Collecting the first sample before any antibiotic or antimicrobial therapy is initiated is necessary. [6], Severe obstructive or structural lung disease, Positive urine antigen test for pneumococcus, Positive urine antigen test for Legionella (special culture media for Legionella needed), Updated IDSA/ATS guidelines from 2019 state that, with regard to CAP, sputum culture is recommended not only for adult patients with severe disease but also for all adult inpatients who have received empirical treatment for methicillin-resistant S aureus and Pseudomonas aeruginosa. Often, erythromycin is prescribed to people who are allergic to penicillin. Understanding these relationships can help the clinical microbiology and infectious disease community better understand how to decipher diagnostic results when it comes to hospital-acquired pneumonia. It can cause bacterial infections ranging from mild (such as bronchitis) to severe (such as septic arthritis). Common contaminant from the upper respiratory tract (where this is a colonizing organism), but also a common cause of lower respiratory tract disease. %Tyk COMMENSAL FLORA in sputum | HealthTap Online Doctor An infants diet also has a substantial effect on the establishment of a healthy microbiota. The most studied population of normal flora in the microbes living in the intestines, often referred to as the gut microbiota. 1752 N St. NW . (E) Coinfection by RBP and NRF. Peptidoglycan is a polymer made from amino acids and sugars. Search for other works by this author on: Can an etiologic agent be identified in adults who are hospitalized for community-acquired pneumonia: results of a one-year study, Community-acquired pneumonia requiring hospitalization among U.S. adults, Aetiology of lower respiratory tract infection in adults in primary care: a prospective study in 11 European countries, Efficacy and safety of intravenous-to-oral lefamulin, a pleuromutilin antibiotic, for the treatment of community-acquired bacterial pneumonia: the Phase III Lefamulin Evaluation Against Pneumonia (LEAP 1) Trial, Etiology of community-acquired pneumonia: increased microbiological yield with new diagnostic methods, Improved detection of respiratory pathogens by use of high-quality sputum with TaqMan array card technology, Comprehensive molecular testing for respiratory pathogens in community-acquired pneumonia, Microscopic and baceriologic analysis of expectorated sputum, The diagnostic value of sputum culture in acute pneumonia, Pneumonia and acute febrile tracheobronchitis due to, Bacteriology of the lower respiratory tract as determined by fiber-optic bronchoscopy and transtracheal aspiration, Polysaccharide conjugate vaccine against pneumococcal pneumonia in adults, Integrated analysis of FOCUS 1 and FOCUS 2: randomized, doubled-blinded, multicenter phase 3 trials of the efficacy and safety of ceftaroline fosamil versus ceftriaxone in patients with community-acquired pneumonia, Diagnostic value of microscopic examination of Gram-stained sputum and sputum cultures in patients with bacteremic pneumococcal pneumonia, Validation of sputum Gram stain for treatment of community-acquired pneumonia and healthcare-associated pneumonia: a prospective observational study, Sputum gram stain assessment in community-acquired bacteremic pneumonia, Value of intensive diagnostic microbiological investigation in low- and high-risk patients with community-acquired pneumonia, Sputum Gram stain for bacterial pathogen diagnosis in community-acquired pneumonia: a systematic review and Bayesian meta-analysis of diagnostic accuracy and yield, Bacterial complications of respiratory tract viral illness: a comprehensive evaluation, Transtracheal aspiration in pulmonary infection, Diagnostic accuracy of transtracheal aspiration bacteriologic studies, Rothia bacteremia: a 10-year experience at Mayo Clinic, Rochester, Minnesota, Corynebacteria as a cause of pulmonary infection: a case series and literature review, Pneumonia among adults hospitalized with laboratory-confirmed seasonal influenza virus infection-United States, 20052008, Clinical significance of the infection-free interval in the management of acute bacterial exacerbations of chronic bronchitis, Acute bacterial exacerbations in bronchitis and asthma, Re-evaluation of the taxonomy of the Mitis group of the genus, Autopsy series of 68 cases dying before and during the 1918 influenza pandemic peak, The significance of mixed infections in pneumococci pneumonia, Comparison of Unyvero P55 pneumonia cartridge, in-house PCR and culture for the identification of respiratory pathogens and antibiotic resistance in bronchoalveolar lavage fluids in the critical care setting, Diagnosis and treatment of adults with community-acquired pneumonia. It is shifts in the proportions of these groups of microbes that are typically studied when investigating the role of normal flora on human health. aOthers include the following: Streptococcus sanguinis, Streptococcus parasanguinis, and Streptococcus salivarius; Corynebacterium propinquum and Corynebacterium pseudodiphtheriticum; Lactobacillus fermentarium; Actinomyces odontolyticus; Rothia mucilagenosa; Candida albicans and Candida glabrata. [QxMD MEDLINE Link]. Do not pool multiple samples in a 24-hr period. Blood cultures were positive in 6 (5.0%) cases, including 6 of 68 (8.8%) patients with pneumonia due to RBP and 0 of 31 (0%) due to NRF (P=.17). 2010. Review of Medical Microbiology and Immunology, 11e, Warren Levinson. Colonize the upper respiratory tract in children who have been in intensive care or have received frequent courses of antibiotics. A final reading of the sputum Gram stain was made by 2 observers without knowledge of the culture results, and agreement was reached by consensus. Before beginning collection, ask the client to rinse the mouth with plain water. In terms of predicting gram-negative bacilli, gram-negative cocci, and gram-positive cocci, sputum Gram stains had specificities of 0.87, 0.98, and 0.87, respectively. what does few normal respiratory flora mean - vivelive.ai i have cvid and interstitial lung disease. Legal. The importance of the normal bacterial flora (a.k.a. Shift in flora suggestive of bacterial vaginosis. Understanding that a single organism may be either normal microbiota or a pathogen encourages the microbiologist and clinician to consider other key factors when making a VAP diagnosis such as which organisms constitute normal respiratory flora and what makes some members of the respiratory microbiota more pathogenic than others. Pediatr Neonatol. It has been known for decades that animals raised without normal flora display a variety of health effects across many body systems. Youll be monitored until youre fully awake. There are many other groups of microbes found in the intestines, including fungi such as Candida. Get prescriptions or refills through a video chat, if the doctor feels the prescriptions are medically appropriate. is it only in rare cases? [1, 2, 3, 4, 5]. Respiratory Culture, Aerobic | MLabs - University of Michigan Throat Culture: Reference Range, Interpretation, Collection - Medscape Studies utilizing molecular techniques with high-quality sputum samples have identified a causative organism in a much higher proportion of cases [6, 7]; the reliance on high-quality sputum helps, in part, to explain the discrepancy, but, even with this technology, no pathogen has been identified in up to 13% of cases [6, 7]. Delmars Guide to Laboratory and Diagnostic Tests. It helps by replenishing the bodys fluid levels and preventing dehydration. Correlation of nasopharyngeal cultures with results of tympanocentesis culture is poor and lacks predictive value in identification of the causative agent of otitis media. Yang K, Kruse RL, Lin WV, Musher DM. A sputum Grams stain is a laboratory test that allows your doctor to diagnose a bacterial infection in your respiratory tract. Categorical values were compared using Fishers exact test. For example, little to no growth might indicate something odd going on if you haven't been taking antibiotics. Metlay JP, Waterer G, Long AC, et al. The infection is spread from person to person through coughing or sneezing. As these secretions pool in the oropharynx, bacteria that live in the respiratory tract can begin to accumulate along the endotracheal tube. Gram positive bacteria. Accessibility StatementFor more information contact us atinfo@libretexts.org. Gram-positive bacterial cell envelopes: The impact on the activity of antimicrobial peptides. Polymerase chain reaction on a nasopharyngeal swab was positive for influenza A virus. It assists in the diagnosis of respiratory infections, as indicated by the presence or absence of organisms in culture. Diagnostic performance of the Sputum Gram Stain in predicting sputum culture results for critically ill pediatric patients with pneumonia. In fact, pneumonia is the second most common nosocomial infection affecting critically ill patients in the ICU. Colonization may be followed by microaspiration of bacteria into the lower airways, a regularly occurring event even in healthy adults [8]. Collect your sample first thing in the morning, before eating or drinking anything. Inspired by Rubik's Cube, Scientists Create a Shape-Shifting Antibiotic to Fight Disease, About the Symptoms of Anaplasmosis, a Serious Tick-Borne Illness, Anaplasmosis: Symptoms, Treatment, Prevention, and More, CDC Investigates if Romaine Lettuce is Source of E.coli Outbreak, thin peptidoglycan layer (2 to 3 nanometers), skin infections, like cellulitis and folliculitis, uncomplicated urinary tract infections (most common), itchy bump that turns into a sore with black center. One frequently cited statistic is that there are 10-100 times more bacterial than human cells in the body. Vazquez-Guillamet C, et al. What is most common diseases or disorders of the respiratory system? Recognized bacterial pathogens were identified by standard microbiologic techniques. This happens because the cells dont completely separate after they divide. An acceptable specimen has more than 25 leukocytes and fewer than 10 epithelial cells per low power field. Fine, beaded Gram-positive filamentous bacteria did not grow in aerobic cultures. Patients are at most at risk of developing ventilator-associated pneumonia (VAP) in the first 48 hours after an endotracheal tube has been placed. The following organisms are the most prevalent. If the test results from your sputum Grams stain are abnormal, it means that bacteria and white blood cells have been detected. (B) Pneumonia due to Corynebacterium pseudodiphtheriticum. Is respiratory allergy one of the many reasons that can cause mild chest discomfort? (C) Staphylococcal pneumonia. You can learn more about how we ensure our content is accurate and current by reading our. Sheng ZM, Chertow DS, Ambroggio X, et al. Ask your doctor if you should do anything to prepare for your bronchoscopy. Symptoms include diarrhea and abdominal cramps that last for less than 24 hours. normal respiratory flora include neisseria catarrhalis, candida albicans, diphtheroids, alpha-hemolytic streptococci, and some staphylococci. After adding the staining agent, the laboratory technician will examine the slide under a microscope. Many respiratory pathogens live normally in the host without causing disease. Listeria and Corynebacterium species dont make spores. Kilian M, Riley DR, Jensen A, et al. The American Society for Microbiology This test can determine if you have TB or another infection. If specimen is . Each area of the human body contains a characteristic population of microbes (Figure \(\PageIndex{1}\)), although the exact composition of each persons flora is unique. The American Society for Microbiology, Growth of these organisms from a culture of the oropharynx/nasopharynx is of no significance. Periodontal bacterial species in hopeless dentitions with severe periodontitis: comparison of levels before extraction and 90 days after immediate implant placement. The fungal genus Candida is also common in the mouth and upper respiratory tract. It is also known as phlegm and, because of its thickness, can contain infectious germs. There is some evidence that children who are not exposed to a variety of microbes early in life or frequently take antibiotics display the effects of an altered microbiome later on such as allergies, metabolic disorders and obesity, and possibly even certain mental disorders. Streptococcus bacteria grow in chains. The Gram stain test can help doctors diagnose an illness. Respiratory Viruses in 120 Cases of Community-Acquired Pneumonia. One or more RBPs were identified in sputum from 68 of 120 (56.7%) patients (Table 1); representative Gram stains and quantitative bacteriologic results are shown in Figure 1. A child who develops a viral upper respiratory tract infection while colonized may develop acute otitis media or sinusitis. In total (Table 4), RBPs caused CAP in 68 (56.7%) of 120 patients; 14 (20.6%) were coinfected with a respiratory virus. Daniela Hermelin, MD is a member of the following medical societies: AABB, American Society for Apheresis, American Society for Clinical Pathology, College of American Pathologists, Heart of America Association of Blood Banks (HAABB), International Society of Blood TransfusionDisclosure: Nothing to disclose. Educational text answers on HealthTap are not intended for individual diagnosis, treatment or prescription. Normal respiratory microbiota can play a key role in human health, but can also play a part in severe respiratory disease. The relationships between humans and bacteria are immensely complex. Sputum, also known as phlegm, is a thick type of mucus made in your lungs. However, absent such a Gram stain, our findings support recommendations by the guidelines for empiric antibiotics for patients hospitalized for CAP even if a viral PCR is a positive because fully 60% of our patients with a positive viral PCR had bacterial coinfection. Nearly one-third of adults are colonized with Staphylococcus aureus in their respiratory tracts. How should I interpret the growth of "normal respiratory flora" from Am J Respir Crit Care Med. Connect with a U.S. board-certified doctor by text or video anytime, anywhere. Sizar O, et al. Learn how we can help 5.4k views Reviewed >2 years ago Thank Dr. Ryan Stanton agrees 1 thank Bacillus bacteria need oxygen to survive (aerobic), while Clostridia bacteria dont (anaerobic). Depending on how anthrax is spread, it can cause a variety of symptoms. 2 doctor answers 4 doctors weighed in Share The novel finding in this study is that bacteria that are generally reported as NRF appears to play a causative role in 25.8% of cases of CAP. Cases in which Gram stain results did not match culture results were ones in which relatively small numbers of RBPs and large numbers of NRF were detected, so it was easy to overlook the RBPs. The test can also help the laboratory technician detect the presence of fungi in your sputum. Ear: Normal flora of the skin of the healthy ear includes Staphylococcus epidermidis, Corynebacterium sp, and Staphylococcus aureus. Brush your teeth and rinse your mouth. (2019). (5) The median number of NRF per milliliter sputum in CAP patients (7106 per mL) was strikingly similar to that observed in patients with pneumonia due to RBP (8106). Gram-negative bacteria stain pink-red. You might feel slightly light-headed when you cough deeply, or feel discomfort in your lungs or throat. More recent calculations, however, result in a ratio closer to 1:1, with an estimated 1013 human cells and 1013 1015 bacterial cells. What does mixed flora, and many wbc's and few epithelial cells mean in a sputum culture? Bacterial coinfection was present in 24 of 40 (60%) cases with viral detection: 14 cases with RBP and 10 with NRF. Median colony-forming units per milliliter for S pneumoniae, H influenzae, M catarrhalis, and S aureus were 2106, 4106, 7107, and 3106, respectively, and, after final review, Gram stain results were consistent with quantitative bacterial cultures in all but 4 of 68 (5.9%) cases. Clostridia are usually involved with foodborne illnesses, but the most concerning bacteria include: The spores of C. botulinum produce the botulinum toxin, the most dangerous toxin to humans. The CCI was significantly greater in patients with NRF pneumonia, consistent with the concept that these individuals were more susceptible to pneumonia caused by less virulent bacteria, and 32.3% of patients with NRF pneumonia had viral coinfection compared with 14.7% in patients with RBPs, suggesting that a second insult may be necessary to allow NRF to cause pneumonia. A nurse will help you cough up sputum. Using the Charlson comorbidity index (CCI), we sought to determine whether patients with pneumonia due to NRF were more likely than those with RBP to be susceptible to pneumonia due to the presence of comorbid conditions. Organisms that normally live within the respiratory tract may end up being the same organisms that cause pneumonia in these patients. Privacy Policy sets forth the information we collect about you, how we use Moist areas, such as axilla (armpits) and groin, tend to have more (and different) bacterial growth compared to drier areas. In a medical setting, a doctor can send a sample of your blood, urine, or tissue to a lab for Gram stain testing. That said, in patients with confirmed VAP, P. aeruginosa is the most common bacterial cause. Normal Respiratory Microbiota in Health and Disease, 2023. In 79 of 120 (65.8%) cases, antibiotics had been given for 2 hours. Streptococcus mitis shares molecular characteristics of S pneumoniae, including the capacity to make capsule, and ample evidence shows their capacity to cause serious infection in humans [25, 32, 33]. Sputum Culture: Reference Range, Interpretation, Collection - Medscape Gram stain testing is a method for classifying bacteria based on their cell wall. Etiologic Role of Normal Respiratory Flora in 120 Cases of Community-Acquired Pneumonia. They will give you a sterile sample cup to use. These criteria were used to stratify pneumonia into 6 etiologic groups: pneumonia due to (1) RBPs; (2) respiratory viruses; (3) coinfection by RBPs and a respiratory virus; (4) NRF; (5) coinfection by NRF and a respiratory virus; and (6) cause undetermined. In normal healthy individual LRT is sterile. However, their presence in such small numbers relative to other bacteria might then raise serious question about their relevance. In the area of health and medicine, flora is the term used to describe the microorganisms that exist on or within the . Approximately 25% of children between 3 months and 4 years of age are colonized, and 5-10%% of older and younger people. Learn what its used for and what to expect. aureus is most often found in the nose of those individuals who carry it in their normal flora. Pneumonia caused by potential pathogens such as as Streptococcus mitis and Streptococcus anginosus group that may be part of the NRF. This will probably be enough to treat your infection if you have a healthy immune system. Keep coughing up sputum until the cup is filled to the marker, which should equal approximately 1 teaspoon. Are organisms present simply colonizing the endotracheal tube and surrounding airway without causing harm, or are they the cause of infection? If an infected tick bites you, you could experience symptoms within a couple of weeks. [7]. (2014). Gram stain (left) shows overwhelmingly predominant small Gram-negative coccobacilli. Ventilator-Associated Pneumonia and The Role of Normal Respiratory Flora Patients are at most at risk of developing ventilator-associated pneumonia (VAP) in the first 48 hours after an endotracheal tube has been placed. Best to see an allergist to determine the cause and to help you prevent complications e.g. Published by Oxford University Press on behalf of Infectious Diseases Society of America. x=]sS5O))cA\5;L*{-6oeI+Q I(j@nZ?mjT'_n>owmWzl6Ul7?K~{0f2K2/K4O3._e#, ]rmnM(T! A doctor typically orders a sputum stain to determine if a person has tuberculosis (TB) or another type of mycobacterial infection. If you have trouble, they may give you a breathing treatment to help loosen the sputum in your airways. Culture of the sputum on blood agar frequently reveals characteristic colonies, and identification is made by various serologic or biochemical tests. The following factors show that this is not the case and support the validity of our results. Determining the cause of your symptoms can help your doctor prescribe an appropriate treatment plan. Staphylococcus aureus (Figure 1C) and Moraxella catarrhalis were detected alone or as coinfecting bacterial agents in 11 and 7 cases, respectively. The World Health Organization (WHO) estimates that this organism is responsible for killing half a million children worldwide each year. Typically, gram-negative organisms have the following the traits: The major difference is the outer lipid membrane. for >20% of VAP cases, 50% of which are caused by MRSA. Bacterial counts exceeded 106 cfu/mL in 65 of 68 cases of pneumonia attributed to RBPs. Pneumonia caused by pathogens that do not grow on standard sputum culture media (eg, atypical organisms, viruses, anaerobes). (2013). Organisms that are generally identified only as "normal respiratory flora" but met quantitative criteria (as defined below) were further studied by matrix-assisted laser desorption ionization time-of-flight (MALDI-TOF). White blood cells per milliliter in liquefied sputum were counted in a hemocytometer. All rights reserved. It is important to understand how some of the most common causes of pneumonia transition from colonizers to opportunistic pathogens. These data imply that, in at least some cases, isolation of Gram-negative rods from sputum of untreated patients may be a normal finding, and that in some patients with pulmonary infection, the pretreatment, upper respiratory tract flora may serve as the source of subsequent superinfection with Gram-negative rods. The placement of the tube disrupts the normal anatomy of the respiratory tract, and prevents the patient from swallowing, coughing or clearing mucus and other secretions normally. As spore-forming bacteria, bacilli make spores that release toxins. More importantly, for purposes of treatment, 24 (60%) of all patients with a positive PCR for a respiratory virus had evidence for bacterial coinfection, whether by RBP or NRF. Our website services, content, and products are for informational purposes only. Lack of normal flora also makes animals more susceptible to infection with a variety of pathogens, particularly those that infect the GI tract. Haemophilus Influenzae: Symptoms, Causes & Treatment - Cleveland Clinic C. difficile causes: C. tetani spores produce the tetanus toxin, a neurotoxic substance. Despite absence of detectable bacteria, sputum is purulent (left, shown in collection cup) and contained 3107 white blood cells per mL. Although only a minority of pneumonia patients produce such a sputum in timely fashion, the sensitivity and specificity of Gram stain and culture of such specimens for RBP have previously been shown to be quite good [1721]. Johansson N, Kalin M, Tiveljung-Lindell A, et al. Microbes that colonize the human body during birth or shortly thereafter, remaining throughout life, are referred to as normal flora [1-2]. The night before you provide a sample, try to drink lots of fluids like water or tea. If you cant cough up enough sputum, try breathing steam in from boiling water, or take a hot steamy shower. Sometimes, severe cases of pneumonia can lead to: Early diagnosis can help your doctor prescribe a treatment plan, which may help improve your outlook. By limiting this study to patients who could provide a high-quality sputum specimen at, or shortly after admission, we found that (1) a causative organism could be identified in >95% of patients hospitalized for CAP, (2) bacteria, whether RBP or NRF, played a causative role in 82.5% of cases, and (3) when PCR demonstrates a respiratory virus, 35% of patients have bacterial coinfection due to RBP and another 25% to NRF. If a human eats contaminated meat, they can get food poisoning. 2nd edition. By using our website, you consent to our use of cookies. Most illnesses require antibiotics that destroy or slow down the bacteria. Additionally, its used in combination with other treatments. Each of these physiological effects can be linked directly to chemical communication within the microbiota and between the microbiota and human. bOverall comparison, P=.01; bacterial pathogen vs normal respiratory flora (NRF), P=.06; all bacterial vs viral, P=.01 (Kruskal-Wallis). The difficulty in diagnosing the cause of VAP comes from the fact that many of these organisms have the potential to cause disease. Learn. Its found in the cell walls of bacteria, and helps laboratory staff learn if bacteria are present in your sputum. Most people recover from, Boils can occur almost anywhere on your body, even in your butt crack. We are unaware of any previous study that has systematically sought a role for NRF in CAP. Depending on your test results, your doctor may prescribe a treatment plan or order more tests. These results support the hypothesis that, just as aspiration of RBPs cause pneumonia after colonization of the nasopharynx, in some proportion of cases, aspiration NRF that colonize the nasopharynx may do the same. DOI: Namvar AE, et al. Polymerase chain reaction identified a respiratory virus in 40 of 120 (33.3%). Take a couple of long, deep breaths. See additional information. There tends to be more bacteria present at this time and can help ensure accurate test results. Gram stain shows many small Gram-negative coccobacilli and Gram-positive cocci, many of which were cell-associated. The intensity of the inflammatory response in the lungs, as measured by median WBC per milliliter in liquefied sputum, was slightly greater in pneumonia due to recognized pathogens than pneumonia due to NRF (1.7107 vs 1.0107 per mL, P=.04), and far greater when all bacterial pneumonias were compared with viral pneumonias (1.5107 vs 3.2106, P=.01). In some cases, treatment might include fluid therapy. Heres why knowing whether. It is interesting to note that occasional polymorphonuclear leukocytes (PMN) are laden with intracellular streptococci. DOI: Gillespie S, et al. these two account for a very large percentage of what we see in pulmonary medicine. Because we were studying patients who were acutely infected, we focused on organisms that could be identified by culture and did not address the lung microbiome [38], although NRF are clearly an important component of that biome and the microbiome is a likely determinant of what organisms emerge to cause bacterial pneumonia. (2014). Gram stain (right) is typical of the findings in viral pneumonia, showing many PMN and no bacteria. Gram positive vs. gram negative. Viruses (e.g. The cecum tends to be enlarged and other GI abnormalities appear. Gram-positive bacteria are bacteria with thick cell walls. gram negative rods not so common and that seems a large amt. Majd Ibrahim, MD Chief Medical Resident, Department of Internal Medicine, University of Illinois College of Medicine at Peoria You will probably stay awake for it. Daniela Hermelin, MD Assistant Professor of Pathology, St Louis University School of Medicine; Associate Director of Transfusion Medicine, Director of Clinical Apheresis, St Louis University Hospital 1r`HpQ 8 y/#+-pDmqvOWsZc-|p.Vu=>exBQ'&M,?~L+TE {nZkP'Dowmskhwo1"K>x (1) Using semiquantitative methods, Chodosh [29, 30] reported that, during infection-free intervals, Gram-stained sputum from patients with chronic bronchitis contained very few bacteria. Sputum is a mixture of saliva and mucus that you cough up from your respiratory tract. The cellular contribution of microbes to the human body, however, is small compared to the genetic contribution. One frequently cited statistic is that there are 10-100 times more bacterial than human cells in the body. This loosens the secretions enough to expectorate. The Grams stain doesnt allow them to identify every specific type of bacteria, but it can help them tell if there are bacteria with thick cell walls or thin cell walls. Obtaining an early-morning expectorated specimen is most desirable. Ramanan P, Barreto JN, Osmon DR, Tosh PK. In a Gram stain test, these organisms yield a positive result. Sterility is important for culture results. These studies have all reported coinfections only with RBPs. Mosbys Manual of Diagnostic and Laboratory Tests. In 21 (17.5%) cases, the viral PCR was negative and no RBP were recognized; in these cases, the cause was attributed solely to NRF.
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