Abstract
BACKGROUND: Pulmonary function tests (PFTs) have historically used race-specific prediction equations. The recent American Thoracic Society guidelines recommend the use of a race-neutral approach in prediction equations. There are limited studies centering the opinions of practicing pulmonologists on the use of race in spirometry. Provider opinion will impact adoption of the new guideline. The aim of this study was to ascertain the beliefs of academic pulmonary and critical care providers regarding the use of race as a variable in spirometry prediction equations.
METHODS: We report data from 151 open-ended responses from a voluntary, nationwide survey (distributed by the Association of Pulmonary Critical Care Medicine Program Directors) of academic pulmonary and critical care providers regarding the use of race in PFT prediction equations. Responses were coded using inductive and deductive methods, and a thematic content analysis was conducted.
RESULTS: There was a balanced distribution of opinions among respondents supporting, opposing, or being unsure about the incorporation of race in spirometry prediction equations. Responses demonstrated a wide array of understanding related to the concept and definition of race and its relationship to physiology.
CONCLUSIONS: There was no consensus among providers regarding the use of race in spirometry prediction equations. Concepts of race having biologic implications persist among pulmonary providers and will likely affect the uptake of the Global Lung Function Initiative per the American Thoracic Society guidelines.
Introduction
Pulmonary function tests (PFTs) are integral to the assessment of lung disease. FEV1 is a predictor of progression of lung disease and correlates with mortality.1 Spirometry guides diagnosis and treatment of respiratory illness, influences surgical referrals for lung cancer and transplantation,2 and dictates occupational fitness and disability qualification.
Clinicians use spirometry to help identify pathologic lung function in symptomatic patients. Since the mid-20th century, normal values have been standardized using race-specific prediction equations, with the assertion that normal lung function is influenced by sex, height, age, and race. For example, in the Global Lung Function Initiative 2012 (GLI-2012) equation, the predicted normal FEV1 for a Black patient is lower than a white counterpart, which has led to underdiagnosis and undertreatment of lung disease among Black communities because established FEV1 value cutoffs are used in the clinical decision-making process.3
The assumption that race influences lung function has long been embedded in medicine, from Thomas Jefferson describing “a difference of structure in the pulmonary apparatus” among enslaved people to 19th century plantation physician Samuel Cartwright, who quantified the racial difference as 20%.4,5 Importantly, the initial equations for lung function were conceptualized at a time in the United States when eugenic policies permeated medical theory and practice.6 By 1974, researchers reduced differences in lung function between Black and white people, to a “scaling factor” of 13.2% for Black people, which continues to be incorporated in equations to this day.7,8
Only in recent years has there been recognition that observed differences in PFTs between socially defined races are due in part to factors related to structural racism such as economic status, housing, occupation, fuel source, and nutrition among many other factors (rather than intrinsic biologic/genetic differences).9,-,13 Specifically, the recently published statement by the American Thoracic Society (ATS) argues that race- and ethnicity-specific equations contribute to health disparities14 and now recommends the use of race-neutral reference equations.15
Many challenges confront the successful implementation of a race-neutral approach, and individual provider adoption is key. However, little is known about the perspectives of contemporary pulmonary practitioners regarding the use of race in spirometry. The aim of this study was to examine the views held by pulmonary and critical care faculty and fellows in United States academic centers on the incorporation of race in spirometry prediction equations.
QUICK LOOK
Current knowledge
The American Thoracic Society has recommended the use of a race-neutral approach in spirometry prediction equations, which have historically included a race variable. Opinions of practicing providers on the use of race in pulmonary function testing are not well understood.
What This Paper Contributes to Our Knowledge
There were varied opinions on the use of race in spirometry prediction equations among pulmonary providers in a nation-wide survey among pulmonary and critical care fellowships. The lack of consensus will likely influence the uptake of a race-neutral approach to the reference equations.
Methods
We conducted a nationwide cross-sectional survey regarding views on race and racism in pulmonary medicine. Members of the Association for Pulmonary Critical Care Medicine Program Directors can apply for the opportunity to have their survey disseminated to the entire membership roster. Every quarter, the Member Survey Committee reviews survey submissions according to published criteria16 and select one survey for dissemination. Our survey was selected in 2020 for dissemination to all program directors (n = 56 critical care medicine [CCM], 194 pulmonary/CCM [PCCM], and 20 pulmonary), associate program directors (n = 16 CCM, 131 PCCM, and 4 pulmonary), and program coordinators (n = 44 CCM, 191 PCCM, and 18 pulmonary) in spring of 2021.
Program coordinators were asked to forward the survey to all fellows, whose total is not quantified. The Association for Pulmonary Critical Care Medicine Program Directors distributed the survey via a secure research collection software program, REDCap link,17,18 followed by 2 reminders to maximize participation. This study was approved with exempt status by the Lifespan Institutional Review Board.
Survey Content
We created a 31-item survey based on items asked in a study evaluating an anti-racism curriculum at the Brown University Pulmonary Critical Care and Sleep Medicine division.19 The parent survey was adapted to include questions pertinent to the division from an open-access assessment created by Living Cities, a New York–based network of foundations and financial institutions dedicated to addressing race-based income and wealth gaps in urban areas. Per Living Cities, survey questions were derived to align with the Government Alliance on Race and Equity’s Employee Survey for Local Governments, D5 initiative’s Field Survey, as well as best practices from the field. This study analyzes responses to one question in this survey (question 18) related to individual provider beliefs about the use of a race variable in PFTs: “How do you feel about race variables incorporated into PFT prediction models like GLI2012? (eg, “this is appropriate and reflects biologically mediated differences among different races” or “I don’t think race should be used in PFT calculations at all”). All responses were anonymous. Results from other items on the survey will be published separately. Participants are identified with a ID created specifically for this paper, this identifies each user’s unique contribution, but does not link to any other study data.
Qualitative Data Analysis
We examined the distribution of participant sociodemographic characteristics and report frequencies and percentages below. We analyzed open-ended survey responses to explore beliefs and practices of providers surrounding race in spirometry.20 An analytical code book was created containing deductive and inductive codes. Deductive, or a priori, codes represented the open-ended survey questions, while inductive, or de novo codes, evolved from reviewing the responses. Survey data were imported into a coding management software program, NVivo (Lumivero, Denver, Colorado). NVivo software identified open-ended responses, aggregating each into their own code. All aggregated open-ended responses were then reviewed and independently coded by 2 reviewers for key concepts and themes within each question. The independent reviewers met regularly to compare coding and discuss discrepancies and come to consensus. Final codes were entered into NVivo 20 software, and an applied thematic content analysis was conducted.21 Summaries for relevant codes were used to develop the themes reported here.
Results
Characteristics of Respondents
Survey response rate varied by respondent type ranging from 9.3% of associate program directors to 11.8% of program directors, resulting in 151 total respondents (Table 1). The majority of respondents were fellows (n = 99, 65.6%). Respondents primarily hailed from sites with 3–4-y PCCM programs (n = 118, 78.1%), with the largest proportion of programs in the Northeast. Approximately half of the programs were located in urban centers (n = 70, 46.3%).
Thematic Analysis of Survey Results
Table 2 illustrates the broad themes and sub-themes, with representative quotations from responses. We identified 3 broad thematic categories, as follows: (1) race variables should be incorporated into PFTs (n = 54, 36%), (2) race variables should not be used in PFTs (n = 53, 35%), and (3) uncertainty regarding the use of race in PFTs (n = 44, 29%).
Perspectives of respondents who favored using race in PFTs (n = 54).
The relative majority of respondents agreed with using race in PFTs (n = 22, 42%) but did not elaborate further (eg, agree or appropriate). We identified 3 distinct sub-themes among more descriptive responses: using race for PFTs (1) has a basis in science, (2) could improve patient outcomes, and (3) is appropriate despite imprecise definitions of race categories.
Using race in PFT has a basis in science
Of the 22 respondents who invoked science as a rationale to use race in PFTs, one person wrote, “I feel this is based on science and this is helpful” (participant 104). Many (n = 16, 30%) used language indicating a belief in biologic differences necessitating the use of race in PFT reference equations. For example, one respondent wrote, “This is appropriate and reflects biologically-mediated differences among different races” (participant 136). One respondent referred to the belief that biologically mediated differences between races translate to anatomic and physiologic differences that influence lung function: “Anatomical variations prevalent amongst a race should be accounted for if relevant to a diagnosis and treatment.” (participant 67). Some respondents (n = 4, 7%) were explicit in referencing genetic differences between races as a reason to use race in spirometry. Such statements included “It is incredibly appropriate. Race underpins genetics, genetics dictate biology” (participant 47).
Using race in PFTs improves patient outcomes
Of the respondents favoring the use of race in spirometry, 5 (9%) specifically cited its beneficial effects such as “ensur[ing] patient safety” (participant 51). Of these, some indicated using race would result in better individualized care and personalized medicine due to assumed biological and genetic difference between races. There were also references to improving equity by keeping race variables: “I think it is important to include so that results are tailored to the individual and they aren’t all assumed to be white men” (participant 132). Another participant suggested that using race is important for future learning: “As we learn more about genetics and healthcare becomes more personalized, sometimes acknowledging racial differences allows for improved care for our patients” (participant 53).
A few respondents stated that there will be harmful consequences of not using race, which could negatively affect patient outcomes (n = 2, 4%). A participant indicated that tracking racial trends is important for attending to the possibility of underdiagnosis or overdiagnosis: “I think it does a disservice to patients to ignore racial trends in PFTs (eg, leads to over/under diagnosis)” (participant 83).
Using race in PFTs is appropriate despite imprecise race categories
Four individuals (7%) felt that current race categories are imprecise but that their incorporation was appropriate. One respondent indicated a belief in real racial differences that should prompt further research: “I think it is appropriate for now, as it seems to relate to real differences between races, but I think it highlights the need for better studies among minority populations” (participant 50). Some respondents suggested that current racial categories in PFT software are not inclusive enough to represent all parts of the world. For example, one respondent wrote, “… it should definitely be included in PFT calculations, but the races represented need to be far more comprehensive to… represent…different parts of the world ” (participant 42). Another responded that the imprecise nature of racial categories could be amplified by an evolving population of racially mixed individuals who would not be adequately described by current race categories: “…as race, such as gender, can account for phenotypic differences. However, I think with interracial marriages becoming more accepted and popular, this may become obsolete as a person may not fit into one race for medical purposes” (participant 28).
Perspectives of respondents who felt race variables should not be used in PFTs (n = 53).
A similar proportion of survey respondents (n = 53, 35%) opposed the use of race in spirometry; sub-themes included (1) race is a social construct (not biologic), (2) there is potential for patient harm, and (3) race is an imprecise tool.
Should not use race in PFTs since race is a social and not a biological construct
Of the 53 respondents who did not favor the use of race, many wrote, “I do not think PFTs should be used in race at all” as per the question stem. A subset (n = 6, 11%) expressed that race is more of a social construct than a biological one.
One participant stated, using race in PFTs is “not appropriate as race is a SOCIAL construct, not a biologic one. They should not be used at all” (participant 131). However, there was variation in the degree to which respondents felt that races share similar biology. One respondent wrote, “While there are biological differences that should be accounted for, using a social construct to do it is not accurate and should not be done. Race in no way reflects that huge diversity of individuals” (participant 111). Another participant offered social determinants of health as explanations for racial differences noted in prior studies: “There are not biologically-mediated differences among different races- these are likely a reflection of environment/systemic racism and may disproportionately harm People of Color/minorities” (participant 73).
Should not use race in PFTs because of the potential for bias and harm
Among respondents who did not favor the use of race in PFTs, 5 (9%) specifically cite the potential for bias and harm by incorporating race. Several respondents stated that incorporating race could perpetuate bias and racism. A respondent indicated that using race could introduce individual bias to testing and interpretation: “I don’t think race should be used in PFT calculations, as this can introduce bias on the part of the technicians and interpreters of the test” (participant 145). Another respondent suggested using race is rooted in structural racism and contributes to health inequity: “[using race] is inappropriate and promotes healthcare disparities, rooted in structural racism that has persisted under the guise of ‘physiology’” (participant 152).
Some respondents stated there will be harmful consequences of using race that could negatively affect patient outcomes. A respondent indicated that biological differences among races are not understood and using race may affect patient access to lifesaving care: “… until any real differences are better understood this should not be used. Especially since these differences may affect whether they are perceived as transplant candidates or therapy candidates” (participant 57).
Should not use race in PFTs because race is an imprecise tool
Of the 53 respondents who did not favor the use of race, 4 (7%) supported abandoning the use of race entirely. One respondent stated that “Race is not an objectively measurable variable and should not be used” (participant 69). Another respondent felt that race is too blunt a categorization to be used for evaluating any potential biologic differences: “I feel that race is such an imprecise tool for trying to identify presumed biologically-mediated differences” (participant 57). A few respondents (n = 3, 6.8%) offered alternatives to using race such as thoracic height and sex.
Perspectives of respondents who were uncertain regarding the use of race in PFTs (n = 44).
A portion of respondents expressed uncertainty about the use of race, stating unknown or unsure, with equal proportions leaning toward or away from using race. Sub-themes included uncertainty about using race due to (1) a belief that it is unclear whether race categories have biological basis, (2) uncertainty about the clinical impacts of using or not using race, and (3) the imprecise nature of race categories.
Uncertain of using race in PFTs because unclear if race has a biological basis
Of the 44 respondents uncertain about the use of race, 12 (27%) felt more evidence is needed to determine if race has a scientific basis to be used in medical algorithms. One respondent called into question the validity of biological differences between races and suggested that it needs to be investigated further: “This is fraught with issues of precision…I think we need to fully investigate if there is anything valid to the idea that there are biologically-mediated differences based on race…” (participant 128) Several respondents (n = 6, 14%) indicated uncertainty about using race but stated that it should be used if there were data validating its use: “Race should be included in calculations if the data indicate that there is a difference” (participant 164).
Other respondents (n = 3, 6.8%) commented on their own uncertainty of using race and acknowledged their belief of race not being rooted in biology: “…[We] have been trained to believe [PFTs] …represent differences in races, but they are likely not biologically mediated” (participant 115). There were additional respondents (n = 2, 4.5%) that recognized racial differences in lung function but indicated uncertainty that those differences stemmed entirely from race: “Not sure - probably need more info but seems influence of race on PFTs may be less about biological differences and more about environment/situational differences” (participant 16).
Uncertain of using race in PFTs because unclear if its inclusion or exclusion will affect patient outcomes
Of the 44 respondents uncertain about the use of race, 4 (9.1%) respondents cited uncertainty about using race due to concerns over the potential bias of using skin color and other racial features as biologic surrogates. One respondent wrote, “…I don’t know what the right answer is…race is such a crude measure of heritage/genetic ancestry and can’t really be separated from all of the social factors that also influence health based on race” (participant 85). Another respondent commented on the effect systematic racism has on overall health and the need for further research on race and physiology: “I don’t know the answer to this but it is clear to me that simply the color of one’s skin (eg, race) should not have profound effects on something as complex as lung function … especially when you consider the clear impact of negative environmental exposure on lung function and the historical (and systematically racist) correlation between undesirable and polluted places to live and housing availability for non-whites…” (participant 29).
Conversely, some respondents indicated uncertainty about not using race because it can lead to patient harm. Three (6.8%%) respondents indicated that if there were data validating its use, the use of race would result in less biased or improved patient care: “If there is a biological difference…between races, different reference values must be used to have unbiased diagnosis and treatment” (participant 163). One respondent gave an example of other medical contexts in which race is used to determine treatment goals, as support for potentially using race in PFTs: “… a lot of studies and prediction models are geared toward white populations… there are difference[s] in guidelines for first-line antihypertensive for [B]lack population, if similar differences in physiology exist in pulmonology it would be to the benefit of the patients to know about them” (participant 36).
Uncertain if race should be used due to race being an imprecise tool
Some respondents (n = 5, 8.8%) were uncertain about using race in PFTs but suggested it is an ambiguous variable that is not well defined: “I’m not sure how much this still applies in modern practice given that race is not as much of a defined categorical variable as 50 years ago” (participant 19).
Discussion
We found that respondents held conflicting views about when and how to use race in spirometry, with equal proportions of respondents reporting that race should be used and arguing against its use. Interestingly, similar concepts emerged in all themes, including the relationship between race and biology, patient impact, and accuracy/precision of race as a tool. The themes we identified in this survey shed light on the ongoing confusion about concepts of race that have informed pulmonary medicine for centuries.22 To our knowledge this is the first qualitative survey examining how pulmonologists in United States training programs view the use of race in spirometry prediction equations.
In a 1990 survey of pulmonary training programs in the United States and Canada, Ghio et al23 found that 47% of programs applied a scaling factor to “the predominant minorities,” ranging from 10–15%, and some included population-specific reference equations for race and ethnicity. The authors concluded, equations are acceptable to account for differences in ethnicity. However, ignoring these differences is unacceptable.23 The ATS/European Respiratory Society recommended the use of race/ethnicity-specific reference equations in spirometry in 2005. The GLI-2012 and other race-specific prediction equations have significant limitations with poor predictive performance in non-white populations.24,25 A newer study by Bowerman et al15 showed that a race-neutral GLI equation that properly weighs non-white sampled populations more heavily performs similarly to “GLI-other,” which was used to capture races not included in the original algorithm. This study, however, had wide SD for normal-range spirometry that could underrecognize pathology and further emphasizes the importance of the clinical scenario in interpretation of PFTs.
Participants’ opinions on the definition of race (as a social construct vs a biologic one) underpinned their justification for including race in spirometry. The biologization of race was prevalent among the respondents who favored the use of race in PFTs. A common theme among those who did not feel that race should be included in spirometric testing was that race does not have a biologic basis. The National Health and Nutrition Examination Survey26 found more variation of lung function within race and ethnic groups than between, a phenomenon first described by Richard Lewontin and later described by Barbujani and Rosenberg.27,-,32 Many respondents also referred to the importance of socioeconomic factors that might be masked using a race-based equation. Indeed, GLI-2012 does not account for many modifiable risk factors for lung function that are often rooted in systemic racism, such as air pollution, nutrition, and violence.33,-,36 Ekström and Mannino37 reported that the use of race-specific equations resulted in better percent-predicted FEV1 among Black subjects yet still correlated with worse symptoms and mortality, implying a danger of missing individuals at higher risk when using a race-based method.
Our analysis also revealed a recurring belief: that race is a widely heterogenous entity and cannot be specifically defined. A systematic review of studies comparing lung function of white to other groups found only 17.3% of included studies defined race in any way, despite the fact that race was a central interpretive variable studied.22 Whereas failing to define race, researchers continued to invoke biogenetics to explain racial difference, perpetuating a fundamental flaw in how the field of pulmonology addressed race. Scientists have suggested using self-identification in biomedical research, but studies show that racial self-identification is fluid, changing over time and place, and not rooted in genetic difference.38,-,40 Social scientists have demonstrated that historically there have never been genetically pure groupings and concepts of race and racial categorization emerged from political and social contexts.39,40 Importantly, respondents who expressed uncertainty regarding the use of race are unclear on viable alternatives to the inclusion of a race variable. Racist concepts about physical traits such as thoracic height or leg length that date to the period of scientific racism remain prominent in the field and are still referenced in our survey.
Many respondents favored or disfavored the use of race in PFT reference equations by its perceived effect on clinical outcomes. For example, as part of preoperative risk stratification, non-white candidates with low lung function (without race correction) may be declined surgery or conversely have delayed referral for lung transplantation (with race correction).2 Decision-making thresholds for these procedures easily can be crossed if relying solely on spirometry and the particular equations used.10
Our study has multiple limitations. We did not collect race and ethnicity identifiers of participants to improve participation; however, this limits our analysis. Whereas our survey was disseminated nationally, our response rate was low even compared to prior Association for Pulmonary Critical Care Medicine Program Directors surveys, which ranged from 28–40% from 2017–2020. We suspect that both the timing of the administration of this survey as well as the content may have contributed to the low response rate. Whereas the impact of clinical burden and moral burnout of PCCM divisions nationally during the COVID pandemic on participation was likely more ubiquitous, aversion to the survey due to the sensitive and possibly triggering nature of the topic may have led to differential and selective participation. Consequently, caution should be taken in generalizing the thoughts and perspectives synthesized above to the pulmonary community at large; however, it is still noteworthy that a third of respondents held misconceptions about race as a biologic variable. It should be noted that a member check was not performed on the responses to confirm our interpretations of the participants’ statements. Moreover, since the survey was distributed in 2021, there has been significant discussion in the pulmonary community about the role of race and racism in PFT interpretation. The views presented here may have evolved since that time. Still, the practicing pulmonologist perspective remains missing in this debate.36 Since our study, the United States House of Representatives Ways and Means Committee released a report outlining the problems with using race in medical algorithms. Chairperson Neal wrote, “divergent understandings of the appropriate use of race and ethnicity…could make it difficult to achieve consensus on the path forward.”41 Our study highlights the lack of consensus about race in PFT reference equations. A large number of respondents inappropriately viewed race as a biologically important variable rather than a social construct. Current understanding about the role of race in spirometry prediction equations will affect the uptake of the new ATS Official Statement on Race Ethnicity and PFT Interpretation guidelines.14 Education about race and its social, economic, and political production may help providers become early adopters of a race-neutral approach.15 Our recommendation is for PFT labs to evaluate their current practice and integrate and update software to include GLI-Global. We propose it is the role of academic pulmonologists in pulmonary and critical care training programs to lead this educational effort.
Conclusions
Among a nationwide sampling of academic PCCM fellowship programs, we found a large range of beliefs on incorporating race in PFT prediction equations. This may have significant implications in the adoption of the current ATS guidelines for using race-neutral spirometry prediction equations.
Footnotes
- Correspondence: Debasree Banerjee MD MSc, Division of Pulmonary, Critical Care and Sleep Medicine, Rhode Island Hospital, 593 Eddy Street, POB Suite 224, Providence, RI 02903. E-mail: debasree_banerjee{at}brown.edu
The authors have disclosed no conflicts of interest.
This study was made possible by the Association of Pulmonary and Critical Care Medicine Program Directors. The project described was supported by Institutional Development Award Number U54GM115677 from the National Institute of General Medical Sciences of the National Institutes of Health, which funds Advance Clinical and Translational Research (Advance RI-CTR). Dr Rosen and Mr Lantini are partially supported by Institutional Development Award Number U54GM115677 from the National Institute of General Medical Sciences of the National Institutes of Health, which funds Advance Clinical and Translational Research (Advance RI-CTR). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
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