what type of shock can result from a reaction to iodinated contrast media?
PLoS One. 2014; 9(6): e100154.
Anaphylaxis to Iodinated Dissimilarity Media: Clinical Characteristics Related with Development of Anaphylactic Daze
Min-Hye Kim
1 Department of Internal Medicine, Division of Allergy and Clinical Immunology, Seoul National University Hospital, Seoul, South korea,
2 Institute of Allergy and Clinical Immunology, Seoul National University Medical Inquiry Center, Seoul, Democracy of Korea,
3 Seoul National University Hospital Regional Pharmacovigilance Center, Seoul, Republic of korea,
four Section of Internal Medicine, Ewha Womans University School of Medicine, Seoul, Democracy of Korea,
Suh-Immature Lee
1 Department of Internal Medicine, Sectionalisation of Allergy and Clinical Immunology, Seoul National University Hospital, Seoul, South korea,
ii Institute of Allergy and Clinical Immunology, Seoul National University Medical Research Center, Seoul, Republic of korea,
Seung-Eun Lee
1 Department of Internal Medicine, Division of Allergy and Clinical Immunology, Seoul National Academy Infirmary, Seoul, Republic of korea,
2 Institute of Allergy and Clinical Immunology, Seoul National University Medical Research Center, Seoul, Republic of korea,
Min-Suk Yang
1 Department of Internal Medicine, Sectionalisation of Allergy and Clinical Immunology, Seoul National University Infirmary, Seoul, Republic of Korea,
2 Institute of Allergy and Clinical Immunology, Seoul National Academy Medical Research Center, Seoul, South korea,
5 Department of Internal Medicine, SMG-SNU Boramae Medical Center, Seoul, South korea,
Jae-Woo Jung
2 Plant of Allergy and Clinical Immunology, Seoul National University Medical Research Center, Seoul, South korea,
vi Department of Internal Medicine, Chung-Ang University College of Medicine, Seoul, South korea,
Chang Min Park
7 Department of Radiology and Institute of Radiations Medicine, Seoul National Academy College of Medicine, Seoul, Republic of Korea,
Whal Lee
7 Department of Radiology and Institute of Radiation Medicine, Seoul National University College of Medicine, Seoul, South korea,
Sang-Heon Cho
1 Department of Internal Medicine, Division of Allergy and Clinical Immunology, Seoul National Academy Hospital, Seoul, Republic of Korea,
2 Institute of Allergy and Clinical Immunology, Seoul National University Medical Research Center, Seoul, Democracy of Korea,
3 Seoul National Academy Hospital Regional Pharmacovigilance Center, Seoul, South korea,
Hye-Ryun Kang
1 Department of Internal Medicine, Division of Allergy and Clinical Immunology, Seoul National University Hospital, Seoul, Democracy of Korea,
2 Plant of Allergy and Clinical Immunology, Seoul National University Medical Research Center, Seoul, Democracy of Korea,
3 Seoul National University Hospital Regional Pharmacovigilance Center, Seoul, Republic of Korea,
Jacques Zimmer, Editor
Received 2014 January 24; Accepted 2014 May 22.
Abstruse
Objective
Anaphylaxis is the most severe form of radiocontrast media (RCM) induced hypersensitivity and can exist life-threatening if profound hypotension is combined. With increased use of iodine based RCM, related hypersensitivity is rapidly growing. However, the clinical characteristics and risk factors of RCM induced anaphylaxis accompanied by hypotension (anaphylactic shock) are not clearly divers. This study was performed to investigate the risk factors of RCM induced anaphylactic shock and the clinical value of RCM peel testing to identify causative agents in affected patients.
Methods
We analyzed the data of RCM induced anaphylaxis monitored by an inhospital pharmacovigilance middle at a third teaching infirmary from Jan 2005 to December 2012 and compared the clinical features and skin exam results co-ordinate to the accompanying hypotension.
Results
Among total of 104 cases of RCM induced anaphylaxis, 34.6% of patients, developed anaphylaxis on their kickoff exposure to RCM. Anaphylactic patients presenting with shock were older (57.iv vs. 50.1 years, p = 0.026) and had a history of more ofttimes exposure to RCM (v.1±7.8 vs. ane.9±three.3, p = 0.004) compared to those without hypotension. Among RCMs, hypotension was more frequent in anaphylaxis related to iopromide compared to other agents (85.0% vs. 61.4%, p = 0.011). Skin tests were performed in 51 patients later on development of RCM induced anaphylaxis. Overall peel examination positivity to RCM was 64.7% and 81.8% in patients with anaphylactic shock.
Conclusion
RCM induced anaphylactic shock is related to multiple exposures to RCM and nigh patients showed skin test positivity to RCM.
Introduction
Anaphylaxis is a rapid-onset severe hypersensitivity reaction that tin can be fatal. Although decease from anaphylaxis is not common and almost episodes of anaphylaxis can be reversed by a single dose of epinephrine, severe anaphylaxis accompanied with cardiovascular collapse can be resistant to treatment and issue in death.
As the use of computed tomography (CT) is chop-chop growing, iodine based radiocontrast media (RCM) is administered almost 75,000,000 times per yr worldwide [1]. As low osmolality non-ionic contrast agents replaced loftier-osmolality ionic ones, the incidence of immediate RCM hypersensitivity diminished remarkably from 3.viii–12.7% to 0.seven–3.1% [2]–[4]. Similarly, the incidence of severe immediate RCM hypersensitivity likewise decreased from 0.ane–0.4% to 0.01–0.04%. However, anaphylactic deaths still occur in i–three per 100,000–1,000,000 administrations regardless of ionicity [5], [6]. Soon, the clinical characteristics and take a chance factors for the development of anaphylactic shock are not conspicuously defined.
The principle of post-anaphylaxis direction is to avoid the causative agents. Although other imaging tin can be used as an culling test in RCM hypersensitivity patients, CT imaging has its own reward and unavoidable in some clinical situations. Although antihistamines and systemic steroids tin be used as preventive measures, they cannot ensure consummate prevention of RCM induced anaphylaxis [7], [8]. Currently, at that place are no established guidelines on premedication for RCM induced anaphylaxis [9]. Therefore, data on a causal agent and safer substitutes will be very useful for patients who need contrast enhanced CT scan despite previous history of RCM induced anaphylaxis. Until recently, diagnostic value of RCM skin test has been underestimated and at that place are but a limited number of studies which evaluated the sensitivity of RCM skin testing to various RCM [10]–[12].
This study was performed to investigate the risk factors for the development of hypotension and the clinical value of RCM pare testing to identify causative agents in RCM induced anaphylaxis.
Methods
1. Study Subjects
This study protocol was approved by the institutional review lath (IRB) of Seoul National Academy Hospital. Informed consents of patients were exempted from IRB considering this report only used retrospective chart review data and all personal information was eliminated and coded as capricious number which were not personally-identifiable. Research data was accessed but by researchers using password.
Nosotros extracted all the cases of RCM induced hypersensitivity based on ATC code of causative agents (V08A: X-ray dissimilarity media, iodinated, V08B: X-ray contrast media, not-iodinated)' and WHOART (ARRN: 0712 allergic reaction, 0713 anaphylactic shock, 0714 anaphylactoid reaction, 2237 anaphylactic reaction, 2268 documented hypersensitivity to administered drug) from our inhospital pharmacovigilance database collected from January 2005 to Dec 2012 at Seoul National University Hospital, in Seoul, Korea. Demographic and clinical data of affected patients such as age, sex, number of contrast exposures, laboratory exam results, and underlying diseases based on ICD-10 were nerveless from electronic medical records. This study dealt only with CT procedures, not with other procedures such as cardiac catheterization or coronary angiography.
All the medical records were thoroughly re-evaluated by ii allergy specialists to assess clinical features of anaphylaxis and the presence of previous contrast hypersensitivity reactions. Anaphylaxis was diagnosed if cases satisfied the criteria of anaphylaxis suggested by the National Constitute of Allergy and Communicable diseases and Food Allergy and the Anaphylaxis Network [13]. Hypotension was considered as a systolic blood pressure less than 90 mmHg or greater than thirty% subtract from an private's baseline. [13] Hypotension unrelated with underlying diseases or other drugs was considered a manifestation of anaphylaxis.
After completing review, patients with anaphylaxis were classified into two groups depending on combined hypotension. We analyzed the data to identify risk factors for the development of anaphylactic daze by comparison anaphylactic patients combined with and without hypotension.
two. Skin Tests with Iodinated Dissimilarity Agents
Skin tests were carried out after experiencing RCM induced anaphylaxis for those patients who agreed to undergo skin testing. Pare prick and intradermal tests were performed on the volar function of the forearm with 6 unlike RCM used in our infirmary - iopromide (Ultravist®, Bayer Healthcare, Brussels, Belgium), iopamidol (Pamiray®, Dongkook Pharm. Co., Ltd, Korea), iomeprol (Iomeron®, Bracco, Milan, Italian republic), iohexol (Omnipaque®, Armersham Health, Princeton, NJ), iodixanol (Visipaque®, Armersham Wellness, Princeton, NJ), and iobitridol (Xenetics®, Guerbet, Gorinchem, Netherlands). Undiluted solution and ane∶10 diluted solution were used for the skin prick exam and intradermal exam, respectively, as used in previous studies [10], [12], [14], [15]. Histamine and normal saline were used as positive and negative control, respectively. The results were interpreted 15 minutes after the prick or the intradermal injection. Skin prick examination was determined to be positive when wheal diameter was greater than 3 mm, and intradermal examination was adamant to be positive when wheal diameter increased 3 mm or more than than the initial bleb [12]. The rate and factors contributing to the positivity of RCM skin examination were analyzed.
3. Statistical Analysis
SPSS (version 19.0) was used to analyze the information. To compare the clinical features of two groups, Student t-exam or Mann-Whitney exam was used for continuous variables, and Chi-foursquare test or Fisher's exact examination was used for categorical variables. To identify the risk factors related with anaphylactic shock and a positive skin test, multiple logistic regression was used. We included adjustment factors that had a P-value less than 0.1 in the univariate analysis, and other clinically important factors such as age and sexual practice. A P-value less than 0.05 was considered statistically meaning.
Results
1. Clinical Characteristics of the Report Subjects and Accompanied Anaphylaxis
A total number of dissimilarity-enhanced CT scans during the study period was 632,513. A full of 104 cases of RCM related anaphylaxis were monitored during the study menstruation. The incidence of contrast-induced anaphylaxis was 0.016%. Every bit the total number of RCM use increased over the written report period, the RCM related anaphylaxis too showed increasing tendency in number (Figure i). The mean age was 55.6±13.1 years and 41.three% (43/104) of them were male person (Tabular array ane).
Anaphylactic reactions and full number of RCM use in every twelvemonth of the study menses.
Table 1
Clinical characteristics according to the development of hypotension.
| Total (Due north, %) | Anaphylactic shock (N, %) | Normotensive anaphylaxis (N, %) | P-value | |
| Number | 104 | 78 | 26 | |
| Age (years)* | 55.6±13.4 | 57.4±13.ii | 50.one±xiii.0 | 0.024 |
| Male gender, % | 43 (41.three) | 35 (44.9) | eight (30.8) | 0.254 |
| Number of previous exposure to RCM* | 4.three±7.1 | 5.one±7.8 | 1.9±3.three | 0.004 |
| None | 36 (34.6) | 24 (xxx.8) | 12 (46.2) | 0.369 |
| 1 | 17 (16.3) | 13 (16.vii) | 4 (15.iv) | |
| ≥2 | 51 (49.0) | 41 (52.half-dozen) | 10 (38.5) | |
| Previous RCM reactions | 21/68 (30.9) | 18/54 (33.3) | 3/xiv (21.4) | 0.362 |
| WBC count (/µL) | 5,844.vii±1,883.eight | five,886±one,921 | v,617±1,720 | 0.668 |
| Eosinophil count (/µL) | 62.0±84.4 | 64.ii±86.nine | 50.0±71.four | 0.574 |
| Hypersensitivity Symptoms | ||||
| Skin symptoms | 69 (66.iii) | 49 (62.8) | 20 (76.9) | 0.235 |
| Urticaria/erythema | 53 (51.0) | 36 (46.2) | 17 (65.iv) | 0.114 |
| Angioedema | 34 (32.seven) | 21 (26.nine) | 13 (50.0) | 0.052 |
| Respiratory symptoms* | fifty (48.i) | 32 (41.0) | eighteen (69.2) | 0.022 |
| Dyspnea† | 42 (twoscore.four) | 24 (thirty.8) | xviii (69.2) | 0.001 |
| Cardiovascular symptoms† | 88 (84.6) | 78 (100.0) | x (38.v) | <0.001 |
| Gastrointestinal symptoms | xx (19.2) | xvi (20.five) | four (xv.4) | 0.775 |
| Underlying allergic diseases | 12 (xi.five) | 8 (ten.3) | 4 (15.4) | 0.464 |
| Radiocontrast media‡ | ||||
| Iopromide* | threescore (57.7) | 51 (65.4) | 9 (34.6) | 0.011 |
| Iopamidol | 12 (xi.6) | 8 (ten.3) | iv (15.4) | 0.726 |
| Iomeprol | 11 (x.half-dozen) | eight (10.3) | iii (11.5) | one.000 |
| Iohexol | 7 (6.7) | 3 (iii.eight) | 4 (15.4) | 0.064 |
| Iobitridol | iii (ii.nine) | 3 (3.viii) | 0 (0.0) | 0.571 |
| Iodixanol | iv (3.8) | iii (three.viii) | one (iii.8) | 1.000 |
| Unidentified agents* | 7 (6.7) | 2 (ii.half-dozen) | v (19.2) | 0.010 |
| Positive skin exam† | 33/51 (64.7) | 27/33 (81.8) | 6/18 (33.3) | 0.001 |
| Skin prick test | 1/51 (2.0) | ane/33 (3.0) | 0/xviii (0.0) | ane.000 |
| Intradermal test† | 33/51 (64.7) | 27/33 (81.8) | 6/18 (33.3) | 0.001 |
The median number of previous RCM exposures was one.0 (interquartile range (IQR), 0.0–five.0) before the development of the first anaphylaxis. While anaphylaxis developed at the first exposure to RCM in 34.half-dozen% (36/104) of patients, 65.iv% (68/104) of patients experienced anaphylaxis on repeated exposure to RCM and 21 of 68 (thirty.9%) had a milder form of hypersensitivity reactions in previous exposure to RCM.
Among hypersensitivity symptoms present in patients with anaphylaxis, cardiovascular symptoms were the most common (88/104, 84.6%), followed by pare symptoms (69/104, 66.iii%) and respiratory symptoms (50/104, 48.1%) (Table one). Most symptoms occurred inside several minutes after the RCM injection. 70-eight patients experienced anaphylaxis with hypotension (anaphylactic stupor) and 26 patients had anaphylaxis without hypotension.
ii. Comparing of Clinical Characteristics Co-ordinate to the Evolution of Hypotension
Compared to anaphylactic patients without hypotension, patients who presented with anaphylactic shock were older (57.4 vs. 50.1 years, p = 0.026) and had significantly college number of previous RCM exposures (5.one±vii.viii vs. 1.ix±3.3, p = 0.004). Of note, the number of patients who underwent previous CT more than two times was 52.6% and 38.five%, respectively in anaphylactic patients with and without hypotension. Peculiarly, the proportion of previous exposure to RCM more than than 5 times showed significant difference between anaphylactic patients with and without hypotension (35.4% vs. 9.1%, p = 0.018, Figure 2).
Comparing of the number of dissimilarity exposures according to the presence of hypotension.
*p<0.05.
In terms of the causative contrast agent, hypotension was more frequent amongst anaphylaxis related to iopromide compared to other agents (85.0% vs. 61.4%, p = 0.011). Iopromide use was more frequently observed in patients with hypotension than in patients without it among patients with anaphylaxis (65.iv% vs 34.6%, p = 0.011). With multiple logistic regression analysis after adjustment of age, sex, diabetes, and number of previous contrast exposure, iopromide utilize was nonetheless a risk gene for an anaphylactic shock (OR 3.088, 95% confidential interval (CI) = i.078–viii.843, p = 0.036).
3. Comparison of Clinical Characteristics According to Skin Test Positivity
L-one patients with anaphylaxis followed the recommendation of allergists and underwent RCM skin exam and the other 53 patients refused to perform peel examination because they did not have a scheduled follow-up CT in the almost future.
The mean interval betwixt the time of anaphylaxis and pare exam was 14.8 months (IQR 3.iv–38.9). Skin exam was performed in 41% of patients within ane year since they experienced anaphylaxis. The remaining patients underwent pare exam at the time when more than than one year passed since anaphylaxis occurred (IQR 21.8–64.1).
Among those 51 patients with RCM skin test results, 33 (64.seven%) had a positive response to at to the lowest degree one RCM while 18 patients (35.three%) did not testify positivity to any RCM tested. In anaphylactic patients accompanied by hypotension, skin examination showed 81.8% positivity. Among 33 patients with positive RCM skin examination results, hateful 1.1 contrast media (1.one±1.1) were positive per person.
Precise data on the culprit RCM was available in 29 patients. Twenty-two (75.9%) patients showed positivity to RCM including their culprit RCM; 14 patients showed single positivity to the culprit RCM; 8 patients showed positivity to other RCMs in add-on to the culprit one. Another seven patients responded to RCM agents other than the culprit 1.
The positivity charge per unit of pare test for each dissimilarity agent is varied from 0.0% to 100.0% (Tabular array 2). Iobitridol showed the highest sensitivity (100%) followed by iopromide (59.3%) and iodixanol (50.0%). Yet, all 5 patients who experienced iohexol induced anaphylaxis were negative in skin test with iohexol.
Table 2
Sensitivity and false negative rate on skin test.
| Causative RCM | Sensitivity | Simulated negative rate | ||
| To whatsoever RCM N (%) | To culprit RCM North (%) | To any RCM N (%) | To culprit RCM N (%) | |
| Iopromide | 20/27 (74.ane) | 16/27 (59.3) | 7/27 (25.ix) | 11/27 (twoscore.7) |
| Iopamidol | ii/5 (xl.0) | 1/5 (20.0) | three/v (60.0) | four/5 (lxxx.0) |
| Iomeprol | 4/5 (80.0) | ii/5 (40.0) | one/5 (twenty.0) | 3/5 (60.0) |
| Iohexol | 1/v (20.0) | 0/v (0.0) | 4/5 (eighty.0) | 5/5 (100.0) |
| Iobitridol | two/two (100.0) | 2/two (100.0) | 0/two (0.0) | 0/2 (0.0) |
| Iodixanol | 1/2 (50.0) | 1/2 (50.0) | one/2 (50.0) | 1/2 (50.0) |
| Total | 30/46 (65.ii)* | 22/46 (47.8) | xvi/46 (32.6) | 24/46 (52.1) |
In patients with a positive RCM skin test, hypotension (79.iv% vs. 35.iii%, p = 0.004) and gastrointestinal symptoms (28.1% vs. 0.0%, p = 0.047) were more frequent compared to patients who had a negative RCM pare examination. With multiple logistic regression assay afterward adjustment by age, sex and diabetes, the presence of hypotension was a characteristic associated with a RCM pare test positivity (OR ten.0, 95% CI two.105–47.098, p = 0.004). However, skin test positive rate was non different according to the history of previous RCM hypersensitivity reactions, accumulated number of exposures to the RCM, and underlying allergic disease.
Discussion
Incidence of anaphylaxis is increasing rapidly and known to exist iv–50/100,000 person-years [sixteen]. In adults, drugs are the most mutual cause of anaphylaxis [16], [17] and radiocontrast media was the most commonly involved drug in a report of Korean tertiary care hospital [18]. Although the incidence of RCM hypersensitivity decreased as high-osmolality ionic contrasts were replaced past low-osmolality not-ionic ones, anaphylactic death still occurred regardless of ionicity [5], [six].
Traditionally, immediate hypersensitivity reactions to RCM were considered representative of not-IgE mediated 'anaphylactoid reaction' since it can occur on the first exposure and does non ever recur on the repeated exposure [1], [10], [11], [19]. However, a previous written report showed that only 30% of firsthand RCM hypersensitivity adult at the first exposure to RCM [20] and our study also revealed that but 35% of RCM induced anaphylaxis occurred at the get-go exposures to RCM. Nosotros found that milder hypersensitivity symptoms heralded anaphylaxis in i/3 of the patients on preceding exposure to RCM. Multiple exposures and a previous hypersensitivity reaction prior to RCM induced anaphylaxis suggest that an immunologic mechanism may have some role in the development of some RCM induced anaphylaxis.
Anaphylaxis is a severe, life-threatening systemic hypersensitivity reaction involving at to the lowest degree two or more organs at the aforementioned time. However, diagnosis of anaphylaxis tin exist made if sudden hypotension develops later exposure to a known allergen. Based upon symptoms, anaphylaxis can be classified into mild, moderate, and severe form. [21] When hypotension occurs as a manifestation of anaphylaxis either as a sole characteristic or with other symptoms, physicians should pay attention to the evolution of potential cardiovascular collapse which is the main cause of mortality in anaphylaxis [22]. There are several known take chances factors for a severe RCM hypersensitivity such as previous history of RCM hypersensitivity, asthma, allergies requiring medical treatment, utilize of beta-adrenergic blockers, female gender, Indian and Mediterranean ethnicity, and malignant tumor [23]. However, there was no data on the risk factors for the development of hypotension in anaphylaxis. In this study, nosotros reported risk factors for anaphylactic stupor such as older age, previous multiple exposures to RCM, iopromide use. Yet, nosotros do non have a articulate picture of what the overall anaphylaxis charge per unit is using iopromide or the other written report contrast agents, since patients without anaphylaxis are not included in the study. Secondly, the number of administrations of other contrast agents was too small-scale to provide statistically pregnant results. In other words, we cannot conclude from this study that iopromide is more than likely to cause anaphylaxis than whatsoever of the other contrast agents, but among the anaphylactic patients, iopromide was associated with more astringent forms of anaphylaxis (anaphylaxis with hypotension). In addition, anaphylaxis with hypotension showed stronger association with RCM pare exam positivity than anaphylaxis without hypotension. Although skin examination positivity might be the result of directly mast prison cell activation by RCM, it is more likely that IgE mediated hypersensitivity may have a office in the development of RCM induced anaphylaxis when presented with hypotension.
Skin examination is widely used to identify the causative agents in IgE mediated hypersensitivity [12], [fifteen], [sixteen]. Previously, sensitivity of the intradermal test was reported as high equally 73% when performed with undiluted solutions [xx]. Yet, this result may have been overestimated by irritation with undiluted RCM and a 1∶10 solution has been preferred for intradermal test with RCM in full general. The positive rate of the intradermal skin test was variable and reported as low equally 4.2% among patients with RCM hypersensitivity [10]. On the other hand, data from the European Network of Drug Allergy multicentre study demonstrated a 50% positive charge per unit of RCM skin test in firsthand reactors [14]. Recently, Kim et al. reported that a significantly higher sensitivity positive charge per unit of RCM pare test in severe immediate reactions (57.1%) compared with mild (12.nine%) and moderate reactions (25.0%) and suggested their minor utility in evaluating severe adverse reactions retrospectively [24]. In this written report, we observed much higher positive rate of RCM pare examination in patient with RCM induced anaphylaxis (64.seven%). Positive charge per unit went up as high as 81.8% among patients with anaphylactic shock and it is the highest value ever reported in RCM hypersensitivity. Iii quarter of patients who showed skin examination positivity responded to the very same RCM used at the time of anaphylaxis and cross reactivity rate to other RCMs was low. These findings suggest that a substantial proportion of patients with RCM induced anaphylaxis, specially anaphylactic stupor, may have specificity to causative agents and pare tests tin provide information on the safe substitutes. Nonetheless, considering negativity in one third of patients, peel test is non helpful to choose safe alternative RCMs in some populations and clinical reasoning is needed on interpreting the results.
Although we could non perform pare test in negative controls, peel test positivity in the negative control is known to be negligible. At that place are several studies which elucidated very low positivity of skin test in the negative controls. Brockow et al. reported that positivity of skin examination was 0.0% (0/11)–four.2% (3/71) in the negative controls [14]. Kim et al. performed RCM skin testing on 1,048 Korean subjects before dissimilarity-enhanced CT and found just 1 case of positive immediate skin examination (0.09%) [24].
There are several limitations in this written report. The main limitation is its retrospective design and underreporting of adverse reaction to spontaneous reporting systems. Some other limitation is the lack of data on the number of private RCM used in dissimilarity-enhanced CT during the study period. Thus, big scale prospective studies including sufficient number of patients reacting to each RCM are needed in order to define the exact incidence and run a risk factors of RCM induced anaphylaxis.
Conclusion
RCM induced anaphylactic shock is related with multiple exposure to RCM and skin exam positivity to RCM.
Funding Statement
This research was supported by a grant from Ministry of Food and Drug Prophylactic to operation of the regional pharmacovigilance heart in 2014. The funders had no function in written report pattern, data collection and analysis, determination to publish, or preparation of the manuscript.
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