Helicobacter pylori (Spanish Edition)

Hospital de la Santa Creu i Sant Pau. It is for this reason that agreeing on indications for eradication, most appropriate diagnostic tests, and better eradicating drugs is of clinical significance. Therefore, it is only natural that various consensus conferences on these issues have been held in America , Europe 5 and Asia 6.

Five years later, in November , the 2 nd Consensus Conference on H. All this was based on a methodology similar to that used 5 years before, a systematic literature review, and a subsequent joint debriefing. Furthermore, evidence grades and recommendation levels have been established in this conference, which had not been considered in the previous consensus.

A literature search was performed including the Medline database, and abstracts from the following international meetings: To answer specific questions efficacy of given therapy or possibilities for easier diagnosis in Spain , reports at national congresses and meetings were also reviewed. Since many of the questions posed had already been reviewed during the 1 st Consensus Conference, new evidence supporting existing recommendations or modifications thereof will be emphasized. Results from the systematic review will include a grading of scientific evidence supporting statements according to the categorization used in the Clinical Practice Guidelines jointly issued by the Cochrane Collaboration 9.

In summary, evidence levels go from grade 1 -supported by multiple clinical trials with homogeneous results or at least a meta-analysis- to grade 5 -based only on expert views on the issue or studies of uncertain reliability Table I. Recommendation grade A -the highest, considered highly recommendable- corresponds to level-1 studies.

Recommendation grade B -meaning a favorable recommendation- corresponds to level-2 or -3 studies or evidence, or extrapolations from level-1 studies.

Muestra de materia fecal: antígeno de H. pylori

Recommendation grade C -interpreted as an inconclusive favorable recommendation- corresponds to level-4 studies or extrapolations from level-2 or -3 studies. Finally, recommendation grade D -which neither recommends nor disapproves of an intervention- corresponds to level-5 studies, or to inconclusive or inconsistent studies at any level. Bermejo Madrid , M. Bixquert Valencia , D. Boixeda Madrid , F. Borda Pamplona , L. Caballero Granada , X. Calvet Barcelona , R.

Carballo Murcia , M. Castro Seville , M. Ducons Huesca , I. Elizalde Barcelona , M. Gisbert Madrid , F. Khorrami Madrid , A. Lanas Saragossa , C. Montoro Huesca , J. Pajares Madrid , J. Sancho Barcelona , S. Santolaria Huesca , C. Taxonera Madrid , J. The steering committee of "Spanish group for the study of H.

All participants were included in one of the three groups; each group manager developed questions on their corresponding topic, which were then answered via e-mail by all group members. Answers failing to reach this level of accord were debated in a workshop prior to the plenary session and, eventually, their approval. Each of the situations and questions posed in the aforementioned consensus meeting, together with their answers as approved during the plenary session, are discussed below.

Patients with dyspeptic symptoms in whom gastroscopy demonstrates no significant macroscopic condition are diagnosed with functional dyspepsia. The indication of H. Literature references are many, but contradictory The dyspeptic subgroup likely to benefit from eradicating therapy is poorly defined, and may in addition correspond to patients with ulcer in whom no lesion was identified at endoscopy.

There is currently extensive scientific evidence available that in patients with gastric or duodenal ulcer H. An indication for eradication is recommended in both active and asymptomatic ulcers, provided they have been properly documented before. Such evidence will be dealt with in greater depth in the therapy section. In patients not receiving aspirin ASA or non-steroidal anti-inflammatory drugs NSAIDs erosive duodenitis may be considered within the spectrum of duodenal ulcerative disease, and eradication is therefore recommended 7,8.

Gastric erosions may represent a heterogeneous group of lesions varying in extension, number and even underlying histologic changes, and scientific evidence available is insufficient to support an indication for eradication. Non-steroidal anti-inflammatory drugs NSAIDs are extensively used in the treatment of rheumatic disease arthritis and osteoarthritis , and sporadically for headaches and menstrual pain as well.

However, their use is clearly restricted -particularly in the long run- by side effects, specifically gastrointestinal and renal toxicity Differences exist depending on age patients with years of age have a fold increased risk versus patients with years of age , and a history of peptic ulcer entails a 6-fold increased risk, this risk growing to 15 times higher for complicated ulcers hemorrhage or perforation. However, as recently noted, increased cardiologic problems in relation to coxibs must be considered.

Most peptic ulcers are associated with H. A group of patients with H. In the eradication group 2 1. When a patient with GERD also has a gastric or bulbar ulcer, the benefit of eradication for his or her ulcer is far greater than the potential but unproven adverse effect on reflux. However, subsequent studies would not confirm this 23 , and a clear stance on this topic remains to be taken Is Helicobacter pylori eradication indicated for gastritis or the prevention of gastric cancer?

Eradicating therapy causes a regression of histologic lesions, and hence it would be theoretically possible to prophylactically target gastric cancer by eradicating this germ in infected patients, most of them asymptomatic Given the prevalence of H. Regarding the possibility of treating only patients with atrophic gastritis and intestinal metaplasia, data suggesting that pre-neoplastic lesions may regress following eradication remain inconclusive In view of this lack of evidence and the high number of therapies needed, systematic eradication cannot be recommended.

Eradication is also recommended for patients undergoing partial gastrectomy for gastric cancer and H. An excellent study 27 posed a new indication for eradication. First-grade relatives of patients with gastric cancer have a higher hypochlorhydria rate when compared to controls 27 vs. The conclusion was that first-grade relatives of patients with gastric cancer had a greater prevalence of mucosal abnormalities with a well-known malignant potential, but only those infected by H.

Indicating eradication in this set of subjects seems only logical for the prevention of gastric cancer. Regarding atrophic gastritis and intestinal metaplasia no evidence supports eradication, but this would seem a reasonable option for intestinal metaplasia with high-risk histological criteria.

Therefore, endoscopy is important before an eradicating therapy is indicated, since eradication is likely to cure the malignancy when the mucosa and submucosa alone are involved. Patients with added muscular involvement will also need oncologic therapy. Treatment should be administered in specialized centers where echoendoscopy is available, and an extension study, the confirmation of total regression, and adequate long-term follow-up are ensured.

For the remaining gastric MALT lymphomas high-grade, advanced disease , eradication is only a therapy component, and other adjuvant therapies should be used. For the remaining MALT lymphomas other therapies should be used in addition to eradication. Is eradication indicated for extraintestinal conditions in relation to Helicobacter pylori infection?

A wide number of extraintestinal conditions have been related to H. It is presumed that H.

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We currently have a wide variety of methods for the diagnosis of this infection. Since the last Spanish Consensus Conference a great number of papers have been published gaining insight into the understanding, usefulness, and clinical applicability of known diagnostic modalities, while others have dealt with new, recently introduced methods. The present Consensus Conference has considered two viewpoints regarding diagnostic modalities for H.

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Regarding diagnosis, agreed-upon recommendations for the following clinical settings will be discussed: Regarding diagnostic modalities, consensus has been reached on the current role of methods based on: A Diagnosis of Helicobacter pylori infection in various clinical situations. In this situation systematic biopsy collection is not indicated for the diagnosis of H. The finding of a gastric or duodenal ulcer during upper gastrointestinal endoscopy requires that the presence of H.

In such situation, it is accepted that the diagnosis of infection be based on modalities performed on biopsy samples 33, Endoscopists must take two biopsy samples from the antrum and one from the body. Rapid urease testing should be first choice because of its simplicity, reliability, economy, and results in just a few hours. It requires a biopsy sample collected from the gastric antrum.

A positive rapid urease test confirms infection 35, In case of a negative urease test or because of a study for gastritis, the two remaining biopsy samples one antral and one from the gastric body should be sent to the Pathology Dept. Naturally, and regardless of H. Lastly, given the relevance of H. For upper digestive hemorrhage, when endoscopy demonstrates the presence of a gastric or duodenal ulcer, the diagnosis of H. Otherwise the diagnosis of infection will be arrived at later using the 13 C-urea breath test For gastric ulcer this diagnosis may be performed using biopsy-based methods in any of the necessary subsequent endoscopic monitorings.

In compromised clinical settings or in case of technical inability high-volume blood remnants , the diagnosis of infection will be subsequently reached using a breath test for duodenal ulcer, or a biopsy study for gastric ulcer during the mandatory endoscopic monitoring. In any patients with a history of previously diagnosed peptic ulcer using adequate modalities, with or without symptoms, the potential presence of H.

Given the fact that no endoscopy is usually needed in this setting, the method of choice for the diagnosis of H. Should this test be unavailable, H. Serologic tests are not recommended in view of their scarce positive predictive value 50, On the other hand, despite the high prevalence of H. Effectiveness should be confirmed in all patients undergoing eradication therapy. This monitoring should be performed at least 6 weeks after treatment completion ,,52, The test of choice in such cases is the 13 C-urea breath test , Treatment with antibiotics on any grounds entails a significant reduction of H.

On the other hand, PPIs are known to exert an inhibitory effect on the germ's urease activity, which also leads to reduced sensitivity regarding H. Similarly, PPIs cause a migration of germs towards more proximal segments within the stomach. As a result, the diagnosis of infection in patients currently or recently on PPIs or antibiotics requires that this treatment be discontinued for at least 2 and 4 weeks, respectively, beforehand 54, Such therapy discontinuation is not required for H 2 antagonists.

Discontinuation is not required for H 2 antagonists. This is first-choice for the diagnosis of H. Rapid urease testing should be performed on a single biopsy sample, preferably from the gastric antrum. A histological study of biopsy samples to diagnose infection is indicated for all patients requiring upper digestive endoscopy with a negative urease test.

This circumstance takes place mainly in the presence of blood and in patients on antibiotic or antisecretory therapy. The histological diagnosis of H. Because of its greater sensitivity, a Giemsa stain is recommended for negative studies using hematoxillin-eosin , The culturing of biopsy specimens is most specific, but its complexity, cost, and diagnostic delay have relegated this method from clinical practice , Cultures and antibiograms may be performed on gastric mucosal biopsies when two eradication regimens primary and salvage treatments fail in order to study antibiotic resistance.

However, this procedure has an uncertain impact in practice ,53 , and its use is then restricted to the setting of epidemiologic or clinical investigation trials. Sample collection using the so-called "thread test" is not recommended in view of its higher complexity and risk of contamination by oropharyngeal bacteria It is a simple, non-invasive, low-cost test that may be easily used in clinical practice.

It is therefore the test of choice for the diagnosis of H. Efficacy is limited in patients with low-density colonization treated with PPIs or antibiotics 54,55 or gastrectomized, as contact between labelled urea and the gastric mucosa is less likely 56, The predictive value of serologic tests is very limited, and their application in clinical practice is therefore not recommended 50,51, However, its use may be considered for patients not requiring endoscopy as an alternative to the breath and stool antigen tests, when both these tests are unavailable. The primary utility of serologic tests lies in population-based epidemiologic studies.

Rapid serologic tests have a low diagnostic yield, and are therefore not recommended 59, The diagnostic efficacy of this stool antigen test is high for both the primary diagnosis of H. Results are better with monoclonal versus polyclonal tests Efficacy, as with the 13 C-urea breath test, is influenced by low-density colonization as a result of PPI or antibiotic therapy, or of the presence of blood in cases of upper digestive bleeding.

The stool antigen test is simple and easy to use in clinical practice, its only limitation being fecal manipulation. As a result, it is considered the most appropriate alternative to 13 C-urea breath testing in the diagnosis of H. May combined ranitidin-bismuth citrate be included among first-choice eradicating therapies as a replacement for PPIs together with two antibiotics? A recent systematic review of the literature showed a mean H. To date, 15 randomized studies comparing proton pump inhibitors PPIs versus R-BC together with clarithromycin and amoxicillin have been carried out, and both alternatives have been shown to be equivalent However, when antibiotics used include clarithromycin and a nitroimidazole, a strategy evaluated in 13 studies, a meta-analysis of said studies showed that R-BC is superior to PPIs The combination of a PPI with clarithromycin and amoxicillin has been most common in Spain.

Since the 1 st Spanish Consensus Conference numerous data have been reported supporting its first-choice role Similarly, as previously suggested, combined R-BC together with two antibiotics may be included among first-choice eradicating therapies. Regarding antibiotics to be combined with both PPIs and R-BC, a recommendation that these should be clarithromycin and amoxicillin is currently favored. Few authors advocate for 1 week of quadruple therapy as first-line treatment In summary, first-choice regimens recommended in Spain include: The 1 st Spanish Consensus Conference concluded that both lansoprazole and pantoprazole were equivalent to omeprazole and therefore may be indistinctly used in triple therapies with two antibiotics.

Various studies have been published since then evaluating pantoprazole in greater detail, and considerable experience has been acquired with other, more recent PPIs such as rabeprazole and esomeprazole. Regarding the latter three PPIs, various meta-analyses demonstrating an efficacy similar to that of omeprazole have been reported Does previous treatment with a proton pump inhibitor reduce the effectiveness of subsequent triple therapy?

In dual therapy a PPI plus one antibiotic , which was dropped because of ineffectiveness, a previous treatment with omeprazole was said to be a predictor of failed eradication. However, a previous PPI does not seem to influence eradication rates with triple therapies Is it necessary to prolong PPI administration in duodenal ulcer following the completion of antibiotic therapy for 7 days? In initial eradicating therapies PPIs were prolonged for additional weeks.

However, a high rate of duodenal ulcer healing has been detected with the use of a PPI plus antibiotics for one week Is it necessary to prolong PPI administration in gastric ulcer following the completion of antibiotic therapy for 7 days? It should be highlighted that, in contrast with duodenal ulcer, no studies directly comparing eradicating therapy alone versus eradicating therapy followed by PPIs are available for gastric ulcer 87, However, the healing rate exponentially decreased with ulcer size increases How long should eradicating therapy last when a proton pump inhibitor and two antibiotics are used?

It has been recently suggested that eradicating therapy is more effective in patients with ulcer, which could bring up the sufficiency of shorter therapy regimens On the contrary, patients with functional dyspepsia seem to respond worse to eradicating therapy, and hence could benefit from prolonged therapy regimens In this regard a Spanish multicenter study has just been completed where eradicating therapy with a PPI, clarithromycin and amoxicillin for 7 versus 10 days has been compared in a large group of patients using a randomized design In patients with ulcer differences seen between both regimens were minimal, whereas the longest regimen proved obviously superior in patients with functional dyspepsia On the other hand a financial analysis showed that therapy for 10 days is more cost-effective in patients with functional dyspepsia; however, prolonged therapy is no cost-effective strategy for patients with ulcer Are cultures and antibiograms necessary prior to the administration of a first course of eradicating therapy?

Prior cultures are not necessary in clinical practice, since empirical treatment i. Are cultures and antibiograms neccessary prior to a second course of eradicating therapy following a failed initial attempt? Cultures are also unnecessary before a second course of eradicating therapy following a failed initial regimen because of the high effectiveness of empirical quadruple therapy It is recommended that a number of specially devoted centers routinely perform cultures, in order to study the incidence of resistance following failed eradication, and to assess the influence of resistance on salvage therapy.

What salvage therapy should be used following a failed first attempt with a PPI, claritromycin and amoxicillin? Various studies have assessed quadruple therapy using a PPI, bismuth, tetracycline and metronidazole in view of failed attempts with a PPI, clarithromycin and amoxicillin More recently the substitution of R-BC for the PPI and bismuth compound in the quadruple salvage regimen has been seen to be associated with encouraging results , , with the advantage that fewer drugs are required and dosage is simpler.

What is to be done when two eradication attempts fail the first one using a PPI, clarithromycin and amoxicillin; the second attempt using quadruple therapy? Are cultures necessary prior to a third eradicating attempt? When two eradicating treatments fail a first option is obviously to perform cultures and an antibiogram, in order to select the most appropriate antibiotic regimen according to bacterial susceptibility. While this "targeted" treatment option is most recommended, its usefulness has not been sufficiently confirmed in clinical practice. On the other hand, there are reasons to hold back cultures before a third eradicating therapy course, and to recommend a new empirical treatment instead No antibiotics previously used should be repeated for empirical treatment, since resistance to clarithromycin and metronidazole is known to arise in most cases when a combination including these two drugs fails.

Therefore, none of the antibiotics to which H. Thus, when a third empirical therapy course -bar clarithromycin and metronidazole- is to be administered, the following options are available:. On the other hand, and even more importantly, no H.

Helicobacter pylori - Wikipedia

However, a number of isolated myelotoxicity events have been reported, which underscores the need to be on the alert when this novel drug is administered. However, since experience with drugs used in third-line combinations is still limited and somehow relevant adverse effects have already been reported, it seems advisable that their assessment be performed by experienced teams specializing in this subject. In patients having suffered from gastroduodenal ulcer-related bleeding, should a maintenance therapy course with antisecretory agents be used following the eradication of Helicobacter pylori infection?

Peptic ulcer is the main cause of upper gastrointestinal bleeding, and H. Long-term maintenance antisecretory therapy has been a standard for the prevention of hemorrhagic recurrence in patients with a prior digestive bleeding episode from peptic ulcer. A systematic review and a meta-analysis have been published of late according to the Cochrane Collaboration's methodology, and they show that treatment for H. Based on the studies assessing the incidence of hemorrhagic recurrence following successful H. The presence of H. There is no consensus regarding the initial diagnostic or therapeutic alternative of choice for young patients cut-off age is usually 50 years with dyspepsia and no symptoms or alert signs.

Three strategies may be considered:. The latter option entails an "indirect" test not requiring endoscopy preferentially a breath test for the diagnosis of H. The "test and treat" strategy has been recommended by most Clinical Practice Guidelines and Consensus Conferences in young dyspeptic patients younger than 50 years with no symptoms or alert signs Following this review other authors confirmed these findings It may be then concluded that the "test and treat" strategy is as effective as initial endoscopy in the management of uninvestigated dyspepsia, and reduces the number of endoscopies.

In addition, a considerable number of cost-effectiveness analyses have been reported, which compared the " test and treat" strategy versus endoscopy; all of them agree that the former is notably more cost-effective than the latter In summary, it may be concluded that the "test and treat" strategy is more cost-effective than initial endoscopy. All of them showed a decrease in symptoms recurrence, as well as reduced dyspeptic symptoms and improved quality of life following the first treatment One study compared the "test and treat" strategy versus empirical antisecretory therapy in patients with uninvestigated dyspepsia, and concluded that the former option is more effective than the latter.

Breath testing is to be preferred to serology for the study of H. Multiple cost-effectiveness studies have shown that, under conditions of moderate to high H. RuvC protein is essential to the process of recombinational repair, since it resolves intermediates in this process termed Holliday junctions. Noninvasive tests for H. An endoscopic biopsy is an invasive means to test for H. Low-level infections can be missed by biopsy, so multiple samples are recommended. The most accurate method for detecting H.

Helicobacter pylori is a major cause of certain diseases of the upper gastrointestinal tract. Rising antibiotic resistance increases the need to search for new therapeutic strategies; this might include prevention in the form of vaccination. The presence of bacteria in the stomach may be beneficial, reducing the prevalence of asthma , [76] rhinitis , [76] dermatitis , [76] inflammatory bowel disease , [76] gastroesophageal reflux disease , [77] and esophageal cancer [77] by influencing systemic immune responses.

Recent evidence suggests that nonpathogenic strains of H. The standard first-line therapy is a one-week "triple therapy" consisting of proton pump inhibitors such as omeprazole and the antibiotics clarithromycin and amoxicillin. Previously, the only option was symptom control using antacids , H 2 -antagonists or proton pump inhibitors alone. An increasing number of infected individuals are found to harbor antibiotic-resistant bacteria.

This results in initial treatment failure and requires additional rounds of antibiotic therapy or alternative strategies, such as a quadruple therapy, which adds a bismuth colloid , such as bismuth subsalicylate. Ingesting lactic acid bacteria exerts a suppressive effect on H. The substance sulforaphane , which occurs in broccoli and cauliflower , has been proposed as a treatment. Helicobacter pylori colonizes the stomach and induces chronic gastritis , a long-lasting inflammation of the stomach.

The bacterium persists in the stomach for decades in most people. Most individuals infected by H. In the absence of treatment, H. The proportion of acute infections that persist is not known, but several studies that followed the natural history in populations have reported apparent spontaneous elimination. Mounting evidence suggests H. Blaser advanced the hypothesis that H. At least half the world's population is infected by the bacterium, making it the most widespread infection in the world. The age when someone acquires this bacterium seems to influence the pathologic outcome of the infection.

People infected at an early age are likely to develop more intense inflammation that may be followed by atrophic gastritis with a higher subsequent risk of gastric ulcer, gastric cancer, or both. Acquisition at an older age brings different gastric changes more likely to lead to duodenal ulcer. Despite high rates of infection in certain areas of the world, the overall frequency of H. Helicobacter pylori is contagious, although the exact route of transmission is not known. Consistent with these transmission routes, the bacteria have been isolated from feces , saliva , and dental plaque of some infected people.

Helicobacter pylori migrated out of Africa along with its human host circa 60, years ago. Using the genetic diversity data, researchers have created simulations that indicate the bacteria seem to have spread from East Africa around 58, years ago. Their results indicate modern humans were already infected by H.

At the time, the conventional thinking was that no bacterium could live in the acid environment of the human stomach. Before the research of Marshall and Warren, German scientists found spiral-shaped bacteria in the lining of the human stomach in , but they were unable to culture them, and the results were eventually forgotten. Among some rod-like bacteria, he also found bacteria with a characteristic spiral shape, which he called Vibrio rugula. He was the first to suggest a possible role of this organism in the pathogenesis of gastric diseases. His work was included in the Handbook of Gastric Diseases , but it had little impact, as it was written in Polish.

Interest in understanding the role of bacteria in stomach diseases was rekindled in the s, with the visualization of bacteria in the stomachs of people with gastric ulcers. After unsuccessful attempts at culturing the bacteria from the stomach, they finally succeeded in visualizing colonies in , when they unintentionally left their Petri dishes incubating for five days over the Easter weekend. In their original paper, Warren and Marshall contended that most stomach ulcers and gastritis were caused by bacterial infection and not by stress or spicy food , as had been assumed before.

Some skepticism was expressed initially, but within a few years multiple research groups had verified the association of H. He became ill with nausea and vomiting several days later. An endoscopy 10 days after inoculation revealed signs of gastritis and the presence of H. These results suggested H. Marshall and Warren went on to demonstrate antibiotics are effective in the treatment of many cases of gastritis. In , the Sydney gastroenterologist Thomas Borody invented the first triple therapy for the treatment of duodenal ulcers.

The bacterium was initially named Campylobacter pyloridis , then renamed C. Results from in vitro studies suggest that fatty acids , mainly polyunsaturated fatty acids, have a bactericidal effect against H. From Wikipedia, the free encyclopedia. Helicobacter pylori Synonym Campylobacter pylori Immunohistochemical staining of H. Helicobacter pylori eradication protocols. Timeline of peptic ulcer disease and Helicobacter pylori. An Illustrated Colour Text. Retrieved 25 April The Sydney Morning Herald. Retrieved 28 January Indigenous microbes and the ecology of human diseases" PDF.

Molecular Genetics and Cellular Biology. Archived from the original on 5 January Retrieved 7 August Cochrane Database of Systematic Reviews. Center for Disease Control.

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Retrieved 7 October Am J Clin Pathol. Retrieved 1 September National Center for Biotechnology Information. Evolution during disease progression". A new paradigm for bacterial carcinogenesis". Retrieved 25 August The Cochrane Database of Systematic Reviews. In Sutton, Philip; Mitchell, Hazel. Helicobacter Pylori in the 21st Century. Stop the killing of beneficial bacteria". Scientific American 1 June Retrieved 18 November A randomized controlled trial".

Nat Clin Pract Gastroenterol Hepatol. The American Journal of Clinical Nutrition. The establishment of a link between light therapy, vitamin D and human cathelicidin LL expression provides a completely different way for infection treatment. Instead of treating patients with traditional antibiotics, doctors may be able to use light or vitamin D [,].

Indeed using narrow-band UV B light, the level of vitamin D was increased in psoriasis patients psoriasis is a common autoimmune disease on skin []. In addition, other small molecules such as butyrate can induce LL expression []. These factors may induce the expression of a single peptide or multiple AMPs [].

It is also possible that certain factors can work together to induce AMP expression. Trichostatin and sodium butyrate increased the peptide expression in human NCI-H airway epithelial cells but not in the primary cultures of normal nasal epithelial cells []. However, the induction of the human LL expression may not be a general approach for bacterial clearance. During Salmonella enterica infection of human monocyte-derived macrophages, LL is neither induced nor required for bacterial clearance [].

Select human antimicrobial peptides and their proposed targets Table 4: World Journal of Gastroenterology Review. Helicobacter pylori and gastro-oesophageal reflux disease". Indigenous microbes and the ecology of human diseases". Best Pract Res Clin Gastroenterol. Implications for Gastric Carcinogenesis". Retrieved 30 August Archived from the original PDF on 30 September Retrieved 2 August Retrieved 21 December International Journal of Systematic Bacteriology.