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Abstract

Background:

Del Nido cardioplegia (DNC) is a single-dose, high potassium, low-volume cardioplegia solution that has grown in favor recently. However, the use of DNC in the Asian population may be associated with certain challenges.

Methods:

Between January 2017 and April 2022, DNC was used for myocardial protection in this single-center retrospective study. In total, 5731 patients underwent open heart surgeries, where 310 patients received DNC for single or multiple procedures. A total of 307 pair of propensity-matched patients from DNC and cold blood St. Thomas cardioplegia (STC) were compared.

Results:

In total, 5085 patients with STC and 310 patients with DNC from the cohort were matched, reflecting the initial group sizes before propensity matching. About 307 patient pairs were included in the final analysis after propensity matching with the interest variables. In the STC group, the requirement for an immediate postoperative intra-aortic balloon pump (IABP) was significantly higher [18 (5.9%) in DNC versus 28 (9.1%) in STC, p = 0.021]. A 30-day mortality was comparable between the DNC and STC groups (2.9% versus 3.3%, p = 1.00). Major adverse cardiac events (MACE) (2.6% versus 3.6%, p = 0.648) showed no difference between the groups. In both single and multiple procedure subgroups, there were no statistically significant differences in 30-day mortality and MACE incidences when comparing STC and DNC.

Conclusion:

The use of DNC in adults is acceptable and adaptable. Comparable clinical outcomes between STC patients and DNC were revealed by our investigation. There were no appreciable differences in 30-day mortality or MACE despite the STC group having a much higher need for immediate postoperative IABP.

Keywords

cardiac surgical procedures cardioplegia Del Nido early outcomes propensity matching

Introduction

Conventional cardioplegia solutions utilize hypothermia and metabolic arrest in order to promote anaerobic glycolysis and scavenging of oxygen-free radicals.^1–4 Additionally, this prevents the accumulation of intracellular calcium.^5,6 However, using conventional cardioplegia solutions results in cardiomyocyte depolarization because these solutions contain high potassium.⁷ A spontaneous influx of sodium ions may occur as a result of progressive membrane depolarization, leading to an accumulation of intracellular calcium ions.^8,9 Further leakage of calcium ions from the sarcoplasmic reticulum occurs,⁹ contributing to the ‘myocardial calcium overload’ that leads to the development of ischemic reperfusion injury.¹⁰

The addition of mannitol, which can reduce edema, magnesium sulfate, which blocks calcium channels, and lidocaine, a sodium channel blocker, are the key differences between Del Nido cardioplegia (DNC) and traditional cardioplegia.^11–14 DNC has been linked to a lower risk of the need for defibrillation.¹⁵ Currently, there exist retrospective studies assessing the efficacy of DNC in a range of adult populations, including patients undergoing coronary artery bypass graft surgery (CABG), minimally invasive aortic valve surgery, and re-operative aortic valve surgery.^16–19 The findings from these studies highlighted either equivalent or superior clinical outcomes of DNC compared to conventional St. Thomas cardioplegia (STC).

In recent years, randomized controlled trials also yielded similar results,¹⁵ while Sanetra et al.²⁰ reported DNC as an acceptable alternative for STC in aortic valve replacement. Nevertheless, implementing DNC in Asian cohorts poses challenges. Patient-specific factors such as body mass index, cardiac anatomy, and comorbidities may influence the effectiveness and safety of this approach.²¹ While DNC has shown effectiveness in safeguarding myocardial function, its application in an Asian population with distinct coronary artery characteristics warrants further exploration and consideration. Consequently, this study aims to assess the optimal strategy for a mixed Asian cohort through a propensity-matched evaluation.

Methods

The data of 5731 patients who underwent open heart surgery for coronary artery revascularization, valve repair and/or replacement, and other concurrent cardiac procedures at a single tertiary cardiac institute between January 2017 and April 2022 were gathered for this single-center retrospective study.

Inclusion characteristics

Data were extracted from operation notes, medical records, and the perfusionist database. Due to the low incidence of DNC cardioplegia use in open heart surgery, the recruitment target was dependent on the number of cases available since the beginning of the use of DNC in our hospital. The data were derived from clinically indicated procedures; the choice of procedure and use of DNC or STC was dependent on the surgeon’s preference. The use of STC had a repeat dose every 15–20 min, whereas, for DNC, a modified cardioplegia solution that has been previously described by our group²² was used for a longer duration of myocardial protection.

Elective, emergency, and urgent cases were all included in the current observation. Redo-procedures were excluded, and there were no other exclusion criteria. Age at operation, gender description, race description, clinical admission reason, smoking history, pulmonary artery systolic pressure, diabetes management, preoperative HbA₁C level, hypercholesterolemia, renal disease at the time of surgery, peripheral vascular disease, carotid disease, neurological dysfunction, immunosuppressive therapy, hepatic failure, and previous cardiac surgery was the baseline patients’ characteristics.

Primary clinical endpoints

This study aimed to examine clinical aspects in this population, focusing on key endpoints: 30-day mortality rate, assessed the effectiveness of DNC, and its correlation with short-term survival. Another vital goal was assessing intra-aortic balloon pump (IABP) use, which enhances coronary perfusion pressure through mechanical circulatory support. Furthermore, myocardial infarction, stroke, and cardiovascular-related death were evaluated individually in addition to the composite endpoint, major adverse cardiovascular events (MACE).

Secondary clinical endpoints

Our study considered several secondary endpoints: postoperative atrial fibrillation (AF), acute renal injury, cardiopulmonary bypass (CPB) and aortic cross-clamp (ACX) durations, procedure length, postoperative stay duration, and operative complications. Monitoring postoperative AF occurrence evaluates cardioplegia effects. Acute renal injury offers insights into post-CPB renal insufficiency and its cardioplegia connection. CPB and cross-clamp durations assess surgical efficiency and impact. Operation duration and postoperative stay reflect resource use and recovery time. Assessing operative complications identifies surgery-related adverse events, ensuring DNC group safety and effectiveness evaluation.

Myocardial protection

STC was prepared using St. Thomas II Formulation, with precise electrolyte concentrations and osmolarity of 80 mOsm/L in 20 mL. It contained 1 mmol of procaine, 16 mmol of Mg++, and 16 mmol of K+. The administration was guided by the Calafiore table using a syringe pump (Supplemental Table 1). The initial dosage was 20 mL/kg (maximum 1500 mL), with an additional 10 mL/kg (up to 500 mL) given every 15–20 min during ACX. For antegrade cardioplegia line pressure 200–240 mmHg, flow rate 360–380 mL/min, bilateral or selective coronary ostia cardioplegia line pressure 120–140 mmHg, or retrograde cardioplegia coronary sinus pressure 35–45 mmHg was maintained.

DNC solution (1250 mL) combined plasmacyte (927.7 mL), components (72.3 mL), and blood additive (250 mL). Components included mannitol, sodium bicarbonate, potassium chloride, magnesium sulfate, and lidocaine. About 1000 mL of DNC was mixed with oxygenated blood (1:4 ratio), and the average initial DNC dose was 15 mL/kg (max 1250 mL). For aortic stenosis or hypertrophied hearts, a 20 mL/kg first dose was given. Surgeons were informed about ischemia intervals, and a second dose of DNC or STC was administered at half the volume. DNC was injected antegrade into the aortic root after cross-clamping, with the same pressure and flow rate as STC.

Statistical analysis

Propensity score matching was employed to create equivalent patient groups, ensuring comparability. Variables with p < 0.05 were identified through a two-test screening process. Logistic regression determined the propensity score for each patient to receive either DNC or STC. Patients receiving DNC were then 1:1 matched with STC recipients using the ‘nearest neighbor’ method using R-studio.^23,24 The normality of continuous variables was assessed using the Shapiro–Wilk method. After matching, baseline variables were compared using the Student’s t-test for continuous variables and the χ² test for categorical variables. Paired univariate analysis and McNemar’s test were employed to compare groups. For continuous data, mean (SD), or median (minimum–maximum) was used depending on the distribution. Nominal and ordinal categorical variables were expressed as frequency (%). The significance level for all data analyses was set at 0.05.

Results

Among 5731 patients, 150 on-pump beating and 186 off-pump coronary artery bypass surgery cases were excluded due to non-use of cardioplegia. In the cohort, 5085 STC patients were aligned with 310 DNC patients after excluding unmatched populations. Initial analysis revealed significant variations in preoperative baseline characteristics between DNC and STC groups, encompassing angiotensin-converting enzyme (ACE) inhibitors, hyperlipidemia, and left ventricle (LV) ejection fraction. Post-propensity matching for variables including age, gender, comorbidities (diabetes, hypertension), EF category, and EuroSCORE II, the final analysis comprised 307 matched pairs. The standardized mean difference (SMD) and matched clinical factors are summarized in Table 1, whereas Figure 1 depicts SMD% of 0.2% on the love plot, signifying well matched DNC and STC groups. Other preoperative baseline traits were also harmonized based on post-matching p-values.

Table 1.

Preoperative baseline patients’ characteristics.

Variables	Before propensity matching				After propensity matching
Variables	DNC (n = 310)	STC (n = 5085)	p Value	SMD%	DNC (n = 307)	STC (n = 307)	p Value	SMD%
Age at operation (mean ± SD)	58.2 ± 13.4	59.9 ± 10.9	0.100	0.15	58.2 ± 13.4)	58.7 ± 12.9)	0.660	0.04
Male (%)	201 (64.8)	3971 (78.1)	<0.001		201 (65.5)	193 (62.9)	0.560
BMI (mean ± SD)	25.8 ± 20.5	24.9 ± 4.4	0.024		25.8 ± 20.6	24.3 ± 4.75	0.210
Race (%)
Chinese (%)	216 (69.7)	3365 (66.2)	<0.001		213 (69.4)	213 (69.4)	0.050
Indian (%)	19 (6.1)	499 (9.8)			19 (6.2)	15 (4.9)
Malay (%)	33 (10.6)	947 (18.6)			33 (10.7)	52 (16.9)
Others (%)	42 (13.5)	274 (5.4)			42 (13.7)	27 (8.8)
Smoking (%)	85 (27.4)	2450 (48.2)	<0.001		84 (27.4)	118 (38.4)	0.070
Diabetes (%)	59 (19)	2251 (44.3)	<0.001	0.51	59 (19.2)	51 (16.6)	0.460	0.05
HbA₁C (mean ± SD)	2.16 ± 3.45	7.78 ± 1.80	<0.001		7.33 ± 1.55	7.37 ± 1.36	0.876
Hypertension (%)	177 (57.1)	3718 (73.1)	<0.001	0.36	176 (57.3)	168 (54.7)	0.570	0.06
Hyperlipidemia (%)	140 (45.2)	1115 (21.9)	<0.001		170 (55.4)	208 (67.8)	0.002
Renal disease (%)	17 (5.5)	358 (7.0)	0.357		16 (5.2)	16 (5.2)	1.000
Peripheral vascular disease (%)	5 (1.6)	366 (7.2)	<0.001		5 (1.6)	13 (4.2)	0.091
Carotid disease (%)	4 (1.3)	296 (5.8)	<0.001		3 (1.3)	9 (2.9)	0.262
Neurological dysfunction (%)	1 (0.3)	45 (0.9)	0.519		1 (0.3)	3 (1.0)	0.624
Ejection fraction (mean ± SD)	56.4 ± 11	50.5 ± 14.1	<0.001		56.3 ± 11	54.3 ± 14	0.050
Ejection fraction
Good (⩾50%)	262 (84.5)	3224 (63.4)	<0.001	0.43	259 (84.4)	243 (79.2)	0.010	0.11
Fair (30–49%)	37 (11.9)	1394 (27.4)		0.34	37 (12.1)	35 (11.4)		0.01
Poor (<30%)	11 (3.5)	465 (9.1)		0.19	11 (3.6)	29 (9.4)		0.20
PASP, mmHg (mean ± SD)	30.2 ± 23.2	36.1 ± 17.2	<0.001		40.4 ± 17	38.7 ± 16.2	0.280
EuroSCORE II (mean ± SD)	3.55 ± 3.74	3.75 ± 5.63	0.526	0.04	3.7 ± 3.6	3.3 ± 3.2	0.410	0.04
Redo-surgery (%)	15 (4.8)	116 (2.3)	0.014		15 (4.9)	12 (3.9)	0.695
Hemodynamic instability (%)	19 (6.1)	199 (3.9)	<0.001		19 (6.2)	12 (3.9)	0.269

BMI, body mass index; DNC, Del Nido cardioplegia; EuroSCORE, European system for cardiac operative risk evaluation; Hb, hemoglobin; PASP, pulmonary artery systolic pressure; SD, standard deviation; SMD, standardized mean difference; STC, St Thomas cardioplegia.

Figure 1.

The propensity score of the current study and the estimated probability. (a) Covariate balance showing similarity or equivalence of the covariate distributions between the DNC and STC groups after propensity score matching; unadjusted red dots became adjusted as blue dots and aligned to the ‘0’ mean difference line. (b) Distribution of the propensity shown in the scattered dot-diagram, both DNC and STC as treated, and the control unit has been well matched.

Perioperative clinical features

Initial antegrade cardioplegia (ACP) was universally administered, while subsequent doses were determined by surgeons’ preference. Notably, the STC group exhibited considerable variability (Figure 2(a)), with DNC patients often receiving only ACP. The urgency of operations significantly differed between DNC and STC groups; elective cases were more prevalent in DNC (73.6% versus 62.9%; p = 0.022). Moreover, DNC had more single non-CABG cases (41.4% versus 18.9%) and dual procedures (33.6% versus 22.8%). Conversely, STC saw more isolated CABG and ⩾3 concurrent procedures. Comparatively, DNC demonstrated extended CPB time (210.3 ± 110.1 min versus 161 ± 87.4 min, p < 0.001), longer ACX duration (108.8 ± 59.2 min versus 93.6 ± 52.3 min, p < 0.001), and overall longer operating time (335.6 ± 126.1 min versus 305.6 ± 110 min, p = 0.002) than STC.

Figure 2.

Clinical outcome summary. (a) In the study population, 55% of patients received only ACP, whereas the rest received a combination of different delivery techniques. (b) Primary clinical outcomes: (I) overall comparison between the groups showed a higher incidence of IABP requirement in the STC group; (II) subgroup comparison for a single procedure showed lower IABP requirement, mortality, MACE compared to other comparisons, but the difference was not statistically significant between the study groups; (III) subgroup comparisons for multiple procedures showed a higher incidence of IABP requirement, mortality, and MACE compared to other comparisons, but the difference was not statistically significant between the groups. (c) Box and whisker plots for the length of the procedure showed a significantly longer duration in the Del Nido group. (d) Box and whisker plots for the cardiopulmonary bypass time showed a significantly longer duration in the Del Nido group. (e) Box and whisker plots for the aortic cross-clamp time showed a significantly longer duration in the Del Nido group. Asterisks are used on the plot to indicate outliers.

Primary and secondary outcomes

The requirement for immediate perioperative IABP was notably higher in the STC group [18 (5.9%) in DNC versus 28 (9.1%) in STC, p = 0.021]. In the single procedure subgroup analysis, STC had a lower rate of IABP necessity (3.6% versus 1.8%, p = 1.00); for multiple procedures, DNC showed a slightly higher rate (8.2% versus 10.2%, p = 1.00), but this wasn’t statistically significant. Thirty-day mortality rates were similar between DNC and STC groups (2.9% versus 3.3%, p = 1.00). MACE incidence showed no difference (2.6% versus 3.6%, p = 0.648). Rates were consistent in single or multiple procedures (Figure 2(b)). Post-surgery, DNC led to more new-onset AF [83 (27%) versus 53 (17.3%), p = 0.003) and acute renal injury [32 (10.4%) versus 7 (2.3%), p < 0.001]. Length of stay, perioperative issues, permanent pacemaker need, neurologic problems, and prolonged ventilation did not significantly differ (Table 2). STC group experienced the shorter procedure, CPB, and ACX times (Figure 2(c)–(e)). Propensity-matched analysis for single and multiple procedures subgroups was conducted and shown in Table 2. Table 3 outlines a subgroup study of DNC group attributes.

Table 2.

Perioperative clinical outcomes.

Variables	After propensity matching			Single procedure			Multiple procedure
Variables	DNC (n = 307)	STC (n = 307)	p Value	DNC (n = 55)	STC (n = 55)	p Value	DNC (n = 49)	STC (n = 49)	p Value
Operative urgency (%)			0.022			0.090			0.336
Elective (%)	226 (73.6)	192 (62.9)		40 (72.7)	40 (72.7)		30 (61.2)	36 (73.5)
Urgent (%)	48 (15.6)	77 (25.1)		10 (18.2)	4 (7.3)		5 (10.2)	5 (10.2)
Emergency (%)	32 (10.4)	36 (11.7)		5 (9.1)	11 (20)		14 (28.6)	8 (16.3)
Salvage (%)	1 (0.3)	1 (0.3)		–	–		–	–
Type of procedure (%)			<0.001	–	–	–	–	–	–
Isolated procedure (%)	185 (60.3)	218 (71.0)		–	–	–	–	–	–
2 procedures (%)	103 (33.6)	70 (22.8)		–	–	–	–	–	–
⩾3 procedures	19 (6.1)	19 (6.2)		–	–	–	–	–	–
CPB time, min (mean ± SD)	210.3 ± 110.1	161 ± 87.4	<0.001	168.5 ± 73.1	142.3 ± 69.2	0.056	245.2 ± 124.6	220.3 ± 117.7	0.310
ACX time, min (mean ± SD)	108.8 ± 59.2	93.6 ± 52.0	<0.001	89.8 ± 37.5	93.2 ± 53.4	0.702	122.7 ± 69.1	131.2 ± 72.9	0.560
Length of procedure, min (mean ± SD)	335.6 ± 126.1	305.55 ± 110	0.002	286.9 ± 78.5	282.8 ± 106.3	0.821	364.7 ± 117.3	371 ± 161	0.827
Length of stay, day (mean ± SD)	13.9 ± 21	12.5 ± 17.7	0.399	10.1 ± 6.5	12.1 ± 10.4	0.249	–	–	–
Perioperative complications (%)	46 (15)	31 (10.1)	0.101	4 (7.3)	3 (5.5)	1.000	5 (10.2)	8 (16.3)	0.549
PPM (%)	18 (5.9)	8 (2.6)	0.064	3 (5.5)	5 (9.1)	0.727	1 (2.0)	1 (2.0)	1.00
New-onset AF (%)	83 (27)	53 (17.3)	0.003	14 (25.5)	10 (18.2)	0.481	15 (30.6)	9 (18.4)	0.180
IABP (%)	18 (5.9)	28 (9.1)	0.021	2 (3.6)	1 (1.8)	1.000	4 (8.2)	5 (10.2)	1.00
Neurological complications (%)	11 (3.6)	5 (1.6)	0.210	1 (1.8)	0	–	3 (6.1)	2 (4.1)	1.00
Prolonged ventilation* (%)	26 (8.5)	29 (9.4)	0.771	0	2 (3.6)	–	5 (10.2)	11 (22.4)	0.180
Acute renal injury (%)	32 (10.4)	7 (2.3)	<0.001	2 (3.6)	1 (1.8)	1.000	7 (14.3)	0	–
30-day mortality (%)	9 (2.9)	10 (3.3)	1.000	0	1 (1.8)	–	1 (2.0)	3 (6.1)	0.500
MACE^$ (%)	8 (2.6)	11 (3.6)	0.648	0	1 (1.8)	–	1 (2.0)	3 (6.1)	0.500

>48 h of mechanical ventilation.

Postoperative MI and cardiac death.

ACX, aortic cross-clamp; AF, atrial fibrillation; CABG, coronary artery bypass graft surgery; CPB, cardiopulmonary bypass; DNC, Del Nido cardioplegia; IABP, intra-aortic balloon pump; MACE, major advance cardiac events; PPM, permanent pacemaker; SD, standard deviation; STC, St Thomas cardioplegia.

Table 3.

DNC group traits.

Variables	DNC (N = 310)
Variables	Mean/N	SD/%
Temperature (°C)	31.4	2.8
DNC volume (mL)	1115.1	453.2
Cannula size (arterial) Fr	NA	NA
Cannula size (venous) Fr	NA	NA
Number of doses given (%)
1	210	684
2	58	18.9
3	30	9.8
4	6	2.0
5	3	1.0
First dose volume (mL)	948.8	242.2
Volume to arrest (mL)	216.7	145.3
Pre-CPB serum K⁺ (mmol/L)	3.7	0.4
Serum K⁺ after DNC dose (mmol/L)	4.6	4.5
Post-CPB serum K⁺ (mmol/L)	4.01	0.4
Pre versus post-CPB serum K⁺ (mmol/L)	0.28	0.53
On-CPB lactate (mmol/L)	3.6	2.3
Post-op lactate (mmol/L)	4.0	2.9
CPB versus post-op lactate (mmol/L)	0.46	1.9
Use of hemo-filter, yes (%)	213	65.5
Hemo-filter filtrate (mL)	2746.9	1918.8
Cell saver volume (mL)	825.5	585.2
Donor blood transfusion volume (mL)	598.3	358
Arrhythmias (%)	36	11.7
Defibrillation (%)
None	269	87.6
Once	20	6.5
>1	20	6.5
Time taken for heart to return to sinus rhythm, (min)	2.1	2.3

CPB, cardiopulmonary bypass; DNC, Del Nido cardioplegia; NA, not applicable.

Discussion

This study reveals that in adult cardiac surgery, using cardioplegia – whether single or multiple procedures – does not significantly impact 30-day mortality or MACE rates post-coronary artery bypass surgery. Compared to STC, the DNC group required more immediate postoperative IABP and had a higher incidence of new-onset AF and acute renal damage. However, no substantial differences were observed between the groups in terms of hospital stay duration, perioperative complications, PPM requirement, neurological disorders, or extended ventilation. These findings suggest that DNC can be a viable alternative to STC in adult cardiac surgery without compromising outcomes.

While prior Asian studies mainly focused on juvenile patients and yielded favorable results for DNC cardioplegia,^24–26 our mixed multiracial Asian population-based study provides a broader representation. Although specific patient characteristics, surgeon training, and institutional procedures influence cardioplegia choice, our results align with studies showing DNC’s non-inferiority- in adult cardiac surgery.^13,15,25

Contrary to Urcun and Pala’s²⁷ findings, our series indicated longer CPB and ACX times in the DNC group. These timings are indicative of safe myocardial protection duration. DNC’s key components – mannitol for scavenging radicals, magnesium sulfate for calcium channel blockage, and lidocaine as an anti-arrhythmic – contribute to its efficacy.²⁸ Notably, DNC’s distinguishing features from STC, including its components, have been associated with reduced defibrillation needs.^15,29 In our study, the DNC group experienced a return to sinus rhythm within approximately 2–4 min, with 87.6% avoiding defibrillation.

Additionally, this study’s findings underscore the importance of examining various outcomes beyond 30-day mortality and MACE rates in cardiac surgery. In a recent meta-analysis conducted by Fresilli et al.,³⁰ the advantages of using DNC cardioplegia become even more evident.³¹ Their research revealed significant reductions in outcomes such as stroke and postoperative acute kidney injury compared to STC. These additional benefits further support the consideration of DNC as a viable alternative in adult cardiac surgery.

Limitation

While this retrospective study was inherent limitations, including susceptibility to confounding variables, potential recall bias, and the absence of randomization, we have tried to mitigate these constraints through propensity matching. However, it is important to recognize that further investigation and a more detailed analysis of specific procedure types within our cohort are necessary. Propensity matching, a robust statistical technique, has been employed to balance patient characteristics and enhance the internal validity of our findings, yet it may not entirely eliminate all potential sources of bias. Additionally, our single-center study design may limit the generalizability of our results to the broader population, as our patient population may not fully represent the wider community.

Conclusion

Our study findings imply that DNC use in adult cardiac surgery should be regarded as appropriate and adaptive. The study found that patients who had STC and those who received DNC had similar clinical results. Although the STC group required a higher IABP immediately after surgery, there were no appreciable differences in 30-day mortality or the frequency of major adverse cardiac events between the two groups. These findings suggest that DNC can deliver outcomes equivalent to STC while posing a possible reduction in the requirement for postoperative assistive therapies.

Supplemental Material

sj-docx-1-tak-10.1177_17539447231210713 – Supplemental material for Non-selective Del Nido and St Thomas cardioplegia in adults: analysis of early clinical experience using propensity matching

Supplemental material, sj-docx-1-tak-10.1177_17539447231210713 for Non-selective Del Nido and St Thomas cardioplegia in adults: analysis of early clinical experience using propensity matching by Faizus Sazzad, Zhi Xian Ong, Geok Seen Ong, Hai Dong Luo, Si Guim Goh, Theo Kofidis and Sorokin Vitaly in Therapeutic Advances in Cardiovascular Disease

Footnotes

Acknowledgements

None.

Declarations

ORCID iD

Faizus Sazzad

Supplemental material

Supplemental material for this article is available online.

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