The national clinical examination. Does this infant have pneumonia?

Margolis P, Gadomski A.

Division of Community Pediatrics, The University of North Carolina at Chapel Hill, 27599-7225, USA. margolis@med.unc.edu

Acute lower respiratory tract illness is common among children seen in primary care. We reviewed the accuracy and precision of the clinical examination in detecting pneumonia in children. Although most cases are viral, it is important to identify bacterial pneumonia to provide appropriate therapy. Studies were identified by searching MEDLINE from 1982 to 1995, reviewing reference lists, reviewing a published compendium of studies of the clinical examination, and consulting experts. Observer agreement is good for most signs on the clinical examination. Each study was reviewed by 2 observers and graded for methodologic quality. There is better agreement about signs that can be observed (eg, use of accessory muscles, color, attentiveness; kappa, 0.48-0.66) than signs that require auscultation of the chest (eg, adventitious sounds; kappa, 0.3). Measurements of the respiratory rate are enhanced by counting for 60 seconds. The best individual finding for ruling out pneumonia is the absence of tachypnea. Chest indrawing, and other signs of increased work of breathing, increases the likelihood of pneumonia. If all clinical signs (respiratory rate, auscultation, and work of breathing) are negative, the chest x-ray findings are unlikely to be positive. Studies are needed to assess the value of clinical findings when they are used together.

 

CLINICAL SCENARIO

 

 A mother brings her 8-month-old infant to your office in midwinter with a bad cough. She reports that the illness began  4 days ago with a runny nose. Two days  ago, the baby developed a fever. Now the baby's symptoms are getting worse. The baby has become more irritable, is eating less, and seems to be having more difficulty breathing. This is the third child you have seen today with a cough.

 

Why Is This an Important Question to Answer With Clinical Examination?

 

Acute respiratory illnesses are among the most common conditions of infants seen in primary care offices. Although the majority of respiratory illnesses involve infections of the upper respiratory  tract, most infants will experience a lower respiratory tract illness (LRI) in

the first year of life. Of those with LRIs, a] about 30% visit a physician, and about 2% are hospitalized. Lower respiratory tract illnesses can be defined simply as infections at an anatomic level below the vocal cords. The majority of LRIs in infants are caused by viruses; only a small proportion are due to bacteria. The differential diagnosis for cough is long (Table 1).

Therapies are available to treat a variety of manifestations of lower respiratory tract disease, so it is important to diagnose these complaints accurately and estimate their severity to deliver the appropriate treatment. Identifying infants at lower risk of bacterial disease may help clinicians :1.void the unnecessary use of antibiotics. This may reduce the risk of subsequent bacterial infection and slow the emergence of resistant strains of bacteria within the population.4 Greater certainty about the presence of a viral LRI may also help clinicians avoid additional testing such as radiography or blood culture.

This overview focuses on the history and physical examination findings of infants that distinguish pneumonia from other LRIs.

 

 

 

METHODS

 

We conducted a MEDLINE search from 1982 to 1995 to identify articles about the diagnosis of pneumonia in children. We searched for articles with any of the following Medical Subject Heading (MeSH) terms: pneumonia, diagnostic tests, sensitivity and specificity, reproducibility of results, physical examination, or medical history taking. This search was further limited to studies published in English about humans that involved children. This search strategy identified 38 articles. Four more articles were identified by reviewing a compendium of references prepared by the World Health Organization.5 Etiologic studies, which did not include a chest x-ray examination as part of the "gold standard," involved only inpatients. Studies of illness in families' homes, rather than in clinical settings, were excluded (n=29).


 

All the articles were reviewed by the authors and disagreements were re- solved by discussion. We used the methods developed for this series to assess the quality of the articles. The highest- quality studies are emphasized in the "Results" section. We did not aggregate statistically the results of the studies be- cause of differences in the ages of the study samples and differences in cut off points of key variables, such as respiratory rate. Confidence intervals were calculated according to the method suggested by Koopman.6.7

 

 

 

Reference Standard for Diagnosing Pneumonia

 

The reference standard for diagnosing pneumonia is an aspirate from the lower respiratory tract obtained by bronchoaveolar lavage or lung puncture. The use of bronchial lavage is appropriate in guiding antibiotic choice in patients with refractory or complicated pneumonia. In general practice, chest x-ray films are readily obtained and can be considered a pragmatic reference standard for pneumonia.

 

A number of studies evaluated the accuracy of the chest x-ray film in differentiating viral from bacterial disease in children. It is difficult to determine the accuracy of the chest x-ray film from these studies because of methodologic limitations, as well as challenges to study design F introduced by the biology of pneumonia. (;1 It is not possible to obtain cultures from a til lung in most patients. Therefore, investigators have had to use combinations of other clinical features as a proxy for bacterial pneumonia. Reliance on less than ti perfect gold standards for diagnosing bacaterial pneumonia may produce over or underestimates of the association of a SI positive chest x-ray finding with bacterial pneumonia. Two studies used the same definition of bacterial pneumonia (duration of symptoms <2 days, temperature >39.5°C, total white blood cell count > 15.0x 109/L}. Both found the sensitivity of the chest x-ray film for diagnosing o bacterial vs. viral pneumonia to be approximately 75%. However, one reported a specificity of 100%, the other, a specificity of 63%. The reported sensitivity for studies with varying definitions ranges from 42% to 80% and the specificity from 42% to 100%. Studies of the accuracy of el chest x-ray films have also been compromised by other methodologic problems, el such as interobserver variability in the al interpretation of the x -ray film, oversampling patients with relatively severe disease, and the relatively small numbers of patients with bacterial pneumonia. Such problems make estimates of chest x-ray film accuracy unreliable.

 

Variation in the biologic manifestations of bacterial pneumonia also presents challenges in the interpretation of el published studies. For example, bacterial bi pneumonia is classically associated with 10- pi bar consolidation on the x-ray film. However, studies report that bacterial pneumonia may be associated with infiltrates that are lobar, perihilar, segmental, interstitial, or nodular infiltrates}4-16 Consolidation can also be seen with viral pneumonia, but it is unclear if this radiologic m appearance is due to segmental consolidation, atelectasis, or bacterial coinfection. Such variability in the radiographic appearance of bacterial pneumonia may produce over- or underestimates of the association of a positive chest x-ray finding with bacterial pneumonia.

 

Clinicians should be aware that the chest x-ray finding may be negative in patients with early bacterial pneumonia. The sensitivity of the chest x-ray film will be reduced in this group. The implications of this observation are important for studies of the clinical examination. For the purposes of this systematic review, we included studies that used the chest x-ray film as the reference standard. Studies that combined the clinical diagnosis with the chest x-ray film results as the reference standard were excluded because inclusion of the diagnostic test in the reference standard may overestimate the accuracy of clinical findings. The significance of clinical findings of pneumonia in the absence of a positive chest x-ray findings remains to be studied.

Normal Anatomy and Pathophysiology of Pneumonia

Lower respiratory tract infections occur at or below the larynx and include epiglottitis, laryngitis, laryngotracheo- bronchitis (croup), bronchiolitis, and pneumonia (Figure 1). Pneumonia typically follows an upper respiratory tract illness in which the lower respiratory tract is invaded by bacteria, viruses, or other pathogens that trigger the immune response and produce inflammation. Histamines, leukotrienes, and chemotactic factors are released that recruit white blood cells to the area. This response fills the air spaces of the lower respiratory tract with white blood cells, fluid, and cellular debris. This process reduces lung compliance, increases resistance, obstructs smaller airways, and may result in collapse of  distal air spaces.

 

The resultant physical findings vary with the site of infection, ranging from coarse breath sounds or rhonchi in bronchopneumonia to crackles in the alveoli in cases of pneumonia or bronchiolitis. Crackles are the result of the explosive 41 equalization of gas pressure between the terminal bronchiole and the alveoli.1B Wheezes result from the oscillation of air through a narrowed airway that produces a musical sound likened to a vibrating reed. Decreased breath sounds may also be noted in areas of consolidation.

How to Elicit the Relevant Symptoms and Signs

There are 2 goals of the history and physical examination in a child who presents with a cough. The first is to identify the clinical syndrome; the second is to estimate the severity of the illness. In taking the history, the examiner should ask the parent about symptoms associated with pneumonia, as well as those that may discriminate pneumonia from other lower respiratory tract diseases. In addition to cough, symptoms that may increase the likelihood of pneumonia include trouble breathing, rattling in the chest, noisy breathing, trouble feeding, fever, rapid breathing, anxiety, or restlessness. Clinicians working in different regions; or with different cultures, need to familiarize themselves with local terminology for lower respiratory tract symptoms. It may also be useful to ask bout prior episodes of these chest symptoms because recurrent bouts of pneumonia or bronchitis may suggest reactive airway disease. In early infancy (<2 months), infants of mothers who had clamydia during pregnancy may develop afebrile pneumonia. Clinicians should note that infants only rarely produce sputum. In older infants, foreign body ingestion and salicylate poisoning should be considered. Although clinical experience suggests that the history of pneumonia may be of acute or gradual onset and that bacterial pneumonia tends to be associated with fever, we were unable to find any studies substantiating these observations.

 

The physical examination should  include an assessment of the child's general appearance, measurement of the respiratory rate, evaluation of the work of breathing, and auscultation of the chest. The child's general appearance may provide important clues about the presence , bacterial illness and its severity. Infants can exhibit a wide range of behaviors and mood changes during the parental interview, while being undressed, and during the physical examination. Therefore, it is important to take a non-threatening approach with the young child. Infants should be observed initially at a distance, while they are comforted, usually the caretaker's lap. The assessment of general appearance should include an evaluation of a number of factors: attentiveness to the environment, ability to 'breast-feed or drink, ability to sustain sucking, vocalization, smiling, movement, color, and consolability. If there is uncertainty about particular findings, it may be helpful to try to elicit them. For example, encouraging the child to smile, having the mother offer the breast, or showing the child a toy to engage his or her attention. Respiratory rates change considerably the first year of life, decreasing from a mean in awake babies of about 50/min at 1 week of age to about 40/min at 6 months of age. The respiratory rate in children can also vary over brief intervals as the child's level of interest in the environment changes, or while the child is asleep or feeding. Polygraphic studies of infants younger than 6 months have demonstrated that mean respiratory rates were 4/min to 13/min higher in active sleep (rapid eye movement) than in quiet sleep. Fever can also increase an infant's respiratory rate by 10/min per degree centigrade in children without pneumonia. However, the effects of fever in the presence of pneumonia have not been studied.

 

The respiratory rate is best measured by observing chest wall movements over 1 minute.Listening to the chest with a stethoscope may stimulate the child and lead to a falsely elevated measurement. Measurement errors in counting the respiratory rate are greater when children are agitated or crying compared with when they are calm, feeding, or sleeping. The examiner should count the respiratory rate before conducting other parts of the examination. Respiratory rate cutoffs that are commonly used to indicate an elevated rate are greater than 60/min in infants youngerthan2 months, greater than 50/min in infants 2 through 12 months of age, and greater than 40/min in children older than 12 months.

 

Assessing an infant's work of breathing is important to estimate the severity of LRI. This assessment includes evaluation of chest wall movements, nasal flaring, and grunting. Chest wall movements include retractions or chest indrawing, best observed with the chest fully exposed. Supraclavicular retractions may be observed as indrawing of the soft tissue above the clavicle or above the sternal notch. Intercostal retractions are seen as indrawing of skin between the ribs. Subcostal retractions occur on or just below the costal margin. Many experts suggest that these types of retractions, involving only the soft tissue, should be distinguished from chest wall indrawing, defined as an inward movement of the lower chest wall (ie, ribs) when the child breathes in. Chest indrawing is more likely to be observed in infants younger than 18 to 24 months whose chest walls are more compliant. The finding may be appreciated best by viewing the chest laterally and looking for indrawing of the ribs and/or lower sternum with inspiration, relative to a fixed point beyond the child's chest that is set as a mental reference point (Figure 2). Normally, the costal margin moves little during quiet breathing. If it does, it moves up and outward because the normal diaphragm lifts the costal margin outward. In disease states, the depressed diaphragm may apply an inward traction on the chest resulting in paradoxical movement of the chest wall during inspiration. Therefore, in airway obstruction, the costal margin tends to move paradoxically (ie, down and inward). Sometimes, the abdomen moves outward while the chest moves inward during inspiration. This has also been called Hoover sign or paradoxical or seesaw breathing.

 


 

 

Nasal flaring is enlargement of both openings of the nose during inspiration. It is due to constriction of anterior and posterior dilators naris muscles. Grunting is a repetitive short upper respiratory tract sound produced by partial vocal cord closure during expiration. Grunting slows expiratory flow and increases lung volume and alveolar pressures. It can be a sign of severe disease and suggests impending respiratory failure. Examiners should be aware that the presence of signs of increased work of breathing may change with the state of the child. For example, chest wall indrawing may be present only when the child is awake or more active.

 

Adventitious sounds that can be appreciated on auscultation include discontinuous or popping sounds, sounds that occur throughout the inspiratory or expiratory phase, or continuous sounds. Discontinuous sounds have been called crackles, rales, or crepitations. They typically occur at the end of inspiration. Continuous sounds include wheezes and rhonchi and can be musical, high- or low-pitched, inspiratory or expiratory, short or long, or monophonic or polyphonic. Clinicians should try to distinguish whether sounds are continuous or discontinuous before applying a name. Many clinicians differentiate continuous sounds that are whistling or high-pitched (usually called wheezes) from low-pitched, snoring or rattling sounds (usually called rhonchi). Many experts consider wheezes to reflect small airway obstruction (ie, bronchioles), while rhonchi reflect obstruction of the large airways (ie, bronchi).

 

It is interesting to note that the language used to describe auscultatory findings can be a source of confusion. For example, rhonchi and rales are, respectively, the Latin and French words for crackles. Indeed, Laennec (the inventor of the stethoscope) distinguished 6 types of crackles.He believed that only 1 of these was associated with pneumonia.

 

Auscultation of the chest is often more difficult in infants when they are crying. For this reason, it should be performed after the visual inspection of the child. It is important to listen to the front, back, and sides of the infant's chest because adventitious sounds may only be heard in 1 location. Even when the infant is crying, adventitious sounds may be heard at the end of inspiration when the infant is quiet and about to take a breath. Examiners should also be aware that wheezes can often be appreciated by listening to the sounds of breaths from infants mouths (audible wheezing). Finally, infants may have several types of adventitious sounds present although this is more common in reactive airway disease or viral LRI). Text- books do not recommend percussion of the hest in infants because it is difficult to get infants to cooperate with this maneuver.


 

 

 

Are These Symptoms or Signs Ever Normal?

 

Premature infants and neonates may app ear to have chest indrawing during normal breathing or exertion. Grunting and groaning noises occur from time to time in normal healthy infants. An infant who is very playful may demonstrate increased respiratory rate, intercostal retractions, and increased work of breathing.

RESULTS

The Precision of Symptoms and Signs

A total of 56 patients with lower respiratory tract symptoms were examined by pairs of general pediatricians from a group that included academic pediatric generalists, pediatric residents, and pe- iatricians in community practice. Agreement was good for most signs on physical examination that could be observed by inspection, including the social interaction markers of attentiveness K, 0.49), smiling (K, 0.51), quality of cry K, 0.63); physical appearance and movement (K, 0.54), color (K, 0,66), respiratory effort retractions (K, 0.48), and use of accessory muscles (K, 0.59). There was only fair agreement about most auscultatory findings: prolonged expiratory phase (K, .22), adventitious sounds (K, 0.3), and inspiratory wheezing (K, 0.29). Agreement was good for audible wheezing (K, .7) and for expiratory wheezing (K, .63). In general, physicians agreed more often that a finding was present than when it was absent. A second study indicated that observers are less likely to agree about the severity of findings than about their presence or absence.

 

Several studies of the precision of the respiratory rate suggest that respiratory rates counted over 30 seconds average 2/min to 4/min faster than respiratory rates counted over 60 seconds. Counting the respiratory rate over 30 seconds will lead to more abnormal rates and may spuriously increase the number of children diagnosed as having pneumonia. More accurate results are obtained t if the average of two 30-second counts is t taken or one 60-second count.

 

Observer agreement is good for most signs on the physical examination. There is better agreement about signs that can be observed than signs that require auscultation of the chest.

The Accuracy of Signs of Pneumonia

The reported accuracy of clinical findings varies considerably among studies because of methodologic limitations and ( differences in the spectrum of illness severity among sites in which the studies were conducted. In most reports, chest x-ray films were used as the gold standard and children who had clinical findings suggestive of pneumonia were more likely to have had an x-ray examination than those who did not (Table 2). Although this approach makes sense clinically, it introduces verification bias that tends to overestimate a test's sensitivity and underestimate its specificity.4°

Two studies, both of which were con- ducted in developing countries, at- tempted to overcome the problem of selective ordering of the gold standard by obtaining chest x -ray films on all children with abnormal clinical findings (eg, elevated respiratory rate), as well as a sample of children without abnormal findings. The reported accuracy was then adjusted statistically for the fraction of

patients sampled in each group. These 2 studies found that there was no single sign that could be used to rule in or rule out pneumonia definitively .In these studies, children with elevated respiratory rates were about twice as likely to have pneumonia (positive likelihood ratio [LR+ ], 1.5-2.1) as children without elevated respiratory rates (Table 3). Conversely, those without elevated respiratory rates were only about 0.36 to 0.5  times as likely to have pneumonia. These studies also found that the presence of chest indrawing (retractions) increased the likelihood of pneumonia (LR+, 2.4- .n 2.5). However, normal chest movements did not rule out pneumonia(negative likelihood ratio [LR- ],0.7-0.78). Other useful findings that increased the likelihood of  pneumonia included nasal flaring (LR+, 1- 3.0), and crepitations (LR+, 3.5). Once again, the absence of nasal flaring and crepitations did not effectively lower the likelihood of pneumonia: no nasal flaring, LR-, 0.71; no crepitations, LR-, 0.69. Other studies in developing countries, even though less methodologically sound, found the accuracy of clinical signs to be more or less in the same range as that found in the 2 more well-designed investigations (Table 3).

 

The lower prevalence of bacterial disease and severe pneumonia found in developed countries might suggest that the accuracy of physical examination signs would be lower than that reported in studies from developing countries. However, the few studies performed in developed countries reported results similar to those cited above. These studies may have overestimated the accuracy of clinical findings because chest x-ray films were more likely to be obtained in patients with signs and symptoms of disease. In a study by Leventhal,so the absence of tachypnea, as observed by the clinician examining the patient, was useful for ruling out pneumonia (LR-, 0.32), while the presence of tachypnea somewhat increased the odds of pneumonia (LR+, 2.03). Grunting and crepitations were more useful in ruling in disease (LR+,3.17 and 2.1, respectively). Their absence did not appreciably lower the likelihood of disease (LR-, 0.86 and 0.73). The study by Taylor et al reported a somewhat higher LR+ for tachypnea (LR+, 3.22), but this study included only febrile children and chest x-ray films were not obtained for all study patients.

 

A study by Crain et al included only infants with fever younger than 8 weeks who were seen in an emergency department. The authors reported that tachypnea (LR+, 8.0; 95% confidence interval (CI], 5.3-12.1) and chest indrawing (LR+, 26.0; 95% CI, 2.7-118.8) substantiallyin- creased the likelihood of pneumonia. Although these likelihood ratios are quite high, the number of patients with pneumonia in this study was small and the reported estimates are imprecise (as indicated by the wide 95% CIs). In addition, the high likelihood ratios also reflect the high specificity of tachypnea and indrawing in a particular group of patients (early infants). The value of the clinical examination may differ in this group of children. As in other studies, the absence of these findings did not dramatically lower the likelihood of disease for tachypnea (LR-, 0.55) or for indrawing (LR-, 0.75).

 

Accuracy of Combinations of Findings

 

Clinicians typically evaluate the presence of many findings simultaneously to rule in or rule out pneumonia. Despite the large number of studies, few have examined the value of clinical findings when they are used together. Two studies assessed the value of combinations of clinical findings. Leventhal found that the absence of pulmonary findings defined as respiratory distress (nasal flaring, grunting, retractions), tachypnea, rales, or decreased breath sounds ruled out pneumonia (LR-, 0.0; 95% CI, 0.0- 0.4). When present, these findings raised the likelihood of pneumonia to 1.6 (95% CI, 1.3-31.3). In this study, information about the presence or absence of respiratory symptoms was used in the decision to obtain the gold standard examination (a chest x-ray examination). Thus, the reported data are likely to overestimate the diagnostic accuracy of these combinations of findings so that the true LR- is not as good as reported and the LR+ is better than reported.

 

In a study of children younger than 2 months, Grain et al found that the absence of any respiratory findings (rhinorrhea, cough, adventitious sounds, or retractions) lowered substantially the likelihood of a positive chest x-ray finding (LR-, 0.10; 95% CI, 0.03-0.4). The presence of any of these findings increased the likelihood of pneumonia to 3.4 (95% CI, 2.6-4.3). Again, since this study included only infants younger than 8 weeks, it is not clear how well the results apply to older age groups. Grain et al also found that as the number of positive respiratory findings increased, so did the probability of an abnormal chest x-ray finding.

 

To summarize, physical examination findings can help primary care physicians be more certain that an infant does or does not have pneumonia. In developed countries, where the prevalence of bacterial pneumonia is lower, pneumonia is unlikely if all signs are negative. The presence of a positive sign will be more useful in increasing clinicians' certainty that an infant has pneumonia in developing countries as compared with developed countries because the prevalence of bacterial pneumonia is higher. In developed countries, clinicians will be more certain if multiple findings are positive. Further studies are needed to examine the diagnostic accuracy of the chest x-ray examination, the value of certain signs (such as fever and toxic appearance), as well as how to best take advantage of combinations of clinical findings.

 

 


 

THE BOTTOM LINE

 

First, the initial observation of the infant may be the most critical component of the examination. Observation is important before interacting with a child.

 

Secondly, because of its moment-to-moment variability, the  respiratory rate should be counted by observing the chest while the child is quiet over tow 30-second intervals or over a full minute. Clinicians need to be especially aware of the variability of the examination as the child’s level or activity changes.

.

Third, auscultation is relatively unreliable when examining infants. Clinicians need better training and better terminology to describe abnormal chest sounds. The overall clinical appearance may be accurate but the delineation of its value needs more study.

 

Fourth, the best individual finding for ruling out pneumonia is the absence of tachypnea. Chest indrawing and other signs of increased work of breathing (eg, nasal flaring) and abnormal auscultatory findings are better for ruling in pneumonia. In developed countries, multiple findings must be present to be more certain about the presence of pneumonia.

 

Fifth, if all clinical signs (respiratory rate, auscultation, and work of breathing) are negative, the chest x-ray finding is unlikely to be positive.

 

 

Margolis P, Gadomski A. Does this infant have pneumonia? JAMA 1998 Jan 28;279( ):308-313. PubMed
00005407-199801280-00043.an.