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Development of a Patient-Reported Outcome Measure

for Children With Streptococcal Pharyngitis

WHAT’S KNOWN ON THIS SUBJECT: There are no validated methods of measuring symptom resolution in children with streptococcal pharyngitis. A validated symptom scale would provide researchers with a tool for measuring and comparing treatment response.

WHAT THIS STUDY ADDS: We developed a patient-reported outcome measure for assessing symptoms of streptococcal pharyngitis (Strep-PRO) from the child’s point of view and present data on its validity and responsiveness.

abstract

OBJECTIVE:The objective of this study was to develop a patient-reported outcome measure (Strep-PRO) for assessing symptoms of group A Streptococcus (GAS) pharyngitis from the child’s point of view and to present preliminary data on its internal reliability, construct validity, and responsiveness.

METHODS:We selected 8 symptoms for inclusion in the Strep-PRO. We used the Strep-PRO to assess improvement in children who were aged 5 to 15 years and had confirmed GAS pharyngitis. Children completed the scale at study visits and as a diary at home. To evaluate internal reliability, we examined correlations between the items on the scale. To evaluate construct validity, we examined the correlation at entry be-tween Strep-PRO scores and scores on other, previously validated mea-sures of pain and functional status. To evaluate responsiveness, we examined the change in score from enrollment to follow-up. The cor-relation between the Strep-PRO score and parental assessment of symptoms was also evaluated.

RESULTS:A total of 131 children were enrolled; 113 returned com-pleted diaries. The internal reliability of the scale was high. The mag-nitude of correlations between Strep-PRO scores and other measures of pain and functional status ranged from 0.39 to 0.63. The responsive-ness of the Strep-PRO was very good. The overall level of agreement between child Strep-PRO scores and parental assessment of symp-toms was 0.57.

CONCLUSIONS:The scale seems to measure effectively both pain and overall functional status in children with GAS pharyngitis. These data support the use of Strep-PRO as a measure of outcome in future clinical trials.Pediatrics2009;124:e557–e563

AUTHORS:Nader Shaikh, MD, MPH,aJudith M. Martin,

MD,bJanet R. Casey, MD,cMichael E. Pichichero, MD,c

Ellen R. Wald, MD,dD. Kathleen Colborn, BS,aMichael A.

Gerber, MD,eDiana H. Kearney, RN, CCRC,aTracy L.

Balentine, RN,aMary Ann Haralam, CRNP,aand Alejandro

Hoberman, MDa

Divisions ofaGeneral Academic Pediatrics andbPediatric Infectious Diseases, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania;cRochester General Research Institute, Pediatric Infectious Diseases, Rochester, New York;dSchool of Medicine and Public Health, University of Wisconsin, Madison, Wisconsin; andeDivision of Infectious Diseases, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio

KEY WORDS

streptococcal pharyngitis, pediatrics, patient-reported outcome, symptoms

ABBREVIATIONS

GAS— group AStreptococcus

Strep-PRO—patient-reported symptom scale for children with streptococcal pharyngitis

SRM—standardized response mean

For the research use of the Strep-PRO scale, please contact the corresponding author.

www.pediatrics.org/cgi/doi/10.1542/peds.2009-0331

doi:10.1542/peds.2009-0331

Accepted for publication Jun 3, 2009

Address correspondence to Nader Shaikh, MD, MPH, Children’s Hospital of Pittsburgh, General Academic Pediatrics, 3705 Fifth Ave, Pittsburgh, PA 15213-2583. E-mail: nader.shaikh@chp.edu

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright © 2009 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE:The authors have indicated they have no financial relationships relevant to this article to disclose.

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children with pharyngitis caused by group AStreptococcus(GAS). The ex-tent and rapidity with which antimicro-bial therapy results in clinically mean-ingful improvements; as measured by a symptom scale, can be used as an additional measure of efficacy in clini-cal trials. Use of a symptom sclini-cale could also facilitate comparisons within and between trials.1Finally, the

US Food and Drug Administration has recommended that “patient-reported outcomes” be included in efficacy trials.2

Previous research has shown that chil-drenⱖ5 years of age can reliably re-port on their symptoms.3Obtaining

in-formation about symptoms directly from the patient rather than from a proxy may provide more insight into treatment effects. This is especially true for school-aged children because they spend most of their day away from their parents. There are no ade-quately validated symptom scales that can be used to reliably measure re-covery in children with streptococcal pharyngitis on a day-to-day basis. The goals of this study were to develop and evaluate a patient-reported symptom scale (Strep-PRO) for children with streptococcal pharyngitis that would enable clinicians and researchers to document more accurately improve-ment in symptoms during treatimprove-ment.

METHODS

Conceptual Model

We developed the Strep-PRO instru-ment specifically to be used as an out-come measure rather than as a diag-nostic or progdiag-nostic tool. We focused on measuring symptoms rather than overall quality of life because mea-surement of quality of life is more prone to variability than measurement of symptoms. In addition, because an-timicrobial therapy for GAS

pharyngi-symptoms would provide a more di-rect and sensitive measure of treat-ment efficacy.

Development

We reviewed English-language, ran-domized, placebo-controlled studies that compared symptoms of children who received placebo with symptoms of children who were treated with an-tibiotics. Six pediatric studies that ex-amined 11 symptoms were reviewed. Seven symptoms clearly improved more rapidly with antibiotics as compared with placebo in ⱖ2 stud-ies: sore throat,4–9abdominal pain,5,6,8

fever,4,7,9decreased activity,5,8

head-ache,5,6,8,9pain with swallowing,5,6,8and

eating less.5,8Because the Strep-PRO is

designed to follow symptoms of chil-dren over time, these symptoms were considered suitable for inclusion in the scale.

We conducted a teleconference with 5 experts on pediatric pharyngitis (Drs Martin, Casey, Pichichero, Wald, and Gerber) to discuss which items would be appropriate for inclusion in the Strep-PRO. The expert panel recom-mended that 5 symptoms be included in the scale: sore throat, fever, eating less, headache, and decreased activity. The panel also provided input on the instructions, format, and choice of words for the scale.

Finally, to determine which symptoms children who are agedⱖ5 years and have GAS pharyngitis consider impor-tant, we interviewed 18 school-aged children with acute pharyngitis con-firmed by a positive streptococcal an-tigen test on the day of diagnosis. We asked children about the presence or absence of 23 symptoms. When the symptom was present, we asked the children to rate its severity (did not bother me⫽0, bothered me a little⫽ 1, bothered me a lot⫽2). We used the

able for inclusion in the Strep-PRO. In this method, mean “importance” for each symptom was calculated by mul-tiplying the prevalence of that symp-tom by its mean severity.10Symptoms

that were ranked lowest in importance were omitted. We also asked parents of children with streptococcal pharyn-gitis (n⫽ 30) to complete a written survey regarding the presence and se-verity of these 23 symptoms. Re-sponses were consistent when com-paring parents and children (data not shown).

On the basis of the literature review, expert teleconference, and child ques-tionnaire, we retained 8 of the 23 con-sidered items: sore throat, abdominal pain, headache, pain with swallowing, fever, eating less, playing less, and de-creased activity. The pilot version of the Strep-PRO asked about the pres-ence of these 8 symptoms during the preceding 24 hours. We used a 3-point Likert scale (none⫽0, a little⫽1, a lot⫽2) and obtained the total score by summing the scores on these 8 equally weighted questions. On the basis of our previous experience with scales in this age group, we used illustrations to facilitate completion by children.11,12

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Evaluation

We prospectively enrolled English-speaking children who were aged 5 to 15 years; had confirmed GAS pharyngitis; and presented to 1 of 4 general ambula-tory pediatric clinics, 3 in Pittsburgh and 1 in Rochester (2 suburban, 2 urban). All children who had sore throat and a pos-itive streptococcal antigen test were eli-gible for enrollment. In addition, 1 of the following 3 signs was required for inclu-sion: history of fever (⬎38.3°C), cervical lymphadenopathy, and pharyngeal ery-thema/exudate. To minimize enrollment of GAS carriers, we excluded children

whose predominant symptom was

cough or rhinorrhea and children whose symptoms had lasted ⬎72 hours. We also excluded children who had received antimicrobial treatment within 7 days before presentation and children with underlying immunodeficiency or devel-opmental delay. All children were treated with antimicrobial agents cho-sen by their respective primary care pro-viders. We conducted physical examina-tions at baseline (day 1) and at the follow-up visit (days 12–14).

Children were asked to complete the Strep-PRO at the enrollment and

follow-up visits. In addition, for the first 7 days after enrollment, we asked children to complete the Strep-PRO twice daily (at the time of the morning and evening medication administration), with their parents help if needed. We called parents on the day after enrollment to assess change in their child’s overall clini-cal status. We asked parents to rate whether, on the morning of day 2 compared with the time of enroll-ment, their child was “a lot better,” “a bit better,” “the same,” “a bit worse,” or “a lot worse.”

FIGURE 1

Strep-PRO scale. (Copyright 2008, University of Pittsburgh, All Rights Reserved.)

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visits:

● Faces pain scale: This scale consists of 6 faces representing the spec-trum from no pain to severe pain.13

The scale has been used in children 4 to 16 years of age and is scored from 0 (no pain) to 10 (severe pain).

● Functional Status Questionnaire IIR14:

This is a 14-item scale that measures overall health status in children 0 to 16 years of age. The questionnaire asks parents about the presence or absence of key behaviors during the preceding 2-week period. Higher scores indicate more favorable sta-tus. For this study, we modified the questionnaire to ask only about the preceding day while leaving un-changed the wording, sequence, and number of questions. Parents were asked to complete the scale at both study visits.

● Parent symptom questionnaire: Par-ents independently completed a symptom questionnaire at each study visit and as a twice-daily diary. Par-ents were asked to complete their as-sessments before helping their child with the Strep-PRO. The parent ques-tionnaire included the same symp-toms as the Strep-PRO; however, the 2 scales differed in 2 respects: (1) the parent questionnaire did not use illus-trations; and (2) the parent question-naire had a range of 0 to 16 as com-pared with the Strep-PRO, which had a range from 0 to 19 (because of the different response options used in the 2 scales).

● Investigator assessment of severity: Investigators (the physician or nurse practitioner who obtained the history and conducted the examina-tion) rated the severity of symptoms at presentation by placing a vertical mark corresponding to symptom severity on a 10-cm visual analog scale anchored at very mild at 1 side

tance from 1 end using a ruler.

The institutional review boards at the University of Pittsburgh and the Uni-versity of Rochester approved this study.

Analysis

To determine whether items on the scale relate to the same construct, we computed inter-item correlations and the overall Cronbach’s␣for the scale. Only the first visit for each child was used for this analysis. In general, a scale with inter-item correlations of

ⱖ0.2 and a Cronbach’s␣value ofⱖ0.7 is considered to have good internal re-liability. In addition, to explore how items could be grouped, we conducted a principal components factor analy-sis by using varimax rotation. In factor analysis, the number of factors with an eigenvalue of⬎1.0 is an indication of the number of constructs that the scale is measuring. Because the symp-toms of pharyngitis evolve rapidly dur-ing the first few days of therapy, we did not assess the test–retest reliability of the scale.

To estimate cross-sectional construct validity, we examined the correlation between Strep-PRO scores and scores on reference measures at the enroll-ment visit. To determine longitudinal

construct validity, we compared

changes in Strep-PRO scores (from day 1 to days 12–14) with changes in scores on reference measures.15

To evaluate responsiveness (ie, the ability of the instrument’s scores to change in conjunction with changes in clinical status), we examined the change in Strep-PRO scores from base-line (day 1) to the follow-up visit (days 12–14). Generally, an instrument is considered responsive when the mean change in scores is large relative to the scores’ variability. We calculated

the standardized response mean

(SRM) by dividing the magnitude of the mean change in score by the SD of the change. An SRM of⬎0.5 usually indi-cates good responsiveness.15–17 With

regard to missing data, we computed a total score only when all of items on the Strep-PRO were completed; incom-plete scales were not included in the analysis.

RESULTS

We enrolled 131 children (71 from Pittsburgh, 60 from Rochester), 113 of whom completed follow-up. There were few missing data: only 8 Strep-PRO forms hadⱖ1 missing item. Mean age was 8.5 years (SD: 2.6). The demo-graphic and clinical characteristics of the children are shown in Table 1. The

Characteristic Children

(N⫽131),

n(%)

Age at entry, y

5–10 85 (65)

10–15 46 (35)

Gender

Male 58 (44)

Female 73 (56)

Race

White 100 (76)

Black 27 (21)

Other 4 (4)

Ethnicity

Hispanic 9 (7)

Non-Hispanic 122 (93)

Maternal Education

Less than high school 2 (2)

High school graduate/GED 20 (15)

Some college 34 (26)

College graduate 69 (53)

Unknown 6 (5)

History of tonsillectomy

Yes 8 (6)

No 123 (94)

Symptoms at presentationa

Sore throat 122 (95)

Abdominal pain 56 (44)

Headache 78 (61)

Pain on swallowing 117 (91)

Fever 78 (61)

Eating Less 100 (78)

Playing less 97 (76)

Tired 119 (93)

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mean Strep-PRO scores at entry or follow-up did not differ significantly by age, race, ethnicity, gender, maternal education, or practice location (rural versus urban, or Rochester versus Pittsburgh).

Reliability

Item-total correlation was ⬎0.2, and Cronbach’s␣was 0.72, indicating that the scale has good internal reliability despite its short length and despite the heterogeneous study population. In general, factor analysis supported the appropriateness of using total rather than subscale scores. Two items on the scale—sore throat and difficulty swallowing—were highly correlated (r ⫽ 0.67) and loaded onto a second factor (eigenvalue of 1.2), suggesting that, in addition to the total score, a subscore that con-sisted of only these 2 items can be used to follow the severity of pharyn-geal symptoms.

Construct Validity

The magnitude of correlations be-tween the Strep-PRO and reference measures on the day of enrollment ranged in the expected directions from 0.39 to 0.63 (Table 2). The correlation between changes in the child Strep-PRO scores and parental assessment of symptoms was high (0.64).

Responsiveness

Mean (SD) Strep-PRO scores at entry and follow-up were 9.3 (3.7) and 1.7 (3.1), respectively. The improvement in symptoms occurred mostly on days 2 through 4, after which time symptom scores plateaued (Fig 2). Table 3 shows the change in score from day 1 to days 12 to 14 and responsiveness for each item on the Strep-PRO. Note that responsiveness for the scale as whole was better than any of the indi-vidual questions and that the item “belly hurt” had a suboptimal SRM (⬍0.5).

Minimal Clinically Important Difference

Among the 25 children who were con-sidered “a bit better” by their parents

on the second day of therapy, Strep-PRO scores decreased by a mean of 6.0 points. This can be used as an estimate for the minimal important difference. 0

1 2 3 4 5 6 7 8 9 10

Entry D1-PM D2-AM D2-PM D3-AM D3-PM D4-PM D5-PM D6-PM D7-PM F/U

Time

Sy

m

pt

om

s

cor

e

FIGURE 2

Day-to-day change in mean Strep-PRO score in 113 children who had GAS pharyngitis and received antimicrobial therapy from entry (day 1) to follow-up (F/U) (days 12–14).

TABLE 2 Magnitude of Correlations Between Strep-PRO Scores and Scores on Reference Measures at the Time of Enrollment and Between Changes in Strep-PRO Scores From Day 1 to Days 12 to 14 and Changes in Scores on Those Reference Measures in That Interval

Reference Measure Correlations

Strep-PRO Scores and Reference Measure

Scores (Day 1)

Changes in Strep-PRO Scores and Changes

in Reference Measure Scores (Day

1 to Days 12–14)

Child pain assessment (Faces pain scale) 0.63 0.65

Parent assessment of functional status (functional status scale)

0.45 0.49

Parent’s symptom score 0.57 0.64

Investigator assessment of severity 0.39 0.45

TABLE 3 Responsiveness of Individual Items and Total Score on Strep-PRO

Parameter Change (SD) in Score

From Enrollment to Follow-up Visitsa

Responsiveness, SRM

Throat hurt ⫺1.61 (1.01) 1.59

Belly hurt ⫺0.41 (1.00) 0.41

Head hurt ⫺0.65 (1.05) 0.62

Hurt to swallow ⫺1.85 (1.20) 1.54

Fever ⫺0.44 (0.53) 0.83

Eating less ⫺0.91 (0.86) 1.05

Playing less ⫺0.95 (0.82) 1.16

More tired ⫺0.91 (0.83) 1.09

Strep-PRO total score ⫺7.73 (4.30) 1.80

aBased on children with completed scales at enrollment and follow-up.

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results need to be confirmed in future studies.

Resolution

A total of 52% and 89% of children were “back to normal” by the morning of day 3 and by evening of day 6, respectively. The mean⫾SD Strep-PRO score at the time when parents reported that their children were “back to normal” was 2.4⫾2.5. This score may be used in the analysis of time to symptom resolution in future studies.

DISCUSSION

This study shows that children who are aged 5 to 15 years and have GAS phar-yngitis can reliably report on their symptoms by completing a symptom scale. We provide data on the reliabil-ity, validreliabil-ity, and responsiveness of the Strep-PRO scale. The Strep-PRO seems to effectively measure both pain and overall functional status and promises to be a useful outcome measure in clin-ical studies of GAS pharyngitis. Change in Strep-PRO scores could be used as a measure of symptom improvement or deterioration. On the basis of findings of this study, we have modified the Strep-PRO by removing from the scale the question about abdominal pain (Fig 1).

It is important to note that our results do not suggest using the Strep-PRO score alone for determining the sever-ity of the illness or for managing indi-vidual cases. Rather, we propose 2 ways to use Strep-PRO scores. In the first approach, time to achievement of a specified score (eg, Strep-PRO score of 2.4, representing resolution) could

be compared between treatment

points (which was endorsed by pa-tients as an important degree of im-provement) could be compared be-tween treatment groups at one or more designated time points.18–20 If a

researcher is particularly interested in the effect of treatment on throat pain, then examination of the 2-item subscale score, in addition to the over-all score, would be appropriate.

Although the correlation between the Strep-PRO and other scales is consid-erable, the Strep-PRO is the only scale to date designed specifically for follow-ing symptoms of children with GAS pharyngitis. As such, it is likely to be more responsive to change in clinical status than generic scales (eg, func-tional status, Faces pain scale).

Although there are convincing data documenting the more rapid clinical improvement of children with GAS pharyngitis who are treated with anti-biotics improve faster than those treated with placebo,4–9no antibiotic

has the relief of symptoms as the basis of its approval. Rather, the focus of Food and Drug Administration drug ap-proval has been on the eradication of GAS pharyngitis and the prevention of suppurative and nonsuppurative com-plications. This may allow evaluation of an additional important outcome mea-sure: symptom improvement. The use of the Strep-PRO in future clinical trials may allow regulatory agencies to de-termine whether the magnitude of benefit, in terms of symptom relief, is large enough to serve as a basis for approval of new therapeutic agents.

This study is limited in several re-spects. Although we excluded children who were asymptomatic, whose

pri-lasted⬎72 hours, a small minority of study patients may still have been car-riers of GAS. In addition, different eval-uators may have conducted the initial and follow-up examinations. This, how-ever, should not affect the validity of the main analysis in which we com-pared the investigator’s assessments of severity with the child’s reported symptoms on the same day. Finally, in this study, we evaluated the validity and feasibility of 1 method of adminis-tration of the Strep-PRO. Future stud-ies will be needed to determine whether other methods of administra-tion of the Strep-PRO (eg, an electronic diary, without parental involvement) are equally feasible and valid.

CONCLUSIONS

This study provides data on the validity and responsiveness of the Strep-PRO. We have shown that Strep-PRO scores correlate with measures of functional status and pain and with parental as-sessment of symptoms. These results support future use of the Strep-PRO as a measure of outcome in clinical stud-ies of children who are aged 5 to 15 years and have GAS pharyngitis.

ACKNOWLEDGMENTS

This research was made possible through a grant from Replidyne, Inc.

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8. Pichichero ME, Disney FA, Talpey WB, et al. Adverse and beneficial effects of immediate treatment of group A beta-hemolytic streptococcal pharyngitis with penicillin.Pediatr Infect Dis J.1987;6(7): 635– 643

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11. Shaikh N, Hoberman A, Paradise JL, et al. Responsiveness and construct validity of a symptom scale for acute otitis media.Pediatr Infect Dis J.2009;28(1):9 –12

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13. Bieri D, Reeve RA, Champion GD, Addicoat L, Ziegler JB. The Faces pain scale for the self-assessment of the severity of pain experienced by children: development, initial validation, and preliminary investigation for ratio scale properties.Pain.1990;41(2):139 –150

14. Stein RE, Jessop DJ. Functional Status II(R): a measure of child health status.Med Care.1990; 28(11):1041–1055

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DOI: 10.1542/peds.2009-0331 originally published online September 28, 2009;

2009;124;e557

Pediatrics

Balentine, Mary Ann Haralam and Alejandro Hoberman

Wald, D. Kathleen Colborn, Michael A. Gerber, Diana H. Kearney, Tracy L.

Nader Shaikh, Judith M. Martin, Janet R. Casey, Michael E. Pichichero, Ellen R.

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DOI: 10.1542/peds.2009-0331 originally published online September 28, 2009;

2009;124;e557

Pediatrics

Balentine, Mary Ann Haralam and Alejandro Hoberman

Wald, D. Kathleen Colborn, Michael A. Gerber, Diana H. Kearney, Tracy L.

Nader Shaikh, Judith M. Martin, Janet R. Casey, Michael E. Pichichero, Ellen R.

Streptococcal Pharyngitis

Development of a Patient-Reported Outcome Measure for Children With

http://pediatrics.aappublications.org/content/124/4/e557

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Figure

FIGURE 1Strep-PRO scale. (Copyright 2008, University of Pittsburgh, All Rights Reserved.)
TABLE 1 Demographic and ClinicalCharacteristics of 131 Children WithGAS Pharyngitis
FIGURE 2Day-to-day change in mean Strep-PRO score in 113 children who had GAS pharyngitis and received

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