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. 2026 Jan 16;19(1):3. doi: 10.1007/s11869-026-01899-5

A comprehensive approach for detecting and locating black carbon in human placentae

Atsuo Chiu 1, Denise Ivey 1, Amanda Sanko 1, Barbara Tisdale 1, Philip J Katzman 2, Thomas G O’Connor 1,3, Kaye Thomas 4, Tanzy Love 5, Rogelio Perez-D’Gregorio 1, Carolyn M Salafia 8, Richard K Miller 1,6,7,9, Philip K Hopke 7,10,11,✉
PMCID: PMC12811366  PMID: 41552391

Abstract

Molecular passage across the placenta generally serves developmental purposes, but some also can induce harm. Particulate matter (PM) affects the pregnancy through the maternal circulation to the placenta. Black Carbon (BC) particles, produced by high temperature fuel combustion, contribute to global air pollution and climate change. Its health impacts likely extend beyond respiratory complications. Thus, studying BC translocation into human tissues provides insights into the mechanisms of observed adverse outcomes. The placenta is a useful organ since it provides further understanding of placental transport mechanisms, impacts on the tissue and embryo/fetus, and for developing prevention strategies. Having well-measured tissue dose metrics would also provide an epidemiological tool to related exposures to a variety of health outcomes in the woman, fetus, and resulting child. Thus, quantitatively establishing their presence in the placenta and blood provides an important exploratory tool. Such submicron particles challenge traditional microscopy limits, requiring effective measurement systems and rigorous assessment strategies. A microscopic methodology for quantifying BC particles in human placental histology slides utilizing multiphoton microscopy has been previously reported. However, there are substantial issues with the prior method and thus, this work has developed a more rigorous approach to demonstrate transplacental movement of BC particles.

Supplementary Information

The online version contains supplementary material available at 10.1007/s11869-026-01899-5.

Keywords: Black carbon, Placenta, Multiphoton microscopy, Image analysis, Exposure assessment

Introduction

Black carbon (BC) particles are an important component of fine particulate matter in the air. They are formed as part of the combustion of any carbon-based fuel (e.g., fossil fuel, diesel, coal) (Martin et al. 2022) and are commonly associated with traffic emissions in urban areas (Jereb et al. 2021) but can also be naturally produced in wildfires (May et al. 2023). BC effectively absorbs solar radiation and converts it to heat, contributing to atmospheric warming (Fierce et al. 2020) and accelerating melting of polar glaciers. Hence, these particles have significant effects on climate (Bond et al. 2013), urban visibility (Li et al. 2022), and human health (WHO, 2012; 2021).

Particulate air pollution has been well documented to exacerbate health issues, including respiratory illnesses (e.g., chronic obstructive pulmonary disease, asthma) (Hopke et al. 2019; Jiang et al. 2016), respiratory infections (Croft et al. 2019), and cardiovascular diseases (Zhang et al. 2018), but has also seriously disrupted ecological and social orders and balances (Weitekamp and Hofmann 2021). Associations have been reported between maternal exposure to ambient PM and poor pregnancy outcomes including preeclampsia (Assibey-Mensah et al. 2019) and low birth weights (Ji et al. 2017). Epigenetic changes have also been reported (Raftis and Miller 2019), but the behavior of PM in the human body is yet to be fully determined. BC particles are an important component in ambient fine PM. Specific clinical implications of BC have been associated with cognitive decline and depression in adults (Colicino et al. 2016) with a possible route to the brain via the olfactory system and/or through blood-brain barrier (Zhang et al. 2021). Thus, BC particles are ubiquitous and obtaining better assessments of exposure to BC particles and their translocation into bodily tissues is critical to fully understanding the role of particulate pollution on health.

As the vital interface between the mother and fetus, the placenta fulfills crucial roles as a physical anchor, endocrinologic controller, and a bidirectional conduit. The permeability of the placenta in respect to certain nutrients and teratogens has been well studied, demonstrating that the placenta bears a highly selective transport system. Indeed, the placenta conveys essential and beneficial molecules to the developing embryo/fetus, as in the transport of vitamins and immunoglobulins via uptake methods including receptor-mediated endocytosis (You et al. 2022). However, deleterious materials can similarly pass, resulting in adverse pregnancy outcomes (Miller et al. 1998; Schneider and Miller 2010). Thus, the detection of these materials in the placenta is the critical first step in linking environmental exposures to adverse pregnancy and early childhood effects.

The placenta also can provide critical tissue for examination that is readily available after the delivery of the child. However, before proceeding to studies that examine the physiological impacts of BC on the placenta and on the fetus, it becomes critical to establish a well-characterized method that accurately demonstrates and quantifies the presence of BC particles in histological samples. Prior work has shown that laser excitation can induce luminescence in carbonaceous nanoparticles producing white light that can be observed microscopically (Bové et al. 2016). There is also prior work reporting the identification of BC particles (Bové et al. 2019; Bongaerts et al. 2022). However, based on the work presented below, these studies will be discussed following the presentation of the current study results. The current study presents the development and testing of a multiphoton optical microscope, a high-power pulsed laser, and a four bandpass filter detection system to observe submicron particles (Inline graphic0.3 μm) found in placental histology slides. The workflow from sample collection to data interpretation permits the determination of the load and localization of BC particles in placental tissue.

Materials and methods

Sample preparation

Fresh placentae were collected within an hour of delivery and were taken to the lab for initial assessments including weight and dimensional measurements. Full depth samples from chorion to basal plate were taken from 4 to 8 different regions of each placenta. Biopsies were placed into standard cassettes and fixed in 10% neutral buffered formalin for 4 to 5 days. Further processing of the tissue was performed by a Shannon Citadel tissue processor, and paraffin embedding by Shandon Histocenter 2 Embedding Center. Section 5 μm thick were placed on precleaned microscopic slides (Fisherbrand Superfrost Plus Microscope Slides, White Tab, Precleaned, Cat. No: 1255015). No adhesives were used.

The selected slides then underwent a deparaffinization process. The details of the procedure are provided in supplemental material Text S1. In our initial work, the slides were stained with hematoxylin and eosin (H&E) for standard histology. However, based on results presented below, the slides that were ultimately used in this study were left unstained and without cover slips to avoid introducing air bubbles that may result in poor image quality. A library of slides with delivery specimens dating from 2016 to 2021 were available for study, in which random placentae were chosen for examination. This study was approved by The Research Subjects Review Board (# 00002064) as part of the larger ECHO Upside study.

Microscopy technique

The two-photon Olympus FVMPE-RS microscope (Olympus) with an 810 nm laser excitation (Spectra-Physics InsightX3 Laser, MaiTai HP DeepSee Ti: Sapphire Laser, 5.5% transmissivity) and four bandpass emission channels with fixed voltage and distinct bandpass filters: 370–410, 425–465, 575–630, and 645–685 nm, was utilized to capture images of regions containing chorionic villi and maternal blood space. With a 25X objective (XLPlan N 25X/1.05 WMP, Olympus), a 3X optical zoom was further introduced to produce scans of 170 × 170 µm2 at sampling speed of 2.0 µs/pixel. Images of 15 randomized fields of view within a particular slide were obtained following the “randomization protocol” where each image was distanced approximately 360 μm from one another. The total area scanned per slide was 2550 × 2550 µm2. For each, a Z-stack dependent on the focused tissue thickness was obtained to produce images with voxel dimensions of 0.167 × 0.167 × 0.50 μm.

Special caution was taken to avoid prolonged exposure of the slide to the laser since the beam subjects the tissue to possible thermal damage as well as photobleaching of the image. Thus, focusing was performed under high-speed, low-resolution galvo-resonant scanning, whereas image acquisition with laser scanning microscopy (LSM) was done by low-speed, high-resolution galvo-galvo scanning. Acquisition of images was always performed under identical conditions of illumination and detection settings, under a temperature of 21 °C. Olympus FV31S-SW software (Olympus) was used in controlling the experiment.

Image analysis

Initial work was performed to assess the ability of the system to measure particles using carbon black particles (Orion Engineered Carbons Carbon Black 40) with nominal particle size of 0.5 μm. Figure S1 shows the images obtained from each of the 4 channels that provide evidence that the particle is truly “black”.

Assessments for detection and localization of the BC nanoparticles were performed by implementing the following criteria: (i) to be present in all four emission channels, and (ii) to be of ≤ 0.3 μm in diameter. Since BC emits white light upon two-photon excitation, to appear in all four of the bandpass emission channels (from 370 to 685 nm) ensures that the produced signals cover the range of the visible light spectrum.

Images were analyzed by combining two key features in the Imaris image analysis software (Oxford Instruments): “Spots” and “Surface”. For BC detection, the Spots feature was implemented to identify spherical objects within the field of view that exhibited an approximate diameter of 0.3 μm and displayed an intensity center that was detectable within a designated range across all four emission channels (Fig. 1A, B, C). Every BC candidate was then manually validated to be within the tissue plane by examining the X-Z and Y-Z cross-section projections of the image (Fig. 1D). Those objects that appeared superficial or embedded relative to the tissue plane were considered to be contamination and were excluded from the data set. Similarly, application of the “Surface” feature aided in the discernment of artifacts by constructing a three-dimensional model of the scanned tissue based on tissue autofluorescence. Simultaneous application of both features generated a topographical map in which BC candidates were superimposed to offer visualization of spatial relationships (Fig. 1E).

Fig. 1.

Fig. 1

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Images of human placental tissue utilizing the Olympus FVMPE-RS microscope (Olympus). A Original image produced by tissue autofluorescence. B BC candidates identified by Imaris (Oxford Instruments) with spherical, oversized grey markers (verified BC particles are highlighted with orange arrows). C 2X magnification of area in white square presented in (B). D XZ and YZ projections of the indicated BC particle shown in the center of the screen (E). Three-dimensional models formed using the Surface feature on Imaris. BC particle markers are superimposed but cannot be visualized due to their presence within the tissue. Scale bar: 15 μm

The identified BC particles were then categorized to reside in one of the three areas: maternal blood space, fetal tissue (including syncytiotrophoblast and cytotrophoblast cells, villous mesenchymal stroma), and fetal capillary lumen (including endothelial cells, Fig. 2). The mean and standard deviations of black carbon counts for each slide were each computed and documented.

Fig. 2.

Fig. 2

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Description of human placental histology. Cross sections of chorionic villi are displayed. The intervillous space (IVS), fetal vessel (FV), and fetal tissue (FT) are labeled. FT includes trophoblast cells and villous stroma. Both fetal (F) and maternal (M) red blood cells (RBC) can be observed in the image. An H&E stained slide was used here for visual enhancement. Scale bar: 10 μm

Computation of BC concentrations

Following quantification of the identified particles, volumetric calculations were performed to report the particle count per cubic millimeter for each field of view. Although X and Y size dimensions were constant for all images, Z-stacks were obtained per tissue thickness of the focused region. Thus, every image file had a unique scanned volume that was computed by multiplying the image dimensions with the voxel dimensions. Dividing particle count by the obtained volume describes particle concentration, which can then be used for estimating total BC count in a given placenta via extrapolation.

Statistical analyses

For every placenta, each view used to measure BC counts is a repeated measurement nested within a block and blocks are nested within a placenta. To compare the numbers of BC particles in two populations, Poisson generalized linear mixed effects models (GLMM) were used to estimate the group (treatment) fixed effect and the individual and block random effects. A significance test for the group fixed effect in this model would reject the null hypothesis that the two populations (for example: control pregnancies and exposed individual pregnancies) have the same average number of BC in their placentae.

Before placenta blocks and fields were selected for measurement, an a priori power analysis was performed. Based on a pilot study of placenta blocks available for analysis, we set standard deviations for individual and block random effects to their estimates of 0.50 and 0.65, respectively. Assuming that the average number of BC particles was 1.5 for controls and 1.7 for cases, the Poisson GLMM with subject and block random effects had 85.5% power to find a significant difference between cases and controls, given an analysis of 25 placenta per group, 4 blocks per placenta, and 15 fields per block.

Results

Formalin precipitation

All of the tissue samples were preserved in formalin. However, formaldehyde has a natural tendency oxidize, producing formic acid. Heme from red blood cells and formalin bind each other to form formalin–heme complex that appears as brown-black amorphous to microcrystalline granules in tissue sections (Pizzolato 1976). Thus, exploration of the potential for artifact particles in the tissue samples was performed. Figure S2 shows an image of a tissue sample with known formalin precipitation seen as observable blackish plaques. The image shows more white spots than the slides without noticeable formalin precipitation. Figure S2a identifies the white dots that may look like BC particles. However, when the 370–410 nm channel was turned off (Figure S2b), the dots disappeared, eliminating them from being BC particles. Formalin fixation does not produce as truly black particles, and therefore, the signal is not intense and can be eliminated as an artifact.

Staining effects

While usage of hematoxylin and eosin (H&E) treated slides is conventional in histological assessments, eosin has been reported to have peak absorption at 830 nm under two photon excitation, leading to the same exited state as single photon excitation (Parravicini et al. 2020). Thus, the excited eosin emits a broad peak at 549 nm. By utilizing a system equipped with an 810 nm excitation laser, we hypothesized that using H&E stained slides for the proposed experimental conditions would lead to eosin fluorescence, potentially overestimating BC particle count given that fluorescence intensity is a BC-determining criterion. In an experiment performed where images of identical regions from the same slide obtained before and after eosin or hematoxylin treatment were compared for their BC content, eosin treated slides demonstrated significant increases in detected particles ascribed to eosin-originating artifacts being introduced or from signal enhancement of previously identified BC aggregates (Fig. 3; Table 1). It was observed that certain individual/smaller groups of BC that were detected in the unstained slide did not appear in the stained slide. Possible explanations include thermal destruction of the particles (discussed below), or washout during the staining process. Nevertheless, the substantial numbers of false positives introduced due to eosin staining presents a serious problem to accurate BC determinations, and thus, it is essential to examine unstained slides for the purpose of identifying BC. Similar increases have been observed in hematoxylin treated slides. Application of both H&E to our slides confirmed previous results, including cases where the image became compromised by obtrusive signals produced by stain precipitates. Numerical comparisons revealed up to nearly a 200% difference in identified BC by Imaris, highlighting the false positive nature of using stained slides for examination.

Fig. 3.

Fig. 3

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Images of slides photographed pre (A and C) and post-eosin staining (B and D). Eosin treatment resulted in additional BC-interpreted particles by Imaris. Enhancement in size of particle aggregates along with newly-introduced particles can be observed. The scale bars in the lower left corner represents 15 μm

Table 1.

Numerical comparisons of identified BC candidates between unstained and Eosin stained slides from selected fields of view

Area Unstained Stained
Area A 13 53
Area B 69 120
Area C 66 478
Area D 5 12
Area E 2 6
Area F 2 7
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Reproducibility

While exploring the reproducibility of the proposed technique to provide confidence in BC identification and quantification, we observed a loss of signal intensity of identified BC during each sequential trial when trying to obtain consecutive acquisitions of the same particle-containing region (Fig. 4). We hypothesize that laser ablation of the particles would lead to possible fragmentation or material loss such that the signal produced becomes undetectable with our current thresholds. Additionally, subsidence of the particles deeper into the tissue due to laser damage to the tissue may also explain the decrease in detected signal per trial.

Fig. 4.

Fig. 4

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Identified BC count per reproduction trial for five selected fields of view for multiple subject samples. Upon imaging a given field of view five times, the identified BC count as reported by Imaris decreased in all cases

Measured particles

Our examination revealed BC presence in all three histological tissue categories with the greatest number in maternal blood. Appearance in fetal tissue and blood confirm transplacental movement of BC. Of the examined placentae, mean ± standard deviation of BC counts per field were 4.5 ± 3.7, 2.8 ± 2.5, and 2.6 ± 2.3, in the maternal blood space, fetal tissue (including syncytiotrophoblast and cytotrophoblast cells, villous mesenchymal stroma), and fetal capillary lumen, respectively. An example of the distributions of particle numbers in the multiple views of the three types of tissue from one sample are shown in Fig. 5. The data for this figure are provided in Table S1. The similarity in the numbers of particles in the fetal tissue and the fetal capillary lumen suggests that the trophoblast is not providing an effective barrier to translocation of the BC particles into the fetal capillary lumen. The detailed study of the transport processes and the verification of the apparent efficiency is planned for future work and is beyond the scope of the current study.

Fig. 5.

Fig. 5

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Histograms of the distributions of BC particles per view of a single selected tissue sample within each of the 3 tissue types (maternal blood space, fetal tissue, fetal capillary lumen)

Statistical precision

For reporting typical counts of BC, we report 95% confidence intervals for the mean BC per field in a population. Using a representative sample of 25 placentae with 4 blocks per placenta and 15 fields per block, we can estimate the count of BC per field to within ± 0.2. The volumetric computations of BC density per biopsy specimen ranged from 2.9 ± 3.1 × 103 to 2.5 ± 1.4 × 104 mm− 3, with a standard error of 2.7 ± 1.4 × 103 mm− 3.

Comparison with prior work

As noted above, there have been several prior papers describing the analysis of BC papers in tissue (Bové et al. 2019; Bongaerts et al. 2022). In their work, they also used an 810 nm excitation laser, but with only 2 viewing channels of 400 to 410 nm and 450–650 nm. With a broad acceptance wavelength window, any photon in this range would be treated as a black particle, even though the particle may not be emitting over the entire spectrum. They use a lower magnification so they would have difficulties in identifying 0.3 μm particles. More importantly, they used stained tissue in which we found substantially increased numbers of “particles.” Thus, it is likely that their reported particle counts between 0.95 ± 0.66 × 104 to 2.09 ± 0.96 × 104 mm− 3 in term placentae may be a substantial overestimation of particles. The present work provides a more rigorous and robust method for identifying and quantifying BC particles in tissue with particle numbers more in line with the likelihood of translocation of 0.3 μm particles into the human body (e.g., Oberdörster et al. 2004).

Limitations

Although the methodology presented here is a substantial improvement over prior approaches in that the potential interferences from formalin precipitate and staining have been identified, the method currently involves laborious review of the images limiting the number of samples that can be analyzed. The use of optical microscopy limits the analyses to the upper end of the distribution of BC particles emitted from onroad diesel engines commonly used in heavy-duty diesel vehicles (Kittleson et al. 2004). Thus, these analyses almost certainly underestimate the numbers of particles in all compartments of the examined placentae. Work is ongoing to automate the image analysis process so that it will be possible to more effectively process samples and become a practical tool for determining BC tissue doses in a variety of available tissues.

Conclusions

This study has demonstrated that it is possible to quantitatively determine the tissue dose of ~ 0.3 μm BC particles in unstained tissue samples. Given that this diameter is the approximate lower limit of optical detection, it is likely that there are more, smaller, undetectable particles present in the samples. However, applications of such techniques can now be employed to investigate changes in BC tissue loads with respect to environmental exposures to particulate matter such as wildfire episodes or other major fires and proximity to other major sources (adjacent to major highways or railyards). To compare specimens from subjects who were and were not exposed to higher concentrations of BC such as from wildfire smoke will further provide insights on the impacts of wildfire-derived BC with respect to translocation and accumulation in peripheral tissues. Similar assessment on cord blood and membrane specimens can also be conducted using this methodology. The availability of an accessible method to quantify BC particles in tissue samples opens multiple opportunities for obtaining a better understanding of the impact of these particles on specific tissues and relate their presence to observed adverse health outcomes.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary Material 1 (4.6MB, docx)

Author contributions

Atsuo Chiu: Investigation, Formal Analysis, Data Curation, Writing: Original Draft; Amanda Sanko: Investigation, Formal Analysis, Data Curation, Writing: Review and Editing; Barbara Tisdale: Resources, Writing: Review and Editing; Denise Ivey: Investigation, Formal Analysis, Data Curation, Writing: Review and Editing; Philip J Katzman: Resources, Writing: Review and Editing; Thomas G O’Connor: Resources, Writing: Review and Editing; Kaye Thomas: Methodology, Resources, Supervision, Writing: Review and Editing; Tanzy Love: Software, Formal Analysis, Investigation, Writing: Review and Editing; Rogelio Perez-D’Gregorio: Resources, Writing: Review and Editing; Carolyn M. Salafia: Resources, Writing: Review and Editing; Richard K Miller: Project Administration, Funding Acquisition, Resources, Writing: Review and Editing; Philip K Hopke: Conceptualization, Methodology, Formal Analysis, Writing: Review and Editing.

Funding

This work was supported in part by a RW & MS Goode Grant and by the University of Rochester Environmental Health Sciences Center (EHSC), an NIH/NIEHS-funded program (P30 ES001247) and NIH/OD grant UG3/UH3 OD023349.

Data availability

Data are available on request from the corresponding author.

Declarations

Ethics approval and consent to participate

This study was approved by The Research Subjects Review Board (# 00002064) as part of the larger ECHO Upside study.

Consent to publish

All of the authors have participated in the review/revision of this paper and consent to have it published.

Conflict of interest

The authors declare that there are no conflicts of interest.

Footnotes

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Material 1 (4.6MB, docx)

Data Availability Statement

Data are available on request from the corresponding author.

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