Acute Bronchitis

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Continuing Education Activity

Acute bronchitis, characterized by inflammation in the bronchi lining, is a frequent condition in emergency departments, urgent care centers, and primary care offices. Acute bronchitis ranks among the top 10 most common outpatient illnesses in the United States, affecting approximately 5% of adults annually. This activity discusses the evaluation and management of patients afflicted by acute bronchitis, accentuating the pivotal role played by the interprofessional healthcare team in delivering comprehensive care for these individuals. This activity provides healthcare professionals with the latest insights and evidence-based approaches to enhance their competence in diagnosing and managing acute bronchitis, ultimately improving patient outcomes and healthcare team performance.

Objectives:

  • Apply the key clinical features of acute bronchitis for an accurate diagnosis to distinguish it from other respiratory conditions and differentiate between viral and bacterial causes.

  • Assess patients presenting with acute bronchitis for underlying risk factors, such as chronic obstructive pulmonary disease (COPD), asthma, or immunosuppression, to develop appropriate management plans.

  • Implement evidence-based guidelines and treatment options for acute bronchitis, emphasizing nonpharmacological and pharmacological interventions as needed.

  • Collaborate with the interprofessional team to collectively provide evidence-based education on acute bronchitis, treatment expectations, and preventive measures.

Introduction

Acute bronchitis, a prevalent respiratory infection, is a significant medical concern, particularly among adult patients. This condition involves the lower respiratory tract, specifically targeting the bronchi, the prominent air passages responsible for air transport within the lungs. Acute bronchitis manifests as an inflammation of these bronchi without evidence of pneumonia and typically affects individuals without underlying chronic obstructive pulmonary disease (COPD).

Acute bronchitis is characterized by an acute onset of a persistent cough, with or without sputum production. As a self-limiting condition, it typically follows a benign course, resolving spontaneously over 1 to 3 weeks. The etiology of these symptoms arises from the inflammatory response within the lower respiratory tract, often triggered by viral infections.[1][2][3] 

Etiology

Acute bronchitis presents as a clinical syndrome characterized by a transient and self-limiting inflammation, specifically targeting the larger and mid-sized airways, and devoid of any evidence of pneumonia upon chest radiography examination.

This condition primarily impacts the bronchial tree, leading to irritation, inflammation, and increased mucus production. Viral infections, such as the common cold or influenza viruses, adenovirus, and rhinovirus, are frequent instigators, although exposure to irritants or other respiratory pathogens can also be putative triggers.[4] These viruses are transmitted through respiratory droplets and induce inflammation and irritation within the bronchial tree, ultimately leading to the characteristic symptoms of acute bronchitis, which encompass coughing, sputum production, and respiratory discomfort. 

Bacterial pathogens play a role in approximately 10% or less of acute bronchitis instances. Among these bacterial pathogens, Mycoplasma pneumoniae, Chlamydia pneumoniae, and Bordetella pertussis are the most commonly identified offenders.[5] In contrast, the majority, approximately 90% to 95%, of cases in healthy adults are attributed to viral infections. Additional factors, including allergens, irritants, and occasionally bacterial pathogens, can also incite acute bronchitis.[6]

A higher prevalence of influenza viruses A and B are seen in the winter months, escalating transmission and infection rates. These viruses exhibit ease in spreading within crowded indoor settings like schools, workplaces, and public gatherings, where close interpersonal contact facilitates their transmission through respiratory droplets. Influenza viruses' efficiency in infecting and replicating within the respiratory tract allows for rapid viral multiplication, culminating in significant damage to the bronchiolar epithelial cells. This damage, coupled with the body's immune response, contributes to the distinctive symptoms of acute bronchitis.[7][8] 

While viral infections are more prevalent during the winter season, acute bronchitis can arise at any time of the year, often linked to strains of adenovirus, rhinovirus, and coronavirus.[9][10] Furthermore, understanding the dynamics of viral infections causing acute bronchitis throughout the year is essential for healthcare providers and public health officials in implementing effective prevention and control strategies, especially in the context of evolving respiratory viruses and changing environmental factors. Examples of this are as follows:

  • Influenza, RSV, and human coronaviruses typically exhibit peak incidence during winter. As stated previously, this seasonal pattern arises as people tend to spend more time indoors and engage in close interpersonal contact, creating an environment conducive to the rapid transmission of these viruses.

  • Rhinoviruses typically experience peaks in incidence during the spring and fall seasons, coinciding with shifts in weather patterns. Seasonal allergies may also contribute to these peaks by potentially facilitating the transmission of the virus during these times.

  • Enteroviruses, a group encompassing several viruses responsible for respiratory and gastrointestinal illnesses, peak in summer. This case surge aligns with increased outdoor activities, providing more significant opportunities for viral transmission. 

Vaccination status, particularly against viruses like influenza, can influence the etiology of acute bronchitis. A study conducted in France revealed that among 164 cases of acute bronchitis in adults who have received influenza vaccination, 37% were found to have a viral origin. Within the identified viral causes, 21% of cases were attributed to rhinovirus. This underscores that despite being vaccinated against influenza, individuals may remain susceptible to rhinovirus infections, which can manifest as bronchitis symptoms.[11] 

Exposure to irritants such as smoke, contaminated air, dust, and other environmental pollutants can also cause acute bronchitis or exacerbate preexisting respiratory conditions. Furthermore, allergens can trigger an allergic response within the airways, ultimately culminating in inflammation and the onset of bronchitis symptoms, particularly in individuals who are susceptible to such triggers.[12]

Epidemiology

Acute bronchitis represents a common clinical presentation across various healthcare settings. In the United States, approximately 5% of individuals annually report physician-diagnosed cases of acute bronchitis. The numbers tend to peak during winter, aligning with the seasonal prevalence of respiratory viral infections like influenza and RSV, which often coincide with flu season.[13][14] 

Similarly, a study conducted in the United Kingdom reported similar rates of acute bronchitis, with an incidence of 54 cases per 1000 persons. Notably, these rates exhibit variability among different age groups, with lower rates among younger men (36 per 1000) and higher rates in individuals older than 85 (225 per 1000).[8] These discrepancies in incidence may be attributed to variations in healthcare-seeking behavior, age-related immune responses, and exposure to viral pathogens in different settings.

In addition, several risk factors contribute to the development of acute bronchitis, including a history of smoking, residence in polluted areas, crowded living conditions, and a prior history of asthma. Specific allergens such as pollen, perfume, and vapors can potentially trigger acute bronchitis in susceptible individuals.

In instances where the infection is of bacterial origin, the isolated pathogens tend to overlap with those commonly associated with community-acquired pneumonia. Examples of such pathogens are Streptococcus pneumonia and Staphylococcus aureus.[15][16]

Pathophysiology

Acute bronchitis is inflammation affecting the large and mid-sized airways (bronchi), frequently precipitated by viral infections. The wide array of anatomical sites within the respiratory tract where these pathogens can take hold underscores the diverse impact of these microorganisms on the respiratory tract. A study involving volunteers exposed to rhinovirus infections demonstrated the various locations within the respiratory system where the virus could be detected.[9] 

The inflammatory process triggers increased blood flow and cellular activity within the affected bronchi, resulting in heightened 18F-fluorodeoxyglucose (FDG) uptake when observed via positron-emission tomography (PET) scan.[17] Additionally, bronchial inflammation can stem from various triggers, with viral infections, allergens, and pollutants among the most common culprits. The inflammation of the bronchial wall leads to mucosal thickening, epithelial cell desquamation, and denudation of the basement membrane. In some instances, a viral upper respiratory infection can progress to a lower respiratory tract infection, resulting in acute bronchitis.[18]

History and Physical

Patients affected with acute bronchitis typically exhibit a range of symptoms, including a productive cough, feelings of malaise, breathing difficulties, and wheezing. Often, the most prominent complaint is the persistent cough, with an accompanying clear or yellowish sputum production. However, on occasion, the sputum can take on a purulent appearance. Purulent sputum does not necessarily correlate with a bacterial infection or necessitate antibiotic treatment.[19] 

Following an episode of acute bronchitis, the cough typically persists for 10 to 20 days, with a median duration of 18 days.[20] Occasionally, bronchitis cough may extend beyond 4 weeks. Paroxysms of cough accompanied by an inspiratory whoop or posttussive emesis should raise concerns for pertussis infection. 

In the early stages of infection, the symptoms of mild upper respiratory infections and acute bronchitis can often overlap, creating a challenge in distinguishing between both based solely on symptoms. Both conditions may present with common respiratory symptoms such as:

  • Cough: Initially, the cough may start as dry and irritating, but as acute bronchitis advances, it can transition to producing sputum. In acute bronchitis, this cough tends to persist for longer, often extending beyond 5 days. Approximately 50% of patients with acute bronchitis report the production of purulent sputum.[21] Prolonged or forceful coughing may lead to chest wall or substernal musculoskeletal pain, usually self-limiting. 

  • Mild fever: A low-grade fever may be present in both conditions, although it is more frequently associated with upper respiratory infections. The presence of high-grade fevers in the setting of acute bronchitis is unusual and warrants further diagnostic evaluation. 

  • Fatigue and body aches: Mild upper respiratory infections and acute bronchitis can cause fatigue and general bodily discomfort.

The differentiation between these 2 conditions becomes more apparent as the infection develops. If the symptoms predominantly affect the upper respiratory tract and resolve within a few days, it is more likely to be a mild upper respiratory infection. Conversely, if the symptoms persist for a week or longer and are accompanied by lower respiratory tract symptoms, this presentation indicates acute bronchitis.

During a physical examination, lung auscultation may reveal the presence of wheezing. In some instances, the detection of rhonchi may improve or clear with coughing, suggesting that the airway secretions or obstruction causing the sound can be alleviated through coughing efforts.

Pneumonia should be considered a potential diagnosis when detecting rales or egophony. Mild tachycardia may accompany these findings, indicating fever and dehydration secondary to the viral illness. It is important to note that similar signs of tachycardia can also be observed in bacterial infections. In general, the evaluation of the rest of the body systems typically falls within normal limits.

Evaluation

Acute bronchitis is typically diagnosed clinically, relying on a comprehensive assessment encompassing a medical history, pulmonary examination, and other pertinent physical findings. The evaluation of oxygen saturation, along with the assessment of pulse rate, temperature, and respiratory rate, serves as a pivotal indicator for gauging the severity of the condition. In cases where vital signs fall within normal ranges and no physical examination findings suggest pneumonia, further diagnostic investigations are generally unnecessary. However, an exception to this rule applies to older patients (>75 years) or individuals with neurocognitive impairment. In such instances, a more extensive workup should be considered part of the evaluation process.

Chest x-ray (CXR) findings in cases of acute bronchitis are generally nonspecific and often appear normal. The CXR findings may occasionally reveal increased interstitial markings indicative of bronchial wall thickening. A CXR proves particularly valuable in distinguishing pneumonia from acute bronchitis when infiltrates are present. Evidence-based guidelines established by the American College of Chest Physicians (ACCP) recommend obtaining a CXR where specific criteria are met, including the following:[14]

  • Heart rate exceeding 100 bpm
  • Respiratory rate greater than 24 breaths/min
  • Oral body temperature surpassing 38 °C
  • Chest examination findings of egophony or fremitus 

Laboratory testing, including a complete blood count and chemistry panel, may be conducted as part of the diagnostic workup for fever. The white blood count might show a mild elevation in some cases of acute bronchitis.

Rapid microbiological testing for respiratory infections may not always be cost-effective or essential in every situation. Nevertheless, specific scenarios exist in which testing can be beneficial and potentially result in alterations to the treatment approach. Some of these circumstances include:

  • Influenza season: During the influenza season, rapid testing for influenza may be recommended in specific patient populations. This population includes individuals at a heightened risk of complications, such as older individuals, young children, pregnant women, and individuals with chronic medical conditions. Healthcare workers who develop respiratory symptoms may also benefit from rapid testing to determine the presence of influenza and assess the appropriateness of the antiviral treatment.

  • Viral pandemics: In the context of viral pandemics, such as the COVID-19 pandemic, rapid testing becomes essential for diagnosing and managing the infection. Swift identification of cases is imperative for promptly implementing appropriate infection control measures, timely administration of treatment, and prevention of further viral transmission.

  • High suspicion of pertussis or bacterial infections: When a strong clinical suspicion of pertussis (whooping cough) or other bacterial respiratory infections arises, rapid testing proves valuable in confirming the diagnosis. Such testing can serve as a guide for initiating antibiotic treatment, thereby aiding in the containment of further transmission.

Multiplex polymerase-chain-reaction (PCR) testing of nasopharyngeal swabs or aspirates is a diagnostic tool that allows for the simultaneous detection of multiple pathogens in a single test. This method helps diagnose infections attributed to specific bacteria, such as B pertussis (the causative agent of whooping cough), pneumoniae, or C pneumonia.[22] 

The advantage of multiplex PCR testing lies in its ability to rapidly and accurately identify the presence of these bacterial pathogens in respiratory samples, facilitating the differentiation of various causes of respiratory infections. By detecting the target bacteria's genetic material (DNA or RNA), PCR testing provides a sensitive and specific diagnosis, especially when compared to traditional culture methods, which may have sensitivity and turnaround time limitations. However, it remains essential to ensure this testing approach is adequately validated and employed within a comprehensive clinical assessment context. This approach provides an accurate interpretation of results and supports sound decision-making regarding patient management. Gram stain and bacterial sputum cultures are typically discouraged in acute bronchitis cases, as bacteria seldom serve as the causative agent. 

Assessing procalcitonin levels can be a valuable tool in determining whether antibiotics should be prescribed when the diagnosis of acute bronchitis is uncertain. A meta-analysis has shown that procalcitonin-guided antibiotic therapy reduced antibiotic exposure and improved overall survival.[23]

Spirometry, when performed, reveals transient bronchial hyperresponsiveness in approximately 40% of patients with diagnosed acute bronchitis. A reported 17% of these patients exhibit reversibility of FEV1 (forced expiratory volume in 1 second) greater than 15%.[14] Airflow obstruction and bronchial hyperresponsiveness typically resolve within 6 weeks.[24]

Treatment / Management

Acute bronchitis is typically a self-limiting condition, and its treatment primarily revolves around providing symptomatic and supportive therapy. For alleviating cough, both nonpharmacological and pharmacological approaches can be considered. Nonpharmacological strategies include remedies such as hot tea, honey, ginger, and throat lozenges. Notably, the efficacy of these interventions has not been evaluated through clinical trials. 

In clinical practice, antitussive agents like dextromethorphan (with or without codeine) are often used to suppress cough based on their effectiveness in managing chronic bronchitis symptoms and data from studies on cough associated with the common cold. No randomized trials specifically assess the efficacy in antitussive agents in acute bronchitis. Codeine usage should be avoided due to its addictive potential.

The available data regarding the use of mucolytic agents in acute bronchitis treatment are conflicting and lack a clear consensus on efficacy. Therefore, these agents' role in managing acute bronchitis remains a subject of ongoing investigation and debate.

Beta-agonists are commonly administered to patients with acute bronchitis who exhibit wheezing. However, the findings from small randomized control trials investigating the use of beta-agonists for cough in acute bronchitis have yielded mixed results. In a Cochrane review encompassing 5 trials, no substantial benefit of beta-agonists on daily cough was observed, except for a minor advantage in a subgroup of patients with wheezing and airflow obstruction at baseline.[25] A more recent Cochrane review reported similar outcomes.[26] 

Analgesic and antipyretic agents may manage associated symptoms like malaise, myalgia, and fever. Additionally, prednisone or other steroids may be administered to address inflammation. While the evidence supporting their benefit in acute bronchitis is limited, they can be useful in patients with underlying chronic obstructive pulmonary disease (COPD) or asthma. Typically, steroids are utilized as a short-term burst therapy. In certain cases, an extended tapering course of steroids may be warranted, especially for patients with underlying asthma or COPD.[27][28]

ACCP guidelines recommend against antibiotic use in cases of uncomplicated acute bronchitis among otherwise healthy adults. A comprehensive Cochrane review of 9 randomized, controlled trials of antibiotic agents found only a minor reduction in the total duration of cough (0.6 days) with no significant decrease in the overall duration of illness.[29]

Consequently, antibiotic use should be avoided in uncomplicated cases of acute bronchitis, considering factors such as the cost of antibiotics, the increasing global concern of antibiotic resistance, and the potential side effects associated with antibiotic usage. Numerous other international medical societies also advise against antibiotic use in cases of viral acute bronchitis. Despite these recommendations, many patients diagnosed with acute bronchitis are prescribed antibiotics.

It is important to emphasize that no empirical data justify the belief that antibiotic therapy leads to less severe or shorter duration of cough in acute bronchitis. Antimicrobial therapy is recommended only when a treatable pathogen is identified, as with pertussis (see Table. Pathogens and Treatments Related to Acute Bronchitis). Antiviral treatment should be considered for influenza infection. 

Table. Pathogens and Treatments Related to Acute Bronchitis

Pathogen Treatment 

Adenovirus

  • Supportive therapy.
  • Antitussives like guaifenesin and dextromethorphan
  • Analgesics such as acetaminophen or nonsteroidal anti-inflammatory drugs (NSAIDs)

Coronavirus

  • Supportive therapy
  • Antivirals such as Nirmatrelvir/Ritonavir may be used for patients with mild-to-moderate COVID-19 who are at high risk of progressing to severe disease.[30] Additional COVID-19 treatment options are discussed separately.[31]
 

Influenza virus

  • Supportive therapy
  • Antiviral therapy*: Neuraminidase inhibitors such as oseltamivir 75 mg twice daily for 5 days [32] or inhaled zanamivir 2 puffs (5 mg/puff) twice daily for 5 days, for a total daily dose of 20 mg [33]
 Parainfluenzavirus
  •  Supportive therapy only 
Respiratory syncytial virus
  •  Supportive therapy only 
Rhinovirus 
  • Supportive therapy only
Bordetella pertussis 

First-line therapy: Macrolides

  • Azithromycin: 500 mg on day 1 and 250 mg on days 2 to 5 [34] 

Second-line therapy:

  • Trimethoprim-sulfamethoxazole: 800 mg twice daily for 14 days [35]
Mycoplasma pneumoniae
  • Supportive therapy

Antibiotics are prescribed in specific circumstances, including preventing outbreaks spread [36] for immunocompromised individuals, lung transplant recipients, or those presenting with non-respiratory associated symptoms.[37][38] 

  • Azithromycin 500 mg on day 1 and 250 mg on days 2 to 5

or

  • doxycycline 100 mg twice daily for 5 days [39]

Chlamydia pneumoniae

  • Supportive therapy only  

* The use of oseltamivir and zanamivir has been shown to offer minor benefits in reducing the duration of influenza symptoms by an average of half a day in adults. These medications are also effective in reducing the risk of symptomatic influenza when used as a prophylactic measure. However, limited evidence supports the claim that these drugs can reduce the risk of hospital admission or pneumonia. Furthermore, a Cochrane review suggests that there is insufficient evidence to support the use of neuraminidase inhibitors in preventing the person-to-person spread of influenza. The complications associated with influenza, such as pneumonia, cannot be reduced by treatment trials due to the lack of clear diagnostic definitions. The use of oseltamivir has been found to increase the risk of adverse effects such as nausea, vomiting, psychiatric effects, and renal events in adults. Therefore, the balance between the benefits and harms of using neuraminidase inhibitors for prophylaxis or treatment should be carefully considered when making decisions.[40]

In summary, robust data are lacking supporting the use of beta-agonists, steroids, neuraminidase inhibitors, and mucolytic agents, particularly in patients without underlying COPD and asthma. Treatment decisions should be based on the individual's response to these interventions and the reported benefits while carefully considering the balance between potential risks and benefits in each case.

Differential Diagnosis

Other potential causes of acute cough should be considered, especially when the cough persists for a duration exceeding 3 weeks. Other conditions to consider are as follows:

  • Asthma: Acute asthma exacerbation can be frequently misdiagnosed as acute bronchitis, with around one-third of patients presenting with acute cough.
  • Acute or chronic sinusitis
  • Bronchiolitis
  • COPD
  • Gastroesophageal reflux disease (GERD)
  • Viral pharyngitis
  • Heart failure
  • Pulmonary embolism
  • Pneumonia

Prognosis

Acute bronchitis typically follows a self-limiting course and frequently improves with symptomatic interventions. However, clinicians should remain aware of potential secondary complications, such as pneumonia. Cases of acute respiratory distress syndrome and respiratory failure associated with acute bronchitis have been documented in the literature. Consequently, while acute bronchitis is often manageable with symptomatic care, the healthcare team should be mindful of potential complications and ready to administer appropriate interventions if necessary.[41][42]

Complications

Complications associated with acute bronchitis include:

  • Secondary pneumonia
  • Acute respiratory distress syndrome
  • Prolonged symptoms
  • Spontaneous pneumothorax
  • Spontaneous pneumomediastinum

Deterrence and Patient Education

Lifestyle modifications like smoking cessation and minimizing exposure to allergens and pollutants are essential in preventing the recurrence of acute bronchitis and reducing the risk of complications. The flu and pneumonia vaccines are particularly advised in specific groups, including adults 65 and older, children younger than 2 years (but older than 6 months), pregnant women, and individuals residing in nursing homes and long-term care facilities. People with conditions like asthma, COPD, and other individuals who are immunocompromised also risk developing complications. Recurrence occurs in up to one-third of acute bronchitis cases.

Additionally, patients should receive education regarding the risks associated with unnecessary antibiotic prescriptions, including the development of antibiotic resistance, cost implications, and potential adverse effects. Patients should be encouraged to engage in open and informed discussions with their healthcare practitioners to ensure that treatment decisions align with their clinical needs, promoting effective and responsible healthcare practices.

Pearls and Other Issues

Acute bronchitis is a very common respiratory symptom that affects the bronchial tree. The majority (90%) of cases are caused by viruses, resulting in inflammation and increased mucus production. Occasionally, secondary pneumonia can develop, typically characterized by worsening symptoms, a productive cough, and fever. In such cases, a CXR is advisable, particularly for adults in an immunocompromised state, older individuals, infants, newborns, and individuals who smoke.

Identifying the pathogen responsible for acute bronchitis is helpful, although not always necessary. In recent years, new technological developments have made this possible, such as multiplex polymerase-chain reaction (PCR) testing of nasopharyngeal swabs that can identify more than one organism at once.

Acute bronchitis is usually a self-limiting condition and rarely requires treatment. Acute bronchitis caused by specific types of pathogens can be treated with antiviral therapies in addition to symptomatic and supportive therapies. 

Ensuring pulmonary emboli are on the list of differentials for patients with cough and shortness of breath is prudent. Aggressive coughing can result in spontaneous pneumothorax or spontaneous pneumomediastinum, underscoring the importance of a CXR when acute symptom deterioration occurs.

Enhancing Healthcare Team Outcomes

In managing acute bronchitis, an interprofessional healthcare team comprising physicians, advanced practitioners, nurses, pharmacists, and other health professionals is critical in delivering patient-centered care, improving outcomes, ensuring patient safety, and optimizing team performance. To achieve these goals, the team must employ various skills and strategies, uphold ethical standards, embrace shared responsibilities, foster open interprofessional communication, and coordinate care effectively. Here are key components for enhancing healthcare team outcomes in acute bronchitis management:

  • Skills and Expertise: Each team member should possess the clinical skills and expertise relevant to their role in acute bronchitis care. Physicians should be proficient in diagnosis and treatment options, nurses should excel in patient monitoring and education, and pharmacists should be well-versed in medication management and potential drug interactions.

  • Evidence-Based Practice: The team should consistently apply evidence-based guidelines and current best practices in diagnosing and managing acute bronchitis. Staying current with the latest research and recommendations is crucial for delivering high-quality care.

  • Responsibilities and Roles: Clearly defined roles and responsibilities within the team are essential. Physicians diagnose and prescribe treatment, nurses provide patient education and monitor progress, pharmacists ensure safe medication use, and other professionals contribute their specialized knowledge.

  • Care Coordination: Coordinating care is central to optimizing patient outcomes. This involves scheduling follow-up appointments, ensuring adherence to treatment plans, and actively involving patients in their care decisions.

  • Patient Education: Nurses are vital in educating patients about their condition, treatment options, and preventive measures. Empowering patients with knowledge encourages active participation in their care and contributes to improved outcomes.

  • Medication Management: Pharmacists should review medication regimens to identify potential interactions and allergies, which can help minimize adverse drug events and improve patient safety.

  • Timely Follow-Up: Patients with persistent symptoms should have timely follow-up appointments scheduled to assess progress and consider alternative treatments if necessary. This underscores the importance of continuity of care. Acute bronchitis can lead to high morbidity in patients with underlying COPD and other preexisting pulmonary conditions. It is crucial to recognize that when symptoms persist for more than 6 weeks, a reevaluation is essential to confirm the accuracy of the initial diagnosis and assess the potential presence of complicating factors.[43][44]


Details

Author

Anumeha Singh

Author

Akshay Avula

Editor:

Elise Zahn

Updated:

3/9/2024 6:51:38 PM

References


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