in each quartile was compared using a 2-way ANOVA and post hoc Tukey test.

RESULTS

At 1 minute, water and bupivacaine had a higher percentage of area of dark saturation compared to contrast. At 15 and 30 minutes, dark and medium-dark saturation percentages of area were also larger in lidocaine, bupivacaine, and water compared to contrast. There were no differences in saturation percentages of areas between groups at 60 minutes. Within groups, all diluents had darker percentages of area saturation at 15, 30, and 60 minutes compared to minute 1.

CONCLUSIONS

In porcine nerves, the staining profiles of 2% lidocaine, 0.5% bupivacaine, and sterile water combined withcommercial food dye appear similar and may be used interchangeably after 15 minutes of exposure. When using iodinated contrast, exposures over 60 minutes yield comparable results to other diluents.

CLINICAL RELEVANCE

Diluents contribute to heterogeneous nerve-staining behavior and should be considered when comparing study outcomes. If contrast is used as the diluent in cadaveric studies with postoperative imaging, researchers should be aware of the significant delay to reach a saturation level comparable to other diluent combinations.

Accurate and precise localization of a target nerve is an essential methodological step in the development of new locoregional techniques. After dissection of the appropriate anatomical landmarks, investigators perform preliminary nerve dye studies in cadaveric models before clinical trials on live patients. In these studies, the site of the target nerve is dissected and visually inspected after injection for saturation of neural tissue with dye, with success determined by subjective confirmation of dye saturation encompassing at least 1 cm of nerve length circumferentially. This distance corresponds to 3 nodes of Ranvier (6-mm length in long axis), shown to provide successful blockade of at least 50% of impulses in vivo for single nerve fibers.1 Until recent work with ImageJ analysis software, nerve dye study outcomes have been evaluated with subjective visual assessment of nerve stain quality by researchers; no image analysis had been used.2

In the current literature, investigators use a variety of dye-diluent combinations based upon personal preference, making reproducibility and interstudy comparability challenging. Dye-diluent combinations for staining nerves include commercial food dye diluted with 0.5% bupivacaine,3 methylene blue diluted with saline,4,5 and yellow tissue marker diluted with 2% lidocaine69 or iodinated contrast.10 Wong et al12 established an objective scoring technique performed using ImageJ, an image processing software developed by the NIH.11 This software has become popular in the biomedical field for the analysis of color pixels being extensively used in immunohistochemistry, detection of pathological markers, 3-D imaging of live cells, and processing of radiologic images. These authors found that the above common dye-diluent combinations have variable dye staining characteristics, with food dye providing the fastest superficial dark color saturation when compared to methylene blue and tissue marker.12 ​Likewise, other studies13 have demonstrated that diluents also constitute active study variables, altering the dorsal-ventral distribution of nerve dyes in cadavers. This collection of work demonstrates the need for further investigation into the measurable effect that dye-diluent combinations have in prospective cadaveric studies.

The objective of this study was to quantify the effect of diluent (2% lidocaine, 0.5% bupivacaine, iodinated contrast, water) on nerve-staining saturation level and timing when used in combination with commercial food dye (10:1). The hypothesis was that there would be no statistically significant difference in saturation level or timing between any food dye-diluent combination.

Methods

Animals

Eight freshly euthanized, 2-month-old, female Yorkshire pig cadavers weighing between 28 and 30 kg (mean, 29.25; SD, ± 0.66) were obtained from an unrelated terminal study. Cadavers were dissected in lateral recumbency with the forelimb abducted. The axilla was sharply incised, transecting the cutaneous trunci and the pectoral muscles. The brachial plexus was identified via blunt dissection, and the axillary artery and vein were clamped to prevent contamination. The radial, axillary, and median nerves were excised and standardized to a length of 2 to 5 cm and a thickness of 0.5 to 1 cm. Any nerves smaller than these parameters or grossly contaminated with blood or tissues were discarded. Contralateral nerves were collected in a similar fashion. Nerves were dissected in bulk and then randomly distributed between treatment groups. Histologically, all nerves are expected to function similarly in vitro.14 All samples were obtained within 1 hour of euthanasia, and nerves were harvested, stained, and photographed within 4 hours of euthanasia. This study was carried out over the course of 1 day, with all pig euthanasias, nerve collections, and image acquisition performed simultaneously within the same environment. Study pigs were acquired from and euthanized at the end of an unrelated primary study, which had its own IACUC approval. No forelimb procedures were conducted on the pigs prior to euthanasia. Institutional ethical committee approval was not required for cadaveric samples after the primary study was completed.

Nerve dye groups and imaging

Forty-eight isolated nerve segments were randomized into 1 of 4 diluent groups (n = 12 each): 2% lidocaine, 0.5% bupivacaine, sterile water, and iodinated contrast. All diluents were combined with blue commercial food dye coloring in a ratio of 10:1. Three nerves in each group of 12 were immersed in their respective dyes for 1 of 4 periods of time: 1, 15, 30, and 60 minutes.

A stage using a black, rectangular table equipped with 2 photography lights (Fovitec Studio Pro-4500K) was utilized for all nerve portraits (Figure 1). The position of the equipment was fixed to the floor to ensure standardization between photographs. A digital camera (Sony a7R III Mirrorless Digital Camera) with a zoom lens (Sony FE Zoom 2.8/24-70 GM) was used to photograph all nerve segments as they were positioned on white, letter-sized paper alongside a black, 15-cm stainless steel ruler for scale reference. Before immersion in specific dye-diluent combinations, baseline images of all nerve segments were obtained for reference.

Figure 1
Figure 1

Stage and lighting equipment used to photograph all baseline and dyed nerve segments on the date of data collection.

Citation: American Journal of Veterinary Research 86, 1; 10.2460/ajvr.24.04.0108

Dye-diluent combinations were mixed in sterile, 100-mL plastic sample containers. Nerve segments were suspended in solution by nylon monofilament, nonabsorbable suture (Ethicon 3-0 Ethilon) for a predetermined immersion time. Nerve segments were placed on clean gauze to dry for 5 minutes prior to moving to postimmersion photograph.

Image analysis

Baseline and stained nerve images were uploaded to and analyzed using an imaging processing software program, ImageJ. To calculate the total area of the nerve, the color threshold was adjusted by modifying 3 individual variables: hue spectrum, saturation, and brightness. Each of these variables had an assigned numerical scale ranging from 0 to 255 (unitless scale). The hue spectrum and the saturation were not altered (0 to 255) to include all colors of the nerve segment. Brightness was adjusted to select the nerve and discard the background. The total nerve area was selected and measured in the number of pixels. Once the total nerve area was calculated, the hue was adjusted to only include the green-blue-purple color spectrum (the colors of the nerve dyes, 70 to 210 on the hue scale). Yellow, orange, and red colors were excluded (0 to 69 and 211 to 255) as they represent residual blood or unstained portions of the nerve. The image was then converted to a formalized grayscale using the software option type 8 bit. With this modality, each pixel was assigned a specific color saturation (0 to 255). Saturation was then subcategorized into a preset quartile system set by the authors to quantify different staining profiles: dark (0 to 62), medium dark (63 to 126), medium light (127 to 190), and light (191 to 255). Pixels per color saturation were charted and subsequently graphed using the histogram tool. The sum of pixels within each quartile was divided by the total nerve area to calculate the percentage of the total area stained. For example, the sum of pixels contained within the dark quartile (0 to 62) is 7,366 in lidocaine group A (1 minute), and the total area of the nerve is 120,692. Therefore, the percentage of the total area stained dark is 7,366 divided by 120,692 and multiplied by 100, which equals 6.1%. The percentage of the nerve not stained was calculated by subtracting the sum of all stained quartiles from the total area and then dividing this difference by the total area. All nerve segments for each dye-diluent combination and time were analyzed in the same manner.

Statistical analysis

All analysis was completed using R, version 4.3.0 (Already Tomorrow). Continuous variables were summarized into means and SDs. The proportion of dark, medium dark, medium light, and light were each modeled using a 2-way ANOVA type 1, with immersion time, diluent, and their interaction as predictor variables. The assumptions of normality and homoscedasticity were visually assessed for each model. Post hoc Tukey tests were performed for each model using the emmeans package. Graphs were constructed using the ggplot2 package.

Results

Before immersion, none of the 48 nerve segments demonstrated any superficial staining within the green-blue-purple hue (Figure 2). After immersion at 1, 15, 30, and 60 minutes, all nerve segments exhibited a characteristic dye quality for each dye-diluent combination (Figure 3).

Figure 2
Figure 2

Images of the representative nerve segments obtained prior to any dye-diluent exposure. These are the baseline images with the dyed segments in each of the 4 diluent groups for 1, 15, 30, and 60 minutes found in Figure 3. These baseline images confirmed no prior dyed color in any of the segments.

Citation: American Journal of Veterinary Research 86, 1; 10.2460/ajvr.24.04.0108

Figure 3
Figure 3

Images of the representative nerve segments obtained following immersion in 1 of 4 diluent groups for 1, 15, 30, or 60 minutes. Each of these images was uploaded to ImageJ to evaluate superficial staining via steps found in Methods: Image Analysis section.

Citation: American Journal of Veterinary Research 86, 1; 10.2460/ajvr.24.04.0108

The percentage of area stained within each saturation quartile was individually graphed for all diluent groups over the predetermined immersion times (Figure 4). At 1 minute, water and bupivacaine had a higher percentage of area of dark saturation when compared to contrast. Alternatively, contrast had a higher percentage of area of light and medium-light saturation when compared to lidocaine, bupivacaine, and water at 1 minute. At 15 and 30 minutes, dark and medium-dark saturation percentages of area were larger in lidocaine, bupivacaine, and water compared to contrast. There were no statistical differences in light and medium-light saturation between groups at 15 and 30 minutes. There were no differences in saturation percentages of area between groups at 60 minutes. All comparisons and corresponding P values of relevant color saturation differences among dye-diluent groups over time and between dye-diluent groups at similar time points can be referenced (Supplementary Tables S1S4).

Figure 4
Figure 4

Average area of nerves (%) stained superficially for each saturation quartile, (A) dark, (B) medium dark, (C) medium light, and (D) light, after immersion in 1 of 4 diluents with commercial food dye for 1, 15, 30, and 60 minutes. All diluents were combined with commercial food dye in a ratio of 10:1.

Citation: American Journal of Veterinary Research 86, 1; 10.2460/ajvr.24.04.0108

There were no statistically significant differences in comparing the percentage of area not stained between all dye-diluent groups across all immersion times. Almost all nerve segments regardless of immersion time or dye-diluent combination stained between 98% and 100% of the nerve area. One nerve segment immersed in sterile water and commercial food dye for 1 minute only stained 95.5% of the nerve area.

Discussion

Contrary to the original hypothesis, individual diluents do contribute to nerve-staining behavior and should be considered active variables when interpreting stain quality in cadaveric studies. Although the staining profiles of all diluent groups were indistinguishable at 60 minutes, the discrepancies noted in immersion times 1, 15, and 30 minutes highlight a significant delay in stain saturation profile found when combining commercial food dye with iodinated contrast compared to bupivacaine, lidocaine, and water. Consequently, if iodinated contrast is utilized and the results are analyzed before the 60-minute mark, the results may be mistaken as falsely negative. Likewise, if any of the 3 alternative dye-diluent combinations are utilized, staining may not be accurately evaluated until at least 15 minutes have elapsed. It is imperative that investigators consider these inconsistencies when interpreting results or comparing results between different study outcomes for successful nerve targeting. Given their almost identical color saturation outcomes, results can be comparable between research studies that use similar proportions of food dye combined with either bupivacaine, lidocaine, or sterile water if a uniform time has elapsed from injection time.

The visual assessment of nerve staining revealed that segments stained with iodinated contrast were markedly lighter in appearance when compared to nerves stained with 2% lidocaine, 0.5% bupivacaine, and sterile water between 1 and 30 minutes. Description of this visually lighter appearance could imply either a decreased staining percentage of dark and medium-dark saturation groups as compared to medium-light and light or a decrease in the overall total stained area of the nerve. The quantification methodology here allows the researcher and the audience to communicate more specifically what subjective interpretation of decreased staining means objectively, with a numerical definition. In the present study, there was no difference in the total area of nerve stained amongst the diluent groups at any immersion time; rather, iodinated contrast-diluent combination exhibited an inverted staining profile compared to all other diluents at times 1, 15, and 30, with more light staining quartiles and fewer dark staining quartiles. Contrast dye–diluent combination has an appreciable temporal factor to its staining profile, which makes both visual inspection of nerve dye success and communication of those results problematic for both the researcher and the reader. The current appraisal for success is based upon visual inspection rather than objective measurements like those used in ImageJ.15 These findings further support an argument for the use of image analysis comparisons and objective scoring in foundational dye studies for locoregional development.

Iohexol is a benzene-dicarboxamide, nonionic, water-soluble compound that has a significant role as a radiopaque medium for diagnostic tests, such as myelography, arteriography, and other radiographic procedures. In nerve-staining cadaveric studies,10,16 it is sought after as a diluent where imaging modalities are also employed to evaluate the anatomical extent of a novel locoregional technique. Previous research13 has proven that the dorso-ventral distribution of nerve dye is different in cadavers with iohexol when compared to bupivacaine and no diluent. This study further supports a discrepancy amongst staining quality specifically of iohexol. As hypothesized by de Miguel Garcia et al,13 physical biochemical differences may generate these appreciable differences in nerve-staining quality and distribution. When compared to the 3 other diluents, iohexol differs dramatically in molecular weight (MW; iohexol MW, 821 g/mmol; bupivacaine MW, 288 g/mmol; lidocaine MW, 234 g/mmol; sterile water MW, 18 g/mmol),1720 which may inhibit the transport of dye through tissue planes in situ or uptake of stain across the epineurium when fully immersed. Differences in MW, however, would not explain the indistinguishable appearance of nerve staining when other diluents were utilized. Absolute viscosity may also play a role in variable staining profiles as iohexol and other diluents can vary significantly depending upon temperature and concentration.21

This project's purpose was to objectively evaluate the variable contribution, if any, that diluents would pose on nerve-staining quality in cadaveric studies, a sequel of previous work investigating the effect of varying dyes on nerve-staining quality. Commercial food dye was selected for its objectively evaluated consistency in nerve-staining qualities, such as faster onset time, darker saturation, and deeper tissue penetration, compared to methylene blue and tissue marker. The ImageJ analysis methodology from Wong et al12 was modified for the present study to account for the high dark saturation level noted specifically with commercial food dye. The histogram tool was employed to ensure that all dark-blue pixels were quantified and included rather than excluded as imperceptibly different from black. Future studies may reveal additional applications of the ImageJ software to further improve upon this image analysis, quantification, and scoring techniques for locoregional studies.

There are several limitations to this study, the first being that the nerve segments were obtained from fresh porcine cadavers, so it is possible that the staining profile may be different in either preserved cadavers or cadavers belonging to other species. Similarly, these nerve segments were fully immersed in the individual solutions, and therefore we cannot anticipate the staining profile of these materials in situ amongst other tissue layers. More research is required to determine if this delay seen in the staining profile of iohexol is even more significant in situ. Additionally, biochemical properties, such as pH, temperature, density, and degree of colorization, were not measured or standardized across immersion solutions. And lastly, the ImageJ software in this research design requires familiarity, where the researchers themselves generate interuser variability (ie, total area calculations of each nerve segment). The investigator performing the analysis with ImageJ software was not blinded to the treatment groups. Overall, the authors feel that this user bias, albeit small, is unlikely to have altered the formal conclusions of this study.

Different dye-diluent combinations utilized in independent cadaveric nerve studies generate inherent result variability that makes directly comparing study outcomes difficult, especially given the fact that current nerve-staining success in the literature is via subjective assessment. The findings of this study support the treatment of diluents as active variables in stain quality. The researcher should be aware of these staining characteristics and affirmatively choose a dye-diluent combination that matches their study requirements (ie, location, length of time from injection to dissection, need for advanced imaging, etc). Successful staining should be objectively defined within the context of the dye-diluent combination, and image analysis with ImageJ provides a methodology to do so. In studies where iohexol is used, the researcher should be aware of the significant delay to reach a saturation level comparable to the other diluents studied here, so false negatives are avoided. Finally, 2% lidocaine, 0.5% bupivacaine, and sterile water may be used interchangeably when combined with commercial food dye after 15 minutes. In cadaveric models, where the clinical effect of local anesthetics is irrelevant, the selection of sterile water in combination with commercial food dye can act as an equitable, environmentally friendly, resource sparing dye-diluent combination unless postimaging modalities are required.

Supplementary Materials

Supplementary materials are posted online at the journal website: avmajournals.avma.org.

Acknowledgments

The authors thank Celia A. Soto, MS, PhD, for her image analysis contributions and ImageJ consulting.

Disclosures

The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.

Funding

The research was funded by the authors' departments.

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