Forward-view photoacoustic (PA) endoscopy (PAE) is promising for achieving noninvasive biopsy in narrow areas of internal organs. However, current schemes that scan the proximal end of fiber bundles' core-by-cores would cause limited spatial sampling confined by the number of cores, which result in lower lateral resolution at smaller probe size. In this paper, a flexible forward-view PAE probe based on a resonant fiber scanner with a diameter of 5 mm was developed, which compactly integrated a piezoelectric (PZT) bender, a fiber cantilever, a lens, an ultrasound transducer, and a coupler inside. Phantom imaging was conducted to evaluate the performance of the flexible forward-view PAE, exhibiting a lateral resolution of 15.6 μm in a field-of-view of approximately 3 mm diameter and the imaging speed is 0.5 frames per second. In vivo imaging shows the clear vascular network of the rat gastrointestinal wall, which demonstrates the feasibility of resonant fiber scanners for photoacoustic endoscopic imaging, and indicates its potential for application as minimally invasive tools in the clinical evaluation of gastrointestinal lesions.

Photoacoustic imaging (PAI) has been rapidly developed as a noninvasive mesoscopic imaging technique to enable more accurate diagnosis, surgical treatment guidance, and disease monitoring.1–61. L. V. Wang and S. Hu, Science 335, 1458 (2012). https://doi.org/10.1126/science.12162102. V. Ntziachristos, J. Ripoll, L. V. Wang, and R. Weissleder, Nat. Biotechnol. 23, 313 (2005). https://doi.org/10.1038/nbt10743. M. Omar, J. Aguirre, and V. Ntziachristos, Nat. Biomed. Eng. 3, 354 (2019). https://doi.org/10.1038/s41551-019-0377-44. P. Beard, Interface Focus 1, 602 (2011). https://doi.org/10.1098/rsfs.2011.00285. D. Das, A. Sharma, P. Rajendran, and M. Pramanik, Phys. Med. Biol. 66, 05TR01 (2021). https://doi.org/10.1088/1361-6560/abd6696. I. Steinberg, D. M. Huland, O. Vermesh, H. E. Frostig, W. S. Tummers, and S. S. Gambhir, Photoacoustics 14, 77 (2019). https://doi.org/10.1016/j.pacs.2019.05.001 Compared to traditional optical imaging based on light reflection, PAI combines the advantages of optical imaging and ultrasound imaging, providing high resolution at depth penetration, high specificity, and high contrast 3D images.7–107. S. Liu, X. Feng, H. Jin, R. Zhang, Y. Luo, Z. Zheng, F. Gao, and Y. J. Zheng, IEEE Trans. Med. Imaging 38, 2037 (2019). https://doi.org/10.1109/TMI.2019.29006568. J. M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, Nat. Med. 18, 1297 (2012). https://doi.org/10.1038/nm.28239. H. Ma, Z. Cheng, Z. Wang, W. Zhang, and S. Yang, Appl. Phys. Lett. 116, 073703 (2020). https://doi.org/10.1063/1.514315510. L. Wang, D. Ke, H. Xin, R. Liu, S. Pan, K. Xiong, and S. Yang, Appl. Phys. Lett. 122, 023701 (2023). https://doi.org/10.1063/5.0135655Until now, a variety of PA endoscopies (PAEs) have been adopted for in vivo imaging.11–1511. H. Guo, Y. Li, W. Qi, and L. Xi, J. Biophoton. 13, e202000217 (2020). https://doi.org/10.1002/jbio.20200021712. T. Guo, K. Xiong, Z. Zhang, L. Li, and S. Yang, Appl. Phys. Lett. 118, 153702 (2021). https://doi.org/10.1063/5.004985513. X. Li, K. Xiong, and S. Yang, Appl. Phys. Lett. 114, 163703 (2019). https://doi.org/10.1063/1.509378914. Y. Li, G. Lu, Q. Zhou, and Z. Chen, Photonics 8, 281 (2021). https://doi.org/10.3390/photonics807028115. Y. Liang, W. Fu, Q. Li, X. Chen, H. Sun, L. Wang, L. Jin, W. Huang, and B.-O. Guan, Nat. Commun. 13, 7604 (2022). https://doi.org/10.1038/s41467-022-35259-5 Due to the narrow natural cavity of the human body, a suitable scanning strategy is needed when designing PAE probes to ensure that the probe size is suitable. Most PAEs employ mechanical scanning by a torque coil to achieve a rotational scan of the imaging probe and a linear motorized stage to produce a pullback along the probe axis to acquire images.16–1916. M. Kim, K. W. Lee, K. Kim, O. Gulenko, C. Lee, B. Keum, H. J. Chun, H. S. Choi, C. U. Kim, and J. M. Yang, Photoacoustics 26, 100346 (2022). https://doi.org/10.1016/j.pacs.2022.10034617. J. Hui, Y. Cao, Y. Zhang, A. Kole, P. Wang, G. Yu, G. Eakins, M. Sturek, W. Chen, and J.-X. Cheng, Sci. Rep. 7, 1417 (2017). https://doi.org/10.1038/s41598-017-01649-918. Y. Li, R. Lin, C. Liu, J. Chen, H. Liu, R. Zheng, X. Gong, and L. Song, J. Biophoton. 11, e201800034 (2018). https://doi.org/10.1002/jbio.20180003419. X. Wen, P. Lei, S. Huang, X. Chen, Y. Yuan, D. Ke, R. Liu, J. Liang, E. Wang, B. Wei, K. Xiong, and S. Yang, Photon. Res. 11, 55 (2023). https://doi.org/10.1364/PRJ.470737 However, using this scanning strategy, PAE systems are only capable of side-view imaging.In recent years, forward-view PAE systems develop rapidly. Comparing to side-view PAE, they have flexibility to locate the complex examined area.20–2520. R. Ansari, E. Z. Zhang, A. E. Desjardins, and P. C. Beard, Light Sci. Appl. 7, 75 (2018). https://doi.org/10.1038/s41377-018-0070-521. C. Lu, K. Xiong, Y. Ma, W. Zhang, Z. Cheng, and S. Yang, Opt. Express 28, 15300 (2020). https://doi.org/10.1364/OE.39249322. H. Guo, Q. Chen, T. Li, D. Sun, and L. Xi, J. Biophoton. 15, e202200116 (2022). https://doi.org/10.1002/jbio.20220011623. T. Zhao, M. T. Ma, S. Ourselin, T. Vercauteren, and W. Xia, Photoacoustics 25, 100323 (2022). https://doi.org/10.1016/j.pacs.2021.10032324. G. Li, Z. Guo, and S.-L. Chen, IEEE Sens. J. 19, 909 (2019). https://doi.org/10.1109/JSEN.2018.287880125. R. Ansari, E. Z. Zhang, A. E. Desjardins, and P. C. Beard, Opt. Lett. 45, 6238 (2020). https://doi.org/10.1364/OL.400295 In previous studies, the schemes that scan the proximal end of bundles for imaging are slightly inadequate, which results in spatial sampling resolution limited by the number of cores.20,24,2520. R. Ansari, E. Z. Zhang, A. E. Desjardins, and P. C. Beard, Light Sci. Appl. 7, 75 (2018). https://doi.org/10.1038/s41377-018-0070-524. G. Li, Z. Guo, and S.-L. Chen, IEEE Sens. J. 19, 909 (2019). https://doi.org/10.1109/JSEN.2018.287880125. R. Ansari, E. Z. Zhang, A. E. Desjardins, and P. C. Beard, Opt. Lett. 45, 6238 (2020). https://doi.org/10.1364/OL.400295 If a smaller probe size is desired, the number of cores in the bundle also decreases, and effective spatial sampling may be less. Microelectromechanical systems (MEMS) scanners enable fine spatial sampling; however, folding the light path inevitably increases the size of the probe.21,2221. C. Lu, K. Xiong, Y. Ma, W. Zhang, Z. Cheng, and S. Yang, Opt. Express 28, 15300 (2020). https://doi.org/10.1364/OE.39249322. H. Guo, Q. Chen, T. Li, D. Sun, and L. Xi, J. Biophoton. 15, e202200116 (2022). https://doi.org/10.1002/jbio.202200116A piezoelectric actuator drives the fiber cantilever to scan in a resonance mode, and it is a widely used strategy for optical endoscopic imaging.26–2926. Y. S. Leong, M. H. H. Mokhtar, M. S. D. Zan, N. Arsad, M. B. I. Reaz, and A. A. A. Bakar, IEEE Access 9, 132705 (2021). https://doi.org/10.1109/ACCESS.2021.311534727. C. M. Lee, C. J. Engelbrecht, T. D. Soper, F. Helmchen, and E. J. Seibel, J. Biophoton. 3, 385 (2010). https://doi.org/10.1002/jbio.20090008728. K. Liang, Z. Wang, O. O. Ahsen, H.-C. Lee, B. M. Potsaid, V. Jayaraman, A. Cable, H. Mashimo, X. Li, and J. G. Fujimoto, Optica 5, 36 (2018). https://doi.org/10.1364/OPTICA.5.00003629. A. Lombardini, V. Mytskaniuk, S. Sivankutty, E. R. Andresen, X. Chen, J. Wenger, M. Fabert, N. Joly, F. Louradour, A. Kudlinski, and H. Rigneault, Light Sci. Appl. 7, 10 (2018). https://doi.org/10.1038/s41377-018-0003-3 Single-fiber-based resonance scanning can achieve more spatial samples than that of fiber-bundles-based core-by-core scanning in the same size of probe. In addition, the fiber-based resonant scanner is proficient in the rapid scanning speed, light weight, and small size.30,3130. H. Guan, D. Li, H.-C. Park, A. Li, Y. Yue, Y.-T. A. Gau, M.-J. Li, D. E. Bergles, H. Lu, and X. Li, Nat. Commun. 13, 1534 (2022). https://doi.org/10.1038/s41467-022-29236-131. K. Hwang, Y.-H. Seo, D. Y. Kim, J. Ahn, S. Lee, K. H. Han, K.-H. Lee, S. Jon, P. Kim, K. E. Yu, H. Kim, S.-H. Kang, and K.-H. Jeong, Microsyst. Nanoeng. 6, 72 (2020). https://doi.org/10.1038/s41378-020-00182-6 In this study, this scanning strategy was applied to PAI. A fiber resonant scanner that integrated a commercial PZT driver was fabricated to form the PAE probe. The experimental results demonstrated that the flexible forward-view PAE has great imaging capability. The fiber-scanning-based PAE provides an effective solution for clinical application.Figure 1(a) shows the detailed internal structure of the probe. The resonant fiber scanner is made by connecting a 2D PZT bender (NAC2710, Noliac) to a single-mode fiber (SMF) cantilever. The SMF cantilever is 15 mm long. A stainless-steel tube (300 μm inner diameter, 400 μm outer diameter, and 2.9 mm long) is attached to the end of the cantilever to adjust the resonant frequency of the SMF cantilever. The 2D PZT bender has four electrodes, two of which are constant voltage electrodes and the remaining two are X and Y electrodes. The constant voltage electrodes are connected to +30 and −30 V. The X and Y electrodes can be controlled by a voltage from −30 to +30 V. The driving voltage applied to X and Y electrodes determines the vibration frequency and amplitude of the PZT bender. Two achromatic lenses with an external diameter of 3 mm are used to collimate and focus the laser beam emitted from the SMF cantilever tip, enabling a two-dimensional spiral scan of the laser beam across the tissue surface. The resulting PA signal is reflected by a 45° tilted glass sheet mounted in the coupler and then detected by a planar ultrasound transducer (15 MHz, effective area 2 × 2 mm2, thickness 0.5 mm) located on the sidewall of the coupler. During the experiment, water was used as the ultrasonic coupling medium, sealed in the coupler with a transparent film. The resonant fiber scanner, lens, unfocused ultrasound transducer, and coupler were compactly integrated into a medical stainless steel tube with an outer diameter of 5 mm. Figure 1(c) shows a photograph of the probe.Figure 1(b) shows the configuration of the PAI system developed with a flexible forward-view PAE probe based on the resonant fiber scanner. The excitation laser beam emits a 532 nm laser from a pulsed laser (Mosquitoo X 532–2-V, InnoLas) at a repetition rate of 100 kHz. The laser is spatially filtered and coupled into the SMF by a fiberport coupler (PAF-X-7 A, Thorlabs). The PZT controller has four output ports that supply the four electrodes of the PZT bender with the suitable voltage. A low noise amplifier (LNA-650, RFBAY) amplifies the PA signal detected by the ultrasound transducer, and a high-speed data acquisition card (M2p.5960-x4, Spectrum) digitizes the amplified PA signal at a sampling rate of 125 MHz. Image reconstruction was performed by user-defined programs in LabVIEW (NI) and MATLAB (R2019a, Math Works).The frequency response of the resonant fiber scanner and the scan range at resonant frequencies are important parameters for optimizing the fiber scan. The laser scan trajectory of the flexible forward-view PAE probe is recorded by a position sensing detector (PSD) (PDP90A, Thorlabs). When the amplitude-modulated sine wave voltage is applied to the scanner's X and Y electrodes individually, the fiber cantilever is scanning in one dimension at the relevant direction. When the drive voltage is 1.4 Vpp, by changing its frequency, the maximum scan range appears at 127 and 130 Hz, as shown in Fig. 2(a). Gradually increasing the drive voltage from 0 to 2 Vpp, the scanning range in both directions increases linearly, as shown in Fig. 2(b). The spiral scan pattern is achieved by two amplitude modulated sine waves with a phase difference of 90°, and the schematic of the drive waveform is shown in Fig. 2(c). As the 128 Hz, 1.5 Vpp drive voltage is applied to X and Y electrodes, the magnitude of the scan range in both directions is approximately the same, and the angle between the scan lines is 89°, showing good orthogonality, as shown in Fig. 2(d). The actual scan trajectory of the resonant fiber scanner is not exactly the same as the expected scan trajectory; therefore, the PSD is used to acquire the actual scan trajectory and store the coordinate data of the trajectory as the reference for image reconstruction. The supplementary material shows the schematic of the PSD-based scanning trajectory acquisition system and flow chart of image reconstruction that using the coordinate data of the trajectory. Figure 2(e) shows the laser scan trajectories recorded by the PSD for one scan cycle, the coverage area of the trajectory is close to circular, and it contains the location information of 100 000 spatial sampling points. Figure 2(f) shows the density of the scan trajectories in Fig. 2(e) and demonstrates that the scan trajectories are most dense in the region at the center of the trajectory. Figure 2(g) shows the imaging scan and natural braking process recorded by the camera, the imaging scan cost 1 s, and the natural braking was about 0.2 s.In order to obtain the best performance index of the PAE probe, the experiments shown in Fig. 3 were performed. A steel mesh is used as an imaging sample to determine the field-of-view (FOV). Figure 3(a) is a microscopic picture of the steel mesh, and Fig. 3(b) is a PA maximum amplitude projection (MAP) image of the steel mesh. It can be seen from Fig. 3(b) that the largest imaging area of PAE is a circular area with a diameter of 3.0 mm. To evaluate the lateral resolution, the sharp edges of the surgical blade were imaged. The black dots in Fig. 3(c) indicate the normalized original edge profile, the blue curve is the edge spread function (ESF) curve, the red curve shows the resulting line spread function (LSF), and the lateral resolution was estimated to be 15.6 μm by calculating the full width at half maximum (FWHM) of the LSF curve. To evaluate the axial resolution of the probe, a typical PA A-line signal (after Hilbert transform) was obtained. After calculating the FWHM of the PA signal, the axial resolution of the system was estimated to be 168 μm, as shown in Fig. 3(d). To demonstrate the complex structure imaging ability of the PAE probe, a leaf vein phantom was imaged, as shown in Figs. 3(e) and 3(f). Figure 3(e) shows a photograph of the black leaf veins. Figure 3(f) shows the PA MAP image in Fig. 3(e), in which the details of the leaf veins can be seen. The imaging results accurately show the morphology and structure of the sample.To verify the ability of the PAE probe to image the blood vessels of organs in vivo, the stomach and intestine wall of rats were imaged. First, anesthetized and maintained the SD rats using isoflurane (concentration: 2% Vol; gas velocity: 0.4 L/min), and then depilated them to avoid being affected by hair during the experiment. Next, the rat's abdominal cavity was opened with a scalpel to expose the stomach and intestine. To ensure complete coupling of the probe to the tissue, a small amount of water was applied to the surface of the imaging area. Finally, hold the probe for the experiment. During the experiment, according to the American National Standards Institute safety limit (20 mJ/cm2),3232. Laser Institute of America, American National Standard for Safe Use of Lasers ANSI Z136.1-2014 ( American National Standards Institute, Inc., Washington, D.C., 2014). the energy focused by a single laser pulse is limited to 800 nJ. All experimental results showed that there was no significant damage to the stomach and intestine. All procedures were approved by South China Normal University. The vascular network of the rat gastric wall is shown in Figs. 4(a) and 4(b). The imaging area of Fig. 4(a) is close to the greater curvature of the stomach, while that of Fig. 4(b) is close to the lesser curvature of the stomach. Figures 4(c) and 4(d) show the vascular network of the rat intestinal wall. Figure 4(c) is the vascular network of the large intestine, and Fig. 4(d) is the vascular network of the small intestine. A Hessian-matrix-based method was used to enhanced the vascular network to reduce the moiré fringe caused by spiral scanning.3333. H.-C. Zhou, N. Chen, H. Zhao, T. Yin, J. Zhang, W. Zheng, L. Song, C. Liu, and R. Zheng, Photoacoustics 15, 100143 (2019). https://doi.org/10.1016/j.pacs.2019.100143Imaging with a large FOV in a short time is very convenient for clinical applications, and a large range of images were obtained by moving the probe and stitching the acquired PA images by a feature-based algorithm.3434. W. Zhang, H. Ma, Z. Cheng, Z. Wang, K. Xiong, and S. Yang, Opt. Lett. 45, 1599 (2020). https://doi.org/10.1364/OL.388863 The results shown in Fig. 5 are stitched together from seven PA images with overlapping areas between two adjacent ones. A larger range of imaging can be achieved based on this method as long as the computer performance allows.

In summary, a flexible forward-view PAE system by using a fiber resonant scanner was demonstrated, which enables adequate spatial sampling at small probe sizes. Phantom and in vivo imaging demonstrated that this approach is possible to obtain clear and correct PA images. In the future, our scheme will be further improved in the following ways. First, the diameter and rigid length of the probe can be reduced by using a smaller PZT tube. Second, the imaging frame rate can be further improved by using a higher repetition frequency laser and simultaneously increasing the scanning frequency of the fiber resonance scanner, or by reducing the braking time between imaging scans. Third, the Fabry–Pérot ultrasound transducer can be applied to better axial resolution and obtain more accurate depth information. In addition, changing the excitation light wavelength for PA imaging can capture other components within the tissue and can also be combined with optical imaging techniques to obtain more comprehensive information for clinical diagnosis.

See the supplementary material for the schematic of the PSD-based scanning trajectory acquisition system and the flow chart of image reconstruction.

This work was supported by the National Natural Science Foundation of China (Nos. 62005084, 61627827, and 61822505), the Natural Science Foundation of Guangdong Province (Nos. 2022A1515010548 and 2022A1515011247), the Science and Technology Program of Guangzhou (Nos. 2019050001 and 202206010094), and STI2030-Major Projects (No. 2022ZD0212200).

Conflict of Interest

The authors have no conflicts to disclose.

Author Contributions

Di Ke: Methodology (lead); Software (lead); Writing – original draft (lead). Li Wang: Software (equal); Visualization (equal). Erqi Wang: Resources (equal); Software (equal). Haishu Xin: Resources (equal); Validation (equal). Sihua Yang: Project administration (equal); Supervision (equal); Writing – review & editing (equal). Kedi Xiong: Conceptualization (lead); Project administration (equal); Supervision (equal); Writing – review & editing (lead).

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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