Low Concordance Between HbA1c and OGTT To Diagnose Prediabetes and Diabetes in Overweight or Obesity

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Low Concordance Between HbA1c and OGTT to Diagnose

Prediabetes and Diabetes in Overweight or Obesity
Kyriazoula Chatzianagnostou; Luisella Vigna; Silvana Di Piazza; Amedea Silvia Tirelli; Filomena Napolitano; Laura Tomaino;
Fabrizia Bamonti; Irene Traghella; Cristina Vassalle
Clin Endocrinol. 2019;91(3):411-416.
Abstract and Introduction

Abstract
Background: Glycated haemoglobin (HbA1c) test, introduced for diagnosing prediabetes and diabetes by the American
Diabetes Association for some years, is currently under extensive discussion for contradictory data on the concordance between
this test and the oral glucose tolerance test (OGTT).
Hypothesis: To assess concordance between HbA1c and OGTT to diagnose prediabetes and diabetes in subjects with
overweight or obesity, focusing on possible gender-related differences.
Methods: A total of 949 outpatients with overweight or obesity at risk for diabetes (mean age 50 ± 15 years; 660 F) were
enrolled and underwent HbA1c test and OGTT.
Results: In both genders, HbA1c test identified more patients with prediabetes than OGTT (42% vs 22% in males, 40% vs 18%
in females, respectively): a slight concordance between HbA1c and OGTT (60% of total tests in both genders).
In subjects diagnosed by OGTT, post-OGTT insulin levels and HOMA INDEX were significantly higher than those found in
HbA1c(+) cases. Instead, those diagnosed with HbA1c were significantly older and showed higher uric acid than those with both
tests (−).
Conclusions: HbA1c test and OGTT did not reach full concordance for the diagnosis of diabetes and prediabetes in both
genders. The two tests likely reflect different physiopathological aspects of dysglycaemia, suggesting that the 'diagnostic
thresholds' could be reconsidered in light of the discordance observed.
Introduction
Some years ago, the American Diabetes Society (ADA) introduced glycated haemoglobin (HbA1c) as biomarker for the
diagnosis of prediabetes (pre-T2D) and diabetes (T2D) in addition to fasting plasma glucose (FPG), and two-hour blood
glycaemia load (oral glucose tolerance test, OGTT).[1,2] FPG is the most easy, cheap and reproducible test, although with low
sensitivity and high level of pre-analytical variability. Moreover, although OGTT is considered the most sensitive test, it takes a
long time and it is costly and retains poor reproducibility. HbA1c test, instead, can be performed at any time of the day without
the need for fasting, is not affected by acute or individual variations (analytical variability less than 2%), is relatively stable over
2-3 months and can be considered a reproducible tool and an ideal candidate for screening of subjects at high risk for T2D.
Nonetheless, it is still on discussion the use of HbA1c for screening of T2D and other forms of impaired glycaemia. In fact, in
some studies, HbA1c test would seem to have lower sensitivity than OGTT in the identification of the different forms of
dysglycaemia.[3,4] More generally, the obtainment of a nondiagnostic value with a test may not exclude positivity to T2D
assessed with another one.[2] In this case, it has also been hypothesized that subjects with altered glycaemic regulation, as
identified by the two different tests, may differ in their pathogenic mechanisms.[3]
In view of the increasing use of HbA1c test to evaluate changes in glycaemic homeostasis, the aim of this study was the
comparison between HbA1c test and OGTT for the diagnosis of T2D and pre-T2D in outpatients with overweight or obesity.
Furthermore, by hypothesizing possible performance of these tests regarding gender-related differences (aspect not yet
evaluated), the concordance between the two tests in men compared to women was also assessed.
Methods
A total of 949 outpatients with overweight or obesity at risk for T2D (mean age 50 ± 15 years; 660 F), performing tests for HbA1c
and OGTT, were recruited at two hospitals (Obesity and Occupational Health Center 'L. Devoto' of Fondazione Ca' Granda
Ospedale Maggiore, Policlinico of Milan, and Fondazione CNR-Regione Toscana G. Monasterio, Pisa, Italy). Upon entering the
study, each participant signed an informed consent form and underwent medical examination. The study was approved by the
Ethics Committee of Milan Policlinico Hospital (Study registration number: 1370). Because of the importance of reducing bias
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associated with obesity, people first language was used according to the standard recommendation of The Obesity Society and
Canadian Obesity Network.[5]
During medical examination, eligibility was evaluated by standard routine examination including body mass index (BMI), waist
circumference, systolic and diastolic blood pressure. Peripheral blood samples were drawn after an overnight fast and after
OGTT. Serum HbA1c levels were measured by ion-exchange high-performance liquid chromatography (HPLC), and routine
biochemical parameters (serum uric acid, glucose, insulin, a complete lipid profile) were measured by standard automatized
laboratory analysers. Serum samples of all the subjects were frozen and stored at −80°C for batch analysis periodically
assessed at Central Laboratory of Policlinico of Milan or FTGM Laboratory, Pisa.
The ADA criteria were followed for diagnosing pre-T2D and T2D. The oral glucose load was performed with morning fasting
intake of 75 g of glucose; the glycaemia was assessed both before taking the load and after 2 hours. Under normal conditions,
glucose concentration 2 hours after loading is less than 140 mg/dL (7.7 mmol/L). Values equal to or higher than 200 mg/dL (11.1
mmol/L) make the diagnosis of T2D, while values between 140 and 199 mg/dL (7.8 and 11 mmol/L) indicate a condition that is
not yet T2D and is defined as 'Impaired Glucose Tolerance' (IGT). The determination of HbA1c levels, which represents the
average glycaemia of the last 2 months, was performed on another serum sample taken the same morning prior to the OGTT.
HbA1c values between 39-46 mmol/mol give the diagnosis of pre-T2D, whereas values ≥47 mmol/mol the diagnosis of T2D.
The Homeostasis Model Assessment of Insulin Resistance Index (HOMA-IR) was calculated as previously described by
Matthews et al[6] using the formula: [insulin (μU/mL) × glucose (mmol/L)]/22.5.
Statistical Analysis
Concordance and correlation between the two tests were evaluated using linear regression and the Spearman coefficient.
Continuous variables were reported as mean ± SD, or median and range minimum and maximum. The logarithmic
transformation of parameters with elevated skewness (eg glycaemia, insulin, triglycerides) was used for the statistical tests.
Then, log-transformed values were back-transformed for data presentation.
Comparisons between continuous variables were evaluated by Student's t test, while differences between categorical variables
made by chi-square analysis. Comparisons among three or more independent groups were analysed by using ANOVA test and
P for trend reported.
Regression analysis was performed to assess the relationship between continuous variables.
Results
Anthropometric characteristics and routine biochemical parameters of subjects with overweight and obesity according to gender
are shown in . In particular, uric acid (UA), fasting glucose and insulin, HOMA INDEX, and triglycerides were significantly higher
in men than in women, whereas total cholesterol, HDL and LDL cholesterol resulted significantly higher in women than in men
().
Table 1. Subjects' characteristics and routine biochemical parameters
Men Women P value

Anthropometric characteristics
n 289 660 –
Age (y) 52 ± 15 49 ± 15 ns
Body mass index (kg/m2) 34 ± 5 33 ± 5 ns
Diastolic blood pressure (mm Hg) 77 ± 16 76 ± 11 ns
Systolic blood pressure (mm Hg) 133 ± 15 128 ± 47 ns
Laboratory biomarkers
Uric acid (mg/dL) 6.2 ± 1.3 4.8 ± 1.2 <0.001
Glucose (mmol/L) 5.6 (4.3-8.1) 5.3 (3.8-9.7) <0.001
2h-glycaemia of the OGGT (mmol/L) 6.3 (2.6-20.5) 6.1 (2.4-22.8) ns
Insulin (mUI/mL) 14 (4-83) 12 (3-65) <0.01
2h-insulin of the OGTT (mUI/mL) 71 (8-469) 75 (7-582) ns
HOMA INDEX 3.7 (0.8-20) 3 (0.5-16) <0.01

Glycated haemoglobin (mmol/mol) 39 ± 6 38 ± 6 ns
Total cholesterol (mg/dL) 194 ± 38 210 ± 46 <0.001
High-density lipoproteins (mg/dL) 48 ± 13 61 ± 15 <0.001
Triglycerides (mg/dL) 115 (41-479) 96 (26-944) <0.001
Low-density lipoproteins (mg/dL) 123 ± 36 131 ± 37 <0.01
Note: Data are given as mean ± SD for normally distributed variables, and as median and interquartile range for non-normally
distributed parameters. Categorical data are presented as number (%).
Men Women P value

n 289 660 –
Age (y) 52 ± 15 49 ± 15 ns
Uric acid (mg/dL) 6.2 ± 1.3 4.8 ± 1.2 <0.001
Glucose (mmol/L) 5.6 (4.3-8.1) 5.3 (3.8-9.7) <0.001
Insulin (mUI/mL) 14 (4-83) 12 (3-65) <0.01
HOMA INDEX 3.7 (0.8-20) 3 (0.5-16) <0.01
Both OGTT and the HbA1c test were assessed in all the subjects following the ADA criteria. In the overall population, according
to the OGTT criteria, 724 tests (76%) were negative but 183 (19%) and 42 (5%) were positive for pre-T2D and T2D, respectively
(Figure 1). Instead, as regards HbA1c assay, 524 (55%) tests were negative, and 384 (41%) and 41 (4%) were positive for the
diagnosis of pre-T2D and T2D, respectively (Figure 1). Considering gender-related differences, the HbA1c test identified more
patients with pre-T2D than OGTT in both sexes (42% vs 22% in males, 40% vs 18% in females, respectively).
Figure 1.
Categorization of the glycaemic state through the ADA criteria for OGTT and HbA1c levels in the whole population
There was a moderate correlation between OGTT and HbA1c in the overall population (r = 0.46, P < 0.001; Figure 2); no
significant differences for the OGTT-HbA1c association were observed in the two genders (r = 0.47, P < 0.001 for females, r =
0.44, P < 0.001 for males). The concordance in the clinical interpretation of the glycaemic state using OGTT or HbA1c test in the
two sexes is shown in . Concordance between the two tests was not very high, occurring in 60% in both genders.
Table 2. Concordance in clinical interpretation of glycaemic status between OGTT and HbA1c test
OGTT OGTT
Males Non-T2D Pre-T2D T2D Females Non-T2D Pre-T2D T2D
HbA1c HbA1c
Non-T2D 132 19 2 Non-T2D 321 44 6
Pre-T2D 73 38 10 Pre-T2D 185 65 13
T2D 4 7 4 T2D 9 10 7
Note: Common category identification (non-T2D, preT2D, T2D) by both tests in bold .
Figure 2.
Correlation between HbA1c and post-OGTT glucose (120 min) in the whole population
shows the clinical characteristics of participants according to different positivity criteria. In the subjects diagnosed by OGTT,
post-OGTT insulin levels and HOMA INDEX were significantly higher than the levels found in HbA1c(+) subjects. Instead, the
cases diagnosed with HbA1c were significantly older and showed higher UA than those with both tests (−) ().
Table 3. Cardiovascular risk factors in subjects with overweight/obesity according to the positivity to the different tests
Both tests (−) HbA1c (+) OGTT (+) Both tests (+)
n 453 271 71 154
Males 132 (29) 77 (28) 21 (30) 59 (38)
Age (y) 45 ± 16 54 ± 12*** °° 51 ± 13 °° 59 ± 11***
Body mass index (kg/m2) 32 ± 5 34 ± 5 34 ± 5 35 ± 6 ***
Diastolic blood pressure (mm Hg) 75 ± 13 79 ± 11 78 ± 17 76 ± 15*
Systolic blood pressure (mm Hg) 129 ± 56 129 ± 14 132 ± 23 133 ± 17
Fasting glucose (mmol/L) 5.2 (3.8-7.1) 5.5 (4.1-7.6)*** °° 5.61 (4.4-7.5)*** °° 6.1 (4.3-9.7)***
Post-OGTT glucose (mmol/L) 5.6 (2.4-7.7) 6.1 (2.6-7.7) ** °°° 8.8 (7.8-13.8)*** °° # 9.22 (7.8-22.8)***
Insulin (mUI/mL) 11 (3-83) 13 (4-68) 17 (4-52)** 16 (4-68)**
Post-OGTT insulin (mUI/mL) 63 (7-469) 74 (8-322)°°° 133 (28-331)*** ## 130 (19-582)***

HOMA INDEX 2.7 (0.5-20) 3.3 (0.7-13) °° 4 (0.8-15)*** # 4.3 (0.8-16)***
Uric acid (mg/dL) 4.9 ± 1.3 5.3 ± 1.4* ° 5.2 ± 1.5 5.8 ± 1.4***
Total cholesterol (mg/dL) 201 ± 38 211 ± 49 206 ± 41 206 ± 49
High-density lipoproteins (mg/dL) 58 ± 16 58 ± 14 54 ± 18 55 ± 16
Triglycerides (mg/dL) 93 (26-479) 106 (29-944) 105 (49-446) 113 (46-899)***
Low-density lipoproteins (mg/dL) 127 ± 34 132 ± 38 131 ± 38 128 ± 43
distributed parameters.
Categorical data are presented as number (%).
*, **, *** <0.05, <0.01, <0.001 vs both tests (−).
°, °°, °°° <0.05, <0.01, <0.001 vs both tests (+).
#, ##, <0.05, <0.01 vs HbA1c(+).
Table 3. Cardiovascular risk factors in subjects with overweight/obesity according to the positivity to the different tests
Both tests (−) HbA1c (+) OGTT (+) Both tests (+)
n 453 271 71 154
Males 132 (29) 77 (28) 21 (30) 59 (38)
Age (y) 45 ± 16 54 ± 12*** °° 51 ± 13 °° 59 ± 11***
Body mass index (kg/m2) 32 ± 5 34 ± 5 34 ± 5 35 ± 6 ***
Diastolic blood pressure (mm Hg) 75 ± 13 79 ± 11 78 ± 17 76 ± 15*
Systolic blood pressure (mm Hg) 129 ± 56 129 ± 14 132 ± 23 133 ± 17
Fasting glucose (mmol/L) 5.2 (3.8-7.1) 5.5 (4.1-7.6)*** °° 5.61 (4.4-7.5)*** °° 6.1 (4.3-9.7)***
Post-OGTT glucose (mmol/L) 5.6 (2.4-7.7) 6.1 (2.6-7.7) ** °°° 8.8 (7.8-13.8)*** °° # 9.22 (7.8-22.8)***
Insulin (mUI/mL) 11 (3-83) 13 (4-68) 17 (4-52)** 16 (4-68)**
Post-OGTT insulin (mUI/mL) 63 (7-469) 74 (8-322)°°° 133 (28-331)*** ## 130 (19-582)***
HOMA INDEX 2.7 (0.5-20) 3.3 (0.7-13) °° 4 (0.8-15)*** # 4.3 (0.8-16)***
Uric acid (mg/dL) 4.9 ± 1.3 5.3 ± 1.4* ° 5.2 ± 1.5 5.8 ± 1.4***
Total cholesterol (mg/dL) 201 ± 38 211 ± 49 206 ± 41 206 ± 49
High-density lipoproteins (mg/dL) 58 ± 16 58 ± 14 54 ± 18 55 ± 16
Triglycerides (mg/dL) 93 (26-479) 106 (29-944) 105 (49-446) 113 (46-899)***
Low-density lipoproteins (mg/dL) 127 ± 34 132 ± 38 131 ± 38 128 ± 43
distributed parameters.
Categorical data are presented as number (%).
*, **, *** <0.05, <0.01, <0.001 vs both tests (−).
°, °°, °°° <0.05, <0.01, <0.001 vs both tests (+).
#, ##, <0.05, <0.01 vs HbA1c(+).
Discussion
According to the present study, the concordance between the two tests in the evaluation of the glycaemic state is not optimal.
The HbA1c test showed a higher percentage of subjects with pre-T2D than that obtained when using criteria based on 2h-
glycaemia of the OGTT. Furthermore, no gender-related differences were observed in our population. However, the two
diagnostic methods showed different relationship with cardiovascular risk factors.
The poor agreement here found between HbA1c and post-OGTT glucose criteria for the identification of individuals with pre-T2D
is comparable to that previously reported in a study on an Italian population.[7] However, for what the agreement between the
two tests is concerned, the data available in the literature are quite different. It should be considered that HbA1c levels in
subjects with impaired glucose tolerance or T2D and its relationship with cardiovascular risk might differ by race and ethnicity, as
reported by Eastwood et al[8] This finding may be affected, almost in part, by genetic traits influencing erythrocyte turnover, or
alternatively, by nutritional or metabolic factors. Accordingly, some studies showed an increase in the prevalence of subjects
with pre-T2D diagnosed by HbA1c test, whereas others reported a decreased prevalence of subjects with pre-T2D compared to
that obtained according to the OGTT criteria.[3,7–9] As suggested by Kanat et al[3] the two tests may highlight different aspects
of dysglycaemia and identify different subjects with glucose intolerance. For example, high glycaemic values at 2h-OGTT may
reflect the inability to cope with an acute glucose load characterized by altered secretion and insulin action, while HbA1c might
evidence a more generalized level of glycaemic alteration. In particular, in a Mexican population, the OGTT identifies better than
HbA1c in patients with impairment of the beta cells, who are at very high risk for the T2D development.[3] Instead, a recent study
in Italian pre-T2D subjects showed that HbA1c together with soluble receptor for advanced glycation end-products (sRAGE) and
endogenous secretory RAGE were independent determinants of subclinical cardiac alterations (Doppler echocardiography)
associated with heart failure development.[10] These subjects would not have been classified as having pre-T2D by evaluating
only the post-OGTT values.[10] Moreover, other data conducted in Italian cohorts suggested a worsened cardiovascular risk
profile in subjects HbA1c (+) rather than in 2h-glycaemia of the OGGT (+) in terms of carotid intima-media thickness, blood
viscosity and inflammatory profile.[8,11] Conversely, several prospective data suggest that a significant percentage of subjects
developing T2D did not present an altered OGTT.[12] It could therefore exist in the group with normal OGTT, a subgroup at
higher risk that the HbA1c test could help to identify. In fact, HbA1c levels could be influenced not only by blood glucose levels,
but also by many other factors, including very important determinants as oxidative stress and inflammation, which increase in
subjects with obesity.[13] In particular, oxidative stress status may influence HbA1c level promoting insulin resistance at adipose
and skeletal muscle tissue levels, and inducing hyperglycaemia, which in turn increases oxidative stress.[14,15] Moreover,
increased oxidative stress promotes the autoxidation of glucose to dicarbonyl intermediates in an early step of the Maillard
reaction, through which takes place the haemoglobin glycation.[16] UA is a potent antioxidant, although at higher levels may
acquire pro-oxidant activity and an adverse role as cardiometabolic risk factor.[13,17] In the present study, UA highest levels
were found in subjects with positivity for both tests, and intermediate in those with one test positive, respect to patients with
negativity for both tests, possibly reflecting a progressively increased cardiometabolic risk.[18]
In our population, concordance between OGTT and HbA1c test to diagnose pre-T2D and T2D was similar in the two genders.
Nonetheless, men showed a higher prevalence of subjects with HOMA INDEX values >2.5 than women (P < 0.001) as well as a
higher prevalence of subjects with impaired fasting glucose than female subjects (5.6-7 mmol/L; P < 0.01), whereas no gender-
related differences were observed for the prevalence of 2h-glycaemia of the OGGT or HbA1c (unshown data). It has been
suggested that fasting glucose criteria may be more useful in detecting patients with hepatic insulin resistance.[19] Our results
suggesting increased HOMA INDEX in males also presenting fasting glucose criteria are consistent with this possibility.
According to previous data, we observed that men showed higher levels of fasting glucose than women (see ).[20] This fact may
reflect gender-related physiological mechanisms, not yet clearly elucidated. Instead, we did not find significant difference 2h-
glycaemia of the OGGT levels according to gender (see ), although other authors reported higher 2h-glycaemia of the OGGT
levels in women than in men.[20,21] However, artefacts due to the same amount of glucose during OGTT given to all subjects
despite their different body size and body composition, especially when belonged to different sexes, must be taken into account
when evaluating results.[21] Nonetheless, the observation that these altered glucose-related biomarkers were found more
prevalent in one sex raises important questions about their underlying aetiology and the ability of the current glucose thresholds
to equally identify men and women at high risk of developing pre-T2D and T2D. In the same way, changes to diagnostic criteria
of T2D or pre-T2D may induce consistent variation in prevalence among other specific clinical populations. For example, a large
study on Chinese population (4325 subjects, aged 20-74, without previous diagnosis of T2D) showed a poor concordance
between OGTT and HbA1c test. Authors suggested that this aspect could be improved by modifying the cut-offs for the
diagnosis of pre-T2D and T2D in patients with different levels of BMI, adopting 37.7 and 46.4 mmol/mol for patients with normal
weight whereas 38.8 and 47.5 mmol/mol for those with overweight and 42.1 and 47.5 mmol/mol for those with obesity.[22]
However, as authors evaluate the diagnostic accuracy of the HbA1c in comparison with OGTT, in view of possible different
pathophysiological mechanisms underlying these tests, further studies are needed to interpret these results.
Men Women P value

n 289 660 –
Age (y) 52 ± 15 49 ± 15 ns
Uric acid (mg/dL) 6.2 ± 1.3 4.8 ± 1.2 <0.001

Glucose (mmol/L) 5.6 (4.3-8.1) 5.3 (3.8-9.7) <0.001
Insulin (mUI/mL) 14 (4-83) 12 (3-65) <0.01
HOMA INDEX 3.7 (0.8-20) 3 (0.5-16) <0.01
Men Women P value

n 289 660 –
Age (y) 52 ± 15 49 ± 15 ns
Uric acid (mg/dL) 6.2 ± 1.3 4.8 ± 1.2 <0.001
Glucose (mmol/L) 5.6 (4.3-8.1) 5.3 (3.8-9.7) <0.001
Insulin (mUI/mL) 14 (4-83) 12 (3-65) <0.01
HOMA INDEX 3.7 (0.8-20) 3 (0.5-16) <0.01
In conclusion, in the present study, both the tests, HbA1c and OGTT, did not reach full agreement for the diagnosis of T2D and
pre-T2D in the observed population, without significant differences between the two sexes. This may reflect the fact that the two
tests can measure different pathophysiological aspects of dysglycaemia; one positive test could not be sufficient to diagnose
possible altered conditions, suggesting that the 'diagnostic thresholds' might be reconsidered in view of the discordance
observed.
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3. Kanat M, Winnier D, Norton L, et al. The relationship between {beta}-cell function and glycated hemoglobin: results from
the veterans administration genetic epidemiology study. Diabetes Care. 2011;34:1006–1010.
4. Bonora E, Tuomilehto J. The pros and cons of diagnosing diabetes with A1C. Diabetes Care. 2011;34:S184-S190.
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regulation, identified by oral glucose tolerance test or HbA1c values, and cardiovascular disease in a cohort of European
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10. Di Pino A, Mangiafico S, Urbano F, et al. HbA1c identifies subjects with pre-diabetes and subclinical left ventricular
diastolic dysfunction. J Clin Endocrinol Metab. 2017;102:3756–3764.
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hemoglobin A1c levels. Nutr Metab Cardiovasc Dis. 2017;27:601–608.
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on definition and intervention. Diabet Med. 2002;19:708–723.
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inflammatory biomarkers and metabolic syndrome in subjects affected by obesity. Biomark Med. 2017;11(10):857–865.
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diabetes. Free Radic Biol Med. 2011;51:993–999.
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diagnosis of diabetes mellitus in Koreans. Diabetes Res Clin Pract. 2011;91:e8-e10.
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Data Accessibilty
Data are available on request from the authors. The data that support the findings of this study are available from the
corresponding author, [CV], upon reasonable request.
Clin Endocrinol. 2019;91(3):411-416. © 2019 Blackwell Publishing

Low Concordance Between HbA1c and OGTT To Diagnose Prediabetes and Diabetes in Overweight or Obesity

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22/12/2019 https://www.medscape.

Low Concordance Between HbA1c and OGTT to Diagnose

Clin Endocrinol. 2019;91(3):411-416.

Abstract and Introduction

Table 1. Subjects' characteristics and routine biochemical parameters

Men Women P value

HOMA INDEX 3.7 (0.8-20) 3 (0.5-16) <0.01

Table 1. Subjects' characteristics and routine biochemical parameters

Men Women P value

Post-OGTT insulin (mUI/mL) 63 (7-469) 74 (8-322)°°° 133 (28-331)* ## 130 (19-582)*

Table 1. Subjects' characteristics and routine biochemical parameters

Men Women P value

Uric acid (mg/dL) 6.2 ± 1.3 4.8 ± 1.2 <0.001

Table 1. Subjects' characteristics and routine biochemical parameters

Men Women P value

corresponding author, [CV], upon reasonable request.

Clin Endocrinol. 2019;91(3):411-416. © 2019 Blackwell Publishing

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