Family Practice Vol. 17, No. 2, 150-155
© Oxford University Press 2000
The prevalence of potentially pathogenic bacteria in nasopharyngeal samples from individuals with a long-standing cough—clinical value of a nasopharyngeal sample
Department of Primary Health Care, Göteborg University and
a Department of Clinical Bacteriology, Umeå University, Sweden.
Correspondence to Ronny K Gunnarsson, MD, Research and Development Unit, Primary Health Care, Borås Hospital, ADM 2, S-501 82 Borås, Sweden.
Gunnarsson RK, Holm SE and Söderström M. The prevalence of potentially pathogenic bacteria in nasopharyngeal samples from individuals with a long-standing cough—clinical value of a nasopharyngeal sample. Family Practice 2000; 17: 150–155.
Received 12 April 1999; Revised 15 October 1999; Accepted 26 October 1999.
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Abstract |
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Background. A long-standing cough is a common cause for visits to a GP. If the patient also has a respiratory tract infection, one of the concerns of the doctor is to decide if the cough is caused by an underlying bacterial infection.
Objectives. Our aim was to investigate whether a nasopharyngeal sample, obtained in routine medical practice, could yield information about the aetiology of a long-standing cough in patients with a respiratory tract infection.
Methods. The prevalence of potentially pathogenic bacteria (Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis) in nasopharyngeal swab samples from 618 healthy individuals was compared with that from 236 patients with a respiratory tract infection and long-standing cough (>9 days) of the same age in a defined geographical area.
Results. The proportion of cultures with potentially pathogenic bacteria decreased with age and was 44% among healthy individuals of pre-school age, 13% in schoolchildren and 6% in adults. The corresponding figures for patients with a long-standing cough were 83, 35 and 36%, respectively. All types of potentially pathogenic bacteria were found more frequently in pre-school children and in adults with a long-standing cough compared with healthy individuals of the same age.
Conclusions. In patients with a respiratory tract infection and a long-standing cough, where a bacterial infection is suspected on clinical grounds, a nasopharyngeal culture could yield information about the aetiology. If M.catarrhalis is found in pre-school children, or if H.influenzae is found in adults, they are likely to be the aetiological agent.
Keywords. Carriers, Haemophilus influenzae, Moraxella catarrhalis, respiratory tract infection diagnosis, Streptococcus pneumoniae.
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Introduction |
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A long-standing cough is a common cause for visits to a GP.1 If the patient also has a respiratory tract infection, one of the concerns for the doctor is to decide whether the cough is caused by an underlying bacterial infection or not. It is often difficult to differentiate between viral and bacterial respiratory tract infections solely on clinical grounds. Microbiological tests such as nasopharyngeal culture could improve our diagnostic accuracy. However, not all patients with a positive test for pathogenic bacteria will have a bacterial infection. Some of these patients may just be carriers of potential pathogenic bacteria with a simultaneous virus infection. Thus, conclusions concerning the significance of bacterial findings should be drawn with caution.
It is assumed that in patients with a respiratory tract infection and long-standing cough, the aetiology is viral in most cases,2 although this has been difficult to prove.3 Mycoplasma pneumoniae4 and Chlamydia pneumoniae5 may occur, sometimes as minor epidemics. Bordetella pertussis is a well-known agent causing a long-standing cough among children and adults. Findings of B.pertussis in a nasopharyngeal sample are easy to interpret since there is no carrier state of this bacterium.6,7 Finding the pathogens Haemophilus influenzae, Moraxella catarrhalis or Streptococcus pneumoniae in a nasopharyngeal sample is usually more difficult to interpret. Healthy carriers of these potentially pathogenic bacteria are prevalent, especially among pre-school children.8 In children with a long-standing cough, it has been shown that the prevalence of M.catarrhalis in the nasopharynx was higher than among healthy controls6 and that antibiotic treatment decreased the days of illness.9 To our knowledge, there is no study investigating the importance of common respiratory tract pathogens such as H.influenzae, M.catarrhalis and S.pneumoniae in adult patients with a long-standing cough.
The aim of the present study was to investigate whether a nasopharyngeal sample, obtained in routine medical practice, could yield information concerning the aetiology of long-standing coughs in patients with a respiratory tract infection.
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Method |
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During a winter and a summer period, 14 January–17 February and 15 July–15 September, respectively, nasopharyngeal samples were collected from individuals living in the county of Elfsborg in the south-western part of Sweden, a mixed urban and rural population. The study was approved by the Ethics Committee, Göteborg University.
Healthy individuals
Nasopharyngeal samples from healthy pre-school children, schoolchildren and adults were obtained. Samples from pre-school children, 
6 years of age, were collected consecutively at visits to child welfare clinics. Samples from schoolchildren, 7–15 years of age, were obtained from children at school. Samples from adults, 
16 years of age, were obtained consecutively at primary health care centres when the adults visited the clinic as patients with a non-infectious condition.
All the healthy individuals lacked signs of respiratory tract infections. They had not received antibiotics during the previous 4 weeks, and did not have known diabetes mellitus or an immunodeficiency disorder. The samples were considered to be representative of healthy children and adults with no known immunodeficiency disorder.
Patients with a long-standing cough (>9 days)
During the same periods, the results were registered from all consecutive nasopharyngeal samples that were sent to the microbiological laboratory in Borås with a referral stating that the patient had had a cough for 10 days or more. The samples came from the same geographical area as the samples from the healthy individuals.
To achieve a better definition of symptoms in the referrals, a protocol was used during the study. In the protocol, the doctors were asked to use a letter to code the referrals, stating the main symptom causing the need for a nasopharyngeal sample. The available codes were; cough >9 days, acute otitis media in a child with a middle ear ventilation tube (grommet), acute otitis media in a child not having a ventilation tube, throat pain, sneezing, sinusitis or ‘other symptoms’.
Nasopharyngeal culture
The samples were collected in routine medical care by the ordinary staff; doctors, nurses or a medical laboratory technologist, trained to collect nasopharyngeal swab samples. The routine method was as follows; insert a thin flexible swab through one nasal aperture into the posterior wall of the nasopharynx and then put the swab into modified Stuart medium.
The samples from patients and healthy individuals were transported to the same microbiology laboratory in modified Stuart medium. The procedure for processing the samples has been described previously.8
Statistical analysis
Chi-square with Yates' correction was used. When the numbers were small, Fisher's exact test (two-tailed) was used. Relative risk with 95% confidence interval was used to compare patients with a long-standing cough with healthy individuals. The statistical program used was Epi-Info version 6.04 from the Center for Disease Control (CDC) USA, and WHO.
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Results |
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Of 236 nasopharyngeal samples with a referral stating that the patient had a long-standing cough, 160 stated only cough, indicating that this was the only or the most predominant symptom of an acute respiratory tract infection. Among referrals stating a long-standing cough in combination with other symptoms of an acute respiratory tract infection, the most common combinations were: cough and sneezing (32 samples) and cough and throat pain (10 samples). The other 34 referrals stated various other combinations of symptoms indicating an acute respiratory tract infection. We found no statistically significant difference in the prevalence of H.influenzae, M.catarrhalis and S.pneumoniae among patients with a referral stating only a long-standing cough compared with patients with a long-standing cough in combination with other symptoms. However, in adults, we found a difference in the prevalence of any potentially pathogenic bacteria (Fig. 1
). Thus, for pre-school children and schoolchildren, patients with a referral stating only a long-standing cough and patients with a long-standing cough and other symptoms of an acute respiratory tract infection are combined into one group.
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Of the 236 samples arriving at the diagnostic laboratory, 167 (71%) came from primary health care centres, 42 (18%) from paediatric clinics, 12 (5%) from clinics for oto-rhino-laryngology, five (2%) from clinics for infectious diseases and 10 (4%) from other clinics. No samples came from a clinic for lung diseases. Very few samples (2 = 0.8%) came from hospitalized patients.
At least one potentially pathogenic bacterium was found in 83% of the nasopharyngeal samples from patients aged 0–6 years (Table 1). The proportion of pathogenic bacteria decreased with age (Table 1). The most common finding in pre-school children was M.catarrhalis and in adults H.influenzae (Table 2). In pre-school children and adults, S.pneumoniae, H.influenzae and M.catarrhalis were found more often in patients with a long-standing cough compared with healthy individuals of the same age (Table 3).
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Growth of more than one bacterium was common in pre-school children (Table 1
). If two kinds of bacteria were found in pre-school children with a long-standing cough, the combinations were: M.catarrhalis and S.pneumoniae (19 samples); M.catarrhalis and H.influenzae (nine samples); and H.influenzae and S.pneumoniae (five samples). Pure growth of M.catarrhalis, H.influenzae or S.pneumoniae was not more common in pre-school children with a long-standing cough compared with healthy pre-school children. The only combinations of potentially pathogenic bacteria in pre-school children associated with a long-standing cough were those including M.catarrhalis. Thus, the prevalence was higher in pre-school children compared with healthy children for M.catarrhalis + H.influenzae (P = 0.02), M.catarrhalis + S.pneumoniae (P = 0.001) and M.catarrhalis + H.influenzae + S.pneumoniae (P = 0.0007). |
Discussion |
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The main finding in this study was the correlation between long-standing coughs and growth of potentially pathogenic bacteria in the nasopharynx, especially in pre-school children and adults. This finding suggests that nasopharyngeal samples may have a place in the diagnostic procedure and management of patients with long-standing coughs.
Methodological aspects
The advantage of defining criteria for selecting patients with a long-standing cough before the samples are collected is that the population of patients with a long-standing cough will be well defined. The disadvantage of this procedure is that our sample may reflect a population that is not the same as the patients from whom a nasopharyngeal culture would be taken as part of routine medical care. We have chosen to evaluate the outcome of nasopharyngeal cultures obtained in routine medical care without an exterior definition of how to select patients with long-standing coughs appropriate for obtaining a nasopharyngeal sample. Consecutive samples arriving at the microbiology laboratory were used. Only samples with a referral stating that the patients had a cough for >9 days were used. The advantage of this procedure is that our sample will be representative for the population of patients from whom a nasopharyngeal culture would be taken in routine medical care.
The selection of patients in this study could be criticized, as patients were only included when their doctor thought a nasopharyngeal swab sample could be of use in the diagnostic and therapeutic procedure. As the doctors had to characterize the patients' symptoms on the referral slip, we postulate that taking a nasopharyngeal sample was preceded by a reflection of its usefulness. Thus, we assumed that doctors would not take a nasopharyngeal sample if, after a preliminary clinical evaluation, they found that the patient had a probable viral infection.
Almost all samples (99.2%) came from patients who were not hospitalized. Thus, our sample represents patients with an acute minor illness. The majority (71%) of samples came from primary health care centres. No samples came from a clinic for lung diseases. It is therefore reasonable to assume that the proportion of patients with asthma or chronic obstructive pulmonary disease in our sample population is not high. Thus, our sample represents patients with a minor illness and symptoms indicating an acute respiratory tract infection.
All cultures were collected as part of routine medical care and, thus, different personnel were involved. The prevalence of bacteria could therefore be expected to be slightly lower compared with samples being collected by one specially trained person; however, no such evaluation was made. Since our purpose was to compare healthy individuals and patients with a cough, this should only have a minimal effect on the outcome. The advantage of using personnel engaged in routine medical care was that our study might then reflect the normal clinical situation.
Nasopharyngeal culture in patients with a cough is evaluated mainly in the context of diagnosing pneumonia or a pertussis infection. The reason for this is that there are gold standards predicting the presence of pneumoniae. Carriers of B.pertussis are rare; therefore, finding the bacterium is almost equivalent to finding the disease caused by this bacterium. To predict the aetiology of pneumonia, the sensitivity of a nasopharyngeal culture is estimated to be 27–43%10,11 and the specificity to be 96–97%.10,11 However, a long-standing cough is a symptom that can be caused by respiratory tract infections other than pneumoniae. An evaluation of how a nasopharyngeal culture can distinguish viral from bacterial disease in patients with a long-standing cough has, to our knowledge, not been published previously. Thus, the predictive values for nasopharyngeal culture used among these patients have not been published. An important issue in all these test evaluations is the question of what our gold standard predicts; the presence of a bacterium or a disease. Since there is no proper gold standard predicting bacterial respiratory tract disease, predictive values are of limited value in this special situation. We found relative risk to be a useful model. In this model, we compare patients with a long-standing cough and healthy individuals.
As is well known, the proportion of positive samples varies with time and geographical location following fluctuations in the prevalence of bacteria. Data showing the prevalence of bacteria in a single group of individuals are therefore of limited value. A comparison of the prevalence of bacteria between two or more groups of individuals, as in this study, would probably be more informative. Such comparisons between groups are only possible if the samples in all groups are obtained from the same geographical area and during the same time periods, as was done in this study.
Pre-school children
Moraxella catarrhalis is usually the most common potential pathogen found in nasopharyngeal samples in healthy children.6,8,12–14 Haemophilus influenzae6,8,13,15,16 and S.pneumoniae6,8,13,16 are also often found in nasopharyngeal samples in healthy children. Due to these facts, many doctors consider that a nasopharyngeal culture in pre-school children is of very little help in diagnosis.7,16
We found that a long-standing cough in pre-school children was strongly correlated with the finding of M.catarrhalis (Table 3). A correlation between M.catarrhalis and long-standing cough has been described previously,6,9 but in the present study we could only establish that M.catarrhalis is of aetiological significance when it is found in combination with H.influenzae, S.pneumoniae or both. We also found a correlation between H.influenzae, S.pneumoniae and long-standing cough (Table 3). However, further analysis showed that H.influenzae and S.pneumoniae were only of clinical relevance in combination with M.catarrhalis.
Thus, in pre-school children, in whom a bacterial aetiology of a long-standing cough is suspected, a nasopharyngeal culture might indicate the aetiology. However, the main reason for taking a nasopharyngeal sample is if the result of the culture will affect the choice of treatment. Darelid et al. found that the presence of M.catarrhalis in children with a long-standing cough increased the risk of prolonged symptoms and bacterial complications; they further found that proper antibiotic treatment improved the prognosis.9 Furthermore, if it is proven that the aetiology is bacterial, and, that antibiotic treatment positively alters the prognosis for the patient, one still has to consider whether the benefits of the treatment outweigh the disadvantages.17
Because of the high carrier rate of potentially pathogenic bacteria among healthy children, a nasopharyngeal sample should not be taken in children who, after a preliminary clinical evaluation, are judged to have an infection of viral aetiology. If, however, the preliminary clinical judgement is not convincing for a viral aetiology and antibiotic treatment is considered for some reason, then a nasopharyngeal culture to detect the presence of M.catarrhalis, H.influenzae and S.pneumoniae may be useful in pre-school children with a long-standing cough. It seems advisable to postpone antibiotic treatment until the aetiology and the antibiotic sensitivity pattern are established. If M.catarrhalis is found, and, if there are no signs of spontaneous improvement, then antibiotic treatment could be considered. However, as mentioned previously, the ecological risks of antibiotic treatment must be taken into account.
Schoolchildren
The group of schoolchildren was small and this might explain why we did not find any correlation between potentially pathogenic bacteria and long-standing cough. The clinical value of a nasopharyngeal culture for school children with a long-standing cough should be investigated further.
Adults
Since the carrier rate of common pathogens in the nasopharynx is low in healthy adults,8 the finding of potentially pathogenic bacteria in patients with a long-standing cough could add valuable information. We found such a correlation for H.influenzae, M.catarrhalis or S.pneumoniae (Table 3), but it was especially strong for H.influenzae. Eradication of M.catarrhalis in adult patients with acute laryngitis has been shown to reduce complaints of cough.18 Thus, it could be expected that, in adults with a long-standing cough, if the nasopharyngeal culture shows the presence of H.influenzae, S.pneumoniae and M.catarrhalis, it is likely that they are involved as aetiological agents.
Conclusions
Patients with a respiratory tract infection with a long-standing cough may benefit from a nasopharyngeal swab sample. Because of the high carrier rate of potentially pathogenic bacteria, especially in healthy pre-school children, a nasopharyngeal sample should not be taken in a patient with a long-standing cough if the preliminary clinical judgement is of a viral infection. If a bacterial aetiology is considered probable, a nasopharyngeal swab sample might establish the aetiology. If M.catarrhalis is found in pre-school children, or if H.influenzae is found in adults, they are likely to be of aetiological significance.
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Acknowledgments |
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We thank the staff at the microbiology laboratory in Borås for processing the cultures. Financial support was obtained from the Research Committee, Health Department of Elfsborg County.
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References |
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