Startseite Serrated lesions of the colon and rectum: Emergent epidemiological data and molecular pathways
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Serrated lesions of the colon and rectum: Emergent epidemiological data and molecular pathways

  • Michele Sacco , Fatima Domenica Elisa De Palma , Elia Guadagno , Mariano Cesare Giglio EMAIL logo , Roberto Peltrini , Ester Marra , Andrea Manfreda , Alfonso Amendola , Gianluca Cassese , Vincenza Paola Dinuzzi , Francesca Pegoraro , Francesca Paola Tropeano , Gaetano Luglio und Giovanni Domenico De Palma
Veröffentlicht/Copyright: 9. November 2020
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Open Medicine
Aus der Zeitschrift Open Medicine Band 15 Heft 1

Abstract

In 2010, serrated polyps (SP) of the colon have been included in the WHO classification of digestive tumors. Since then a large corpus of evidence focusing on these lesions are available in the literature. This review aims to analyze the present data on the epidemiological and molecular aspects of SP. Hyperplastic polyps (HPs) are the most common subtype of SP (70–90%), with a minimal or null risk of malignant transformation, contrarily to sessile serrated lesions (SSLs) and traditional serrated adenomas (TSAs), which represent 10–20% and 1% of adenomas, respectively. The malignant transformation, when occurs, is supported by a specific genetic pathway, known as the serrated-neoplasia pathway. The time needed for malignant transformation is not known, but it may occur rapidly in some lesions. Current evidence suggests that a detection rate of SP ≥15% should be expected in a population undergoing screening colonoscopy. There are no differences between primary colonoscopies and those carried out after positive occult fecal blood tests, as this screening test fails to identify SP, which rarely bleed. Genetic similarities between SP and interval cancers suggest that these cancers could arise from missed SP. Hence, the detection rate of serrated-lesions should be evaluated as a quality indicator of colonoscopy. There is a lack of high-quality longitudinal studies analyzing the long-term risk of developing colorectal cancer (CRC), as well as the cancer risk factors and molecular tissue biomarkers. Further studies are needed to define an evidence-based surveillance program after the removal of SP, which is currently suggested based on experts’ opinions.

Keywords: colorectal cancer; serrated adenomas; molecular pathways; interval cancer; BRAF

1 Introduction

The prevention of colorectal cancer (CRC) is carried out through the identification and removal of premalignant lesions [1]. The last decade has witnessed the appearance of new protagonists in this scenario, the serrated polyps (SP), which are reported to be at the origin of 15–30% of all CRCs [2,3].

The term “serrated adenoma” was coined by Longacre and Fenoglio-Preiser in 1990 to describe a new type of colorectal polyp presenting with peculiar characteristics [4]. In this lesion, the colonic mucosa presented a saw-toothed appearance, similar to hyperplastic polyps (HPs), but with some cytological atypia and, in some cases, dysplasia [4–7]. In 1996, Torlakovic and Snover described the serrated sessile adenomas/polyps and traditional serrated adenoma (TSA) [6].

In 2010, the inclusion of serrated lesions in the WHO classification of digestive tumors [8] let grow up the attention of the scientific community about the malignant potential of SP, which present peculiar characteristics. In contrast to the well-known conventional adenomas, SP usually presents as flat lesions with indistinct borders and can have rapid growth. Also, SP show genetically peculiarities, being characterized by several mutations and changes in phenotype, which occur within a specific pathway [5,9–13].

In the last years, there has been widespread of literature focusing on SP. This review aimed to analyze the available data on the epidemiological and molecular aspects of these lesions.

2 Classification

The 2019 WHO Classification recognizes four subtypes of SP [8]: HPs, sessile serrated lesions (SSLs), sessile serrated lesions with dysplasia (SSLsD), and traditional serrated adenomas (TSAs) [14]. The new classification strongly discouraged the use of the term adenoma or polyp previously used to indicate nondysplastic SSLs. Some histopathologic features of SPs are shown in Figure 1.

Figure 1 Histopathologic features of serrated lesions. (a) Goblet cell-rich hyperplastic polyp. The crypts show the typical sawtooth architecture, which is more evident superficially and contain a large number of goblet cells. (Hematoxylin and eosin stain, 200× magnification.) (b) Sessile serrated lesion. Deep serration and basal crypt dilation can be observed in the present field. (Hematoxylin and eosin stain, 100× magnification.) (c) Sessile serrated lesion with dysplasia. Besides crypt serration and dilation, low-grade dysplastic foci can be observed in the present case. (Hematoxylin and eosin stain, 100× magnification.)
Figure 1

Histopathologic features of serrated lesions. (a) Goblet cell-rich hyperplastic polyp. The crypts show the typical sawtooth architecture, which is more evident superficially and contain a large number of goblet cells. (Hematoxylin and eosin stain, 200× magnification.) (b) Sessile serrated lesion. Deep serration and basal crypt dilation can be observed in the present field. (Hematoxylin and eosin stain, 100× magnification.) (c) Sessile serrated lesion with dysplasia. Besides crypt serration and dilation, low-grade dysplastic foci can be observed in the present case. (Hematoxylin and eosin stain, 100× magnification.)

2.1 Hyperplastic polyps

HP is the most common SP, accounting for 70–90% of all SP [15]. HPs are considered benign lesions, with a minimal or null risk of progression to CRC. In the course of a colonoscopy, HPs appear as smooth, symmetric, and pale lesions and are mainly found in the rectum and sigmoid colon. HPs are characterized by the presence of straight crypts, rising perpendicularly from the muscolaris mucosae. They have a jagged infolding crypt epithelium, more pronounced near the luminal surface, which gives them a “serrated” appearance (Figure 1a) [5,16].

According to the mucin content of the epithelial cells, HPs are subdivided into three subtypes: microvesicular HPs (MVHP), whose cells have a vacuolated cytoplasm with small mucin droplets; goblet cell HPs (GCHP), with large mucin apical vesicles, and mucin-poor HPs (MPHP), with scarce cytoplasm mucin [9,17]. MVHP is mainly characterized by BRAF V600E mutation (substitution of valine for glutamic acid in position 600) and CIMP-H (CpG island methylator phenotype with high methylation status), while GCHP harbors KRAS mutation (often missense substitutions at glycine codons 12 or 13) in 50% of cases and CIMP-L (CpG island methylator phenotype with low methylation status) [18,19]. The consequence of BRAF or KRAS mutations is the activation of the MAP kinase signaling pathway, which inhibits apoptosis and promotes the proliferation of tumoral cells.

2.2 SSLs

SSL is the second most common SP subtype, representing 10–20% of SP [7,15,20]. The majority of SSLs (75–80%) is found in the proximal colon, including the cecum, ascending, or transverse colon [9,21]. Among SP, they show the highest potential for malignant transformation. From a genetic point of view, SSL is associated with the serrated neoplasia pathway [22].

It is characterized by deep crypt distortion (Figure 1b), because the proliferation zone moves to the crypt side, causing horizontal growth along the muscolaris mucosae, dilation of the crypt base, serrations extending into the crypt base, and asymmetrical proliferation. The presence of at least one of these features in sufficient to define a crypt as abnormal, as well as this feature must be unequivocal in ≥1 crypt [9].

In the course of a colonoscopy, SSAs are pale, usually larger than 5 mm, flat or only slightly raised and irregular borders. The majority of SSA produces a large amount of mucin and is surrounded by a rim of “debris.” However, the diagnosis cannot be based on the size, the location, and the endoscopic appearance of the lesion.

2.3 SSLs with dysplasia

The occurrence of dysplasia within a sessile serrated lesion is a rare condition (Figure 1c). Usually, dysplasia is more heterogeneous than in conventional adenomas, and for this reason, the distinction between low- and high-grade forms is not indicated. In general, it is considered a transient step during progression to cancer.

2.4 TSAs

TSAs are the rarest subtype of SP, accounting for only 1% of SP [21]. TSAs usually present as large polypoid lesions located in the distal colon and rectum [21]. Histologically, they present “sawtooth” crypts arranged in a slit-like pattern. TSA is classically composed of tall columnar cells with intensely eosinophilic cytoplasm and penicillate nuclei [9]. TSA initially present KRAS and BRAF mutations, which cause uncontrolled cellular proliferation. In a recent study, Hashimoto et al., evaluated the WNT mutational status of TSAs and described the malignant evolution from precursor polyps to TSAs [23]. In this study, RNF43, APC, or CTNNB1 mutations were exclusively present in TSAs [23]. The occurrence of epigenetic silencing of DNA repair genes, with the subsequent accumulation of mutations, leads the transformation into CRC.

2.5 Unclassified serrated adenomas

This is a “basket” category including serrated dysplastic cases whose morphological features do not fall into any of the categories described earlier.

3 Serrated lesions and CRC

Two different molecular pathways underlie the colonic neoplastic transformation: the conventional and the serrated neoplasia pathways. They both are driven by the accumulation of specific molecular alterations, corresponding morphologic features and clinicopathological manifestations [24–26].

The conventional model, or the so-called adenoma-carcinoma sequence, has been proposed by Vogelstein et al. in 1988 [27] and is characterized by adenomas (including tubular or tubulovillous adenomas) as the only precursor lesions capable to give rise to CRC [28,29]. However, over the last ten years, it has been demonstrated that approximately 15–30% of all CRCs develop from the alternative/serrated pathway [25,30].

The association between SP and CRC has been demonstrated at several levels. First, both low- and high-grade dysplasia and adenocarcinoma have been found in the context of SSA lesions [31]. Also, peculiar BRAF mutations and the presence of CpG island methylation phenotype are characteristics of serrated lesions and are found, with an increasing frequency, in HPs, SSL without dysplasia, and SSL with dysplasia. These genetic changes are rarely present in conventional adenomas but are found in more than 15% of CRCs [32,33]. They occur in a structured and well-defined pathway, which is known as the serrated-neoplasia pathway [22]. The molecular and genetic progression along this pathway parallels the progression of SP to dysplasia and adenocarcinoma, according to a stepwise modality.

The time required for the malignant transformation of SP is unknown. Lash et al. observed that the presence and grade of dysplasia in the context of SP was age-related [31]. This led the authors to hypothesize that the malignant transformation needs a long time frame from 10 to 15 years [31]. However, it has been shown that this progression can also occur rapidly [34]. Interestingly, the majority of interval CRCs shows a genotype consistent with the serrated neoplasia pathway [35,36]. This evidence suggests that SP could be considered as responsible for interval CRCs. Whether this occurs because SPs are easily missed during a colonoscopy [37,38] or because SPs develop rapidly and present an accelerated malignant transformation, it is unknown.

4 Association between gut microbiota and serrated pathway

Important players of human health and disease are microbial species that colonize the gastrointestinal tract [39,40]. A different bacterial population can be identified in the human gut system, with a particular incidence of Firmicutes (30–50%), Bacteroidetes (20–40%), and Actinobacteria (1–10%) [40]. The microbial gut composition can significantly contribute to and affect several human diseases, as well as the carcinogenesis of the colorectum [40–42]. The presence of Fusobacterium species, particularly of Fusobacterium nucleatum (F. nucleatum), interacting with genetic changes and the innate immune system has been linked with the development of CRC, as demonstrated by its overabundance in colorectal tumor tissues when compared with the adjacent normal tissues [43,44].

The role of the Gram-negative F. nucleatum in the serrated pathway is not fully understood. Studies have proven F. nucleatum increased levels in MSI and CIMP molecular subsets, and in TA and SSL lesions, highlighting its putative involvement in the serrated pathway [44–47]. Ito et al. showed that F. nucleatum was associated with premalignant lesions characterized only by CIMP-H status and large tumor size [45]. Furthermore, they demonstrated that F. nucleatum gradually increases in SSLs from the sigmoid colon to the cecum [45]. Then, Park et al. showed a similar F. nucleatum abundance in TA and SSL but lower when compared with the CRC group [46]. Although these data demonstrate the F. nucleatum contribution to the serrated pathway, more studies are necessary to characterize its role in the carcinogenetic sequence.

5 MicroRNAs and long non-coding RNAs: other potential biomarkers of the serrated pathway

The important role of non-coding RNAs (ncRNAs), such as microRNAs (miRNAs) and long non-coding RNAs (lncRNAs), as biomarkers is increasingly growing in the diagnosis and management of CRCs [47]. miRNAs and lncRNAs regulate gene expression at translational and post-translational levels [48]. In addition, their alteration, in terms of low or high expression, has been associated with the traditional adenoma-carcinoma and serrated-carcinoma sequences [49–51].

Several ncRNAs profiling-based studies have identified specific miRNAs/lncRNAs associated with the serrated lesions, whose differentially expression has allowed, in addition to the canonical tests, to better distinguish between the different CRCs subtypes and serrated and nonserrated lesions. Examples are miR-335, -222, and -21, significantly differentially expressed in nonserrated when compared with serrated lesions [51], and miR-125b and miR-320a described as specific biomarkers predictive of the evolution to CRC through the serrated pathway [51]. The well-known miR-31, already associated with BRAF mutation in CRC, is involved in the progression of the serrated lesions and has been frequently found overexpressed in SSLs [49,52]. Recently, Kanth and collaborators have identified a serrated-specific miRNA signature using a small RNA sequencing approach. In particular, among all the differentially expressed detected miRNAs, miR-31-5p and -135B-5p have been described to be significantly overexpressed in SSLs when compared with HPs [49].

Regarding lncRNAs, several studies have demonstrated their role in the serrated pathway [50,53]. Chen et al. have identified dysregulated lncRNAs to be able to classify the 888 CRC samples analyzed into five distinct molecular subtypes [53]. In a recently published study, de Bony and collaborators have detected 282 lncRNAs corresponding to CRCs heterogeneity [50].

Thus, these findings suggest that miRNAs and lncRNAs play an important role in CRC and the serrated pathway. Further researches will be necessary to explore ncRNAs role in CRCs not only to distinguish the heterogeneous CRCs types but also for rapid and noninvasive diagnosis, and to reveal unknown mechanisms of the pathogenesis of serrated lesions.

6 Prevalence of serrated lesions

The prevalence of SP, namely the rate of detection of at least one SP among patients undergoing a colonoscopy, has been studied by several authors. The interest in this data goes beyond a pure epidemiological sake. Indeed, the adenoma detection rate (ADR) is considered nowadays as the main indicator of the quality of a colonoscopy, as it is negatively correlated with the occurrence of interval CRCs [54]. For example, an ADR ≤ 25% in colonoscopies performed on male patients older than 50 years is indicative of the low-quality of the procedures [55]. As missed SP is probably at the origin of interval CRCs, the SP detection rate naturally promotes itself as a quality indicator of colonoscopy, being potentially even more accurate than ADR.

Studies trying to address the prevalence of SP have shown variable results [56,57]. This variability mainly depends on the period of the study (e.g. before/after WHO classification), the awareness of the risk of cancer of SP, and the quality of pathologic and endoscopic examination. Indeed, SPs are at risk of being missed, in consideration of their morphology (flat or sessile) and their location (often in the right colon) [2,3]. Great variability in the proximal SP detection has been shown among the endoscopists, with low-detectors (referred to ADR) showing also the lowest detection rate of SP [58–60]. In addition, some of the variability is also due to the pathologist experience, as the interpathologist agreement on the diagnosis of SP is moderate [61].

Studies on autopsies have defined a wide range for the prevalence, from 6% to 29% [56,62]. However, the contribution from these studies to the daily practice remains limited, due to different methodologies.

Recently, Ijspert and colleagues published the results of a European multicenter study based on data from five screening cohorts [61]. The quality of this study relies on the expertise of endoscopists (the lowest ADR was around 30%) and the expertise of the pathologists, who were gastrointestinal-dedicated pathologists. The detection rate of SP varied between 15% and 27.2%, while SSAs were detected in the 2–6% of the patients. The rate of SPS varied between 0.03% and 0.5% [61].

Interestingly, the low prevalence of SP within cohorts undergoing a screening colonoscopy after a positive occult fecal blood test [61,63] support data from a recent study showing that this screening test has no role in the detection of SP, which rarely bleed [64].

7 Risk factors for SP

Some factors have been studied as potential influencers of the development of SP (Table 1). The diagnosis of SP is age-correlated, and the median age of presentation of SP is 60 years [21]. With regard to gender, SPs are equally found in females as males [21]. However, some studies indicate a higher prevalence in females [56].

Table 1

Factors associated with the development of serrated lesions

FactorStrength of association Risk
Smoking (≥30 packs/year)OR, 2.52 (95% CI, 2.29–2.78)aIncreased
Alcohol intake (>14 g/day in males; 7 g/day in females)OR, 1.33 (95% CI, 1.24–1.43)aIncreased
Obesity (body mass index >35)OR, 1.34 (95% CI, 1.23–1.46)aIncreased
Vitamin D – intake (4th quartile)OR, 0.92 (95% CI, 0.86–0.98)aReduced
Marine omega-3 fatty – intake (4th quartile)OR, 0.90 (95% CI, 0.84–0.96)aReduced
Regular acetylsalicylic acid useOR, 0.72 (95% CI, 0.59–0.87)aReduced

OR, odds ratio.

  1. a

    Data from He et al. [68]

Similar to other colorectal polyps, SPs are more frequently found in the Western world, probably because endoscopy is more accessible [56].

The association between several lifestyle habits and SP factors has been investigated. Smoking is strongly associated with the risk of developing SP, especially SSAs and HPs [65,66]. In particular, Anderson et al. observed an increased risk of SSA in heavy smokers (more than 20 packs/year) [67]. Interestingly, the association seems to be stronger with SP than conventional adenomas [68].

Alcohol intake is related to a high risk of developing SP especially, in the left colon and rectum, although evidence is limited to heavy drinkers (>14 g/d in male; 7 g/d in female) [69]. Some authors even investigated the risk linked to different beverages, without reaching any significant conclusion [70]. Obesity (BMI > 30) has been described as a risk factor for SP in some studies, although others did not find any correlation [56,67,71].

Dietary factors such as red meat and fatty acid consumption seem to increase the risk of SP [67,71]. Physical activity and the intake of folate, calcium, fruit, and vegetables do not affect the occurrence of SP, while a high intake of vitamin D and marine omega-3 fatty acid seems to have a protective role [65,68].

Among medications, aspirin and other non-steroidal anti inflammatory drugs have been investigated and could have a protective role. Bouwens et al. demonstrated a decreased risk with the use of aspirin, especially for right-sided lesions [69].

Based on this evidence, Bouwens et al. proposed a score to predict the risk of detection SP in patients undergoing colonoscopy. This score takes into account four variables, including age (>50 years), a previous diagnosis of SP, the smoker status, and the assumption of aspirin [69].

8 Risk of CRC and surveillance

Determination of the long-term risk of developing CRC in patients diagnosed with an SP is essential to establish an effective surveillance program for these patients [72]. Lazarus and colleagues showed the occurrence of a metachronous CRC in the 5% of patients diagnosed with an SSL presenting dysplasia [73]. In this group of patients, Teriaky et al. found a similar risk at 5 years [74]. A higher risk was described by Lu et al.; they found CRC in 12.5% of patients being previously diagnosed with an SSL, independently from the presence of dysplasia [13]. On the contrary, Burnett-Hartman and colleagues did not find an increased risk of advanced CRC diagnosis in the 5 years following the removal of serrated lesions [75]. These studies, however, suffer from a limited sample size. Studies reporting long-term results after SP removal are still awaited and recommendations on the endoscopic surveillance in these patients are, at the moment, mainly based on expert opinions.

A panel of experts from the US recommends that patients diagnosed with an HP should receive a colonoscopy in 10 years unless HPs are found proximally to the sigma [10]. In this case, patients should receive a colonoscopy within 5 years if HPs are ≥4 or larger than 5 mm. Patients with SSL or TSA need a colonoscopy in 5 years if the lesions are small (<10 mm) and less than 3; otherwise, the colonoscopy should be anticipated at 3 years or even before, especially in case dysplasia is found [10].

European Guidelines consider at high-risk patients diagnosed with SP of large size (≥10 mm) or presenting dysplasia [76]. These patients should receive surveillance colonoscopy within 3 years. Patients with SPS should be addressed to genetic counseling. Other patients with SP should receive a colonoscopy in 10 years [76].

Serrated polyposis syndrome (SPS) is characterized by the contemporary presence of multiple serrated lesions. According to WHO criteria, SP is defined as:

  1. the presence of at least 5 SP proximal to the sigmoid colon, with ≥2 larger than 10 mm

  2. the presence of any number of SP proximal to the sigmoid colon in an individual who has a first degree relative with SP

  3. The presence of more than 20 SP of any size is distributed throughout the colon.

Patients with SPS have a higher risk of developing CRC [16,77] and therefore require strict surveillance [10]. First-degree relatives of these patients also present a high risk of CRC and should undergo a tailored colonoscopy surveillance program [10].

In conclusion, since the inclusion in 2010 of SP in the WHO classification, a large corpus of evidence regarding the epidemiology of these lesions has become available in the literature. In particular, the interest in tumor molecular changes and its connections to the external exposures and the tumor behavior is increasing. In this area of research, we think that molecular pathological epidemiology can lead to a better understanding of tumor natural history, by providing a better comprehension of the pathogenic processes and help tailoring personalized prevention strategy and therapy [78–79]. Further studies in these fields are needed. Another epidemiological aspect to focus is that serrated lesions of the colorectum account for around one-fifth of all precancerous lesions of the large bowel: proper identification, treatment, and surveillance of these lesions play a primary role within an adequate cancer prevention program. The current data suggest that a detection rate of serrated lesions ≥15% should be expected in screening colonoscopies. The detection rate of serrated-lesions, and in particular of SSL lesions, need to be evaluated as a quality indicator of colonoscopy. High-quality longitudinal studies are needed to identify the long-term risk of CRC in patients with SP, to define an evidence-based surveillance program, which is currently suggested on the base of expert opinions.

  1. Conflict of interest: All the authors declare no conflict of interest.

  2. Funding: None of the authors received funding for this work.

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Received: 2019-09-09
Revised: 2020-07-14
Accepted: 2020-08-07
Published Online: 2020-11-09

© 2020 Michele Sacco et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/med-2020-0226
Schlagwörter für diesen Artikel
colorectal cancer; serrated adenomas; molecular pathways; interval cancer; BRAF
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  8. Optimization of the Convolutional Neural Networks for Automatic Detection of Skin Cancer
  9. NEAT1 promotes LPS-induced inflammatory injury in macrophages by regulating miR-17-5p/TLR4
  10. Plasma matrix metalloproteinase-9 and tissue inhibitor of matrix metalloproteinase-1 as prognostic biomarkers in critically ill patients
  11. Effects of extracorporeal magnetic stimulation in fecal incontinence
  12. Case Report
  13. Mixed germ cell tumor of the endometrium: a case report and literature review
  14. Bowel perforation after ventriculoperitoneal-shunt placement: case report and review of the literature
  15. Research Article
  16. Prognostic value of lncRNA HOTAIR in colorectal cancer : a meta-analysis
  17. Case Report
  18. Treatment of insulinomas by laparoscopic radiofrequency ablation: case reports and literature review
  19. Research Article
  20. The characteristics and nomogram for primary lung papillary adenocarcinoma
  21. Undiagnosed pheochromocytoma presenting as a pancreatic tumor: A case report
  22. Bioinformatics Analysis of the Expression of ATP binding cassette subfamily C member 3 (ABCC3) in Human Glioma
  23. Diagnostic value of recombinant heparin-binding hemagglutinin adhesin protein in spinal tuberculosis
  24. Primary cutaneous DLBCL non-GCB type: challenges of a rare case
  25. LINC00152 knock-down suppresses esophageal cancer by EGFR signaling pathway
  26. Case Report
  27. Life-threatening anaemia in patient with hereditary haemorrhagic telangiectasia (Rendu-Osler-Weber syndrome)
  28. Research Article
  29. QTc interval predicts disturbed circadian blood pressure variation
  30. Shoulder ultrasound in the diagnosis of the suprascapular neuropathy in athletes
  31. The number of negative lymph nodes is positively associated with survival in esophageal squamous cell carcinoma patients in China
  32. Differentiation of pontine infarction by size
  33. RAF1 expression is correlated with HAF, a parameter of liver computed tomographic perfusion, and may predict the early therapeutic response to sorafenib in advanced hepatocellular carcinoma patients
  34. LncRNA ZEB1-AS1 regulates colorectal cancer cells by miR-205/YAP1 axis
  35. Tissue coagulation in laser hemorrhoidoplasty – an experimental study
  36. Classification of pathological types of lung cancer from CT images by deep residual neural networks with transfer learning strategy
  37. Enhanced Recovery after Surgery for Lung Cancer Patients
  38. Case Report
  39. Streptococcus pneumoniae-associated thrombotic microangiopathy in an immunosuppressed adult
  40. Research Article
  41. The characterization of Enterococcus genus: resistance mechanisms and inflammatory bowel disease
  42. Case Report
  43. Inflammatory fibroid polyp: an unusual cause of abdominal pain in the upper gastrointestinal tract A case report
  44. Research Article
  45. microRNA-204-5p participates in atherosclerosis via targeting MMP-9
  46. LncRNA LINC00152 promotes laryngeal cancer progression by sponging miR-613
  47. Can keratin scaffolds be used for creating three-dimensional cell cultures?
  48. miRNA-186 improves sepsis induced renal injury via PTEN/PI3K/AKT/P53 pathway
  49. Case Report
  50. Delayed bowel perforation after routine distal loopogram prior to ileostomy closure
  51. Research Article
  52. Diagnostic accuracy of MALDI-TOF mass spectrometry for the direct identification of clinical pathogens from urine
  53. The R219K polymorphism of the ATP binding cassette subfamily A member 1 gene and susceptibility to ischemic stroke in Chinese population
  54. miR-92 regulates the proliferation, migration, invasion and apoptosis of glioma cells by targeting neogenin
  55. Clinicopathological features of programmed cell death-ligand 1 expression in patients with oral squamous cell carcinoma
  56. NF2 inhibits proliferation and cancer stemness in breast cancer
  57. Body composition indices and cardiovascular risk in type 2 diabetes. CV biomarkers are not related to body composition
  58. S100A6 promotes proliferation and migration of HepG2 cells via increased ubiquitin-dependent degradation of p53
  59. Review Article
  60. Focus on localized laryngeal amyloidosis: management of five cases
  61. Research Article
  62. NEAT1 aggravates sepsis-induced acute kidney injury by sponging miR-22-3p
  63. Pericentric inversion in chromosome 1 and male infertility
  64. Increased atherogenic index in the general hearing loss population
  65. Prognostic role of SIRT6 in gastrointestinal cancers: a meta-analysis
  66. The complexity of molecular processes in osteoarthritis of the knee joint
  67. Interleukin-6 gene −572 G > C polymorphism and myocardial infarction risk
  68. Case Report
  69. Severe anaphylactic reaction to cisatracurium during anesthesia with cross-reactivity to atracurium
  70. Research Article
  71. Rehabilitation training improves nerve injuries by affecting Notch1 and SYN
  72. Case Report
  73. Myocardial amyloidosis following multiple myeloma in a 38-year-old female patient: A case report
  74. Research Article
  75. Identification of the hub genes RUNX2 and FN1 in gastric cancer
  76. miR-101-3p sensitizes non-small cell lung cancer cells to irradiation
  77. Distinct functions and prognostic values of RORs in gastric cancer
  78. Clinical impact of post-mortem genetic testing in cardiac death and cardiomyopathy
  79. Efficacy of pembrolizumab for advanced/metastatic melanoma: a meta-analysis
  80. Review Article
  81. The role of osteoprotegerin in the development, progression and management of abdominal aortic aneurysms
  82. Research Article
  83. Identification of key microRNAs of plasma extracellular vesicles and their diagnostic and prognostic significance in melanoma
  84. miR-30a-3p participates in the development of asthma by targeting CCR3
  85. microRNA-491-5p protects against atherosclerosis by targeting matrix metallopeptidase-9
  86. Bladder-embedded ectopic intrauterine device with calculus
  87. Case Report
  88. Mycobacterial identification on homogenised biopsy facilitates the early diagnosis and treatment of laryngeal tuberculosis
  89. Research Article
  90. The will of young minors in the terminal stage of sickness: A case report
  91. Extended perfusion protocol for MS lesion quantification
  92. Identification of four genes associated with cutaneous metastatic melanoma
  93. Case Report
  94. Thalidomide-induced serious RR interval prolongation (longest interval >5.0 s) in multiple myeloma patient with rectal cancer: A case report
  95. Research Article
  96. Voluntary exercise and cardiac remodeling in a myocardial infarction model
  97. Electromyography as an intraoperative test to assess the quality of nerve anastomosis – experimental study on rats
  98. Case Report
  99. CT findings of severe novel coronavirus disease (COVID-19): A case report of Heilongjiang Province, China
  100. Commentary
  101. Directed differentiation into insulin-producing cells using microRNA manipulation
  102. Research Article
  103. Culture-negative infective endocarditis (CNIE): impact on postoperative mortality
  104. Extracorporeal shock wave therapy for the treatment of chronic pelvic pain syndrome
  105. Plasma microRNAs in human left ventricular reverse remodelling
  106. Bevacizumab for non-small cell lung cancer patients with brain metastasis: A meta-analysis
  107. Risk factors for cerebral vasospasm in patients with aneurysmal subarachnoid hemorrhage
  108. Problems and solutions of personal protective equipment doffing in COVID-19
  109. Evaluation of COVID-19 based on ACE2 expression in normal and cancer patients
  110. Review Article
  111. Gastroenterological complications in kidney transplant patients
  112. Research Article
  113. CXCL13 concentration in latent syphilis patients with treatment failure
  114. A novel age-biomarker-clinical history prognostic index for heart failure with reduced left ventricular ejection fraction
  115. Case Report
  116. Clinicopathological analysis of composite lymphoma: A two-case report and literature review
  117. Trastuzumab-induced thrombocytopenia after eight cycles of trastuzumab treatment
  118. Research Article
  119. Inhibition of vitamin D analog eldecalcitol on hepatoma in vitro and in vivo
  120. CCTs as new biomarkers for the prognosis of head and neck squamous cancer
  121. Effect of glucagon-like peptide-1 receptor agonists on adipokine level of nonalcoholic fatty liver disease in rats fed high-fat diet
  122. 72 hour Holter monitoring, 7 day Holter monitoring, and 30 day intermittent patient-activated heart rhythm recording in detecting arrhythmias in cryptogenic stroke patients free from arrhythmia in a screening 24 h Holter
  123. FOXK2 downregulation suppresses EMT in hepatocellular carcinoma
  124. Case Report
  125. Total parenteral nutrition-induced Wernicke’s encephalopathy after oncologic gastrointestinal surgery
  126. Research Article
  127. Clinical prediction for outcomes of patients with acute-on-chronic liver failure associated with HBV infection: A new model establishment
  128. Case Report
  129. Combination of chest CT and clinical features for diagnosis of 2019 novel coronavirus pneumonia
  130. Research Article
  131. Clinical significance and potential mechanisms of miR-223-3p and miR-204-5p in squamous cell carcinoma of head and neck: a study based on TCGA and GEO
  132. Review Article
  133. Hemoperitoneum caused by spontaneous rupture of hepatocellular carcinoma in noncirrhotic liver. A case report and systematic review
  134. Research Article
  135. Voltage-dependent anion channels mediated apoptosis in refractory epilepsy
  136. Prognostic factors in stage I gastric cancer: A retrospective analysis
  137. Circulating irisin is linked to bone mineral density in geriatric Chinese men
  138. Case Report
  139. A family study of congenital dysfibrinogenemia caused by a novel mutation in the FGA gene: A case report
  140. Research Article
  141. CBCT for estimation of the cemento-enamel junction and crestal bone of anterior teeth
  142. Case Report
  143. Successful de-escalation antibiotic therapy using cephamycins for sepsis caused by extended-spectrum beta-lactamase-producing Enterobacteriaceae bacteremia: A sequential 25-case series
  144. Research Article
  145. Influence factors of extra-articular manifestations in rheumatoid arthritis
  146. Assessment of knowledge of use of electronic cigarette and its harmful effects among young adults
  147. Predictive factors of progression to severe COVID-19
  148. Procedural sedation and analgesia for percutaneous trans-hepatic biliary drainage: Randomized clinical trial for comparison of two different concepts
  149. Acute chemoradiotherapy toxicity in cervical cancer patients
  150. IGF-1 regulates the growth of fibroblasts and extracellular matrix deposition in pelvic organ prolapse
  151. NANOG regulates the proliferation of PCSCs via the TGF-β1/SMAD pathway
  152. An immune-relevant signature of nine genes as a prognostic biomarker in patients with gastric carcinoma
  153. Computer-aided diagnosis of skin cancer based on soft computing techniques
  154. MiR-1225-5p acts as tumor suppressor in glioblastoma via targeting FNDC3B
  155. miR-300/FA2H affects gastric cancer cell proliferation and apoptosis
  156. Hybrid treatment of fibroadipose vascular anomaly: A case report
  157. Surgical treatment for common hepatic aneurysm. Original one-step technique
  158. Neuropsychiatric symptoms, quality of life and caregivers’ burden in dementia
  159. Predictor of postoperative dyspnea for Pierre Robin Sequence infants
  160. Long non-coding RNA FOXD2-AS1 promotes cell proliferation, metastasis and EMT in glioma by sponging miR-506-5p
  161. Analysis of expression and prognosis of KLK7 in ovarian cancer
  162. Circular RNA circ_SETD2 represses breast cancer progression via modulating the miR-155-5p/SCUBE2 axis
  163. Glial cell induced neural differentiation of bone marrow stromal cells
  164. Case Report
  165. Moraxella lacunata infection accompanied by acute glomerulonephritis
  166. Research Article
  167. Diagnosis of complication in lung transplantation by TBLB + ROSE + mNGS
  168. Case Report
  169. Endometrial cancer in a renal transplant recipient: A case report
  170. Research Article
  171. Downregulation of lncRNA FGF12-AS2 suppresses the tumorigenesis of NSCLC via sponging miR-188-3p
  172. Case Report
  173. Splenic abscess caused by Streptococcus anginosus bacteremia secondary to urinary tract infection: a case report and literature review
  174. Research Article
  175. Advances in the role of miRNAs in the occurrence and development of osteosarcoma
  176. Rheumatoid arthritis increases the risk of pleural empyema
  177. Effect of miRNA-200b on the proliferation and apoptosis of cervical cancer cells by targeting RhoA
  178. LncRNA NEAT1 promotes gastric cancer progression via miR-1294/AKT1 axis
  179. Key pathways in prostate cancer with SPOP mutation identified by bioinformatic analysis
  180. Comparison of low-molecular-weight heparins in thromboprophylaxis of major orthopaedic surgery – randomized, prospective pilot study
  181. Case Report
  182. A case of SLE with COVID-19 and multiple infections
  183. Research Article
  184. Circular RNA hsa_circ_0007121 regulates proliferation, migration, invasion, and epithelial–mesenchymal transition of trophoblast cells by miR-182-5p/PGF axis in preeclampsia
  185. SRPX2 boosts pancreatic cancer chemoresistance by activating PI3K/AKT axis
  186. Case Report
  187. A case report of cervical pregnancy after in vitro fertilization complicated by tuberculosis and a literature review
  188. Review Article
  189. Serrated lesions of the colon and rectum: Emergent epidemiological data and molecular pathways
  190. Research Article
  191. Biological properties and therapeutic effects of plant-derived nanovesicles
  192. Case Report
  193. Clinical characterization of chromosome 5q21.1–21.3 microduplication: A case report
  194. Research Article
  195. Serum calcium levels correlates with coronary artery disease outcomes
  196. Rapunzel syndrome with cholangitis and pancreatitis – A rare case report
  197. Review Article
  198. A review of current progress in triple-negative breast cancer therapy
  199. Case Report
  200. Peritoneal-cutaneous fistula successfully treated at home: A case report and literature review
  201. Research Article
  202. Trim24 prompts tumor progression via inducing EMT in renal cell carcinoma
  203. Degradation of connexin 50 protein causes waterclefts in human lens
  204. GABRD promotes progression and predicts poor prognosis in colorectal cancer
  205. The lncRNA UBE2R2-AS1 suppresses cervical cancer cell growth in vitro
  206. LncRNA FOXD3-AS1/miR-135a-5p function in nasopharyngeal carcinoma cells
  207. MicroRNA-182-5p relieves murine allergic rhinitis via TLR4/NF-κB pathway
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Heruntergeladen am 9.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/med-2020-0226/html
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