Arch Dis Child 2012 Grant 21 7

Original article

Arch Dis Child 2012;97:2127. doi:10.1136/archdischild-2011-300604 21

Additional fi gures are published online only. To view the fi les please visit the journal online (http://adc.bmj.com/content/97/1.toc)1Department of Paediatrics, University of Auckland and Starship Childrens Hospital, Auckland District Health Board, Auckland, New Zealand2Department of Primary Health Care, University of Oxford, Oxford, England3General Paediatrics, Starship Childrens Hospital, Auckland District Health Board, Auckland, New Zealand4General Practice and Primary Health Care, The University of Auckland, Auckland, New Zealand

Correspondence to Cameron Grant, Department of Paediatrics, Faculty of Medical and Health Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand; [email protected]

Received 01 July 2011Accepted 25 October 2011Published Online First 18 November 2011

ABSTRACTBackground Although antibiotics are recommended for the primary care management of community-acquired pneumonia, a recent UK study reported that most children admitted to hospital had not received antibiotics.Objective To describe primary care antibiotic use for children subsequently hospitalised with community-acquired pneumonia.Design/methods A case series of 280 children 15109/l (RR=2.29; 95% CI 1.61 to 2.98) and bacteraemia (RR=6.68, 95% CI 1.08 to 58.44).Conclusions Young children with community-acquired pneumonia may not receive an antibiotic before hospital admission because the illness evolves rapidly or the prescribed medicine is not given by parents. However, missed opportunities for appropriate antibiotic prescribing by health professionals in primary care appear to be common.

INTRODUCTIONAntibiotics are recommended as rst-line treat-ment for community-acquired pneumonia and are almost always prescribed to preschool aged chil-dren on hospital admission with pneumonia.1 2 For example, the British Thoracic Society rec-ommends amoxicillin as rst-line treatment for children

Original article

Arch Dis Child 2012;97:2127. doi:10.1136/archdischild-2011-30060422

Pneumonia severity was de ned from variables abstracted from the hospital medical records using the British Thoracic Society criteria (table 1).3 Socioeconomic status was measured using the NZ Index of Social Deprivation which divides house-holds in NZ into socioeconomic deprivation deciles based upon national census data.9

Data analysisDouble-entered data were analysed using SAS-PC version 9.1 statistical software package (SAS Institute Inc, Cary, North Caroline, USA). Adjusted ORs and 95% CIs were estimated using logistic regression. As the ORs were determined on a cohort in which non-prescription of antibiotics was common, the rate ratio (RR) estimated from the OR was adjusted to more accurately represent the true relative risk.10

RESULTSOf 415 children admitted with a diagnosis of pneumonia dur-ing the study period, 280 were included in the analysis; 65 children were ineligible and the parents of 70 children declined participation (see online supplementary gures). The childs age or household deprivation (data not shown) did not differ between the 280 children included in the analysis and the 70 whose parents declined participation.

The median age of participating children was 17 months (IQR 926 months). The children were from a range of eth-nic groups: Maori 13%, Paci c 54% and European/other 33%. Households in socioeconomically deprived areas were over-represented (34% in the bottom quintile).

Prehospital use of antibioticsOne hundred and seventy-two (61%) of the 220 children did not receive an antibiotic before hospital admission. There had been no opportunity for 60 children (21% of 280) to receive antibiotics before admission because either they were not seen in primary care (eight) or parents were advised at the rst pri-mary care visit to go directly to hospital (52). However, for the remaining 112 children (40%, 95% CI 34% to 46%) an oppor-tunity to receive antibiotics in primary care was missed.

Of the 220 children who had an opportunity to receive antibi-otics before hospital admission, 202 (92%) had severe pneumo-nia and eight (4%) had mild pneumonia at hospital admission. The 10 remaining children had a respiratory rate between the criteria for mild (70 if an infant) pneumonia. Slightly more than a third of the 280 children (39%; 95% CI 33 to 44%) had received an antibiotic before hospital admis-sion. In these 108 children, antibiotics had been given for a median of 4 days (IQR 26 days). Twenty-three (21%) chil-dren had received two (and in one case four) antibiotic courses. Amoxicillin, the recommended antibiotic for pneumonia in this age group in NZ,11 was prescribed to 72 (67%) and was the rst antibiotic given to 67 children (62%). Other antibiotics prescribed were (in order of frequency): cefaclor, amoxicillin-clavulanate, trimethoprim-sulphamethoxazole, erythromycin and phenoxy-methyl penicillin.

Reasons for missed opportunitiesFigure 1 shows the prehospital time-course of the illness. The children with no opportunity to receive antibiotics in primary care had a more rapidly evolving illness with a median time to admission of only 2 days (IQR 03 days). In contrast, the chil-dren with an opportunity to receive antibiotics had a median duration of preadmission illness of 4 days (IQR 37 days)

reviewing primary care records to explore why this might happen.

METHODSStudy design and settingThis was a case series of children

Original article


with a median of two visits (IQR 23 visits) to a primary care doctor.

Table 2 shows that receipt of an antibiotic was more likely if the child was seen by their own general practitioner (GP). An anti-biotic was less likely to be received if the primary care clinician failed to make the diagnosis of LRTI (21% vs 36%, p=0.03).

None of the parent-reported symptoms, including increased rate and effort of breathing, were associated with an increased likelihood of antibiotic prescription (table 3). At the last GP visit temperature was recorded for 67% and breathing rate for only 40% of the children. Based upon these two variables and the childs age, 87 of the children had severe pneumonia and 15 had mild pneumonia when seen at this GP visit. Having mild pneumonia was associated with an increased likelihood of being prescribed antibiotics (p=0.004). Table 3 also gives more detail about the clinical ndings recorded in primary care, showing that even if a diagnosis of pneumonia was recorded only 45/70 (64%) children were prescribed an antibiotic.

Figure 2 explores the reasons for the missed opportunity to receive an antibiotic in primary care. Twenty-four children made one GP visit, 55 children made two GP visits and 33 chil-dren made three or more GP visits before admission. For 23 of the 112 children a prescription was written but not collected from the pharmacy. For 24 children the GP diagnosed pneu-monia/bronchopneumonia but no antibiotic was prescribed.

Of the remaining 64 children, based upon parental reporting, 28 presented with increased respiratory rate or breathing dif- culty, 23 with other respiratory symptoms (cough, wheeze or noisy breathing), 49 with systemic symptoms (vomiting, poor feeding, increased sleeping, irritability or lethargy). Forty-one of these children had both respiratory and systemic presenting symptoms. In 19 of these children (30%) the diagnosis of LRTI was not missed by the primary care clinicians.

Consequences of missed opportunitiesTable 4 shows the potential consequences of a missed opportu-nity to give antibiotics before hospital admission. These anal-yses were adjusted for demographic and health service factors associated with the child receiving antibiotics in primary care (table 2). In a multivariate model of these variables two factors were associated with receipt of antibiotics in primary care. These were the number of primary care visits before hospital admission (p=0.007) and whether the child was seen by their own GP on any of these visits (p=0.004).

The univariate association (p=0.04) of having more severe pneumonia on hospital presentation if antibiotics had not been received was not evident in the multivariate analysis. Failure to receive prehospital antibiotics was associated with an increased risk of focal chest radiological abnormalities (RR=2.14; 95% CI 1.49 to 2.83), peripheral leucocytosis (RR=2.29; 95% CI 1.61 to 2.98) and of bacteraemia (RR=6.68; 95% CI 1.08 to 58.44).

DISCUSSIONSummary of the main fi ndingsMost children admitted to hospital with community-acquired pneumonia (61%) did not receive antibiotics before admis-sion. This had no impact on overall disease severity at admis-sion but did increase the likelihood of focal chest radiograph changes, peripheral leucocytosis and bacteraemia. Failure to prescribe in primary care was explained by rapid symptom evolution requiring urgent hospital admission for about half

Figure 1 Length of illness before hospital admission according to whether the child received antibiotics, had no opportunity to receive antibiotics, or was seen in primary care and the opportunity to receive antibiotics was missed. Error bars indicate the standard error around the cumulative proportions. Data were available for 89 children (82%) who had received an antibiotic, 57 children (95%) who had no opportunity to receive an antibiotic and 99 (88%) of children who had been seen in primary care and the opportunity to receive an antibiotic was missed.

Table 2 Demographic characteristics and health service contacts associated with (1) the opportunity to prescribe antibiotics in primary care before the hospital admission and (2) whether this opportunity was missed

Opportunity to prescribe antibiotics in primary care Received antibiotics in primary care if opportunity

Yes (n=220) No (n=60) Yes (n=108) No (n=112)

Median Median p Value Median Median p Value

Age (months) 16 17 NS 17 15 NSVisits to primary care this illness 2 1

Original article


The increased risk of bacteraemia that was associated with not receiving antibiotics in primary care needs to be inter-preted with caution given the small sample size and wide CIs. It also needs to be considered in an immunisation context. At the time this study was conducted conjugate pneumococ-cal vaccine was not part of the NZ national immunisation schedule.17

We were surprised by the lack of association between parent-reported symptoms and antibiotic prescribing. Parental obser-vation of fast or dif cult breathing identi es children with an increased risk of pneumonia.18 Parental concern that this ill-ness is different from previous illnesses also predicts serious illness.18 19 It is impossible to know if the lack of association we observed re ects the inadequacy of our methods or a pri-mary care failure to listen to parents. However, we did observe that appropriate antibiotic prescribing was more likely if the child was rst seen by their own GP. A doctor who is familiar with a child will be more able to discern the extent to which the childs presenting behaviour differs from normal. A better relationship with the primary care provider is likely to enable a parent who has non-speci c concerns that this illness is dif-ferent to seek care, and for these concerns to in uence treat-ment decisions.

One in ve of the children prescribed an antibiotic in pri-mary care did not receive it (because the prescription was not lled), which may be a particular problem in NZ. In NZ there is a co-payment for prescriptions. The government subsidises the manufacturers price but this varies in a complex manner involving multiple patient subsidy levels and differential costs to the patient depending upon their primary care enrolment status and whether they are seen in an after-hours facility.20 The majority of the NZ public are uncertain what amount they will be charged by the pharmacy for a prescription.20 Uncertainty about cost adds another barrier to that caused by prescription co-payments.2022

of the children. Additionally, in about one-in- ve children pre-scribed an antibiotic (18%), the prescription was not taken to the pharmacist by the parent. However, in about a third of all children (32%) the opportunity to prescribe in primary care was missed. This sometimes re ected diagnostic failure but also failure to implement national (and international) guidance on when to prescribe and what antibiotic to use, when a cor-rect diagnosis of pneumonia was made.3 11 12

Comparison with existing literatureThe study con rms the earlier UK report that only about a third of children admitted to hospital with community- acquired pneumonia will have received an antibiotic in the community.1 It is interesting that the impact of not receiving an antibiotic appears limited to speci c disease features rather than overall severity of symptoms.

Prescribing antibiotics appears to make no difference to the time-course of prehospital illness in those eventually admit-ted to hospital. This might be because the pneumonia was not bacterial in origin in the majority, the rst-line antibiotic was not effective at the dose prescribed, or the antibiotic was given too late in the illness.

The existing literature already makes clear the potential for diagnostic failure in primary carehalf the cases of serious infection in children may be missed at rst presentation.13 GPs are urged to avoid antibiotic prescribing to children with respiratory tract infection in order to minimise the real risk of causing resistance to rst-line treatments.14 Most childhood respiratory tract infections for which GPs consider prescribing an antibiotic are of viral origin.15 However, secondary bacte-rial infection is not uncommon, particularly with in uenza infection,16 and the clinical guidelines cited above argue that any LRTI in young children causing other than mild symptoms carries a suf cient risk of bacterial sepsis to warrant treating it with antibiotics.3 12

Table 3 Information from parents about symptoms prompting them to seek medical care for their child and from GP record about the clinical features present when the child was last seen in primary care. (Children with no opportunity to receive an antibiotic in primary care are excluded from this table)

Prescribed an antibiotic* (n=131)

Not prescribed an antibiotic (n=89) Rate ratio

n/N (%) n/N (%) RR (95% CI) p Value

Symptoms reported by parents Fast breathing 43/131 (33) 29/89 (33) 1.02 (0.71 to 1.38) 0.97 Diffi culty breathing 23/131 (18) 12/89 (13) 1.03 (0.59 to 1.72) 0.42 Cough 96/131 (73) 60/89 (67) 1.05 (0.87 to 1.20) 0.35 Fever 85/131 (65) 54/89 (61) 0.95 (0.74 to 1.13) 0.53 Irritable, grumpy or grizzly 66/131 (50) 44/89 (49) 1.03 (0.79 to 1.27) 0.89 Lethargy 55/131 (42) 32/89 (36) 1.10 (0.80 to 1.43) 0.37Vital signs recorded in GP record Fever >39C 26/89 (29) 20/58 (34) 0.85 (0.53 to 1.24) 0.50 Tachypnoea 34/53 (64) 27/35 (77) 0.83 (0.72 to 1.11) 0.20Severity of pneumonia based upon GP observations

Severe pneumonia 47/67 (70) 40/47 (85) 0.92 (0.75 to 1.04) 0.07 Mild pneumonia 14/46 (30) 1/30 (3) 2.55 (1.03 to 6.21) 0.004Diagnosis recorded in GP record Pneumonia 45/102 (44) 25/70 (36) 1.25 (0.75 to 1.44) 0.27 LRTI (but not pneumonia) 33/102 (32) 19/70 (27) 1.19 (0.79 to 1.73) 0.47 Other diagnosis 24/102 (24) 26/70 (37) 0.63 (0.47 to 1.11) 0.05

*Includes the 23 children prescribed an antibiotic but whose parents did not obtain the prescription.Respiratory rate >60/min age50/min age 211 months, >40/min age>12 months.33Based upon respiratory rate, temperature and childs age.3

GP, general practitioner; LRTI, lower respiratory tract infection; RR, rate ratio.

07_archdischild-2011-300604.indd Sec1:2407_archdischild-2011-300604.indd Sec1:24 12/9/2011 4:33:06 PM12/9/2011 4:33:06 PM

group.bmj.com on October 30, 2012 - Published by adc.bmj.comDownloaded from

Original article


resistance) unless we can help them increase their diagnostic precision.

Implications for clinical practice and researchRespiratory tract infections account for most antibiotic prescribing, and overprescribing is a key factor leading to increased rates of antibiotic resistance. Concerted efforts have been made to reduce antibiotic prescribing.23 In the UK, USA and NZ antibiotic prescribing rates for acute respiratory infec-tions have decreased by one-third or more over the past two decades.2426 Some of the largest decreases have been in pre-school aged children.

As the proportion of children treated with antibiotics decreases, the risk of not treating an illness that requires antibiotics increases. Reducing antibiotic treatment for upper respiratory tract infection does not appear to have led to an increase in complications from streptococcal infection such as quinsy, mastoiditis and rheumatic fever.27 However, a recent study among adults presenting with LRTI in primary care sug-gested that failure to prescribe antibiotics is associated with an increased risk of hospital admission and respiratory infection-

Strengths and limitations of the studyThe strength of the study, particularly in the context of other publications, is that (1) it reports a consecutive series of admis-sions from a de ned catchment population and (2) the data on prehospital care are based on parent interviews and primary care records. However, we were unable to conduct a face-to-face interview with each GP who saw the child and the inter-view with the care giver occurred a median of 6 days after hospital presentation. There was therefore a substantial risk of recall bias.

The key limitation in interpreting the study ndings is that we included only children admitted to hospital. We have no data on children who avoided admission because their pneu-monia was successfully treated. It is therefore impossible to determine whether primary care antibiotic treatment of pneu-monia reduces the risk of hospital admission. We can be clear that existing guidance on prescribing is not being followed but we need to be cautious in drawing the conclusion that GPs are being too parsimonious with antibiotics. It is certainly pos-sible that encouraging GPs to lower their prescribing threshold would do more harm than good (by exacerbating antibiotic

Figure 2 Care process for the 112 children who missed an opportunity to receive an antibiotic before hospital admission with community-acquired pneumonia. LRTI, lower respiratory tract infection.



Original article


National Child Health Research Foundation. CCG was supported by an overseas fellowship with the National Institute of Health Research National School of Primary Care.

Competing interests None.

Ethics approval The Ministry of Health Northern Regional Ethics Committee approved the study.

Provenance and peer review Not commissioned; externally peer reviewed.

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present and how are they managed? Arch Dis Child 2007;92:3948. 2. Michelow IC, Olsen K, Lozano J, et al. Epidemiology and clinical characteristics

of community-acquired pneumonia in hospitalized children. Pediatrics 2004;113:7017.

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13. Thompson MJ, Ninis N, Perera R, et al. Clinical recognition of meningococcal disease in children and adolescents. Lancet 2006;367:397403.

14. Chung A, Perera R, Brueggemann AB, et al. Effect of antibiotic prescribing on antibiotic resistance in individual children in primary care: prospective cohort study. BMJ 2007;335:429.

related death.28 Our ndings underline the need to improve the precision of diagnosis of bacterial LRTI in primary care.

The documentation of disease severity for infants with cough and wheeze presenting to primary care in NZ has been shown to be variable but also to improve in response to imple-mentation of a clinical guideline.12 The incomplete documen-tation of vital signs in primary care seen in this study implies that disease severity is still not as well assessed at primary care visits as it is on presentation to hospital emergency depart-ments. Case management of pneumonia in children in develop-ing countries has been shown to reduce pneumonia mortality substantially.29 Developing a successful clinical-decision rule to diagnose childhood pneumonia in primary care is not easy as it is dif cult to achieve high sensitivity with adequate speci- city.19 Use of near-patient C-reactive protein testing may help to target antibiotic use in primary care.30 But in order to be successful, implementation of any diagnostic decision-rule will need to recognise and deal with the socioeconomic and ethnic disparities in healthcare for pneumonia.31 As 100% sensitivity for any diagnostic strategy will never be obtained, an effective safety-netting is also likely to be crucial, particu-larly in economically deprived areas.32

Young children with community-acquired pneumonia may not receive an antibiotic before hospital admission simply because a rapidly evolving illness requires urgent admission. However, missed opportunities for appropriate antibiotic pre-scribing in primary care appear to be common. We must focus on helping GPs to diagnose pneumonia in children more effec-tively and better target their antibiotic use in treating LRTI. If we fail to do this, our justi ed efforts to avoid missed treat-ment of community-acquired pneumonia might easily render rst-line antibiotics ineffective by encouraging overprescrib-ing in primary care.

Contributors CCG obtained funding and ethical approval for the project. CCG, AH and DM designed the study, participated in the data analysis and completed the fi rst draft of the manuscript. CCG and DE led the project through the collection and management of the data and the data analysis. DE and GC edited the draft manuscript.

Funding This project was funded by research grants from the Health Research Council of New Zealand, the Auckland Medical Research Foundation and the

Table 4 Effect on illness severity at hospital admission of children not receiving prehospital antibioticsNo antibiotics (n=112) Antibiotics (n=108) Univariate rate ratio Adjusted rate ratio*

n/N (%) n/N (%) RR (95% CI) RR (95% CI)

Severe pneumonia 107/112 (96) 95/108 (88) 1.09 (1.00 to 1.12) 1.08 (0.98 to 1.12)Mild pneumonia 3/112 (3) 5/108 (5) 0.58 (0.14 to 2.27) 0.80 (0.15 to 3.17)Triage assessed urgent 17/101 (17) 15/96 (16) 1.08 (0.56 to 1.92) 1.23 (0.62 to 2.23)Focal consolidation on CXR 50/112 (45) 25/108 (23) 1.93 (1.34 to 2.56) 2.14 (1.49 to 2.83)Pleural effusion on CXR 13/112 (12) 8/108 (7) 1.57 (0.67 to 3.39) 1.93 (0.80 to 4.31)WBC >15109/l 51/100 (51) 23/99 (23) 2.20 (1.56 to 2.84) 2.29 (1.61 to 2.98)Bacteraemia 5/97 (5) 1/90 (1) 4.66 (0.56 to 29.89) 6.68 (1.08 to 58.44)Increased work of breathing 70/104 (67) 73/100 (73) 0.92 (0.73 to 1.08) 0.95 (0.75 to 1.11)Tachypnoea** 94/112 (84) 103/107 (96) 0.86 (0.64 to 0.98) 0.87 (0.60 to 0.98)Temperature >39C 57/112 (51) 44/108 (41) 1.25 (0.93 to 1.56) 1.17 (0.84 to 1.51)Oximetry 97th centile for age and temperature.34

**Respiratory rate >60/min age 50/min age 211 months, >40/min age >12 months33.CXR, chest radiograph; GP, general practitioner; RR rate ratio; WBC, peripheral white blood cell count.



Original article


25. Grijalva CG, Nuorti JP, Griffi n MR. Antibiotic prescription rates for acute respiratory tract infections in US ambulatory settings. JAMA 2009;302:75866.

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27. Sharland M, Kendall H, Yeates D, et al. Antibiotic prescribing in general practice and hospital admissions for peritonsillar abscess, mastoiditis and rheumatic fever in children: time trend analysis. BMJ 2005;331:3289.

28. Winchester CC, Macfarlane TV, Thomas M, et al. Antibiotic prescribing and outcomes of lower respiratory tract infection in UK primary care. Chest 2009;135:116372.

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30. Cals JW, Schot MJ, de Jong SA, et al. Point-of-care C-reactive protein testing and antibiotic prescribing for respiratory tract infections: a randomized controlled trial. Ann Fam Med 2010;8:12433.

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32. Almond S, Mant D, Thompson M. Diagnostic safety-netting. Br J Gen Pract 2009;59:8724; discussion 874.

33. Pio A. Standard case management of pneumonia in children in developing countries: the cornerstone of the acute respiratory infection programme. Bull World Health Organ 2003;81:298300.

34. Thompson M, Harnden A, Perera R, et al. Deriving temperature and age appropriate heart rate centiles for children with acute infections. Arch Dis Child 2009;94:3615.

15. Harnden A, Perera R, Brueggemann AB, et al. Respiratory infections for which general practitioners consider prescribing an antibiotic: a prospective study. Arch Dis Child 2007;92:5947.

16. Spaeder MC, Milstone AM, Fackler JC. Association of bacterial pneumonia and respiratory failure in children with community-acquired infl uenza infection. Pediatr Crit Care Med 2011;12:e1813.

17. Ministry of Health. Immunisation Handbook 2011. Wellington: Ministry of Health 2011.

18. Van den Bruel A, Aertgeerts B, Bruyninckx R, et al. Signs and symptoms for diagnosis of serious infections in children: a prospective study in primary care. Br J Gen Pract 2007;57:53846.

19. Van den Bruel A, Haj-Hassan T, Thompson M, et al. Diagnostic value of clinical features at presentation to identify serious infection in children in developed countries: a systematic review. Lancet 2010;375:83445.

20. Willmot EJ, Lawton BA, Rose SB, et al. Exploring knowledge of prescription charges: a cross-sectional survey of pharmacists and the community. N Z Med J 2009;122:1924.

21. OReilly D, ODowd T, Galway KJ, et al. Consultation charges in Ireland deter a large proportion of patients from seeing the GP: results of a cross-sectional survey. Eur J Gen Pract 2007;13:2316.

22. Doran E, Robertson J, Rolfe I, et al. Patient co-payments and use of prescription medicines. Aust N Z J Public Health 2004;28:627.

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doi: 10.1136/archdischild-2011-3006042011

2012 97: 21-27 originally published online November 18,Arch Dis Child

CC Grant, A Harnden, D Mant, et al.

primary care?pneumonia not receive antibiotics in Why do children hospitalised with

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