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* Center for Applied Ethics and Professional Practice, Education Development Center, Newton, Massachusetts
Harvard Medical School, Boston, Massachusetts
Chevy Chase, Maryland
Verbar; Palliative Care Institute, Methodist Hospital, Houston, Texas
¶ Johns Hopkins University and Children’s Center, Baltimore, Maryland
# Albert Einstein College of Medicine, Bronx, New York
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Methods. Three children’s hospitals and 4 general hospitals with PICUs in eastern, southwestern, and southern parts of the United States were surveyed. This population-based sample was composed of attending physicians, house officers, and nurses who cared for children (age: 1 month to 18 years) with life-threatening conditions in PICUs or in medical, surgical, or hematology/oncology units, floors, or departments. Main outcome measures included concerns of conscience, knowledge and beliefs, awareness of published guidelines, and agreement or disagreement with guidelines.
Results. A total of 781 clinicians were sampled, including 209 attending physicians, 116 house officers, and 456 nurses. The overall response rate was 64%. Fifty-four percent of house officers and substantial proportions of attending physicians and nurses reported, "At times, I have acted against my conscience in providing treatment to children in my care." For example, 38% of critical care attending physicians and 25% of hematology/oncology attending physicians expressed these concerns, whereas 48% of critical care nurses and 38% of hematology/oncology nurses did so. Across specialties, 
20 times as many nurses, 15 times as many house officers, and 10 times as many attending physicians agreed with the statement, "Sometimes I feel we are saving children who should not be saved," as agreed with the statement, "Sometimes I feel we give up on children too soon." However, hematology/oncology attending physicians (31%) were less likely than critical care (56%) and other subspecialty (66%) attending physicians to report, "Sometimes I feel the treatments I offer children are overly burdensome." Many respondents held views that diverged widely from published recommendations. Despite a lack of awareness of key guidelines, across subspecialties the vast majority of attending physicians (range: 92–98%, depending on specialty) and nurses (range: 83–85%) rated themselves as somewhat to very knowledgeable regarding ethical issues.
Conclusions. There is a need for more hospital-based ethics education and more interdisciplinary and cross-subspecialty discussion of inherently complex and stressful pediatric end-of-life cases. Education should focus on establishing appropriate goals of care, as well as on pain management, medically supplied nutrition and hydration, and the appropriate use of paralytic agents. More research is needed on clinicians’ regard for the dead-donor rule.
Key Words: pediatric palliative care • end-of-life care • clinical decision-making • pain management • ethics
Since Duff and Campbell1 first brought the issue to public attention, the federal government,2 medical3 and nursing4 specialty societies, independent ethics institutes,5 and the courts6–10 have addressed a number of vexing issues regarding how best to make decisions about the use of life support in neonatal and pediatric cases. There is general agreement that life support may be forgone when children are terminally ill or permanently unconscious, in instances of "medical futility," and when the burdens of treatment outweigh the benefits from the child’s perspective.11 In the many ambiguous cases, where the burdens of illness and continued treatment seem great and the benefits uncertain, parental preferences are granted a great deal of authority.2,11 Policy documents also require the provision of adequate analgesia and offer guidelines related to organ donation.12 Since the publication of these landmark reports, new ethical issues in the care of gravely ill children have arisen, and the Institute of Medicine has called for more attention to the ethics of pediatric palliative care.13
A major purpose of the research reported here was to ascertain physician, house officer, and nurse beliefs with respect to the range of issues presented in Table 1, which summarizes key national recommendations published to date. A second purpose was to determine the extent to which health care professionals are concerned with problems of overtreatment. In previous research, a member of the study team documented significant concerns of conscience regarding inappropriate use of technology among clinicians caring for gravely ill adults.14 We hypothesized that pediatric health care professionals might experience similar concerns. To address these issues, we surveyed attending physicians, house officers, and nurses working in PICUs and medical and surgical services of children’s hospitals and general hospitals with pediatric units in the United States.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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This article reports on 3 types of items from the survey, ie, (1) opinion items, which probe for respondents’ agreement or disagreement with existing national guidelines; (2) knowledge items, which probe for the extent to which respondents are or are not aware of existing guidelines; and (3) belief items, which probe for respondents’ attitudes and concerns about the care they provide. Five-point Likert response options ranging from strongly disagree to strongly agree were appropriate for all 3 types of items.
Pilot testing was conducted by administering the instrument to 71 subjects in 3 institutions. The extent of variation and the percentage of missing data were examined for each item. To assess test-retest repeatability, 49 of these respondents completed the instrument a second time within a 2- to 3-week period. Responses were consistent 70% to 90% of the time among respondents with retesting of items.
Sample
Seven teaching hospitals with broad geographic representation participated, in Georgia, Maryland, Massachusetts, New Jersey, Pennsylvania, and Texas (where 2 sites were located). Four of the 7 hospitals are children’s hospitals, and 3 are general hospitals with PICUs. The study protocol was approved by institutional review boards at the Education Development Center and participating hospitals. The survey was administered to pediatric physicians and nurses who cared for children (age: 1 month through 18 years) with life-threatening conditions in PICUs, medical units, surgical units, and/or hematology/oncology units. Providers who worked solely in NICUs were excluded, because the survey items were relevant mainly to pediatric decision-making and were not designed specifically to target special issues arising in the care of neonates.
Analysis
Our analytical interest was twofold, ie, (1) to determine the overall pattern of responses to individual survey items and (2) to determine whether the pattern of responses varied according to professional discipline, subspecialty, and/or site. Professional discipline included 3 groups, ie, attending physician, house officer, and nurse. With regard to subspecialty, attending physicians and nurses were grouped into 3 categories, ie, critical care, hematology/oncology, and other. Among attending physicians, the other category included, for example, pulmonology, cardiology, rehabilitation medicine, orthopedics, and anesthesia. These subspecialties were combined into a single category because most were represented by <5 respondents. Among nurses, the other category included those who simply recorded their specialty as pediatrics and those who answered the question by listing the unit or service in which they worked, such as trauma, emergency transport, or dialysis. Because house officers have not yet completed their training, subspecialty was not categorized for them.
To examine the pattern of differences for each survey item according to discipline, subspecialty, and site, 
2 tests of independence were used. Because a subspecialty was not designated for house officers, separate 2 tests of independence were performed to ascertain differences according to subspecialty for attending physicians and for nurses. In addition, a 2 test of independence was performed for each subspecialty group to examine differences between attending physicians and nurses. Finally, site differences for each outcome were examined with a 2 test of independence between the survey item and the site. To facilitate interpretation and presentation, the 5-point Likert scale was collapsed into 3 categories, ie, agree, uncertain, and disagree.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Table 2 provides details about respondents’ demographic and professional characteristics and about their perceptions of their knowledge of basic principles and issues in medical ethics. The specialty of 2 attending physicians and 13 nurses could not be determined, and these 15 subjects were excluded from analyses. Approximately 12% of attending physicians were from critical care, 25% were from hematology/oncology, and 62% were from other specialties. In contrast, 57% of nurses worked in critical care, 19% in hematology/oncology, and 21% in other specialties. The vast majority of respondents considered themselves knowledgeable regarding medical ethics. Regardless of subspecialty, attending physicians were less likely than house officers or nurses to report that they were "not very knowledgeable."
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A similar pattern was noted with respect to the statement, "Sometimes I feel the treatments I offer children are overly burdensome." More than one half of the critical care attending physicians (56%), two thirds of the other non-hematology/oncology subspecialists (66%) and house officers (63%), and more than one half (53%) of other subspecialty nurses agreed with the statement, whereas only one third of the hematology/oncology attending physicians (31%) and hematology/oncology nurses (33%) did. Critical care nurses were more similar to their hematology/oncology nurse counterparts for this item than they were for other items. Across all subspecialties and disciplines, very few agreed with the statement, "Sometimes I feel we give up on children too soon."
Clinicians’ Views Related to Published Recommendations
Withholding and Withdrawing Life Support
Table 4 presents the percentages of respondents who agreed, were uncertain, or disagreed on 3 items related to withholding and withdrawing life support. Critical care attending physicians were much more likely than other attending physicians, house officers, or nurses to agree with the frequently promulgated ethics recommendation, "There is no ethical difference between withholding (not starting) a life support measure and stopping it once it has been started." Similarly, only 14% of critical care attending physicians agreed with the false statement, "There is a prevailing consensus among ethicists that withdrawing a treatment is ethically different from withholding it." In contrast, at least 40% of hematology/oncology attending physicians, attending physicians from other specialties, house officers, and nurses agreed with this false statement. In addition, one third or more of all respondents, except critical care attending physicians, were uncertain about the nature of the "prevailing consensus." With these groups added together, 
70% of all respondents except critical care attending physicians were unaware of existing guidelines regarding the ethical equivalence of withholding and withdrawing treatments.
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Pain Management
Table 5 presents clinicians’ beliefs regarding 5 pain-related items. Two items showed high levels of agreement with broadly accepted clinical and ethical guidelines. At least 80% of all respondents agreed with the true statement, "For a child whose death is inevitable, it is appropriate to provide opioid pain medication before withdrawing a ventilator." An even higher percentage of respondents agreed with the true statement, "Sometimes it is appropriate to give pain medication to relieve suffering even if it may hasten a child’s death."
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Ethical Aspects of Managing the Dying Process
Table 6 presents 3 items related to decisions that clinicians may encounter while they manage the dying process or immediately after a child’s death. Regarding the first question, more hematology/oncology attending physicians and nurses (32% and 48%, respectively) than critical care attending physicians (16%), other specialty attending physicians (14%), house officers (19%), critical care nurses (14%), and other specialty nurses (25%) were likely to agree with the controversial statement, "For a child whose death is inevitable, it is appropriate to provide neuromuscular blocking agents such as Pavulon (pancuronium) with analgesia before withdrawing a ventilator."
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45% of hematology/oncology attending physicians, other specialty attending physicians, and other specialty nurses. However, substantial numbers of respondents disagreed or were uncertain. Answers to the next question were also widely divergent. Approximately 30% of critical care and other specialty attending physicians and 43% to 47% of all other groups agreed, "The organs of pediatric patients who are on life support and permanently unconscious, but not technically brain dead, should be used for transplantation if requested by the parents." However, substantial numbers of respondents disagreed with the statement.
Beliefs That Vary According to Site
Table 7 shows the questions for which site differences were statistically significant. At 6 of the 7 institutions, two thirds to three fourths of all respondents agreed with the statement, "Sometimes I feel we are saving children who should not be saved." At 1 institution, however, only approximately one fourth of respondents felt that way. The same institution also differed from other institutions in attitudes toward medically supplied food and water; there, 60% of respondents agreed, "Medically supplied food and water should always be continued." That view was shared by only 31% to 49% of respondents at the other institutions. The proportions of respondents who agreed that there was inadequate pain medication for children at their institutions ranged from 11% to 51%.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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10 times as worried and nurses were >20 times as worried about "saving children who should not be saved" as about giving up too soon. These findings suggest that concerns about overly burdensome treatment are greater in pediatric end-of-life care than in adult end-of-life care. Interestingly, fewer physicians and nurses in hematology/oncology had concerns of conscience, compared with their counterparts in critical care. Even among hematology/oncology clinicians, however, approximately one third agreed, "Sometimes I feel we are saving children who should not be saved" and "Sometimes I feel the treatments I offer children are overly burdensome." The differences between critical care clinicians and hematology/oncology clinicians warrant additional study. Perhaps more intensivists have concerns of conscience about providing overly burdensome treatments because they care for neurologically devastated patients for whom restoration to a meaningful existence may seem impossible. Conversely, fewer hematology/oncology clinicians may express concerns of conscience because prognostic uncertainty for pediatric cancer is so great and therefore cure-oriented interventions are more likely to be justifiable. Oncologists are also more likely to have had longer-term relationships with patients and families than intensivists, and these emotional bonds may impair oncologists’ ability to provide objective counseling and advice. Interestingly, Wolfe et al17 reported that oncologists knew a full 6 months before parents that death was virtually certain but cure-oriented treatment plans continued. The difficulty of holding end-of-life conversations with parents and the understandable desire to ensure that everything that could be done was done may account for the time lag between oncologists’ and parents’ understanding of a dire prognosis. However, none of these factors fully explains why the hematology/oncology clinicians we surveyed were less likely to see life-sustaining treatments as burdensome to the children in their care than were intensivists.
Other items in the survey may help explain these concerns of conscience. If clinicians do not think they can stop treatments already underway, then they may feel compelled to continue disproportionately burdensome interventions. In our survey, with the exception of critical care attending physicians, who were more knowledgeable, 70% of respondents mischaracterized or were uncertain about the prevailing national consensus that holds that there is no morally relevant distinction between withholding and withdrawing treatment.
Clearly, withdrawing treatments already begun may feel different psychologically than never instituting a treatment. However, when allowing death is justifiable, parents and health care professionals should know that there is no sanction against withdrawing treatments already underway. If the view is that any intervention already being offered cannot be withdrawn, then many children may suffer needlessly and opportunities for comfort care and for interactions with parents and siblings may be diminished. Conversely, if health care professionals do not realize that they can later withdraw treatments that are no longer beneficial, then they may be reluctant to initiate trials of treatments that could be beneficial.
Medically Supplied Nutrition and Hydration
The American Medical Association,18 the American Academy of Pediatrics,3 and the American Nurses Association4 have clarified that medically supplied nutrition and hydration are not ethically and legally required in all clinical circumstances. When their benefits outweigh their burdens and when their use is inconsistent with agreed-on goals of care, medically supplied food and fluids can be forgone or withdrawn.
In our survey, however, more than one third of critical care attending physicians, one fourth of hematologists/oncologists, and >40% of other subspecialty attending physicians, house officers, and nurses believed that medically supplied nutrition and hydration should always be continued. Although the survey item asked about "medically supplied food and water," it is possible that, in answering, some respondents did not distinguish between the provision of food and fluids by hand and that by medical means; indeed, food and water should always be offered to children and adults who can take them by mouth. Even if there was some confusion in how the item was interpreted, this finding suggests that different members of the same care team may hold radically different views about the permissibility of withholding these interventions. Such diverse opinions could lead to conflicts among health care professionals, confusing messages for parents, and inappropriate prolongation of the dying process.
Given the symbolic nature of food and water, withdrawing or withholding medically supplied nutrition and hydration for children is one of the most emotionally wrenching decisions that can be made. Reluctance to forgo these interventions may also be attributable to the mistaken impression that forgoing artificial nutrition and hydration leads to an uncomfortable death. In fact, medically supplied nutrition may prolong the dying process and, near the end of life, can cause congestion, excessive bodily secretions, and considerable discomfort.19 In certain instances, and with careful attention to symptom management, a child’s interests may best be served by forgoing enteral and parenteral nutrition and hydration.20,21
Pain Management
Our data suggest that concerns about hastening death affect clinicians’ pain management behaviors; approximately one half of the attending physicians and >40% of house officers and nurses agreed, "When clinicians give inadequate pain medication, they do so most often out of fear of hastening the child’s death." More than two thirds of the hematology/oncology nurses held this view. However, such fear is misplaced on clinical, ethical, and legal grounds.
Clinically, this fear is misplaced because data showed that respiratory depression is extremely rare, especially among children >2 months of age.22–24 Indeed, Partridge and Wall25 showed that patients who receive effective pain relief may actually live longer than patients whose pain remains undertreated.
It is important to note, "In some patients, opioids must be given with caution. These patients include children (and adults) with altered mental status, disordered control of respiration, and abnormal renal and hepatic functioning."24(p713) However, even these patients can receive very high levels of opioids safely if the drugs are administered gradually and with titration to effect.24
Although it is rare, it is sometimes the case (particularly in the ICU) that appropriate pain management shortens the dying process. However, the appropriateness of providing adequate levels of pain medication, even if it hastens death, is both ethically and legally well established, with approval by the US Supreme Court.26
The preponderance of our respondents seemed to be in agreement with the longstanding ethical principle of "double effect,"27 but substantial numbers were uncertain about its legality. For example, most of the nurses agreed, "Sometimes it is appropriate to give pain medication to relieve suffering even if it may hasten a child’s death." However, one third or more believed that it is illegal to do so, and 17% were uncertain about its legality. Attending physicians were the most well informed but, among hematology/oncology and other specialty attending physicians, 17% believed that it is illegal to give pain medication in doses that risk respiratory depression to the point of death, and another 10% were uncertain. Health care institutions, professional medical and nursing societies, and palliative care experts need to be relentless in reinforcing the message that the provision of adequate pain medication is appropriate (indeed mandatory) on clinical, moral, and legal grounds.
Given that approximately one third of pediatric intensivists and critical care nurses either were uncertain or thought that it was appropriate to provide neuromuscular blocking agents (such as Pavulon) with analgesia before withdrawing a ventilator, PICUs should consider auditing their practices and developing policies to guide the use of paralytic agents. These agents have no analgesic or sedative properties; therefore, clinicians can never logically justify introducing them at the end of life by claiming that the intention is to relieve the patient’s pain and suffering. If patients have been receiving these agents as part of their therapeutic care, then neuromuscular function should be restored before life support is withdrawn, to allow for optimal assessment of the patients’ comfort during the withdrawal process. In rare cases, when the patient’s death is expected to be certain and rapid after withdrawal of ventilatory support even if neuromuscular function is restored, and if the time required to restore function would subject the patient to unwarranted suffering from the continuation of life-sustaining treatments, then withdrawal may occur in the presence of neuromuscular blockade, with careful attention to providing sufficient analgesia and sedation to ensure the comfort of the patient despite the presence of pharmacologic paralysis.28,29
Family Prerogatives With Respect to Artificial Support After Brain Death
The diagnosis of brain death is determinative of death in all 50 states; therefore, physicians have no obligation to continue medical interventions when patients have died according to neurologic criteria.12 Two states, namely, New York and New Jersey, have special provisions for accommodating religious objections to brain death. But what of parents who simply may need more time to accept the fact that their child has died? Do objections to withdrawal of artificial support for a brain-dead patient merit accommodation if those objections are based on parents’ emotional needs, rather than religious objections?
Although there are no legal grounds for families to demand continued treatment of the deceased, it may be appropriate to allow time for parents to take in the devastating news, especially because brain death is so often attributable to a sudden unexpected event. A time-limited approach can help families come to grips with the tragic reality and begin the process of grieving, which may remain blocked as long as parents are in conflict with health care providers. In our survey, approximately one half of hematology/oncology nurses, one third of hematology/oncology attending physicians, other specialty attending physicians, and other specialty nurses, and one fifth of house officers, critical care attending physicians, and critical care nurses seemed willing to make such accommodation. Given the substantial number of "uncertain" responses, it is possible that even greater numbers might be willing to do so.
Family Prerogatives for Organ Donation and the Dead-Donor Rule
The Uniform Anatomical Gift Act clearly establishes that only the organs of deceased persons can be donated for organ transplantation. However, sizeable proportions of respondents agreed with the statement, "The organs of pediatric patients who are on life support and permanently unconscious, but not technically brain dead, should be used for transplantation if requested by the parents." One interpretation is that respondents are simply confusing permanent unconsciousness with brain death. A second alternative is that they know that permanent unconsciousness is distinct from brain death but they believe that parental preferences should be determinative, given the child’s profound degree of neurologic damage. Perhaps, in addition to honoring parental choice, these clinicians are taking a basically consequentialist perspective, hoping to see some good come from a terrible situation. In this light, responses to this item might be interpreted as principled objections to the dead-donor rule.
Other researchers have also documented clinicians’ belief that the organs of permanently unconscious patients could be used for transplantation. For example, in a 1996 national survey of neurologists and medical directors, Payne et al30 found that two thirds of respondents believed that it would be ethical to use the vital organs of patients in a persistent vegetative state for transplantation. However, neither prior research nor our study helps explain why these clinicians hold these views. Additional empirical studies are needed to discover the reasons why so many clinicians seem to feel that parental choice, not the dead-donor rule, should be determinative in these heart-wrenching cases.
Limitations
There are many other ethical issues regarding pediatric end-of-life decision-making that sensitive clinicians and committed institutions will need to examine; in this article, we reported on only some of the issues our survey probed. Future papers will address other components, such as the discretion adolescents should be granted in making decisions regarding termination of treatment and the role of caregiver suffering in pediatric palliative care.
Our results are also limited in that we did not have a probability-based sample of institutions. This limitation is mitigated by the facts that the institutions were geographically diverse and substantial site differences were detected, which indicated variation in the sample.
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CONCLUSIONS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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The findings also bring attention to the fact that health care professionals (both within and across disciplines and subspecialties) can and do hold different points of view on a range of inherently complex issues in the care of gravely ill children. An ethically strong culture within hospitals should encourage diversity of opinions, but the opinions should be well informed. Health care professionals should be aware of the ethics literature and the published guidelines, should know why they hold the views they do, and should be familiar with alternative positions. Surveys such as this one can demonstrate how many different points of view health care professionals working within the same institution bring to the clinical choices they face. Findings can be used to prompt individual reflection, interdisciplinary dialogue, and institutional self-examination.
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ACKNOWLEDGMENTS |
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We thank Erica Jablonski for assistance with survey preparation and data analysis. Thanks also go to Jane Barnsteiner, Brian Carter, Gina Emge, Polly Hesterberg, Javier Kane, Elaine Meyer, Beverly Ryan, Kay Sandor, and Jane Schneck for administering the surveys. We are grateful to Andrea Kydd of the Nathan Cummings Foundation for her original vision and continuing support. We thank all of our funders for enabling us to bring these findings to the attention of hospitals across the country and for their combined support of the next training phase of this national initiative.
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FOOTNOTES |
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Reprints requests to (M.Z.S.) Center for Applied Ethics and Professional Practice, Education Development Center, 55 Chapel St, Newton, MA 02458. E-mail: msolomon{at}edc.org; Mildred_Solomon{at}hms.harvard.edu
No conflict of interest declared.
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REFERENCES |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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