The Impact of Caregiver Health Literacy on Pediatric Asthma: An Integrative Review

Abstract

Importance:

There is increasing literature on the role of health literacy in asthma outcomes. Despite less than half of Americans having proficient health literacy, health literacy is an essential component in providing quality medical care.

Observations:

Most of the literature on the impact of health literacy on asthma outcomes is from the adult asthmatic population, where lower health literacy is associated with poorer asthma outcomes, including decreased quality of life, worse asthma control, and more Emergency Department visits for asthma. Although a few studies look at caregiver health literacy and pediatric asthma outcomes, the results have been congruous, demonstrating an effect across the board. Challenges exist in the evaluation of caregiver health literacy by physicians. Various tools are available to assist in the evaluation although a few are validated for asthma. There is no uniform strategy that is successful in the management of health literacy. When counseling on asthma medications, the use of a teach-back method with caregivers to ensure proper understanding of the inhaler device technique may be beneficial. Various educational materials have been demonstrated to improve the caregiver inhaler technique. Asthma action plans that incorporate picture-based written plans may be more suitable for caregivers with poor health literacy. Improving verbal and written communication as well as a physician's focus on how numerical data are presented to families may be beneficial. For verbal communication, strategies include using patient-centered language, speaking slowly, and repeating/confirming understanding of key points. A significant step forward has been an increasing focus on health literacy within asthma guidelines both in the United States and internationally. Moving forward, further research into the effects of health literacy, specifically within the pediatric asthma population, and improved means to assess and mediate that impact are required.

Conclusions and Relevance:

An appreciation of the role of health literacy is essential in providing proper asthma care.

Introduction

Health literacy is defined as “the degree to which an individual has the capacity to obtain, communicate, process and understand basic health information to make appropriate health decisions.”¹ It has been noted that in the United States (US), less than half of people have an intermediate level of health literacy and a few have proficient health literacy.^2,3 A cross-sectional nationally representative study of more than 6,100 US parents found that 28.7% had below-basic/basic health literacy, 68.4% were unable to enter names and birth dates correctly on insurance forms, 65.9% were unable to calculate the annual cost of a health insurance policy, and 46.4% were unable to perform one of two medication-related tasks.⁴ A literacy survey of US adults similarly found that almost half of adults had difficulty understanding health information or acting on it.⁵ A report on Health Literacy by the American Medical Association has found that “professional and public awareness of the health literacy issue must be increased” due to its profound impact on health outcomes.⁶ In fact, it has been stated that the impact of health literacy is a stronger predictor of health status than age, income, educational level, race, or ethnicity.³ The annual cost of poor health literacy in the US ranges from $106 billion (lower bound) to $238 billion (upper bound).⁷ In addition, if accounting in the modeling for future costs of low health literacy that result from current inaction, the present-day cost of low health literacy is in the range of $1.6 trillion to $3.6 trillion.⁷

Asthma is one of the most common chronic diseases of childhood.^8,9 The Centers for Disease Control (CDC) 2018 national data found the national current asthma prevalence among children to be 7.5%.^10,11 Of those children, 45.4% reported having one or more asthma attacks.^10,11

It has been found that lifelong complications of asthma, such as airway remodeling, begin in early childhood and are often lifelong.^8,9 In a long-term follow-up study of 1,041 school-aged children with mild to moderate asthma, 75% had abnormal patterns of lung growth and by a mean age of 26 years, and 11% met criteria for chronic obstructive pulmonary disease.⁸ As a result, addressing factors contributing to asthma outcomes is instrumental in reducing long-term and potentially irreversible complications of asthma.¹²

There is increasing literature on the role of health literacy in asthma outcomes, including asthma exacerbations. In fact, it has been recognized that health literacy is an “essential component in providing quality health care.”³ The goal of this article is to review the role of caregiver health literacy in pediatric asthma outcomes, strategies to improve health literacy among families of asthmatic children, and what remains to be done moving forward.

Methods

To complete this article, a PubMed search was conducted for articles from January 1, 1980 to March 1, 2020 by using the terms “asthma,” “pediatric,” “pediatric asthma,” and “health literacy,” with or without the term “social determinants of health.” The search was filtered with the terms “humans” and “English.” The initial search was initially limited to the relevant subject age range with the term “child: birth-18 years” but the literature in adults was also informally searched for adult outcomes as well. Reports resulting from these searches, relevant references cited in those reports, and applicable gray literature were reviewed and cited on the basis of their relevance.

Discussion/Observations

Health literacy and asthma outcomes

A review of the impact of health literacy on health outcomes outlines the steps in which caregiver health literacy plays a role in mediating pediatric health outcomes: access to care, access to health insurance, access to emergency care, adherence to care recommendations, adherence to healthy lifestyle, interpretation of health information, and proper medication use.¹³ A systematic review on caregiver health literacy and child health outcomes found that parental low health literacy is associated with poorer health outcomes, less parental health knowledge, and negative parental behaviors.¹⁴

Most of the literature on the impact of education and health literacy on asthma outcomes is derived from the adult asthmatic population, where it has been noted that lower health literacy is associated with poorer asthma outcomes, including decreased quality of life,^15,16 worse physical function,¹⁵ worse asthma control,¹⁶ and more Emergency Department (ED) visits for asthma.¹⁵ Part of this association in the adult literature has been hypothesized to be related to the technique with asthma medications, as the poor metered dose inhaler (MDI) technique has been found in up to 89% of adult asthmatics who read at a grade 3 level or below.¹⁷ It has been noted that education and health literacy (or lack thereof) may impact adherence to asthma medications, especially if the information provided is largely written.¹⁸

There are a few studies looking specifically at how caregiver health literacy impacts pediatric asthma outcomes. However, the results of the observational studies to date have been relatively congruous and demonstrated an effect of caregiver health literacy on pediatric asthma outcomes across the board. A cross-sectional study of 281 English-speaking school-aged children with asthma and their parents noted low parental health literacy to be associated with worse asthma control, both as evaluated by the health care provider (P = 0.007) and as evaluated through the asthma control questionnaire (ACQ; P = 0.013).¹⁹ A retrospective cohort of 150 children with asthma and their parents noted that, even after adjusting for asthma-related knowledge, disease severity, and medication use, children of parents with low literacy had a greater incidence of ED visits [adjusted incidence rate ratio (IRR) 1.4; 95% CI: 0.97–2.0], hospitalizations (IRR 4.6; 95% CI: 1.8–12), and days missed from school (IRR 2.8; 95% CI: 2.3–3.4).²⁰ A cross-sectional study of 351 children with asthma found that low parental numeracy was associated with an increased odds of ED or urgent care visits for asthma (aOR 1.7; 95% CI: 1.03–2.7).²¹ A single-center study of 499 school-aged children with asthma and their parents noted that low parental health literacy was independently associated with parental perception of greater asthma burden (OR 3.96; 95% CI: 2.4–6.4; P < 0.001), and increased parental worry related to asthma (OR 1.85; 95% CI: 1.2–2.8; P < 0.001) although interestingly measures of health care use such as ED visits (41.2% vs. 40.9%; P > 0.999) did not differ between the groups.²²

Limitations exist in the literature to date. A significant relationship has been noted among caregivers' health literacy level and perceived efficacy in managing their child's asthma, which could be a confounder.²³ In a study of 281 parents of school-aged asthmatic children, pediatric provider estimates of parental health literacy had low concordance with validated measures of health literacy; however, they influenced treatment recommendations and instructional practices, all of which could affect asthma outcomes.²⁴ Also, as noted in a 2012 literature review, the majority of studies on the effects of health literacy and asthma are observational, with small sample sizes, and there is little literature that incorporates objective measures of asthma control such as lung function testing.²⁵

Finally, as with all categories of determinants of health, it is hard to separate out effects of caregiver education/literacy and other health determinants such as the family's physical environment, access to health services, and race. For example, low health literacy is more prevalent among families living in poverty and among minorities.^4,19,23,26 An integrative review published this year notes low socioeconomic status (and particularly educational attainment) to be the most important determinant of health literacy.²⁷ In addition, it found that health literacy is a mediator in the relationship between socioeconomic status and health status, quality of life, health-related outcomes, health behaviors, and use of preventative services.²⁷ In a prospective longitudinal cohort of 284 adult asthmatic patients, although significant differences were noted between numeric and print health literacy and asthma adherence (P = 0.01 and P = 0.08 respectively), asthma control (P = 0.005 and P < 0.001 respectively) and quality of life (P < 0.001 for both), only quality of life (P = 0.03 and P = 0.006 respectively) and asthma control (P = 0.005 for print) were significantly associated with health literacy, after adjusting for age, sex, and race/ethnicity.¹⁶ Separating out the effects of health literacy from the myriad of the larger interplay of various social determinants of health can be challenging.

Evaluation of health literacy

One common issue in the studies to date is how to evaluate caregiver health literacy, as health literacy is limited not only to reading skills but also to listening, speaking, and numeracy skills.²⁵ In fact, a recent conceptual model of health literacy developed through the Health Literacy Survey-Europe consortium includes 12 dimensions: four competency levels that evaluate accessing, understanding, appraising, and applying health information in the three domains of health care, disease prevention, and health promotion.²⁸ Although there are various validated instruments to assess health literacy, predominantly in the research setting, no one test measures all the component skills necessary for a full evaluation of health literacy.²⁵ Some caregiver behaviors that may indicate low health literacy in the absence of screening include missed appointments, excuses for not filling out medical forms or asking assistance to fill out such forms, filling out forms incompletely, and answering yes to all questions on a form.²⁵ However, none of these behaviors is sensitive or specific for health literacy and cannot be used diagnostically.

Challenges exist in the subjective evaluation of caregiver health literacy by physicians. Studies have noted a poor correlation between physician perception and caregivers' actual health literacy level, with both overestimation and underestimation of caregiver health literacy noted.²⁹ When medical residents were asked to estimate the health literacy of 182 adult patients, they identified 10% with poor health literacy whereas in fact 36% of these adults failed the literacy screen.³⁰ Part of the discrepancy between perceived and actual caregiver health literacy from the perspective of physicians may be reliance on incorrect measures, such as educational level or patients' assessment of health literacy, both of which have been shown to be unreliable.⁶ In addition, caregivers are often hesitant to reveal poor health literacy and/or are unreliable in assessing their own level of health literacy.³¹ It is common for caregivers to feel shame about their degree of health literacy, and in fact a study of 202 adults noted that of those with low functional health literacy, 67.2% had never told their spouses and 53.4% had never told their children.³¹ Physicians' subjective assessment of caregiver health literacy in the absence of a standardized tool has potential consequences if misestimated, as physician-perceived differences have been shown to impact asthma prescription patterns³² and treatment recommendations.^33,34

Various tools are available to assist in the evaluation of caregiver health literacy, although most are predominantly used in a research setting and a few are validated specifically in the context of asthma (Table 1).^35,36 One such example is the Rapid Estimate of Adult Literacy in Medicine (REALM), which takes 2–3 min to complete.^37,38 However, it has been noted that the REALM does not evaluate sight-reading or reading comprehension, and it does not “completely include the components of health literacy, particularly those specific to patients with asthma.”³⁹ Another rapid scale is the Brief Health Literacy Screen, which can be completed in 1 min time.⁴⁰ The Asthma Numeracy Questionnaire (ANQ) and the mini-Asthma Quality of Life Questionnaire (miniAQLQ) are the available questionnaires that are specific to asthma.⁴¹

Table 1.

Tools to Assist in the Measure of Health Literacy

Name	Description	Specific to asthma
ANQ⁴¹	Four-item questionnaire of numerical concepts adapted from standard asthma education scored based on number of correct answers	Yes
miniAQLQ⁴¹	Fifteen-item questionnaire in 4 domains of symptoms, activity limitation, emotional function, and environmental stimuli that are graded on a scale of 1–7	Yes
BHLS⁴⁰	Three items on a 5-point response scale: How confident are you in filling out medical forms? How often do you have someone help you read hospital materials? How often do you have problems learning about your health condition because of difficulty understanding written information?	No
REALM³⁷	Instrument of health words in increasing order of difficulty, which are said out loud. Scored based on number of incorrect pronunciations or skipped words, which are subtracted from the total number of words for the final score.	No
REALM-Teen³⁸	Same as REALM but validated in adolescents.	No

ANQ, Asthma Numeracy Questionnaire; miniAQLQ, mini-Asthma Quality of Life Questionnaire; BHLS, Brief Health Literacy Screen; REALM, Rapid Estimate of Adult Literacy in Medicine; S-TOFHLA, short Test of Functional Health Literacy in Adults.

Thus far, the use of standardized models has been limited largely to adult caregivers; a few studies have looked specifically at assessing or incorporating the child's health literacy, or the impact of childhood health literacy on asthma outcomes.³⁹ A systematic review on health literacy in children with asthma noted that although a few instruments are available to assess health literacy in children, they are “unsatisfactory and did not completely include the components of health literacy, particularly those specific to patients with asthma.”³⁹

In addition to the absence of a standardized tool, specifically in the context of asthma, there is a controversy over whether to screen for caregiver health literacy at all. It has been argued that as many caregivers with low health literacy are either ashamed and/or unaware of their level of literacy, as tests used to measure health literacy are not validated and can be time consuming, and as there is no evidence that the act of screening alone improves health outcomes, health professionals may be better served to assume that all families have low health literacy.²⁵ Open-ended questions, such as “are you satisfied with how well you read” may be helpful, but they could be of low yield in the context of shame.²⁵ If any evaluation is done, it is noted that it should always be done in a confidential and highly supportive environment.²⁵

Alleviating the impact of health literacy

There is no one uniform strategy that is successful in the management of caregiver health literacy (Table 2). An integrative approach may be necessary, looking at specific areas of asthma care and ways to optimize communication and understanding.

Table 2.

Means to Ameliorate Health Literacy^{44–47,49–52,55,}⁵⁶

Use of inhaler devices	“Teach back” method
	Educational supplements such as illustrated simplified leaflets
	Inhaler instructional videos
Asthma action plans	Incorporate language at below a grade 6 level
Asthma action plans	Incorporate pictograms and picture-based written plans
Physician communication	Use patient-centered language
	Speak slowly
	Include pictures
	Repeat/confirm understanding
	Avoid medical words
	Limit information to 3 points or less
	Include bi-directional conversation
	Include clear form of written instruction
Addressing broader social determinants of health	Take steps to mitigate broader social determinants such as school-based asthma programs

Use of inhaler devices

It has been argued that although different spacers improve drug delivery, “differences in efficacy become trivial, or even disappear, when the device is used with the proper inhalation technique.”³ Among the general population of asthmatics, inhaler technique is often poor.⁴² When counseling caregivers on asthma medications, use of the “teach back method” is essential to ensure proper understanding of inhaler device use, and a shared decision-making approach may improve the inhaler technique.^3,43 Various educational materials as supplements have been demonstrated in small trials to improve inhaler technique, especially in patients and caregivers with low health literacy. A recent study found that an illustrated, simplified leaflet on correct MDI technique significantly improved correct technique in low-literacy asthmatic patients.⁴⁴ A study of children with asthma demonstrated that a 3-min MDI video resulted in an immediate improvement in technique postintervention.⁴⁵

Asthma action plans

Although asthma action plans are recommended, studies have found that most are written at above a level that is suitable for families with poor health literacy. A study of 30 asthma action plans in the US (27 state Department of Health-endorsed, 3 national action plans endorsed by 6 states) found that 70.0% were written at above a grade 6 level.⁴⁶ It has been noted that the action plans written by the American Academy of Allergy, Asthma and Immunology (AAAAI) are written “well above” the grade 6 level.³

Two recent asthma action plans have been developed more recently that incorporate pictograms and picture-based written plans that may be more suitable for caregivers with poor health literacy. A randomized controlled study of parents of 217 children with asthma noted that caregivers randomized to the pictogram- and photograph-based low-literacy written asthma action plan (WAAP) were less likely to make an error in knowledge about everyday asthma medications (P = 0.03) and less likely to make an error regarding spacer use (P < 0.001) compared with use of the AAAAI action plan.⁴⁷ It was also shown that when 119 physicians at 2 academic centers were randomized to the same low-literacy WAAP or AAAAI action plan, those randomized to the low-literacy WAAAP were more likely to use the times of day recommendation (P < 0.001), recommended spacer use (P < 0.001), and addressed the need for daily medications when sick (P < 0.001) compared with those randomized to the standard action plan.⁴⁸ Another similar asthma action plan, the asthma-related picture-based medication plan (PBMP) written at a fourth grade level has been evaluated for feasibility by assessing caregiver attitudes to the PBMP at an urban pediatric clinic.⁴⁹ It was noted that a high proportion of low-literate parents of asthmatic children consistently endorsed the PBMP as being a useful educational tool for asthma medications.⁴⁹

Physician communication strategies

Various strategies have been proposed to combat caregiver health literacy, based on improving verbal and written communication as well as a physician focus on how numerical data are presented to children and their families. For optimizing verbal communication, strategies include using patient-centered language, speaking slowly, including pictures in the verbal communication, and repeating/confirming understanding of key points.^13,50 For written communication, strategies include using materials that are at no higher than grade 5–6 level, using short written sentences with words that are two syllables or less, and bolding key words.¹³ No matter what the form of communication, avoiding medical words, limiting key information to 3 points or less, focusing on patient/caregiver participation, using a “teach back” method to confirm understanding, and including a clear form of written instruction have been suggested.^13,51 If English language is a barrier, the use of proper interpretation services has been recommended, and it has been shown to improve asthma outcomes.³ Use of different forms of communication, such as written, verbal, and video communication, may improve caregiver knowledge. A recent study of parents presenting to the ED with an asthmatic child due to an asthma exacerbation noted that both written materials and video interventions resulted in an improvement in asthma knowledge in low-literacy parents.⁵²

Addressing broader social determinants of health

Consistent, culturally appropriate care is required broadly to understand how various determinants contribute to asthma morbidity and prevalence within the US.⁵³ At the neighborhood level, steps can be taken to help mitigate the effects of broader familial determinants of health, including income/social status, physical environment, access to health services, and race/ethnicity.^54,55 However, some determinants may be easier to mitigate than others. Focus within the school allows the opportunity to mitigate several familial determinants, including physical environment (with integrated pest measures), health literacy, access to care, and poverty through interventions such as provision of medications, prioritization to children at higher risk, and school-based educational programs.^56,57 Within the community, trials have also evaluated the role of community clinics, demonstrating that team-based approaches that involve community health workers and a focus on continuous quality improvement can significantly improve asthma outcomes in school-aged children.⁵⁸

Health literacy and health policy

A significant step forward has been an increasing focus on overall health literacy within the asthma guidelines both within the US and internationally. A key change to the National Asthma Education and Prevention Program Expert Panel Report 3 (EPR3) guideline was the inclusion of the role of health literacy in asthma.⁵⁹ The EPR3 guideline recommends tailoring education to the literacy level of the patient, and developing an active partnership with the family that considers their health literacy needs. In addition, it recommends a variety of educational strategies (individual instruction, written materials at a 5th grade reading level or below, group programs, video/audiotapes, or internet programs) as a means of addressing various levels of health literacy among asthmatic families.

The Global Initiative for Asthma (GINA) 2019 report includes as a key point that the patients' health literacy should be taken into account with respect to the patient-health professional partnership.⁶⁰ The GINA includes specific instructions about how to reduce the impact of low health literacy, including ordering information from most to least important, speaking slowly with simple words, simplifying numerical concepts, using illustrations as an adjunct, including a teach-back method, and repeating main messages. The GINA also includes, as a modifiable risk factor to reduce exacerbations, ensuring that patients have an asthma action plan that is appropriate for their level of health literacy.

Federally, the US Department of Health and Human Services has worked with more than 700 public and private sector partners in the development of a National Action Plan to Improve Health Literacy.⁶¹ It is based on the broad goal that all families have the right to information about their health that allows them to participate in health decisions, and that health services should be provided in a way that is not just beneficial but also understandable. Recommendations include simplifying written material, improving providers' communication skills, and improving self-management skills.

There has been a broader call to action to focus on health literacy within the US. It has been argued that to combat health literacy within public policy, the following steps should be taken: incentivizing health insurers to identify and address health literacy problems, building costs into public and private health insurance payment systems associated with adapting health care to recognize and promote literacy, increasing funding for research into health interventions to improve health literacy, creating centers of excellence to promote the study of health literacy and adoption of best practices related to it, and finally including health literacy skills as a component of medical training programs.⁷ As noted, “it is fair to suggest that low health literacy exacts enormous costs on both the health system and society, and that current expenditures could be far better directed through a commitment to improving health literacy.”⁷

Conclusion and next steps

Although most of the literature on the impact of health literacy on asthma outcomes is derived from the adult population, there is relative consistency in the observational studies to date that poor caregiver health literacy impacts pediatric asthma outcomes, including asthma exacerbations, asthma medication use, ED visits, days missed from school, and increased parental worry related to asthma and asthma burden. As the majority of the literature on asthma outcomes and health literacy has been observational and of small sample sizes, larger scale population studies on the impact of health literacy on asthma are required. Ideally, some of these studies in the pediatric/adolescent population would incorporate objective measures of lung function such as spirometry. Adjusting for the effects of other social determinants of health, as much as possible, may help further delineate the impact of health literacy specifically.

Challenges exist to date in the evaluation of caregiver health literacy, as physicians' subjective evaluation of health literacy does not correlate with objective measures. There is controversy on whether to evaluate health literacy at all. Culturally sensitive and expedient measures to evaluate health literacy are required. Alleviating health literacy focuses on clear communication, “teach back” methods, repeating steps, and using a multi-media approach at a grade 5 level or below. Validation of an asthma action plan that is more suitable to caregivers with poor health literacy is required.

There is increasing incorporation of health literacy into guidelines, although there is a broader call to action to focus on health literacy within the US. This year, a protocol for a systematic review on how to improve health literacy with asthma⁶² may help inform research priorities in the future.

Poor caregiver health literacy has a tremendous impact on the lives of children with asthma and their families. A focus on ameliorating this impact, as much as possible, will improve the lives of children with asthma moving forward.

Footnotes

Acknowledgments

This narrative review was completed as a master's thesis (Capstone) for the Johns Hopkins Bloomberg School of Public Health MPH program. The author wishes to thank Dr Corinne Keet for her mentorship.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

References

Ratzan. SC, Parker RM. Introduction. In: Selden CR, Zorn M, Ratzan SC, Parker RM, eds. National Library of Medicine current bibliographies in medicine: Health literacy. NLM Pub. No. CBM 2000. Bethesday, MD: National Institutes of Health, 2000, pp. v–vi.

Weiss

BD.

Health literacy and patient safety: help patients understand. A manual for clinicans, 2nd ed. Chicago, IL: American Medical Association Foundation, American Medical Association, 2007. [Internet]. Available from: www.pogoe.org/sites/default/files/Health Literacy - Reducing the Risk by Designing a Safe, Shame-Free Health Care Environment.pdf

Myers

, Murray

. Overcoming health literacy barriers to improve Asthma inhaler therapy adherence. Ann Am Thorac Soc, 2019; 16:182–186.

Yin

, Johnson

, Mendelsohn

, et al. The health literacy of parents in the United States: a nationally representative study. Pediatrics, 2009; 124 Suppl:S289–S298.

Kirsch

IS.

Adult literacy in America: A first look at the results of the National Adult Literacy Survey. Washington, DC: Office of Educational Research and Improvement, U.S. Dept. of Education; 1993. Educational Testing Service & National Center for Educa [Internet]. Available from: https://nces.ed.gov/pubsearch/pubsinfo.asp?pubid=93275

Health literacy: report of the Council on Scientific Affairs. Ad Hoc Committee on Health Literacy for the Council on Scientific Affairs, American Medical Association. JAMA, 1999; 281:552–557.

Policy Document: Health Literacy and Policy [Internet]. Available from: https://publichealth.gwu.edu/departments/healthpolicy/CHPR/downloads/LowHealthLiteracyReport10_4_07.pdf

McGeachie

, Yates

, Zhou

, et al. Patterns of Growth and Decline in Lung Function in Persistent Childhood Asthma. N Engl J Med, 2016; 374:1842–1852.

Saglani

, Payne

, Zhu

, et al. Early detection of airway wall remodeling and eosinophilic inflammation in preschool wheezers. Am J Respir Crit Care Med, 2007; 176:858–864.

10.

CDC National Asthma Data [Internet]. [cited 2020 Jun 5]. Available from: www.cdc.gov/asthma/most_recent_national_asthma_data.htm

11.

Centers for Disease Control and Prevention. Vital Signs: Asthma in Children—United States, 2001–2016. Morb Mortal Wkly Rep, 2018; 67:149–155.

12.

Abrams

, Szefler

, Becker

. Does inhaled steroid therapy help emerging asthma in early childhood?. Lancet Respir Med, 2017; 5:827–834.

13.

Hersh

, Salzman

, Snyderman

. Health literacy in primary care practice. Am Fam Physician, 2015; 92:118–124.

14.

DeWalt

, Hink

. Health literacy and child health outcomes: a systematic review of the literature. Pediatrics, 2009; 124 Suppl:S265–S274.

15.

Mancuso

, Rincon

. Impact of health literacy on longitudinal asthma outcomes. J Gen Intern Med, 2006; 21:813–817.

16.

Apter

, Wan

, Reisine

, et al. The association of health literacy with adherence and outcomes in moderate-severe asthma. J Allergy Clin Immunol, 2013; 132:321–327.

17.

Williams

, Baker

, Honig

, et al. Inadequate literacy is a barrier to asthma knowledge and self-care. Chest, 1998; 114:1008–1015.

18.

David

. Preventive therapy for asthmatic children under Florida Medicaid: changes during the 1990s. J Asthma, 2004; 41:655–661.

19.

Harrington

, Zhang

, Magruder

, et al. The Impact of Parent's Health Literacy on Pediatric Asthma Outcomes. Pediatr Allergy Immunol Pulmonol, 2015; 28:20–26.

20.

DeWalt

, Dilling

, Rosenthal

, et al. Low parental literacy is associated with worse asthma care measures in children. Ambul Pediatr, 2007; 7:25–31.

21.

Rosas-Salazar

, Ramratnam

, Brehm

, et al. Parental numeracy and asthma exacerbations in Puerto Rican children. Chest, 2013; 144:92–98.

22.

Shone

, Conn

, Sanders

, et al. The role of parent health literacy among urban children with persistent asthma. Patient Educ Couns, 2009; 75:368–375.

23.

Wood

, Price

, Dake

, et al. African American parents'/guardians' health literacy and self-efficacy and their child's level of asthma control. J Pediatr Nurs, 2010; 25:418–427.

24.

Harrington

, Haven

, Bailey

, et al. Provider perceptions of parent health literacy and effect on asthma treatment recommendations and instructions. Pediatr Allergy Immunol Pulmonol, 2013; 26:69–75.

25.

Rosas-Salazar

, Apter

, Canino

, et al. Health literacy and asthma. J Allergy Clin Immunol, 2012; 129:935–942.

26.

Kutner

, Greenberg

, Jin

, et al. The Health Literacy of America's Adults: results from the 2003 National Assessment of Adult Literacy. [Internet]. Available from: https://nces.ed.gov/pubs2006/2006483.pdf

27.

Stormacq

, Van den Broucke

, Wosinski

. Does health literacy mediate the relationship between socioeconomic status and health disparities? Integrative review. Health Promot Int, 2019; 34:e1–e17.

28.

Sorensen

, Van den Broucke

, Fullam

, et al. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health, 2012; 12:80.

29.

Wittich

, Mangan

, Grad

, et al. Pediatric asthma: caregiver health literacy and the clinician's perception. J Asthma, 2007; 44:51–55.

30.

Bass

PF 3rd

, Wilson

, Griffith

, et al. Residents' ability to identify patients with poor literacy skills. Acad Med, 2002; 77:1039–1041.

31.

Parikh

, Parker

, Nurss

, et al. Shame and health literacy: the unspoken connection. Patient Educ Couns, 1996; 27:33–39.

32.

Mendenhall

, Tsien

. Evaluation of physician and patient compliance with the use of peak flow meters in commercial insurance and Oregon health plan asthmatic populations. Ann Allergy Asthma Immunol, 2000; 84:523–527.

33.

Warman

, Silver

, McCourt

, et al. How does home management of asthma exacerbations by parents of inner-city children differ from NHLBI guideline recommendations? National Heart, Lung, and Blood Institute. Pediatrics, 1999; 103:422–427.

34.

McDermott

, Silva

, Rydman

, et al. Practice variations in treating urban minority asthmatics in Chicago. J Med Syst, 1996; 20:255–266.

35.

Parker

, Baker

, Williams

, et al. The test of functional health literacy in adults: a new instrument for measuring patients' literacy skills. J Gen Intern Med, 1995; 10:537–541.

36.

Baker

, Williams

, Parker

, et al. Development of a brief test to measure functional health literacy. Patient Educ Couns, 1999; 38:33–42.

37.

Davis

, Long

, Jackson

, et al. Rapid estimate of adult literacy in medicine: a shortened screening instrument. Fam Med, 1993; 25:391–395.

38.

Davis

, Wolf

, Arnold

, et al. Development and validation of the Rapid Estimate of Adolescent Literacy in Medicine (REALM-Teen): a tool to screen adolescents for below-grade reading in health care settings. Pediatrics, 2006; 118:e1707–e1714.

39.

Tzeng

Y-F

, Chiang

B-L

, Chen

Y-H

, et al. Health literacy in children with asthma: a systematic review. Pediatr Neonatol, 2018; 59:429–438.

40.

Wallston

, Cawthon

, McNaughton

, et al. Psychometric properties of the brief health literacy screen in clinical practice. J Gen Intern Med, 2014; 29:119–126.

41.

Apter

, Wang

, Bogen

, et al. Linking numeracy and asthma-related quality of life. Patient Educ Couns, 2009; 75:386–391.

42.

Gillette

, Rockich-Winston

, Kuhn

, et al. Inhaler Technique in Children With Asthma: a systematic review. Acad Pediatr, 2016; 16:605–615.

43.

Scichilone

. Asthma control: the right inhaler for the right patient. Adv Ther, 2015; 32:285–292.

44.

Wrench

, Van Dyk

, Srinivas

, et al. Outcome of illustrated information leaflet on correct usage of asthma-metered dose inhaler. Afr J Prim Heal Care Fam Med, 2019; 11:e1–e9.

45.

Carpenter

, Lee

, Blalock

, et al. Using videos to teach children inhaler technique: a pilot randomized controlled trial. J Asthma, 2015; 52:81–87.

46.

Yin

, Gupta

, Tomopoulos

, et al. Readability, suitability, and characteristics of asthma action plans: examination of factors that may impair understanding. Pediatrics, 2013; 131:e116–e126.

47.

Yin

, Gupta

, Mendelsohn

, et al. Use of a low-literacy written action plan to improve parent understanding of pediatric asthma management: a randomized controlled study. J Asthma, 2017; 54:919–929.

48.

Yin

, Gupta

, Tomopoulos

, et al. A Low-Literacy Asthma Action Plan to Improve Provider Asthma Counseling: a randomized study. Pediatrics, 2016; 137:1–11.

49.

Mitchell

, Bilderback

, Okelo

. Feasibility of picture-based Asthma Medication Plans in Urban Pediatric Outpatient Clinics. Pediatr Allergy Immunol Pulmonol, 2016; 29:95–99.

50.

Williams

, Davis

, Parker

, et al. The role of health literacy in patient-physician communication. Fam Med, 2002; 34:383–389.

51.

Safeer

, Keenan

. Health literacy: the gap between physicians and patients. Am Fam Physician, 2005; 72:463–468.

52.

Macy

, Davis

, Clark

, et al. Parental health literacy and asthma education delivery during a visit to a community-based pediatric emergency department: a pilot study. Pediatr Emerg Care, 2011; 27:469–474.

53.

Szefler

, Gergen

, Mitchell

, et al. Achieving asthma control in the inner city: do the National Institutes of Health Asthma Guidelines really work?. J Allergy Clin Immunol, 2010; 125:521–528.

54.

Government of Canada: Social determinants of health and health inequalities [Internet]. Available from: www.canada.ca/en/public-health/services/health-promotion/population-health/what-determines-health.html

55.

WHO: The determinants of health [Internet]. Available from: www.who.int/hia/evidence/doh/en/

56.

Kakumanu

, Antos

, Szefler

, et al. Building school health partnerships to improve pediatric asthma care: the School-based Asthma Management Program. Curr Opin Allergy Clin Immunol, 2017; 17:160–166.

57.

Lemanske

RFJ

, Kakumanu

, Shanovich

, et al. Creation and implementation of SAMPRO: a school-based asthma management program. J Allergy Clin Immunol, 2016; 138:711–723.

58.

Fox

, Porter

, Lob

, et al. Improving asthma-related health outcomes among low-income, multiethnic, school-aged children: results of a demonstration project that combined continuous quality improvement and community health worker strategies. Pediatrics, 2007; 120:e902–e911.

59.

Expert Panel Report 3 (EPR-3). Guidelines for the Diagnosis and Management of Asthma-Summary Report 2007. J Allergy Clin Immunol, 2007; 120:S94–S138.

60.

GINA 2019 update [Internet]. Available from: https://ginasthma.org/wp-content/uploads/2019/04/GINA-2019-main-Pocket-Guide-wms.pdf

61.

Benjamin

. Improving health by improving health literacy. Public Health Rep, 2010; 125:784–785.

62.

Salim

, Young

, Shariff Ghazali

, et al. Protocol for a systematic review of interventions addressing health literacy to improve asthma self-management. NPJ Prim Care Respir Med, 2019; 29:18.