Whole-mount Serial Sections Research Articles

Whole-mount pathology of breast lumpectomy specimens improves detection of tumour margins and focality.

Technical limitations in conventional pathological evaluation of breast lumpectomy specimens may reduce diagnostic accuracy in the assessment of margin and focality. A novel technique based on whole-mount serial sections enhances sampling while preserving specimen conformation and orientation. The aim of this study was to investigate assessment of focality and margin status by the use of whole-mount serial sections versus simulated conventional sections in lumpectomies. Two pathologists interpreted whole-mount serial sections and simulated conventional sections for 58 lumpectomy specimens by reporting the closest margin and focality. Measurements were compared by the use of McNemar's chi-squared test. Statistically significant differences were observed in the assignment of both margin positivity (P = 0.014) and multifocality (P = 0.021). A positive margin or multifocal disease was identified by the use of whole-mount serial sections but missed in the simulated conventional assessment in 10.3% and 17.2% of all cases, respectively. There was no case in which a positive margin was detected only in the simulated conventional assessment. The whole-mount technique is more sensitive than conventional assessment for identifying a positive margin or multifocal disease in breast lumpectomy specimens. Undersampling in conventional sections was implicated in almost all cases of discordance. The majority of positive margins or secondary foci identified only in whole-mount serial sections concerned in-situ disease.

Is the striated urethral sphincter at risk by standard suture ligation of the dorsal vascular complex in radical prostatectomy? An anatomic study.

To perform an anatomic study of the dorsal vascular complex (DVC) and the underlying striated sphincter (SS) to investigate if the SS might be harmed by standard suture ligation in radical prostatectomy. Transverse wholemount serial sections were created from adult male autopsy cadavers. The total surface area of the DVC and the SS were measured at the prostatic apex and 5 mm distal to it using the ImageJ software. The dorsal boundary of the DVC and the ventral border of the SS were defined digitally. The percentage of the surface area of the SS that would be entrapped by a ligation stitch including the entire DVC was then calculated. In addition, 3-dimensional reconstruction of the lower urinary tract was performed using the SURFdriver software. Five adult male cadavers were investigated. The mean surface area of the SS was 116.1 ± 80.7 and 78.0 ± 63.3 mm(2) at the apex and 5 mm distal to it, respectively. On average, 36.7% (42.6 ± 41.4 mm(2)) and 29.9% (23.3 ± 13.6 mm(2)) of the surface area of the SS were located ventral to the lower boundary of the DVC at the apex and 5 mm distal to it, respectively, and would thus be entrapped by standard suture ligation. Our anatomic findings suggest that standard suture ligation of the DVC is associated with the risk of affecting sphincter tissue. Our study is in accordance with recent clinical studies showing improved early postoperative continence rates by primary transection of the DVC followed by selective suture ligation.

Clinicopathological study of safe resectional margin in mid and low rectal cancer after neoadjuvant chemoradiotherapy

To investigate the regression pattern of mid and low rectal cancer treated with neoadjuvant chemoradiotherapy and then to provide the pathological proofs for reasonable resectional margin in rectal cancer surgery. Forty cases of mid and low rectal cancer patients received concurrent chemoradiotherapy and then underwent radical operation. The whole-mount serial sections of resected rectal cancer specimen were stained with cytokeratin antibody using immunohistochemical techniques to show the residual cancer cells under the mucosa. The microscopic measurement was performed to determine the reverse infiltration of cancer cells in the rectal wall and to describe the cancer cells scatter ways in the cancer mass. The Ki-67 immunohistochemical stain was also performed to show the proliferation activity of residual cancer cells after neoadjuvant chemoradiotherapy. The length of specimen was shrinking continuously during the pathologic section production and the shrink rate was 18%. There were remanent cancer cells which showed positive Ki-67 expression and the chemoradiotherapy decreased the Ki-67 expression significantly. The lower edge of remaining ulcers or scars could be used as the reference point from which the cancer infiltration could be measured. According to our measurement, the average reverse infiltration of cancer cells in the whole-mount section was (6.1±4.7) mm, the deepest one was 11.0 mm in the section which could be converted into fresh bowel length of 12.98 mm. The pathology showed that the residual cancer cells scattered in the fibrous tissue of ulcers, scars and manifested a regression of spatial distribution. The rectal cancers show regression in different degrees after neoadjuvant chemoradiotherapy. The residual cancer cells in the fiber tissues manifest proliferation activity. The distal end of resection should be at least 2 cm away from the lower edge of ulcers or scars of primary tumor in the rectal wall in patients after neoadjuvant chemoradiotherapy. The circumferential resection margin should include all the fibrous scar of the tumor area to ensure the remove of tumor cells completely.

Determination of an Optimal Standardized Uptake Value of Fluorodeoxyglucose for Positron Emission Tomography Imaging to Assess Pathological Volumes of Cervical Cancer: A Prospective Study

PurposeTo determine the optimal standardized uptake value (SUV) of 18F-fluorodeoxyglucose (18F-FDG) for positron emission tomography (PET) imaging, at which the PET-defined gross tumor volume (GTVPET) best matches with the pathological volume (GTVPATH) in the cervical cancer.Materials and MethodsTen patients with the cervical cancer who underwent surgery were enrolled in this study. The excised specimens were processed for whole-mount serial sections and H-E staining. The tumor borders were outlined in sections under a microscope, histopathological images were scanned and the GTVPATH calculated. The GTVPET was delineated automatically by using various percentages relative to the maximal SUV and absolute SUV. The optimal threshold SUV was further obtained as the value at which the GTVPET best matched with the GTVPATH.ResultsAn average of 85±10% shrinkage of tissue was observed after the formalin fixation. The GTVPATH was 13.38±2.80 cm3 on average. The optimal threshold on percentile SUV and absolute SUV were 40.50%±3.16% and 7.45±1.10, respectively. The correlation analysis showed that the optimal percentile SUV threshold was inversely correlated with GTVPATH (p<0.05) and tumor diameter (p<0.05). The absolute SUV was also positively correlated with SUVmax (p<0.05).ConclusionThe pathological volume could provide the more accurate tumor volume. The optimal SUV of FDG for PET imaging by use of GTVPATH as standard for cervical cancer target volume delineation was thus determined in this study, and more cases are being evaluated to substantiate this conclusion.

Comparison of imaging-based gross tumor volume and pathological volume determined by whole-mount serial sections in primary cervical cancer

ObjectiveTo investigate the accuracy of imaging-based gross tumor volume (GTV) compared with pathological volume in cervical cancer.MethodsTen patients with International Federation of Gynecology and Obstetrics stage I–II cervical cancer were eligible for investigation and underwent surgery in this study. Magnetic resonance imaging (MRI) and fluorine-18 fluorodeoxyglucose positron emission tomography (18F-FDG PET)/computed tomography (CT) scans were taken the day before surgery. The GTVs under MRI and 18F-FDG PET/CT (GTV-MRI, GTV-PET, GTV-CT) were calculated automatically by Eclipse treatment-planning systems. Specimens of excised uterine cervix and cervical cancer were consecutively sliced and divided into whole-mount serial sections. The tumor border of hematoxylin and eosin-stained sections was outlined under a microscope by an experienced pathologist. GTV through pathological image (GTV-path) was calculated with Adobe Photoshop.ResultsThe GTVs (average ± standard deviation) delineated and calculated under CT, MRI, PET, and histopathological sections were 19.41 ± 11.96 cm3, 12.66 ± 10.53 cm3, 11.07 ± 9.44 cm3, and 10.79 ± 8.71 cm3, respectively. The volume of GTV-CT or GTV-MR was bigger than GTV-path, and the difference was statistically significant (P < 0.05). No significant difference was observed between GTV-PET and GTV-path (P > 0.05). Spearman correlation analysis showed that GTV-CT, GTV-MRI, and GTV-PET were significantly correlated with GTV-path (P < 0.01). There was no significant difference in the lesion coverage factor among the three modalities.ConclusionThe present study showed that GTV defined under 40% of maximum standardized uptake value in PET images was very similar to the pathological volume of cervical cancer. This result should be replicated in a larger number of patients with cervical cancer in a future study of ours.

Abstract P1-14-17: Study of breast cancer shrinkage modes after neoadjuvant chemotherapy with whole-mount serial sections and three-dimensional pathological and MRI reconstruction

Abstract Background: The main clinical goal of NAC is to down-stage the primary tumor for BCS, yet BCS after NAC has been associated with significantly higher ipsilateral breast tumor recurrences. The main reseason might be the uncertain shrinkage modes of the breast cancer after NAC. The primary objective is to observe the shrinkage modes of the primary tumor after 3 cycles and whole cycles of NAC, respectively, with whole-mount serial section (WMSS) and three-dimensional (3D) pathological reconstruction of the residual tumor. The second objective is to investigate the predictive value of 3D MRI reconstruction for the shrinkage modes of the primary tumor after NAC. Methods: A total of 60 pts were enrolled. The first 30 pts received 3 cycles NAC and the second 30 pts received whole cycles of NAC. Breast specimens were obtained according to the original tumor border extending 3cm, and WMSS at 3mm intervals were performed. The residual tumor area were microscopically outlined on each slides. The 2D images were processed with Adobe Photoshop 9.0 and the 3D model of the residual tumor was reconstructed with the 3D-DOCTOR software. MRI were performed for the second 30 pts before, at the middle, and after NAC, respectively. The 3D MRI reconstructions at different times of NAC were compaired with the 3D pathological reconstruction to investugate its predictive value. Results: For pts received 3 cycles of NAC, pCR was obtained in 1 case. Of the other 29 pts, honeycomb shrinkage mode was observed in 28 cases (96.6%) with no significant decrease of the histological range after NAC (p &amp;gt; 0.05); and concentric shrinkage mode was observed only in 1 case (3.9%). More diffusive residual DCIS was observed in pts with diffusive microcalcifications on mammography before NAC than those without (76.5% vs. 7.7%, κ=0.670, p &amp;lt; 0.01). For pts received whole cycles of NAC, pCR and pPR were achieved in 7 (23.33%) and 23 pts (76.67%), respectively. For the 23 pts with pPR, the shrinkage modes were concentric in 10 (43.48%) and honeycomb in 13 pts (56.52%), respectively. Altogether, 17 pts (56.67%, pCR in 7 + pPR with concentric shrinkage mode in 10 pts) suitable for BCS after NAC. The 3D MRI reconstruction after NAC was highly predictive for the shrinkage modes of the primary tumor (r = 0.747, P&amp;lt;0.001). Whole cycles of NAC significantly improved the pCR rate and concentric shrinkage mode (both p &amp;lt; 0.01) compaired with 3 cycles of NAC. The shrinkage modes were not significantly associated with patient age, tumor size, axillary node status, histopathological type, ER, PR, HER2, and Ki67 (all p &amp;gt; 0.05). Conclusions: The main shrinkage mode was honeycomb mode (96.6%) after 3 cycles of NAC, indicating that 3 cycles of NAC was not enough to down-stage the primary tumor for BCS. Whole cycles of NAC significantly improved the pCR rate and concentric shrinkage mode compaired with 3 cycles of NAC, and more than half of the patients suitable for BCS after NAC. Patients with diffusive microcalcification might not suitable for BCS after NAC. The 3D MRI reconstruction after NAC was highly predictive for the shrinkage modes of the primary tumor after NAC. WMSS and 3D pathological and 3D MRI reconstruction provided a new platform in this area. Citation Information: Cancer Res 2012;72(24 Suppl):Abstract nr P1-14-17.

Relationship of Imaging and Pathological Gross Tumor Volume Determined by Whole-mount Serial Sections Technique in Primary Cervical Cancer

Relationship of Imaging and Pathological Gross Tumor Volume Determined by Whole-mount Serial Sections Technique in Primary Cervical Cancer

3D Pathology Volumetric Technique: A Method for Calculating Breast Tumour Volume from Whole-Mount Serial Section Images

Tumour size, most commonly measured by maximum linear extent, remains a strong predictor of survival in breast cancer. Tumour volume, proportional to the number of tumour cells, may be a more accurate surrogate for size. We describe a novel “3D pathology volumetric technique” for lumpectomies and compare it with 2D measurements. Volume renderings and total tumour volume are computed from digitized whole-mount serial sections using custom software tools. Results are presented for two lumpectomy specimens selected for tumour features which may challenge accurate measurement of tumour burden with conventional, sampling-based pathology: (1) an infiltrative pattern admixed with normal breast elements; (2) a localized invasive mass separated from the in situ component by benign tissue. Spatial relationships between key features (tumour foci, close or involved margins) are clearly visualized in volume renderings. Invasive tumour burden can be underestimated using conventional pathology, compared to the volumetric technique (infiltrative pattern: 30% underestimation; localized mass: 3% underestimation for invasive tumour, 44% for in situ component). Tumour volume approximated from 2D measurements (i.e., maximum linear extent), assuming elliptical geometry, was seen to overestimate volume compared to the 3D volumetric calculation (by a factor of 7x for the infiltrative pattern; 1.5x for the localized invasive mass).

Increasing specimen coverage using digital whole-mount breast pathology: Implementation, clinical feasibility and application in research

Conventional histopathological evaluation is performed on breast specimens using a highly limited sampling of tissues visualized in a two-dimensional (2D) manner although important tumor measurements are three-dimensional. Here we describe a ‘3D’ technique for whole-mount, whole-specimen processing which reduces conformational change and dramatically increases specimen coverage, based on digitizing whole-specimen, whole-mount (up to 12.7 cm × 17.8 cm) serial sections. We describe hardware and software tools for acquiring, viewing and processing the large image datasets (up to 400 GB), validation studies investigating the clinical significance of the additional information gleaned from the 3D approach, and application to radiologic-pathologic correlation and biomarker visualization.

Anatomical description of the periprostatic nerves in the male rhesus monkey (Macaca mulatta)

Recent publications have revealed a variable course of the periprostatic nerves in humans. It is unclear to what extent nerves outside the dorsolateral region of the prostate are involved in the physiology of erectile function. As functional studies in humans are limited by ethical aspects investigations in animal models could provide further insight. The intention of this study was to give a detailed description of the topographical anatomy of autonomic nerves along the seminal vesicles and the prostate in male rhesus monkeys (Macaca mulatta) to investigate its suitability as an animal model for future physiological studies. Wholemount serial sections of pelvic organ blocks of ten male rhesus monkeys were investigated. Autonomic nerves were stained with an antibody against S100. Autonomic nerves were dispersed along the dorsolateral to the ventrolateral aspect of the capsule of the prostate within a layer of connective tissue. There was no accumulation of vessels and nerves in the dorsolateral position of the prostate. The prostate is located dorsally to the urethra and does not encircle it. No adjacent nerves were found in the cranial two-thirds of the seminal vesicles. The male rhesus monkey is limited suitable as an animal model for studies on the periprostatic nerves provided the following differences to humans are considered: the special topography of the prostate, the nerve course along the seminal vesicles and the missing nerve accumulation dorsolaterally to the prostate.

An Improved Processing Method for Breast Whole-Mount Serial Sections for Three-Dimensional Histopathology Imaging

To develop and validate improved processing methods for producing diagnostic-quality, whole-mount serial sections for 3-dimensional imaging of whole-breast histopathologic studies, we subjected 4-mm-thick whole-specimen slices to a 38-hour microwave-assisted protocol. Morphologic features, antigenicity, and tissue shrinkage were evaluated. A schedule using the tissue processor was optimized by evaluating the serial section yield for 3 schedules. The microwave-based processing schedule is adequate for producing diagnostic-quality whole-mount breast serial sections of an area up to 6,000 mm(2) and is compatible with a variety of immunohistochemical stains. A mean +/- SE total tissue shrinkage of 8.4% +/- 0.2% resulted. For the tissue processor, optimal results are obtained using a 59-hour schedule. Total fixation and processing time for whole-mount serial breast sections has been reduced from 21 days to 38 hours, with microwave assistance, and to 59 hours without. No adverse effects of microwaves on morphologic features, antigenicity, or gross tissue dimensions were observed.

Whole‐specimen histopathology: a method to produce whole‐mount breast serial sections for 3‐D digital histopathology imaging

To develop a method for preparing diagnostic-quality, whole-mount serial sections of breast specimens while preserving 3-D conformation. This required supporting the fresh specimen prior to breadloafing and refining the conventional tissue processing method. The overall goal is to use digital images of whole-specimen histopathology to improve the estimation of extent of disease. To maintain a 3-D conformation, the specimen is suspended in 3.5% agar at 55 degrees C. The block is sliced at 5-mm intervals. Sectioning is performed after extended fixation in 4% formaldehyde from paraformaldehyde in 0.1 m Millonig's buffer, followed by paraffin processing using a non-routine schedule and extended paraffin infiltration. Whole-mount serial breast sections are produced with features of equal or superior quality to that which can be achieved using conventional methods. The method is compatible with some immunohistochemical stains but requires further optimization for others. The technique is currently suitable for research applications. With the reduction in processing time achievable with microwave-assisted processing, there is the potential for its use as a routine clinical method. This tool may improve the accuracy of margin estimates and identification of multifocality in breast cancer; further evaluation is necessary.

The Prevalence of Prostate Carcinoma and Its Precursor in Hungary: An Autopsy Study

Objectives: The prevalence of incidental prostatic adenocarcinoma (PCa) and its precursor, high grade intraepithelial neoplasia (HGPIN) in an autopsy series from Hungarians (Central European Caucasians) was assessed and compared to similar data from the United States and European countries. Methods: Autopsy cases ( n = 139; 18–95 years) with no history of urological disease were histologically examined for prostate cancer and HGPIN. After en block removal, the prostate glands were fixed in formalin, sectioned at 3–5 mm intervals and embedded in paraffin. Whole-mount serial sections were stained with Hematoxylin-eosin and examined for the presence of PCa and HGPIN. The frequency of PCa and HGPIN was compared to autopsy data obtained from other geographical areas. Results: We found a 38.8% prevalence of incidental PCa with increasing age-related incidence. Both PCa and HGPIN are first detected in the 3rd decade and show a steady increase with age with respect to number of foci, tumor grade and volume. In the age group 81–95, 86.6% and 60% of men had PCa and HGPIN, respectively. Conclusions: Incidental PCa and HGPIN are very prevalent in Hungarian population, comparable with the high US and the Scandinavian epidemiological data for Caucasians.

Three-dimensional Analysis of Supracricoid Hemilaryngopharyngectomized Hypopharyngeal Cancer

The aims of this study were to demonstrate the technical aspects of processing high-resolution three-dimensional (3D) images and to describe the value of this approach for studying partially removed hypopharyngeal cancer. Supracricoid hemilaryngopharyngectomy was conducted in three sinus-type hypopharyngeal cancers as a salvage operation. A histopathologic study was conducted in order to fully examine the resection margin of the surgical specimens and to ensure the credibility of our case selection. The morphological features of each specimen were analyzed and demonstrated using 2D and 3D settings. Whole-mount serial histological sections were developed from the surgical specimens and 3D images were reconstructed based on these sections. In each case the 3D images demonstrated the characteristic patterns of cancer extension, such as superior extension under the intact epithelium and the formation of multiple skip lesions. The overall resection margin was proven to be free of cancer in all three cases. In conclusion, 3D study was useful for evaluating the overall resection margin of surgical specimens and provided valuable information for use in future follow-up. Using this technique, the morphological findings from serial sections are more comprehensive and impressive. 3D reconstruction is and will be a crucial modality for studying the morphological behavior of hypopharyngeal cancer.

Disturbed vagal nerve distribution in embryonic chick hearts after treatment with all-trans retinoic acid.

The distribution of the vagal nerve was studied in whole-mount specimens and serial sections of chick embryos after retinoic acid treatment. White Leghorn chick embryos were treated at stage 15 either with 1 microg all-trans retinoic acid (n=11), or with the solvent dimethylsulphoxide (sham-operated embryos, n=8). Eight embryos served as normal controls. At stage 34 all 27 embryos were examined with a dissecting microscope. In order to reveal the vagal patterning, the hearts were removed and whole-mount stained with the HNK-1 antibody. In three hearts of the retinoic acid-treated group a morphologic intracardiac anomaly -- a double outlet right ventricle -- was found. To explore in depth the vagal nerve distribution in the heart, a separate set of hearts of retinoic acid embryos (n=5), sham-operated (n=4) and control embryos (n=5), was devised solely for serial sectioning and staining with the HNK-1 antibody. All hearts of retinoic acid-treated embryos showed a disturbed vagal nerve distribution both over the surface of the heart and within the heart wall. The vagal patterning was not altered in the sham-operated embryos compared to controls. It is concluded that retinoic acid disturbs the development of vagal nerve patterning regardless of the concurrent presence of intracardiac malformations. The mechanism and functional implications remain to be investigated.

Three-dimensional Computer-reconstructed Image for Studying Cancer Extension Within the Hypopharynx

Hypopharyngeal cancer is one of the head and neck cancers with poor prognosis. This is due to the unpredictable extension of the local disease and the high ratio of distant metastasis. To verify the morphological behavior of hypopharyngeal cancer, whole-mount horizontal serial sections were developed using the larynges obtained from total pharyngolaryngoesophagotomy. The technique of processing high-resolution three-dimensional (3D) images of the larynges using Nikon Cosmozone 2SA software is presented. Two representative surgical specimens were used and 3D images reconstructed. In these two particular cases, the cancer infiltrated superiorly through submucosal lymphatic ducts and formed separate daughter nests under the intact mucosal epithelium far above the main tumor. 3D images enhanced the morphological features of these cases. These cases also suggested the difficulty of defining the upper resecting limit in the operation of hypopharyngeal cancer. 3D reconstruction is and will be a crucial modality for studying the morphological behavior of hypopharyngeal cancer.

喉頭癌病理組織像とＣＴ画像

Since the development of conservation laryngeal surgery and the advent of computed tomography (CT) scanners, a precise preoperative evaluation of the extent of laryngeal cancer has been of prime importance.Eight patients with known carcinoma of the larynx were examined with CT of the larynx prior to surgery, and whole-mount serial sections of the extirpated larynx were compared with the corresponding level of CT sections to evaluate the reliability of CT during my study abroad in Japan from Dec. 1985 through Dec. 1986.1. The results indicated that CT scanning accurately delineates the anatomic location and pathologic extent of the tumor three-dimensionally in all cases examined. There is also good demonstration of the anterior commissure and preepiglottic, paraglottic and subglottic spaces which are sometimes poorly seen by laryngoscopy or by any other means.2. Determination of invasion of the laryngeal cartilage by tumor proved to be very difficult to diagnose with CT.3. The CT images obtained while the patient is breathing quietly, coupled with additional sections at the level of the vocal cord during slight valsalva maneuver afford good visualization of laryngeal tumors.4. It should be emphasized that a thorough pathologic examination of extirpated specimens with serial sections is essential for laryngeal surgeons, because it is impossible to determine the patient's prognosis without microscopic demonstration of the degree of invasion.

Patterns of serotonin-immunoreactive neurons in the central nervous system of the earthworm Lumbricus terrestris L.

The distribution of serotonin-immunoreactive cell bodies and fibers in the ventral nerve cord of the earthworm has been investigated from whole-mount preparations and serial sections. Serotonin-immunoreactive neurons are organized in seven soma groups per ganglion; these are defined by cell number, soma shape, diameter and fiber projections. Positional variations of this pattern have been studied quantitatively. The number of labeled perikarya is constant in midbody ganglia, but increases markedly rostral to the posterior margin of the clitellum. Variability of position and cell number differs between the cell groups. Stained nerve fibers could only be partially traced; their distribution is described in relation to defined neuronal fiber bundles and segmental nerves. The distribution and morphology of serotonin-immunoreactive cells are compared with previous observations, based on pattern analysis of primary catecholamines and indolamines with the use of a formaldehyde-induced fluorescence technique. The possible role of serotonin-immunoreactive nervous elements in different nerve cord compartments is discussed with respect to physiological effects of serotonin in earthworms and other invertebrates.

STUDIES ON THE TREMATODE GENUS RENICOLA: OBSERVATIONS ON THE LIFE-HISTORY, SPECIFICITY, AND SYSTEMATIC POSITION

Previous article No AccessJournal ArticlesSTUDIES ON THE TREMATODE GENUS RENICOLA: OBSERVATIONS ON THE LIFE-HISTORY, SPECIFICITY, AND SYSTEMATIC POSITIONHORACE W. STUNKARDHORACE W. STUNKARDThe American Museum of Natural History, Central Park West at 79th Street, New York 24, New York Search for more articles by this author The American Museum of Natural History, Central Park West at 79th Street, New York 24, New YorkPDFPDF PLUS Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The Biological Bulletin Volume 126, Number 3June 1964 Published in association with the Marine Biological Laboratory Article DOIhttps://doi.org/10.2307/1539314 Views: 20Total views on this site Citations: 1Citations are reported from Crossref © 1964 Marine Biological LaboratoryPDF download Crossref reports the following articles citing this article: F Tetreault , JH Himmelman , and L Measures Impact of a castrating trematode, Neophasis sp., on the common whelk, Buccinum undatum, in the northern Gulf of St. Lawrence, The Biological Bulletin 198, no.22 (Sep 2016): 261–271.https://doi.org/10.2307/1542529