Getting to Grips With Gastric Pathology

The purpose of this article is to offer an overall approach to gastric mucosal disorders in children. In collaboration with a pathologist who has special expertise in gastrointestinal histopathology, the pediatric endoscopist can gain a wealth of useful information. This lode of information can be mined without much difficulty, but requires attention to detail and accuracy. In children, gastric mucosal disorders are underrecognized and poorly characterized, probably because of the flawed tendency to rely on macroscopic appearances at endoscopy, the use of imprecise and nonstandardized descriptive terminology, and an apparent reluctance to take multiple gastric biopsy specimens. Practical advice for endoscopists about endoscopic landmarks, terminology, and acquisition of biopsy specimens may facilitate consistency of communication among endoscopists, and between endoscopists and pathologists. The author aims to propose an approach to, and a classification of, gastric mucosal disorders that is pertinent to practicing pediatric endoscopists, focusing attention on this little-studied area and facilitating diagnosis or exclusion of the various entities that comprise the classification. This will serve the ultimate goal of accurate diagnosis and an appropriate approach to the child under our care. In addition, with adequate biopsy specimen harvesting and careful tissue handling, a quantity and quality of tissue can be obtained to enable scientific studies, the results of which can be taken back to the bedside for the benefit of many children. For many years, Professor Walker-Smith and his team have successfully taken clinical material to the lab and scientific studies back to the clinic. In short, the pediatric endoscopist can obtain a wealth of useful information for direct clinical care and for scientific study. In this regard the importance of collaboration with a pathologist who has special expertise in gastrointestinal histopathology cannot be overstressed. RECOGNIZING THE DISTINCTION BETWEEN -OPATHY AND -ITIS IN THE STOMACH The categorization of entities into gastropathies and gastritides is important and helps to narrow the differential diagnosis in a given case. By understanding the different endoscopic and histologic responses of the stomach to injury, the endoscopist can consider the various diagnostic possibilities and how best to identify them. The term gastritis often is used loosely. For example, clinicians may refer to a patient with epigastric pain or dyspepsia as having gastritis, whereas radiologists may diagnose gastritis on the basis of nonspecific changes seen on radiograph images, such as mucosal irregularity or swelling. This colloquial use of the term imparts a false impression to both user and patient that the patient actually has gastritis of some type. Offering this “diagnosis” is not helpful, because a myriad of things cause gastritis, many of which require quite different approaches. Gastritis is neither a clinical nor a radiologic diagnosis; most often it is solely a histologic diagnosis, made by the use of random or targeted endoscopic biopsy specimens. Although some conditions that injure the gastric mucosa may result in inflammation, others do not. Thus, gastritis, as the suffix -itis implies, is characterized by the presence of inflammatory cells. In contrast, the term gastropathy refers to conditions in which inflammation is not a prominent feature, although epithelial damage and regeneration may occur. Although in a specific clinical context, endoscopic appearances sometimes may be suggestive of a particular condition, the diagnosis of gastritis or gastropathy is almost always a biopsy diagnosis. The categorization of entities into gastritises and gastropathies is important and helps narrow the diagnostic possibilities in a given case. The above notwithstanding, in this article, for the sake of simplicity, the term gastritis often is used generically to refer to both gastritides and gastropathies. (Strictly speaking, the word gastropathy refers to any and all histologic disorders of the stomach. However, in this article, we use its narrower and more recent application.) WHAT IS MUCOSAL PATHOLOGY IN THE PEDIATRIC STOMACH To answer this question, one first has to know what is normal, macroscopically (i.e., endoscopically) and microscopically (histologically). For example, with regard to endoscopic appearances, is erythema normal, or is it pathologic? If the mucosa appears normal at endoscopy, does it mean that no pathology is present? What is known of the normal histology of the stomach in childhood? Proper gross (endoscopic) and microscopic assessment of the stomach requires proper and standardized information-gathering techniques. If an abnormality is present, can the child's symptoms be ascribed to it, or does it represent a distinct, known entity? To answer this requires knowledge of specific entities in the stomach and their presenting symptoms and signs in childhood. Given the many disorders that occur, and acknowledging the space constraints for this article, the reader is referred to a more comprehensive account of specific gastric mucosal disorders in children (1). Herein are comments on an overall approach to gastric mucosal disorders in children. APPROACH TO DIAGNOSIS: HIGH-YIELD GASTROSCOPY When a child is scheduled for diagnostic upper gastrointestinal endoscopy, the endoscopist has an obligation to maximize the diagnostic potential of the procedure. Central to this must come the recognition that making a diagnosis based on macroscopic appearances alone is limited (1–6). For example, gastric mucosa that appears normal at endoscopy may harbor marked inflammation on microscopy. The converse is also true, in that a markedly red mucosa at endoscopy may be normal and the redness caused by contact with the endoscope; redness may reflect underlying microvascular congestion without the presence of inflammatory cells. In other words, often a poor correlation exists between endoscopy and histologic findings. Therefore, multiple gastric biopsy specimens from different zones of the stomach must be an integral part of a proper examination of the gastric mucosa (1–6). The more tissue and the better its quality, the better the chance of accurate diagnosis. A high yield of accurate diagnoses, including definitively ruling out mucosal disease, largely depends on the endoscopist's care and attention to detail in the following areas. Endoscopic Landmarks, Histologic Zones In reporting endoscopic appearances, the endoscopist describes the gross pathology of disease. Gastric disorders often have a predilection for a particular area or zone of the stomach; therefore, inaccurate landmark identification may result in poorly targeted biopsies and erroneous or missed diagnoses. The histologic zones of the stomach correspond to the different gross anatomic zones thereof, although not precisely because some overlap and interdigitation of histologic zones always occur at areas of transition, hence the term transitional mucosa for these. A more detailed description of gastric landmarks and their histologic correlates is given elsewhere (7–9). Terminology The use of nonstandardized terminology or interpretative terms to describe macroscopic appearances often leads to overinterpretation of findings, poor interobserver reliability of findings, and uninterpretable endoscopy reports. It is more helpful to record endoscopic findings in factual, descriptive terms. The endoscopist should report only what is seen in standard and unambiguous terminology. Jargon, -itis terms, or interpretative terms should be avoided in the factual or objective part of the endoscopy report. For example, use of the term gastritis could mean anything from erythema to distinct erosions; if the mucosa is red it should be documented as “red” or “erythematous” (mild/moderate/intense or hemorrhagic) and not as “antritis” or “gastritis” because inflammation may not be present (3). The human eye, even with the aid of an endoscope, is not a microscope. The only place we can “see” gastritis is under the microscope. An erosion is a mucosal break that does not penetrate the muscularis mucosae, whereas an ulcer extends through the muscularis into the submucosa. Endoscopists cannot accurately determine depth of lesions, but they have some clues: erosions are often multiple, usually have white bases, and each erosion usually is surrounded by a ring of erythema. When erosions have recently bled, their bases may be black. Hemorrhage refers to a bright, shiny red appearance of the mucosa in patches, streaks, or discrete petechiae, not associated with a visible mucosal break. Although the term submucosal hemorrhage sometimes is used, endoscopists cannot see through the muscularis mucosae; therefore, the term subepithelial hemorrhage is preferable, to allow for varying depths of hemorrhage. Other confusing terms used for subepithelial hemorrhage and that are best avoided include acute gastritis, hemorrhagic gastritis (inflammation is usually absent from hemorrhagic lesions), or hemorrhagic erosion (usually no erosion present) (10). If gastric rugae are large, accurate terms of description are thick or swollen folds or rugae, not edematous or hypertrophic folds, because edema and hypertrophy are histologic, not endoscopic, findings. It is also important to accurately describe nodules in the stomach. For example, a nodule or patch of nodules may be seen occasionally, especially at the antral–body junction; these may represent a prominent areae gastricae (11) and usually are unimpressive. In contrast, a continuous diffuse carpet of nodules virtually throughout the antrum is characteristic of Helicobacter pylori infection, past or present (12,13). The nodules of chronic varioliform gastritis also are different; they are larger, discrete, more raised, often have an umbilicated central erosion or shallow ulcer, and predominate in the gastric fundus and body (14–16), although they may extend into the antrum. Large nodules, more like blebs, may occur in the proximal stomach with cytomegalovirus gastritis (3); similar nodules in the antrum may occur in eosinophilic gastritis. Therefore, it is best for the endoscopist to accurately describe only what is seen and to offer an impression or differential diagnosis only at the end of the endoscopy report, based on the factual findings. Biopsy Sampling Different disorders may have a predilection for one topographic zone or another of the stomach. Sometimes, the same agent causes different patterns of injury in different populations, for example, as with H. pylori (17–20). Sometimes disease may occur in more than one zone of the stomach, for example, as with H. pylori, Crohn's disease, eosinophilic gastritis, atrophic gastritis, and cytomegalovirus infection, as indicated below. Thus, biopsies must be taken from different topographic zones of the stomach (2,9,10,20). Even with careful biopsy specimen handling by trained personnel, endoscopic biopsy specimens may sustain crush or other artefacts; thus, when biopsy is indicated, at least two specimens should be taken from a particular lesion or zone of the stomach. Although the optimum number of specimens has yet to be determined, when mucosa appears normal, my practice is to take at least two specimens from the prepyloric or midantrum and two from the greater curve of midbody. Others take two from the antrum–body transition zone of the lesser curve, a zone in which inflammation and metaplasia occur in adults (2). In addition, many take biopsy specimens from the gastric cardia, immediately below the Z line, when H. pylori infection, Barrett metaplasia, carditis (caused by gastroesophageal reflux or H. pylori) (20–24) or MALT lymphoma (25) may be present. When endoscopic findings are puzzling or a lesion is present, more specimens should be taken randomly and from the lesion or edge thereof. The size of biopsy specimens also is important. Usually not much is gained from deep biopsy specimens, deeper than muscularis mucosa. However, surface area is important. Larger surface area means less sampling error and that relatively less of the specimen has crush or mounting artefact. Specimens taken with pediatric forceps (biopsy channel of 2 mm or less) often are of little value. In most children older than 2 or 3 months of age, an endoscope with a 2.8-mm biopsy channel usually can be used (e.g., Olympus XQ20) and specimens taken with these forceps often are adequate, if several are taken. In contrast, each biopsy specimen taken with jumbo or large-cup forceps offers at least twice or three times the amount of mucosa for diagnosis, and these specimens can often be obtained in older children. Although the number of inflammatory cells in the gastric mucosa of normal children has not been extensively studied, some published data summarize this elsewhere (9). CLASSIFICATION A system for grading the severity of pediatric gastritis has been previously described(12). However, other than an earlier pathologic description of pediatric gastritis from our group (9), no classification or approach to pediatric gastritis has been published. Proposing a conceptual framework of gastritis and gastropathy, describing the specific entities encountered in the pediatric stomach, and describing their differential diagnosis may make accurate diagnosis easier for the clinician. No classification of gastritis satisfies everyone, and published classifications have different objectives. Some are a glossary of appearances (26), and some list clinical disorders (3). The Sydney system is essentially a checklist to help the pathologist review biopsy specimens and uniformly report findings, by use of a visual analogue scale. Therefore, it is aptly named a system rather than a classification (19,26–28). Its usefulness to pediatric endoscopists is limited because its major focus is grading the severity of chronic gastritis, atrophy, and intestinal metaplasia, which are of concern more in adults than in children. Furthermore, the Sydney system does not integrate histopathology with endoscopic appearance, and it does not address noninflammatory conditions (19). We have chosen to classify mucosal disorders of the stomach in children primarily by their endoscopic appearances. In this system, gastritis is classified into two groups:erosive, hemorrhagic gastritis or gastropathy, and nonerosive gastritis or gastropathy. Although some disorders can present as either erosive or nonerosive, each is classified by its most common presentation. The disorders in each group are placed in approximate sequence of their prevalence in the practice of the author. Its cause and any distinctive clinical, endoscopic, and histologic features then describe each disorder. The advantages of this approach are simplicity and ease of use for the practicing pediatric endoscopist. Based on this approach, a diagnosis or differential diagnosis occasionally may be made at the time of endoscopy, with varying degrees of certainty. However, for the majority of disorders, confirmation of the initial impression, or definitive diagnosis, still depends on biopsy specimens, and therefore on active dialogue and close collaboration with a pathologist. Erosive and Hemorrhagic Gastritis or Gastropathy Most of these entities are diagnosed endoscopically, usually in patients seeking treatment for gastrointestinal bleeding. Because inflammation is not a feature of most hemorrhagic lesions, most conditions in this category are gastropathies. Biopsy specimens usually are not required from erosive or hemorrhagic lesions. However, gastritides not in the erosive or hemorrhagic category may present with erosions or hemorrhagic lesions, and in these cases, biopsy specimens are essential for the diagnosis, for example, H. pylori, Crohn's disease, cytomegalovirus, and allergic gastritis. Specific Disorders: Each disorder or group of disorders is discussed in detail elsewhere (1). Stress gastropathy Neonatal gastropathies Traumatic gastropathy Aspirin and other nonsteroid antiinflammatory drugs Other drugs Portal hypertensive gastropathy Uremic gastropathy Chronic varioliform gastritis Bile gastropathy Henoch-Schonlein gastropathy Corrosive gastropathy Exercise-induced gastropathy/gastritis Radiation gastropathy Nonerosive gastritis or gastropathy In nonerosive gastritis, a poor correlation usually exists between endoscopic appearance and histologic findings, that is, the diagnosis is usually purely histologic. An exception is the nodular antrum of H. pylori–associated ulcer disease in children. However, nodularity persists even after eradication of H. pylori infection, so in this case the diagnosis is endoscopic and histologic. Furthermore, nodularity is not always present, and therefore the diagnosis still ultimately depends on histology. Some of the entities in this section also may present as an erosive gastropathy or gastritis, but are included here because they more commonly present without erosions. Lymphocytic gastritis deserves special mention and may be seen in disorders as apparently diverse as celiac disease, cytomegalovirus gastritis, Menetrier disease, H. pylori infection, and chronic varioliform gastritis. Because ours is an endoscopic classification, lymphocytic gastritis is mentioned under each of those disease entities. Specific Disorders: Each disorder or group of disorders is discussed in detail elsewhere (1): H. pylori gastritis Crohn's gastritis Allergic gastritis Proton-pump inhibitor gastropathy Celiac gastritis Gastritis of chronic granulomatous disease Cytomegalovirus gastritis Eosinophilic gastritis Collagenous gastritis Graft versus host gastritis Menetrier gastritis Gastritis of pernicious anemia Gastritis with autoimmune diseases Other granulomatous gastritides Phlegmonous and emphysematous gastritis Other infectious gastritides

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