纳米碳-二氧化锰注射液在大鼠和猪胃肠道染色标记定位中的应用

doi:10.12300/j.issn.1674-5817.2026.047

实验动物与比较医学 ›› 2026, Vol. 46 ›› Issue (5): 727-739.DOI: 10.12300/j.issn.1674-5817.2026.047

纳米碳-二氧化锰注射液在大鼠和猪胃肠道染色标记定位中的应用

陈婉琳¹(), 董庆睿², 李孟淘², 林楠³, 赵虎¹^,³, 张再重³, 曾令军⁴, 李佩⁵, 杨劲³, 王瑜¹^,²^,³, 黄爱文⁴()()

^1. 福建医科大学福总临床医学院普通外科, 福州 350025
^2. 厦门大学附属东方医院普通外科, 福州 350025
^3. 中国人民解放军联勤保障部队第九〇〇医院普通外科, 福州 350025
^4. 中国人民解放军联勤保障部队第九〇〇医院药剂科, 福州 350025
^5. 福建中医药大学福总教学医院(第九〇〇医院)普通外科, 福州 350025

收稿日期:2026-03-12 修回日期:2026-06-11 出版日期:2026-10-25 发布日期:2026-10-16
通讯作者: 黄爱文（1983—），女，博士，主任药师，研究方向：临床药学、药剂学。E-mail：hawen83@sina.com。ORCID：0009-0006-9848-4868
作者简介:陈婉琳（2002—），女，硕士研究生，研究方向：纳米材料在胃肠道手术精准定位与影像导航中的应用研究。E-mail：1578125112@qq.
com。ORCID：0009-0008-1856-8864
基金资助:
福建省科技计划项目“纳米炭染色联合钛夹标记技术提高腹腔镜辅助胃食管结合部腺癌根治术精准性、安全性和有效性的临床应用研究”(2024Y01010181)

Application of Carbon Nanoparticle-Manganese Dioxide Injection in Gastrointestinal Staining-Based Marking and Localization in Rats and Pigs

CHEN Wanlin¹(), DONG Qingrui², LI Mengtao², LIN Nan³, ZHAO Hu¹^,³, ZHANG Zaizhong³, ZENG Lingjun⁴, LI Pei⁵, YANG Jin³, WANG Yu¹^,²^,³, HUANG Aiwen⁴()()

^1. Department of General Surgery, Fuzong Clinical Medical College of Fujian Medical University, Fuzhou 350025, China
^2. Department of General Surgery, Dongfang Hospital Affiliated to Xiamen University, Fuzhou 350025, China
^3. Department of General Surgery, 900th Hospital of PLA Joint Logistic Support Force, Fuzhou 350025, China
^4. Department of Pharmacy, 900th Hospital of PLA Joint Logistic Support Force, Fuzhou 350025, China
^5. Department of General Surgery, Fuzong Teaching Hospital of Fujian University of Traditional Chinese Medicine (900th Hospital), Fuzhou 350025, China

Received:2026-03-12 Revised:2026-06-11 Published:2026-10-25 Online:2026-10-16
Correspondence to:
HUANG Aiwen (ORCID:0009-0006-9848-4868), E-mail: hawen83@sina.com

摘要/Abstract

摘要：

目的设计一种兼具肉眼染色与磁共振（magnetic resonance，MR）T₁/T₂双模态显像功能的纳米碳-二氧化锰（carbon nanoparticle–manganese dioxide，CN-MnO₂）注射液，并系统评价其理化性质、关键质量属性、生物相容性及胃肠道标记定位效能。方法采用温和液相原位氧化还原沉积原理制备CN-MnO₂，并进行透射电子显微镜、动态光散射（dynamic light scattering，DLS）、zeta电位（zeta potential）、X射线光电子能谱（X-ray photoelectron spectroscopy，XPS）和X射线衍射表征检测；采用pH计直接检测CN-MnO₂的pH，采用冰点下降法测定CN-MnO₂的渗透压，采用不依赖吸光度读数的凝胶法鲎试验检测细菌内毒素；观察4 ℃避光密封保存0、5、10 d CN-MnO₂注射液的外观，并检测其水合粒径、多分散指数、zeta电位及pH；以钆喷酸葡胺（gadopentetate dimeglumine，Gd-DTPA）作为阳性对照，设置不同浓度梯度，测定弛豫时间T₁、T₂，从而构建体外浓度-MR显像效能（r₁、r₂）曲线，比较弛豫效能并确定后续体内实验工作浓度；采用噻唑蓝比色法（methyl thiazolyl tetrazolium，MTT）、活/死细胞（live/dead）染色法评价细胞相容性。选取16只6周龄雄性SD大鼠，随机分为实验组和对照组，每组8只，皮下注射总Mn浓度为0.80 mmol/L的CN-MnO₂注射液或等体积生理盐水，通过定期监测体重、对主要脏器进行组织学HE染色观察、血常规与血清生化检测、炎症因子检测及电感耦合等离子体发射光谱法检测，以评价CN-MnO₂的短期体内安全性。选取8只5～6月龄的雄性巴马小型猪，随机分成CN-MnO₂注射液组（n=6）及纳米碳混悬注射液（carbon nanoparticle suspension injection，CNSI）组（n=2），分别在胃、小肠和结肠浆膜下注射CN-MnO₂注射液或CNSI，于注射完成后5 min内测量并记录各注射点晕染的最大直径，并于注射后第3、7天行MR T1WI/T2WI扫描，评价注射部位MR显像效果，末次观察后取注射部位（胃、小肠、结肠）及主要脏器，通过HE染色进行组织病理学评价。结果 CN-MnO₂注射液呈现黑色悬液状态，于室温（20～25 ℃）下静置15 d后未见明显团聚沉降，其平均水合粒径为（228.7±15.3）nm，多分散指数为0.184±0.021，zeta电位为（-24.6±2.8）mV；XPS显示CN-MnO₂主要由C、O和Mn元素组成，其中O元素含量占68.82%，Mn 2p在642.4 eV、653.1 eV呈现双特征峰；X射线衍射显示δ-MnO₂以低结晶度分散于碳基质中；其pH值为6.82±0.06，渗透压为（298.4±6.7）mOsm/kg，细菌内毒素水平低于检测限；体外MR显示，CN-MnO₂具有明显浓度依赖性，r₁及r₂分别为9.6 L·mmol⁻¹·s⁻¹和17.2 L·mmol⁻¹·s⁻¹，具备较好的T₁/T₂对比效能，且均优于Gd-DTPA；在0.80 mmol/L浓度下，CN-MnO₂的体外细胞实验未见明显细胞毒性。CN-MnO₂在SD大鼠体内的短期安全性评价均未见明显炎症反应、肝肾功能损伤或主要脏器Mn异常蓄积。巴马小型猪体内实验显示，CN-MnO₂组胃、小肠和结肠晕染平均直径分别为（0.65±0.12）cm、（0.61±0.11）cm和（0.58±0.10）cm，不同注射部位晕染直径差异无统计学意义（P>0.05），但CN-MnO₂组平均晕染直径明显小于CNSI组（P<0.05）；MR检查显示，CN-MnO₂组在第3天和第7天均可辨认注射部位，且第3天信号更明显；末次观察时，CN-MnO₂组的注射部位及主要脏器未见明显的异常病理改变。结论本研究成功制备出粒径均一且理化性质稳定的CN-MnO₂注射液，可实现胃肠道术前染色标记与MR T₁/T₂双模态显像的统一，为胃肠道术前标记定位和术中精准切除提供了新策略。

关键词: 纳米碳-二氧化锰, T₁/T₂双模态显像, 胃肠道手术, SD大鼠, 巴马小型猪

Abstract:

Objective To develop a carbon nanoparticle-manganese dioxide (CN-MnO₂) injection integrating visually identifiable staining and magnetic resonance (MR) T₁/T₂ dual-modal imaging, and to systematically evaluate its physicochemical properties, critical quality attributes, biocompatibility, and efficacy for gastrointestinal marking and localization. Methods CN-MnO₂ was prepared using a mild liquid-phase in situ redox deposition strategy and characterized by transmission electron microscopy (TEM), dynamic light scattering (DLS), zeta potential analysis, X-ray photoelectron spectroscopy (XPS), and X-ray diffraction (XRD). The pH of CN-MnO₂ was directly measured using a pH meter. The osmolality pressure of CN-MnO₂ was determined by the freezing point depression method. The bacterial endotoxin was detected using the gel-clot Limulus amebocyte lysate test, which did not rely on absorbance readings. The appearance of the CN-MnO₂ injection solution stored at 4 ℃ under light shielding and sealed for 0, 5, and 10 days was observed, and its hydrated particle size, polydispersity index, zeta potential, and pH were also measured. With gadopentetate dimeglumine (Gd-DTPA) as the positive control, different concentration gradients were established, and T₁ and T₂ relaxation times were measured to construct concentration-dependent plots of the longitudinal and transverse relaxation rates (R₁ and R₂) and calculate the corresponding relaxivities (r₁ and r₂), compare relaxivity performance, and determine the working concentration for subsequent in vivo experiments. Cytocompatibility was assessed using the methyl thiazolyl tetrazolium (MTT) assay and live/dead staining. Sixteen male 6-week-old SD rats were randomly assigned to an experimental group and a control group (n=8 per group) and subcutaneously injected with CN-MnO₂ injection at a total Mn concentration of 0.80 mmol/L or an equal volume of normal saline, respectively. Short-term in vivo safety was evaluated by regular body weight monitoring, hematoxylin-eosin (HE) staining of major organs, hematological and serum biochemical analyses, inflammatory cytokine detection, and inductively coupled plasma optical emission spectrometry (ICP-OES) analysis. Eight male 5–6-month-old Bama minipigs were randomly assigned to a CN-MnO₂ group (n=6) and a carbon nanoparticle suspension injection (CNSI) group (n=2). CN-MnO₂ injection or CNSI was injected subserosally into the stomach, small intestine, and colon. Within 5 min after each injection, the maximum staining diameter at each injection site was measured and recorded. MR T1WI/T2WI scans were performed on days 3 and 7 after injection to evaluate MR visualization at the injection sites. At the end of observation, the injection sites and major organs were collected for histopathological evaluation by hematoxylin-eosin staining. Results CN-MnO₂ appeared as a black suspension, with no obvious aggregation or sedimentation after standing at room temperature (20-25 ℃) for 15 days. Its average hydrodynamic diameter was approximately (228.7±15.3) nm, the polydispersity index was 0.184±0.021, and the zeta potential was (-24.6±2.8) mV. XPS showed that CN-MnO₂ was mainly composed of C, O, and Mn, with oxygen accounting for approximately 68.82%. The Mn 2p spectrum exhibited two characteristic peaks at 642.4 and 653.1 eV. XRD indicated that low-crystallinity δ-MnO₂ was dispersed within the carbon matrix. The pH was 6.82±0.06, the osmolality was (298.4±6.7) mOsm/kg, and the bacterial endotoxin level was below the detection limit. In vitro MR imaging showed a clear concentration-dependent response, with r₁ and r₂ values of 9.6 L·mmol^-1·s^-1 and 17.2 L·mmol^-1·s^-1, respectively, indicating favorable T₁/T₂ contrast performance superior to that of Gd-DTPA. At 0.80 mmol/L, CN-MnO₂ showed no obvious cytotoxicity in vitro. Short-term safety evaluation in SD rats revealed no obvious inflammatory response, impairment of liver or renal function, or abnormal manganese accumulation in major organs. In Bama minipigs, the mean staining diameters of the CN-MnO₂ group in the stomach, small intestine, and colon were (0.65±0.12) cm, (0.61±0.11) cm, and (0.58±0.10) cm, respectively, with no significant difference among the three injection sites (P>0.05). The overall mean staining diameter was smaller in the CN-MnO₂ group than in the CNSI group (P<0.05). MR examinations showed that the injection sites were identifiable on both day 3 and day 7, with stronger signals observed on day 3. At the end of observation, no obvious pathological abnormalities were observed at the injection sites or in major organs. Conclusion A CN-MnO₂ injection with uniform particle size and stable physicochemical properties can be successfully prepared. This formulation integrates visible gastrointestinal staining with MR T₁/T₂ dual-modal imaging, providing a new strategy for preoperative gastrointestinal marking and localization as well as precise intraoperative resection.

Key words: Carbon nanoparticle-manganese dioxide, T₁/T₂ dual-modal imaging, Gastrointestinal surgery, SD rats, Bama minipigs

中图分类号:

陈婉琳,董庆睿,李孟淘,等. 纳米碳-二氧化锰注射液在大鼠和猪胃肠道染色标记定位中的应用[J]. 实验动物与比较医学, 2026, 46(5): 727-739. DOI: 10.12300/j.issn.1674-5817.2026.047.

CHEN Wanlin,DONG Qingrui,LI Mengtao,et al. Application of Carbon Nanoparticle-Manganese Dioxide Injection in Gastrointestinal Staining-Based Marking and Localization in Rats and Pigs[J]. Laboratory Animal and Comparative Medicine, 2026, 46(5): 727-739. DOI: 10.12300/j.issn.1674-5817.2026.047.

图/表 3

图1 CN-MnO2注射液的理化性质表征

注：A，静置15 d后的CN-MnO₂注射液；B，CN-MnO₂的透射电子显微镜观察结果（标尺=200 nm）；C，CN-MnO₂的水合粒径分布；D，CN-MnO₂的zeta电位分布；E～H，CN-MnO₂的X射线光电子能谱总谱及C、Mn、O元素谱；I，CN-MnO₂的X射线衍射图谱。CN-MnO₂，纳米碳-二氧化锰。

Figure 1 Physicochemical characterization of CN-MnO2 injection

Note： A， Appearance of CN-MnO₂ injection after standing for 15 days； B， Transmission electron microscopy （TEM） image of CN–MnO₂（scale bar=200 nm）； C， Hydrodynamic size distribution of CN-MnO₂； D，Zeta potential distribution of CN-MnO₂； E–H， X-ray photoelectron spectroscopy （XPS） survey spectrum and high-resolution spectra of C， Mn， and O of CN–MnO₂； I， X-ray diffraction （XRD） pattern of CN-MnO₂. CN-MnO₂，carbon nanoparticle–manganese dioxide.

图2 CN-MnO2的体外显影性能与生物安全性评价

注：A～B，CN-MnO₂注射液与L929细胞作用24 h和48 h后的MTT检测结果；C，SD大鼠注射CN-MnO₂注射液后的体重变化；D，注射CN-MnO₂注射液后SD大鼠心脏、肝脏、脾脏、肺脏和肾脏的HE染色结果（标尺=50 μm）；E，不同浓度梯度CN-MnO₂注射液和Gd-DTPA的肉眼外观；F，CN-MnO₂注射液及Gd-DTPA在不同质量浓度下的体外磁共振（MR）T₁/T₂显像结果及弛豫速率拟合曲线。CN-MnO₂，纳米碳-二氧化锰；Gd-DTPA，钆喷酸葡胺。

Figure 2 In vitro imaging performance and biosafety evaluation of CN-MnO2

Note： A-B， MTT assay results of L929 cells after incubation with CN-MnO₂ injection for 24 h and 48 h； C， Body weight change curves of SD rats after CN-MnO₂ injection； D， HE staining of major organs （heart， liver， spleen， lung， and kidney） in SD rats after CN-MnO₂ injection （scale bar=50 μm）； E， Visual observation of CN-MnO₂ injections and Gd-DTPA at different concentration gradients； F， In vitro magnetic resonance （MR） T₁/T₂ imaging results and relaxivity fitting curves of CN-MnO₂ injection and Gd-DTPA at different concentrations. CN-MnO₂， carbon nanoparticle-manganese dioxide； Gd-DTPA， gadopentetate dimeglumine.

图3 巴马小型猪注射CN-MnO2后的体内实验结果及组织病理学检查结果

注：A，注射CN-MnO₂注射液后第3天和第7天巴马小型猪胃、小肠和结肠浆膜的磁共振（MR）显像结果；B，CN-MnO₂组与CNSI组巴马小型猪胃、小肠和结肠注射部位的晕染直径比较；C，巴马小型猪CN-MnO₂注射部位（胃、小肠、结肠）的HE染色结果，标尺=50 μm；D，巴马小型猪主要器官（心、肝、脾、肺、肾）的HE染色结果，标尺=50 μm。CN-MnO₂，纳米碳-二氧化锰；CNSI，纳米碳混悬注射液；MR，磁共振。与CNSI组相比，^* P<0.05。

Figure 3 In vivo experimental results and histopathological examination of Bama minipigs following CN-MnO2 injection

Note： A， MR images obtained on days 3 and 7 after subserosal injection of CN-MnO₂ into the stomach， small intestine， and colon of Bama minipigs； B， Comparison of staining diameters at the injection sites in the stomach， small intestine， and colon between the CN-MnO₂ group and the CNSI group； C， HE staining of the injection site （stomach， small intestine， colon） in Bama minipigs after CN-MnO₂ injection， scale bar=50 μm； D， HE staining of major organs （heart， liver， spleen， lung， kidney） in Bama minipigs after CN-MnO₂ injection， scale bar=50 μm. CN-MnO₂， carbon nanoparticle-manganese dioxide； CNSI， carbon nanoparticle suspension injection； MR， magnetic resonance. Compared with the CNSI group， ^* P<0.05.

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纳米碳-二氧化锰注射液在大鼠和猪胃肠道染色标记定位中的应用

Application of Carbon Nanoparticle-Manganese Dioxide Injection in Gastrointestinal Staining-Based Marking and Localization in Rats and Pigs

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