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Abstract
Stimulated Raman scattering (SRS) has been widely used in functional photoacoustic microscopy to generate multiwavelength light and target multiple chromophores inside tissues. Despite offering a simple, cost-effective technique with a high pulse repetition rate; it suffers from pulse-to-pulse intensity fluctuations and power drift that can affect image quality. Here, we propose a new technique to improve the temporal stability of the pulsed SRS multiwavelength source. We achieve this by lowering the temperature of the SRS medium. The results suggest that a decrease in temperature causes an improvement of temporal stability of the output, considerable rise in the intensity of the SRS peaks, and significant increase of SRS cross section. The application of the method is shown for in vivo functional imaging of capillary networks in a chicken embryo chorioallantois membrane using photoacoustic remote sensing microscopy.
© 2021 Optical Society of America under the terms of the OSA Open Access Publishing Agreement
1. Introduction
Photoacoustic microscopy (PAM) is among the most rapidly growing optical imaging techniques. This modality is well-known for its practical functional and molecular imaging capabilities [1]. PAM has the unique imaging contrast of optical absorption and is the preferred modality for a wide range of biomedical applications [2,3]. This technology has been applied to many clinical and pre-clinical applications including but not limited to functional brain imaging, measurement of the oxygen consumption rate of a tumor, imaging of lipid-rich samples [4], and detection of circulating melanoma cells [5,6]. Functional photoacoustic measurements (e.g., blood oxygenation) require a tunable wavelength excitation laser that can target multiple chromophores inside the tissue [7]. Optical parametric oscillators (OPOs) and dye lasers are commonly used for functional photoacoustic studies [8,9]. In addition to being expensive and bulky, these tunable laser systems typically have low pulse repetition rates (PRR) that severely compromise image acquisition speed for in vivo imaging applications (10 Hz – 10 kHz) [10]. For example, in ophthalmic applications, where functional imaging could help with early diagnosis of major blinding diseases, imaging speed is a critical parameter [11]. Conventionally, OPO lasers have been used for photoacoustic ophthalmoscopy, however, their low PRR would result in long acquisition time which is not compatible with clinical applications [12]. In contrast, the high speed offered by tunable SRS sources, may improve imaging time by several orders of magnitude, mitigating image artifacts due to involuntary eye motion [13].
Stimulated Raman scattering provides a simple, cost-effective technique that has been widely used to create multispectral pulsed sources with high PRR [14,15]. SRS is a nonlinear optical effect that generates one or more Stokes wavelengths downshifted from the frequency of the pump laser [16]. This phenomenon occurs when the light intensity inside a non-linear medium reaches a certain threshold level [17]. In multispectral photoacoustic imaging applications, silica fibers are typically used as the SRS medium. Here, if the peak power of the pump light is strong enough, cascading Raman shifts will occur (spaced at 13.2 THz), generating higher-order Stokes waves [6]. In 2011, Koeplinger et al. demonstrated the first application of the method for photoacoustic imaging [18]. The concept has been extended by other groups for generation of multispectral light sources with different pulse energies and pulse repetition rates [19,20]. Free-space multiwavelength SRS light sources have been also developed for functional photoacoustic imaging. They are reported to have better monochromaticity compared to the fiber-based versions, however the cavity is more sensitive to environmental changes and misalignment compared to fiber-based SRS sources [21,22]. Despite all the advantages provided by SRS sources, they suffer from pulse-to-pulse output energy fluctuations and power drift that will directly affect imaging quality [23,24].
In this manuscript, we propose a new technique to improve the temporal stability of the SRS-based multispectral pulsed source. We achieve this by lowering the temperature of the SRS medium. There are two main reasons that temperature is an important factor in Raman-based optical components. First, Raman scattering involves nonlinear phonon-photon interactions. The characteristics of phonons, which are quantized lattice vibrations, are highly temperature-dependent [25,26]. Second, Raman based devices may suffer from high operating temperatures, since they require high average intensity optical beams to produce their nonlinear effects [27]. Therefore, temperature plays an important role in designing and/or operating Raman-based devices. The experiment is performed by keeping the optical fiber inside a temperature-controlled unit. The temperature of the unit is adjustable between 195 K and 300 K. It is shown that by controlling and decreasing the temperature, the temporal fluctuations of the generated output peaks are reduced. The proposed method is used to generate stable multiwavelength light at a high pulse repetition rate. The light source is used as the excitation laser for a photoacoustic remote sensing (PARS) microscope and applied to in vivo functional imaging of capillary networks in chicken embryo chorioallantois membrane (CAM). The proposed method offers a promising technology for creating reliable, cost-effective multiwavelength light sources with a sufficiently high pulse energy and PRR for a variety of photoacoustic imaging applications.
2. Methods
2.1 Temperature-controlled stimulated Raman scattering
The experimental setup used in this study is shown in Fig. 1. A 532-nm 1.5 ns pulse-width, ytterbium-doped fiber laser (IPG Photonics) capable of PRRs from 20 to 600 kHz is used as the pump laser. To stabilize the laser output prior to the experiment, the source was continuously operated for 30 minutes at an output power of ∼370 mW with 50 kHz PRR. The output of the laser was coupled to the fiber by a 10x microscope objective lens. The coupling efficiency for all the experiments was measured to be 63 ± 2%. The optical fiber (PM-460- HP, Thorlabs, Inc) used in this study is single-mode (SM) with 3 µm core diameter, and 6 m in length. Polarization maintaining (PM) fibers are selected for this study since they make SRS generation more efficient compared to non-PM SM fibers [28,29]. The fiber is kept in a custom-designed isolated passive temperature-controlled unit during the experiment. The temperature of the unit is adjusted at 300 K, 273 K, and 195 K, by adding water, mixture of water and ice, and dry ice. Once the temperature was stable at the required value, the experiments were conducted. The temperature of the unit stays stable over the several seconds data acquisition time since the thermal mass of the fiber is negligible relative to the cooling media. To prevent the effect of reduced temperature on the fiber coupling efficiency, the fiber coupler is kept outside of the temperature unit. SRS efficiency may also be affected by airflow which can cause random errors and long-term drift in the pulse energy [24]. To avoid this, the fiber was covered and placed at the bottom of the chamber and by sealing the unit, its airflow was isolated. The fiber output is coupled to a collimator, and spectral filters were used to select the SRS peak values. A measuring system made up of a beamsplitter, spectrometer, photodiode, power meter, data acquisition card and computer were used to collect and analyze the required information.
Fig. 1. Schematic of the experimental setup. MO: microscope objective, C: collimator, BS: Beamsplitter, PD: Photodiode, PM: Power meter.
2.2 Multiwavelength photoacoustic remote sensing microscopy
The multiwavelength light source is applied in a functional photoacoustic imaging study. The imaging system used in this study is based on photoacoustic remote sensing microscopy, previously described in [13,30]. Figure 2(A), shows the schematic of the PARS system. Briefly, the multispectral light source operates as the excitation laser for the setup. Concurrently, the detection light is provided by an 830-nm Superluminescent Diode (SLD830S-A20, Thorlabs). A polarized beam splitter is used to transmit the majority of the forward detection light onto a quarter wave-plate, which transforms the linearly polarized light into circularly polarized light. The detection and excitation beams are then combined using a dichroic mirror. The co-aligned beams are directed toward the sample using a large-beam galvanometer scanning mirror (GVS012/M, Thorlabs, Inc.), and are co-focused into the sample using an objective lens. The back-reflected light from the sample is collected via the same objective lens and guided towards a balanced photodiode. The photodiode outputs are connected to a high-speed digitizer (CSE1442, Gage Applied, Lockport, IL, USA) that performs analog to digital signal conversion. A point acquisition is made for each image pixel and is recorded by the digitizer. Each point acquisition is converted to an intensity value by computing its maximum amplitude and is plotted at its respective location in the image. All images and signal processing steps were performed in the MATLAB environment. Figure 2(B) shows the spectra of the individual SRS peaks acquired after spectral filters (FL532-1, FL543.5-10, FB560-10, FB570-10, FB590-10, Thorlabs, Inc.) and demonstrated the available wavelengths for the functional imaging. The spectral peaks at 573 nm and 588 nm wavelengths are broader compared to the other SRS peaks. This can be explained by the broadness of the Raman gain spectra and also the existence of other non-linear effects such as four-wave-mixing [31]. When it comes to functional measurements, this type of spectral broadening should be considered in the unmixing model to maintain accuracy.
Fig. 2. (A) Schematic of the PARS imaging system, P: polarizer, PBS: polarized beamsplitter, L: lens, PD: photodiode, GM: Galvanometer mirrors, QWP: quarter waveplate, MO: microscope objective, DM: dichroic mirror, C: collimator. TCU: Temperature control unit (B) spectra of the individual SRS peaks acquired after spectral filters.
3. Results
3.1 Temperature-controlled stimulated Raman scattering
We first characterized the temporal stability of the laser itself. The root-mean-square (RMS) temporal fluctuation of the light source at an output power of ∼ 370 mW was measured as ± 0.7%, which is in correspondence with the values reported by the manufacturer. The output of the laser was then coupled into the fiber and the spectra of the generated SRS peaks were measured using the spectrometer. Figure 3 shows the spectra of SRS peaks acquired at different temperature levels. In this case, the coupling efficiency was ∼ 62%, resulting in ∼ 220 mW power coupled into the fiber. As the temperature increases, the bandwidth of the spectra expands which is in agreement with previous reports [32–34]. This could be explained by decreasing of chromatic dispersion of the fiber with increasing temperature [35]. From a phenomenological standpoint, raising the temperature results in decreasing the phonon lifetime which leads to a broadening of the optical phonon spectra [27]. Later it is shown that this temperature-dependent spectra narrowing is accompanied with an increase in the output power intensity for the wavelengths at the higher end of the spectra.
After evaluating the effect of temperature on the generated spectra, we analyzed the temporal stability of the SRS peaks at different operating temperatures. We analyze the RMS stability using a photodiode to measure the SRS intensity generated by each laser pulse. To have high temporal resolution in the acquisitions, a 350 MHz-bandwidth silicon photodetector is used to collect the output pulses after the spectral filters. The timescale of the measurements is based on the potential photoacoustic imaging applications, thus the pulse-to-pulse fluctuations over several seconds are considered in this study. At selected temperature levels and for each measurement 1000 datapoints are collected. Figures 4(A)-(C) show an example of the light intensity measured using the photodetector, for the 558 nm Raman peak, which directly relates to the number of photons detected, at 300 K, 273K and 195 K, respectively. Here, if the 558 nm SRS peak is not generated (failed SRS event), it will cause a zero voltage on the detector output. The black arrows in Figs. 4(A)-(C) refers to these failed SRS datapoints. In the graphs it can be observed that by reducing the temperature the number of datapoints contributing to SRS events increased, from ∼ 690/1000 to ∼ 999/1000, at 300K and 195 K, respectively. This represents a ∼30% increase in the probability of the SRS event, corresponding to a significant improvement in the temporal stability of the source. This can be explained by the substantial growth of SRS cross section (i.e., the probability that the process will happen) and increase of SRS conversion coefficient as the temperature reduces [36].
Fig. 4. Temporal stability of SRS peaks at different temperature levels. (A) 300 K, (B) 273 K, (C) 195 K. Dashed boxes highlight the SRS peaks intensity. Inset figures show the deviation in SRS peak intensity. (D) Bar chart graph showing relative power of individual filtered out SRS peaks measured at different temperature levels. The error bars in this plot show the standard deviation of the SRS peaks.
In addition to the rate of failed SRS events, we also observe the variation in generated SRS peak intensity. We use the RMS deviation of the peak intensities in the acquired data as a stability metric. The dashed box in each figure highlights these corresponding SRS peaks. Here, the 300K temperature exhibits an obviously large amount of peak variation in comparison to the 195K and 273K cases. Observing the inset figures, the standard deviation of the SRS pulses can be directly visualized. The differences in the variation at each temperature level, clearly shows the improvement in temporal stability with reduced temperature. In this case, both the peak variation, and the failed SRS events contribute greatly to the very large RMS deviation in the SRS peak at 300K. Conversely, the 273K and 195K each exhibit substantially improved pulse-to-pulse stability and substantially reduced SRS failures. Thus, corresponding to a significant improvement in the RMS stability.
We have also extended these measurements across each of the 545 nm 558nm, 573nm and 588nm SRS peaks. The relative power of individually filtered SRS peaks at different temperature levels is shown in Fig. 4(D). The bar chart presented here reveals the relative SRS intensity, while the error bars show the RMS fluctuations of the peaks. The results suggest that by lowering the temperature, the standard deviation of the pulse energy is reduced as well. In other words, as the temperature reduces, the generated SRS peak intensities become more uniform and their temporal power fluctuations decrease as well. In other words, by lowering temperature the consistency of SRS events increases, which may result in higher accuracy and better repeatability for applications such as photoacoustic microscopy.
Tables 1–3 summarize the numerical results of the graphs shown in Fig. 4 at each temperature level. Here, to decouple the SRS measurements from the fiber coupling efficiency, the results are shown in terms of the power coupled into the fiber. The stability is measured as the standard deviation of the pulse energies, and it is shown in term of nJ and also the percentage of deviation (RMS). Based on the measured data, a significant difference was observed between the temporal stability of individual peaks at selected temperature levels. The conversion efficiency, i.e., how much of the coupled light gets converted into each wavelength, is also improved by reducing the temperature of the SRS medium. This is in agreement with previous reports [27]. The total efficiency which is measured using cumulative energy converted from the 532 nm pump wavelength into other wavelength is also improved by lowering the temperature. We observed that higher pump powers lead to higher efficiency in all cases, which is to be expected. Additionally, the tables show that decreasing temperature causes a considerable rise in the intensity of the wavelengths at the higher end of the spectra. This might be related to the rise in the Kerr constant by lowering the temperature which can affect the SRS intensity [37]. It is worthwhile to mention that the general effect of temperature was consistent for other stock configurations and input powers.
Table 1. SRS characteristics at 300 K temperature
Table 2. SRS characteristics at 273 K temperature
Table 3. SRS characteristics at 195 K temperature
3.2 Multiwavelength photoacoustic remote sensing microscopy
The PARS system with the stabilized SRS-based multispectral system was applied to in vivo oxygen saturation measurement of a CAM model. Figure 5(A) shows a corresponding white light photograph of the CAM model. The temperature of the unit is set to 273 K to achieve temporally stable emissions with large enough pulse energies at 532 nm, 545 nm, and 558 nm spectral wavelengths. The output pulse energy measured on the sample was equal to 150 nJ, 100 nJ and 120 nJ at 558 nm, 545 nm, and 532 nm, respectively. Due to the motion of the CAM model, slight spatial shifts are observed between images. These shifts are corrected for using non-rigid image registration so that the spectral unmixing algorithm can subsequently be applied. Briefly, the unmixing algorithm solves the inverse problem of estimating the relative concentrations of oxy- and deoxyhemoglobin, [HbO2] and [Hb] respectively, on a per-pixel basis. The PARS response is approximately linear with respect to hemoglobin concentration, and a regularized least-squares solution is used to estimate the relative concentrations. In addition to the effects of absorption at the excitation wavelengths, the reflectivity of the detection wavelength for both oxy- and deoxyhemoglobin must be considered due to its scaling effect on the detected PARS amplitude. To account for this, estimates of the relative concentrations are normalized by the associated reflectivity. Reflectivity is approximated as inverse absorption at the detection wavelength of 830 nm. In future works, the scattering information provided through the probe beam of PARS can be used the same way as other scattering-based imaging modalities such as fundus photography or OCT to measure the amount of absorption inside the tissue. Figures 5(B)-(D) shows capillary beds in the CAM model imaged with 532 nm, 545 nm, and 558 nm, respectively. Each image was acquired over 10 seconds and the temporal sequence between images is ∼ 5–8 seconds. The oxygen saturation of the CAM model is presented in Fig. 5(E). Blood oxygenation saturation level is indicated using pseudocolor, ranging from blue to red in an ascending order.
Fig. 5. Functional oxygen saturation measurement of microvasculature in capillary beds. (A) Corresponding white light photograph of the CAM model. (B) PARS images acquired at 532 nm wavelength, (C) 545 nm, and (D) 558 nm. (E) Oxygen saturation map acquired using images shown in B, C, and D.
4. Conclusions
To summarize, we have investigated the effects of temperature on the spectral shape and temporal stability of SRS peaks generated in single-mode silica fibers. In a temperature-controlled condition, with constant laser output, we observed that by lowering the temperature of the fiber the temporal stability of the SRS peaks increases by as much as 60%. This temporally stable multispectral light source could improve the repeatability and may lead to more accurate functional measurements. Therefore, it is expected that in a longitudinal SO2 study, the temperature controlled multiwavelength light source will result in more accurate measurements. To accurately test the full implications of the improved SRS will require a system capable of satisfying the simultaneity therefore reducing the systematic error in measuring functional information. Several groups have reported methods to achieve ultrashort switching time (a few hundred nanoseconds) among wavelengths [24,38]. In future studies, similar methods can be used to evaluate the effect of light source stability on the accuracy of the measured values. It is also shown that as the temperature increases, the spectral bandwidth of the output beam broadens. Additionally, decreasing the temperature causes a considerable rise in the intensity of SRS peaks and significant growth of SRS cross section. The proposed method can be used to generate a cost-effective multiwavelength light source with high enough pulse energy and PRR for several imaging applications.
Funding
illumiSonics (SRA #083181); University of Waterloo; Centre for Bioengineering and Biotechnology; Mitacs (IT13594); Canada Foundation for Innovation (JELF #38000); Natural Sciences and Engineering Research Council of Canada (DGECR-2019-00143, RGPIN2019-06134); New Frontiers in Research Fund – Exploration (NFRFE-2019-01012).
Acknowledgments
The authors would like to thank Jean Flanagan for her continuous support and help. The authors would also like to thank Kevan Bell for his help. The authors acknowledge funding from the University of Waterloo, NSERC Discovery grant, MITACS accelerator program, Canada Foundation for Innovation (CFI-JELF), Centre for Bioengineering and Biotechnology seed funding, New Frontiers in Research Fund –exploration, and research partnership support from illumiSonics Inc.
Disclosures
Authors P. Haji Reza and B. Ecclestone have financial interests in illumiSonics Inc. illumiSonics partially supported this work.
Data availability
Data underlying the results presented in this paper are not publicly available at this time but may be obtained from the authors upon reasonable request.
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