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PII: S1055-8586(18)30008-8
DOI: https://doi.org/10.1053/j.sempedsurg.2018.02.008
Reference: YSPSU50739
To appear in: Seminars in Pediatric Surgery
Cite this article as: Derek Wakeman and Max R. Langham, Creating a Safer
Operating Room: Groups, Team Dynamics and Crew Resource Management
P r i n c i p l e s , Seminars in Pediatric Surgery,
https://doi.org/10.1053/j.sempedsurg.2018.02.008
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Creating a Safer Operating Room: Groups, Team Dynamics and
Abstract
The operating room (OR) is a special place wherein groups of highly skilled individuals
must work in a coordinated and harmonious fashion to deliver optimal patient care. Team
dynamics and human factors principles were initially studied by the aviation industry to better
understand and prevent airline accidents. As a result, crew resource management (CRM) training
was designed for all flight personnel to create a highly reliable industry with a commitment to a
culture of safety. CRM has since been adapted to health care, resulting in care improvement and
harm reduction across a wide variety of medical specialties. When implemented in the OR, CRM
has been shown not only to improve communication and morale for OR staff, but also reduce
morbidity and mortality for patients. As increasing focus is placed on quality, safety, and high-
reliability, surgeons will be expected to participate and lead efforts to facilitate a team approach
patient safety
A three-year-old girl presents to the emergency room with hematuria. Overnight, she fills
multiple diapers with bloody urine and ultimately requires blood transfusion for anemia. Cross-
sectional imaging demonstrates a large right-sided kidney tumor consistent with a Wilms tumor
with no evidence of metastases. She is taken to the operating room for a right radical
nephrectomy. Due to the urgent nature of the case, the operation takes place with an
inexperienced nursing team that rarely performs general surgical cases. The case bridges a shift
change for nurses and anesthesiologists. Additional hand-offs for work breaks occur during
Pathologic examination of the specimens confirms a Wilms tumor with favorable histology that
does not extend beyond the renal capsule. However, no lymph nodes are received. This finding
potentially upstages the patient’s disease from stage 1 to stage 3, which would mandate
escalation of chemotherapy and the addition of abdominal radiation. The surgeon recalls
providing additional tissue to be separately sent as nodes but this is not documented in the
nursing flow sheet or dictated operative report. The general surgery nurses usually help remind
the surgeon to remove lymph nodes during nephrectomy for Wilms tumors. No surgical sign out
Pediatric surgeons have multifaceted responsibilities for patients with problems that
range from common to exceedingly rare. Beyond creating a therapeutic atmosphere for the
patient and family, surgeons are constantly interacting with other healthcare providers, each of
whom has his or her own perspective and background. The complexities of these interactions are
often coupled with critical time constraints of delivering high acuity care. Although every effort
is made to provide responsible, comprehensive, safe, and efficient care to our patients, there are
described. Over the past decade, a growing body of evidence has emerged surrounding the
importance of human factors in high-stakes, high acuity settings such as the operating room
(OR).
The perioperative experience brings together multiple people with different backgrounds
toward a common goal – to bring a patient through an operation as effectively, efficiently, and
safely as possible. This requires coordination among providers with different expertise and skill
sets. The pre-operative phase begins with a surgeon recommending a specific operation to the
patient and their family. The risks and benefits of surgical intervention are reviewed, and
informed consent is obtained. Depending on operative and patient factors, careful coordination
between physicians, nurses, and administrative support staff in the surgeon’s, anesthesiologist’s,
and primary care provider’s offices may be required to optimize a patient’s medical
of safe transitions through phases of care from admission, to pre-anesthesia, to the OR, to the
post-anesthesia recovery unit (PACU), to the intensive care unit or floor, and, lastly, to home.
ORs were created in the 1800’s as advances in anesthesia allowed surgery to be
performed for a wider variety of more complex indications. ORs have evolved in lock step with
the evolution of surgical specialties incorporating advances in technology, equipment, and safety
standards. ORs are usually staffed by skilled groups of healthcare professionals performing
specific tasks. In the United States, a Doctor of Allopathic or Osteopathic Medicine must be
involved, in at least a supervisory manner, for the performance of the procedure and the
provision of anesthesia.1 Nurses may plan, implement and evaluate treatment of the patient2. The
professional requirements and scope of practice for surgical technologists varies considerably
and include creating, maintaining, and monitoring aseptic surgical techniques; anticipating the
instruments and supplies needed for a procedure; and ensuring the efficient conduct of the
procedure is possible. Custodial staff usually maintain a clean, safe environment as required by
the Joint Commission. An efficient supply chain is essential for stocking thousands of
Administrative staff responsible for handling the complexity and human resources
aspects of the OR environment are most often recruited from a nursing background, while
scheduling and daily workflow is usually handled by an anesthesiologist. While physicians may
practice at several hospitals or surgical centers, other OR staff are usually full-time at a specific
geographic location. Within a large, multi-specialty OR, groups of healthcare professionals may
be aligned or assigned into various types of working groups depending on the type of procedure
being performed and the specific context within which it is being conducted. Group interactions
are of at least 3 types: Crew, Team, and Flash Mob (Figure 1).
Hospitals often provide a continuum of patient care that includes peak hours with full OR
staffing and capability to provide emergent services 24-hours a day throughout the year. To
maintain this level of availability, staffing models for anesthesiologists, nurses and other
personnel are generally based on shifts worked for specific durations. Beyond maintaining an
elective practice during normal working hours, most surgeons provide emergency coverage for
their institutions on a rotating basis, and are available for required operative procedures at night,
on weekends, and during holidays. Staff sizes can be quite large resulting in an astronomical
It is out of necessity that crews perform most operations. Historically, the structure of the
OR is hierarchical with the surgeon as the sole leader. While decisions about preparation and
timing of operations are usually shared with an anesthesiologist, once the operation begins, the
surgeon’s role is primary. While other members of the crew may come and go during the
operation, the surgeon is the constant presence and leader. Hierarchy is vital for effective crew
work, but must not be confused with the abusive behaviors often associated with the term. An
important aspect of crews is an acceptance of new crewmembers who have limited experience.
As long as the individual is qualified and competent, his or her presence has little negative
impact on crew function. The level of comfort with inexperienced crewmembers may be highest
with common operations and lowest in tense situations or technically difficult operations.
Though being part of a high functioning surgical team is rewarding, teams are talked
about in surgery more often than they actually exist. The more complex an operation, the more
likely an institution is to create a team. Examples are Cardiac surgical teams, Transplant teams
and special teams such as those created to separate conjoined twins. Within the team setting there
is limited acceptance for team members to rotate in and out during an operation, or to leave
before the operation is completed. While it is normal for the primary surgeon to serve as leader,
teams tend to be less hierarchical, with more comfort and social equality between members. In
turn, teams often have better interpersonal communication. Teams are especially good at learning
highly complex, time sensitive, coordinated procedures. They have real advantages over crews in
the realm of collective learning and rapid process improvement. They are, however, less flexible
While not routine for surgical teams, one fundamental of the team dynamic is the
importance of a coach. The coach’s role observing the team’s performance, and adjusting roles
and responsibilities based on these observations is accepted by the team. This allows the coach to
lead individual and group learning. Most often a senior surgeon, who may or may not be doing
most of the technical part of the procedure, assumes this role. Inherent in the position is
responsibility for administrative oversight of the team and accountability for the team’s results.
Flash mobs are assembled rapidly during unexpected events that may include loss of an
airway, cardiopulmonary arrest during an operation, unexpected massive blood loss, or a mass
casualty event. The make-up of flash mobs is highly variable depending on the event. Typically,
mobs devolve into subgroups performing specific tasks. Leadership is often uncertain or shared.
Recruits from outside the OR may be pulled into service such as Emergency Department
personnel or intensive care providers. At the end of the event, the mob disperses quickly, often
without a collective debrief. Record keeping is typically problematic and group learning requires
Much of the current medical literature uses the term “team” broadly and does not differentiate
between crews, teams, and flash mobs. In this review we will focus on teams and crews, with
specific emphasis on human factors principles that underlie most of this work.
Team dynamics describe how unconscious, psychological forces affect the behavior and
impact performance of groups of people working together. The landmark Institute of Medicine
report To Err is Human declared the need to “promote effective team functioning” as one of five
values for creating safe hospitals.3 In the OR, teamwork is fundamental to patient safety and a
Beyond patient safety concerns, team dynamics have a significant impact on job
among OR staff have been found to enhance employee job satisfaction and reduce OR nursing
staff turnover.5 Moreover, high-quality teamwork has been correlated with reduced sick leave
taken by health professionals.6 It has been suggested that low perceptions of teamwork by nurses
leads to job dissatisfaction and contributes to nursing shortages.4 For these reasons, Makary’s
team at Johns’ Hopkins Medical Center developed a tool to measure teamwork in the OR. In
validating their Safety Attitudes Questionnaire, they found discrepant perceptions of teamwork
in the OR. While surgeons and anesthesiologists perceived good teamwork among OR staff,
nurses rated teamwork as mediocre.4 In fact, surgeons had the most egregious misperceptions
rating their collaboration with nurses as good 88% of the time, while nurses rated it as high-
Understanding roles in the OR is a key first step to understanding team dynamics. At the
University of Southern California, OR personnel were queried about which behaviors they
thought most affected the performance of an operation.7 Surgeons most frequently cited their
own management of the team and case, while others (anesthesiologists, technicians, and nurses)
believed the surgeon’s preparation was most important. All parties agreed that the
anesthesiologist’s technical competence is the most important factor for providing quality
anesthesia care. From the nursing perspective, circulating nurses noted technical competence and
preparation most often. Interestingly, non-nurses believed the circulator’s management of the
case was their most important role.7 Surgical technicians cited their own preparation as most
important while other OR staff thought the technician’s technical competence was most
important. Overall, preparation and technical competence were found to account for two-thirds
of the role behaviors affecting performance.7 Team factors were reported to account for
(30%), teamwork (26%), and interpersonal relations (19%) were cited as being most influential.7
A group in Auckland, New Zealand recently developed a computer based model to assess
perceptions of role responsibilities among OR teams (surgery, anesthesia, and nursing). They
found differences in individual mental models regarding accountability for tasks during
simulated emergency laparotomies.8 The operation was divided into 20 tasks; the groups lacked
agreement for who was responsible for half of the tasks.8 Without a shared mental model
teamwork is jeopardized. Creating a shared mental model of OR tasks within crews or teams that
may rarely work together is even more challenging. A model of leadership, situation awareness,
communication, and a joint commitment to patient safety are vital for clearly establishing roles
Leadership in the OR
The surgeon most often assumes the role of leader as the team member with continuity
throughout the perioperative period and the person ultimately responsible for the patient’s well-
being. It is critical not to confuse leadership with absolute authority or dictatorial style. An
effective leader sets the team at ease, encourages communication, and allows team members the
freedom to think critically and function effectively in their role. Effective leaders also must
designate authority promptly in situations that preclude them from maintaining perspective, and
leading the crew. Crewmembers should be empowered to ask for help or designate leadership
authority if the surgeon is so occupied with a particular task that he or she cannot survey the
entire room and manage it appropriately. In these crucial times, another surgeon, an
anesthesiologist, or another key team member must lead the group. Having the crew or team
The circulating nurse also has a vital leadership role. Anesthesiologists and surgeons
frequently cite the circulating nurse as “being in charge of the OR”.7 Surgeons should respect
and encourage the leadership role for nursing staff in the OR.
While the OR has a hierarchical structure with the surgeon traditionally at the top of the
team dynamic, too often surgeons have not understood the proper conduct of teams and have
displayed abusive or destructive behavior. An autocracy, with surgeons “pulling rank” over
anesthesiologists and physicians “outranking” nursing staff is not appropriate and leads to
increased errors.9 In these settings, effective communication is stifled, and staff are afraid to
speak up. Effective communication and collaboration in the OR require elimination of autocracy
and support of all staff contributing to the procedure. This flattening of the hierarchy can be
support between crewmembers allows all members to enjoy the experience as they contribute to
an increasingly safe patient experience. Significant education and culture change will be required
Instances may arise when a leader’s authority must be set aside against his or her will.
Substance abuse issues, mental illness (often depression), physical illness, exhaustion, and other
issues may render a surgeon unfit to provide safe care. This is best handled by the surgeon
recognizing the problem and voluntarily removing him or herself from direct patient care.
Similar issues affect pilots. The Federal Aviation Administration (FAA) has added training on
mnemonic that is easily modified to fit surgeons and members of the surgical team (Table 2).10
Cognitive factors involving IMSAFE elements have been correlated with medical malpractice
cases.11
coverage often causes surgeons to have interrupted sleep cycles and some level of fatigue.
Fatigue leads to diminished ability to deal with frustration, impaired judgement, and suboptimal
decision-making. If working in crews, other health professionals may not know the surgeon well
or be able to judge his or her actions in a manner informed by personal knowledge of the
surgeon’s strengths and weaknesses. In contrast, close team members are often the first to
recognize when surgeons need assistance and should be empowered to raise concerns to OR
leadership. Hospitals are grappling with how to handle situations when surgeons do not fulfill
their professional responsibilities. The American College of Surgeons12 and the Joint
Situation awareness involves appreciating the conditions that affect one's work such as
environment, time, and place. Having awareness requires constant monitoring of an ever-
changing situation. Ideally, all crew or team members would have a similar level of situation
awareness, or share a mental model of the task at hand. The concept of situation awareness was
developed from investigations of airline accidents. Most airline crashes were found to be
communication between crew members. Human factors, or what many might call “human error,”
is responsible for most plane crashes instead of instrument or mechanical failures.14 These errors
technical. Over half of accidents in civilian, military, and private aviation are decisional and
Research into human factors developed the principle of a shared mental model. In
aviation, the pilot and co-pilot gain a shared understanding of a fluid scenario that is
communicated to the cabin and ground crew. These principles provide the framework for Crew
Resource Management (CRM) which is taught ubiquitously to improve flight crew effectiveness,
Central to creating a shared mental model is effective communication. Crew members are
empowered to speak up and share ideas. The saying “If you see something, say something” has
roots in principles of CRM. While airplane design has certainly improved with time, many
attribute the phenomenal safety record of the American airline industry, which has not had a
Preventable medical errors have long been recognized as a cause of morbidity and
mortality.17 Medical errors are now estimated to be the third leading cause of death in the United
States.18 Further reports expose that communication failure accounts for 70% of sentinel events
reported to the Joint Commission from 2004-201119 and about 75% of approximately 7000 root
surgical techniques, and anesthesia have been made, patients continue to suffer preventable harm
ascribed to imperfect team dynamics (or non-technical skills) rather than technical failures.21, 22
Lack of teamwork and information sharing in the perioperative setting has been correlated with
Given its exemplary safety record, the American aviation industry serves as an example
from which the health care industry can learn. In the 1970’s and 80’s CRM principles were
developed by the National Aeronautics and Space Administration and airline industry experts
after scrutinizing the role of human error on plane crashes.24 Human errors, communication
failures, leadership problems, and cockpit decision making were found to be major contributors
to errors in aviation. In many instances, other personnel in the aircraft knew a mistake was being
made and did not speak up to an established captain. CRM values input for all available
information sources including equipment and personnel to ensure efficient and safe flights. The
goal is not to eliminate the hierarchy but to improve performance by increasing the support for
and importance of all crew and to affirm everyone’s responsibility and right to be assertive and
and feedback to the leader are that it be timely, specific, and constructive.15 It is important that
the captain or leader specifically acknowledge and respond to all issues that are raised.
Simulation, crewmember debriefings, and crew performance measurement are used to improve
CRM has been applied in medicine and surgery to promote teamwork and patient safety.
Aviation-style CRM team training focusing on teamwork and communication was studied in
maxillofacial, vascular, and neuro-surgical OR teams in the United Kingdom.25 After training,
OR teams performed significantly more briefings, time outs, and debriefings after surgical
procedures. Another group at the Baylor College of Medicine found that CRM-based training
The Veterans Administration (VA) National Center for Patient Safety built a Medical
Team Training Program based on CRM. The program, using team training and surgical
VA medical centers between 2003 and 2006.20 Based on favorable data from this pilot study, the
VA Medical Team Training Program was implemented nationwide starting in 2006.27 Medical
centers that completed the CRM training program (74 facilities) had an 18% reduction in annual
procedural mortality compared to the 7% decrease seen in 34 centers that had not completed the
program.27 Importantly, a dose-response relationship was found in that every quarter of a year of
team training was associated with 0.5 fewer deaths per 1000 procedures.27 This program was also
associated with reductions in venous thromboembolism, surgical site infections, all infections,
More recently CRM-based training was found to improve staff perceptions of the safety
climate at a VA hospital in Shreveport, LA.29 They adopted a clinical team training curriculum
from the VA National Center for Patient Safety.30 The program was administered through
didactic learning sessions coupled with group discussion and simulation training to reinforce
content. They measured their institutional safety climate with a 27 point questionnaire. After 6
months, improvements were noted for all 27 elements. After one year, 23 of 27 points
cooperation between doctors and nurses, valuing contributions from nursing staff, patient safety
debriefing with a surgical pause (time out) when developing their surgical safety checklist (SSC).
Implementation of the WHO SSC has been shown to significantly reduce surgical morbidity and
mortality across disparate hospitals globally31 and in emergency situations32. As a result of this
seminal work, many hospitals have added a SSC to the workflow in their OR’s. SSC’s are
adaptable and may work best when customized to local patterns of care (Table 3). While the
utility of the surgical pause or time out is nearly universally accepted, performance of the brief
and debrief have lagged33 (authors’ observations). Hopefully, in time, adoption of briefing and
debriefing will be as engrained in OR culture as completion of the time out before skin incision.
TeamSTEPPS®
The Agency for Health Care Research and Quality (AHRQ) adapted CRM training and
created a team training curriculum for medical practitioners called TeamSTEPPS® (Strategies
and Tools to Enhance Performance and Patient Safety).34 The principles were borrowed from a
curriculum that focuses on teaching communication and leadership qualities shown to reduce
errors. In 2006 the AHRQ released the TeamSTEPPS® course free of charge under public
domain. The course focuses on teaching strategies for improving leadership, communication,
situation monitoring, and mutual support (Figure 2).35 The curriculum, course materials, and a
(http://www.ahrq.gov/teamstepps/index.html).
providers across medical disciplines; the course material can also be customized for specialty
adapted to the OR environment. Urology OR teams at the San Antonio Military Medical Center
focused on a “Brief” at the beginning of the day and a “Debriefing” at the end of each
operation.36 After implementing TeamSTEPPS® mean OR case durations were shorter and first-
start on-time rates increased. Further, patient safety concerns discussed during the debriefing
In 2011 a group at Creighton University published their experience with team training in
the perioperative setting.37 They taught TeamSTEPPS® to all OR staff including surgeons,
anesthesiologists, nurse anesthetists, residents, nurses, and technicians in early 2007. They
reported significant improvements in teamwork and communication measures in the OR. Metrics
of OR efficiency, percentage of first-case on-time starts, and room turnover time improved from
2006 to 2010. Compliance with several perioperative quality improvement measures rose
administration (78% to 97%), venous thromboembolism prophylaxis (74% to 91%), and beta-
blocker administration (20% to 100%).37 Morbidity (20% to 11%) and mortality (2.7% to 1%) as
Program (NSQIP) also declined after TeamSTEPPS® training. Importantly, many of the
favorable outcomes were not enduring. Outpatient surgical patient satisfaction scores peaked
after TeamSTEPPS® training and declined to prior baseline levels in subsequent years when no
team training was offered.37 The authors note that administrative support for team training ceased
after its initial roll out due to financial cutbacks. Nearly all measures returned to the prior
baseline one or two years after training, underscoring the need for continued commitment to
training.
A group at The Mount Sinai Hospital recently reported their experience after
information), check-back (when a provider repeats something to ensure it was heard correctly),
and 2- challenge rule (when a provider repeats information if initially dismissed). Compliance
with measures of communication (time out, check-backs), situation monitoring, and mutual
support increased dramatically over the study period during the time out (58% to 92%) and
debrief (58% to 95%). Perhaps more strikingly, the number of wrong patient/wrong site surgeries
and unintentionally retained foreign bodies decreased by 67% after TeamSTEPPS® training.39
This evidence demonstrates the efficacy of crew resource management and team training
for surgical teams. The aviation industry requires ongoing, repetitive training in CRM
environments. The FAA requires operational ‘line checks’ every 24 months for captains of
aircraft. Rigorous continued practice and training in CRM has not been adopted by most
hospitals or surgical groups. Given the dose-response benefit to the amount of CRM offered to
the VA OR staff,27 and the finding that benefits of TeamSTEPPS® degrade over time with
eventual return to the pre-training baseline if instruction is not continued,37 it is clear that a “one
and done” approach to team training will likely not have lasting results. Optimal training content
Simulation Training
Simulation is deeply entrenched in the aviation industry, and has been adopted in
teaching surgical skills such as minimally invasive techniques. Airline pilots do not fly a
commercial plane until certified in a flight simulator. Further, pilots and crew simulate handling
emergencies during required semi-annual certifications. The medical literature is replete with
evidence of the value of simulation. However, most of the research has been on technical skills,
such as intubating and placing central lines.40 Training non-technical skills such as
communication and team work in the OR during simulation has been less well-studied, and very
few studies include all three major disciplines involved during an operation (surgery, anesthesia,
and nursing). A recent review identified only 10 studies that trained entire OR teams in non-
technical skills.40 Certainly, these training efforts require considerable time and resources to
implement and their value is not yet known. However, initial testing of a crisis management
simulation for entire OR teams at the University of Rochester has already caught a potentially
Training for teamwork is working its way into children’s surgery. Most hospitals are
focusing on events that were historically cared for by “flash mobs.” Team-based simulation
education has been found to prevent errors and improve injury-specific management during
pediatric trauma.41 The timeliness and efficiency of task completion during resuscitations was
recently shown to be improved by closed loop communication within pediatric trauma teams.42
CRM training has been shown to enhance nontechnical skills for pediatric trauma crews43 and
increase confidence in pediatric critical care units during crisis scenarios44. The use of simulation
to improve collective learning and performance during these uncommon events is exciting and
encouraging.
To the authors’ knowledge, there have been no studies to date investigating the results of
team dynamics and training for team work in the OR in children’s hospitals. A recent survey of
children’s surgeons and anesthesiologists in the American Academy of Pediatrics found that only
about a third of children’s hospitals/institutions offered team training.45 The programs were
reported to be beneficial by pediatric surgeons and anesthesiologists who have completed them.
children’s hospitals. Future research into how often team training should occur, development of
standardized curricula, and creation of tools to accurately measure team work and the efficacy of
Surgeons and hospitals are beginning to invest in the improved understanding of group
dynamics, human factors, and adoption of CRM principles. Preliminary data suggest that training
results in reduced medical errors, improved OR efficiency, and better morale among surgeons
and hospital staff. We anticipate that initial and recurrent training in human factors will become a
part of surgical residency training and maintenance of certification for surgeons. By embracing
the principles of CRM surgeons can foster a team approach to deliver optimal and safer care to
our children.
communication, situation monitoring, and mutual support amongst health care team members.
Reproduced from the Agency for Healthcare Research (AHRQ) with permission.35
Table 2. The mnemonic IMSAFE was created by the Federal Aviation Administration to assess
a pilot’s fitness to operate aircraft.10 It has been adapted here for surgeons.
Table 3. A sample surgical Brief and Sign Out/Debrief implementing CRM principles modified
from a surgical checklist used at the University of Rochester. The surgical Time Out has been
omitted.
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Table 1. Staffing at a hypothetical Children’s Hospital demonstrating the possible number of
staff combinations assuming one individual from each group. (CRNA = Certified Register Nurse
Technicians Combinations
8 16 20 50 45 5,760,000
Table 2. The mnemonic IMSAFE was created by the Federal Aviation Administration to assess
a pilot’s fitness to operate aircraft.10 It has been adapted here for surgeons.
Illness Is the surgeon suffering any acute or chronic illness that distracts him or her
Medication Is the surgeon taking any medications that could affect performance or
judgment?
Stress Is the surgeon under significant stress from events in his or her professional or
personal life?
Alcohol Is the surgeon under the influence of alcohol? (Pilots are required by work
Fatigue Has the surgeon had adequate rest and nutrition? This issue may most often
from a surgical checklist used at the University of Rochester. The surgical Time Out has been
omitted. (OR = operating room, VTE = Venous Thromboembolism, PACU = post anesthesia
Crew: A crew refers to a group of people who work together in shared activity toward a
common goal, often in a structured or hierarchical organization.
Team: A team is a group of people linked in a common purpose. Human teams are especially
appropriate for conducting tasks that are high in complexity and have many interdependent
subtasks.
Flash Mob: A flash mob refers to an assembly of individuals who gather quickly in public to
carry out a brief, unusual act, and then quickly disband.
communication, situation monitoring, and mutual support amongst health care team members.
Reproduced from the Agency for Healthcare Research (AHRQ) with permission.35