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In 1795, the Scottish physician Alexander Gordon suggested that patients’ fevers were often the result of contagious processes and wrote that he believed that physicians (including himself) often carried this contagion to patients. Nearly 50 years later Sir Thomas Watson, a professor at King's College Hospital, London, who became president of the Royal College of Physicians, warned that colleagues who attended women with puerperal fever, a major cause of maternal mortality, were at risk for transmitting the disease to subsequent patients. He suggested that practitioners rinse hands with chlorine solution and change clothing following interactions with infected patients to avoid spreading puerperal fever from one patient to the next.
By David K. Henderson, MD; Laura M. Lee, BSN, MSc; and Tara N. Palmore, MD
"Those who cannot remember the past are condemned to repeat it."
-- George Santayana, Spanish Philosopher 1863-1952
In 1795, the Scottish physician Alexander Gordon suggested that patients’ fevers were often the result of contagious processes and wrote that he believed that physicians (including himself) often carried this contagion to patients.(1) Nearly 50 years later Sir Thomas Watson, a professor at King's College Hospital, London, who became president of the Royal College of Physicians, warned that colleagues who attended women with puerperal fever, a major cause of maternal mortality, were at risk for transmitting the disease to subsequent patients. He suggested that practitioners rinse hands with chlorine solution and change clothing following interactions with infected patients to avoid spreading puerperal fever from one patient to the next.(2)
In 1843, the American physician Oliver Wendell Holmes joined the discussion. Holmes, who was truly a renaissance man – not only a physician, but a published poet and accomplished author (a close friend and colleague of Ralph Waldo Emerson), a professor and, ultimately, dean of the Harvard Medical School – published “The Contagiousness of Puerperal Fever” in the New England Quarterly Journal of Medicine and Surgery (a forerunner of the New England Journal of Medicine). He concluded that puerperal fever could easily be carried from patient to patient by healthcare professionals and suggested that clean clothing and avoidance of autopsies by those aiding birth would prevent the spread of the disease.(3)
Holmes went to great lengths to collect substantial anecdotal data supporting his hypothesis. Reading his monograph is an humbling experience: he had enormous insight into the transmissibility of this deadly syndrome. In spite of the carefully amassed, formidable evidence presented in his paper, Holmes’ comments aroused the ire of many of his surgical colleagues at the time, including some who were recognized as regional and national leaders in their fields. One such individual who took substantial umbrage at Holmes’ writings was the esteemed professor of obstetrics and diseases of women at the Jefferson Medical College in Philadelphia, Dr. Charles Delucena Meigs. Meigs openly opposed Holmes’ idea that physicians’ hands could transmit disease to their patients by writing in 1854 that, "Doctors are gentlemen, and gentlemen’s hands are clean."(4)
In 1846, three years after Holmes’ publication, Ignaz Semmelweis, a Hungarian physician who is an icon in the healthcare epidemiology community, reached a similar conclusion independently as a result of his careful evaluation of an increased maternal mortality rate on one obstetrical ward compared with another in his hospital. Semmelweis noted that patients on one ward had a mortality rate of 11.4 percent compared with only 2.7 percent for patients on the other ward. In a seminal event that led him to a breakthrough, one of Semmelweis’ close friends, a pathologist, sustained a scalpel injury during an autopsy on a patient who had died from puerperal fever. The pathologist quickly became ill with a syndrome that was, to Semmelweis, indistinguishable from that seen in severe puerperal fever, and that ultimately resulted in his death. Semmelweis formed an hypothesis that medical staff,and, in particular, physicians were spreading the disease from one patient to another.
He required physicians and medical students to dip their hands into a solution containing chlorinated lime (calcium hypochlorite) after participating in autopsies and before examining obstetrics patients, in essence conducting the first clinical trial of hand hygiene as an infection prevention intervention. As a result of his intervention (an intervention that was unpopular with his colleagues), the death rate on the first ward decreased by nearly 90 percent. Of note is the fact that the death rate also decreased on the second ward by more than 50 percent. Nonetheless, despite the dramatic evidence of efficacy of his intervention, his ideas were met with skepticism – and even derision – by the contemporary medical community, including many of the leading medical experts of his time. So significant was the backlash to his findings that 150 years later, we now refer to a circumstance in which factual knowledge is unthinkingly and systematically dismissed because the evidence runs contrary to existing culture or contradicts existing paradigms as “the Semmelweis reflex.”(5)
All three of these sets of observations occurred long before the so-called “germ theory” of infectious diseases was postulated. Louis Pasteur conducted perhaps the best known of the experiments documenting the clear relationship between bacteria and disease in the early 1860s.(6) Ironically, Pasteur’s work confirmed a clear relationship between the Streptococcus and puerperal fever. The elegant work of Robert Koch, Carl Friedländer, Josef Lister and many others helped establish, with certainty, the “germ theory” as fact.
Some of these observations were made more than 200 years ago. Semmelweis published his magnum opus in 1861.(7) Despite the fact that the healthcare industry has had more than a century and a half to assimilate the incontrovertible evidence that hand hygiene prevents the transmission of healthcare-associated infections, the industry has been unable to modify its culture to incorporate the use of hand hygiene as a consistent patient safety practice.
Perhaps even more troubling is that 150 years after the publication of Semmelweis’ treatise, we continue to encounter a contemporary ‘Semmelweis reflex’ about the use of hand hygiene in healthcare. In an era in which we encounter multidrug-resistant organisms with ever-increasing frequency, crucial infection prevention strategies, and, most notably, effective hand hygiene, remain the primary tools available to prevent the spread of these problematic pathogens in our healthcare environments. Multidrug-resistant organisms, some of which are not treatable with any antimicrobial agent or combination of agents, can represent life-threatening emergencies, particularly for immunocompromised patients. Healthcare personnel should be redoubling efforts to prevent infections that cannot be successfully treated; sadly, the enduring healthcare culture remains a substantial barrier to patient safety.
Carefully designed hand hygiene studies over the past three decades have failed to demonstrate the kind of compliance to workplace regulations that are routinely illustrated by employees in the computer manufacturing, nuclear power, or air traffic control industries.(8-11) Even the best results from these studies fail to achieve adherence rates that approach those expected in high-reliability organizations. Results from carefully conducted studies have been disappointing, at best, with many showing compliance/adherence rates of 60 percent or less. So, a century and a half following the elegant work of Holmes and Semmelweis, how can the discipline of healthcare epidemiology, collectively, move our industry toward the goal of 100 percent adherence to hand hygiene, as would be expected in other “high-reliability organizations”?
Characteristics of “high reliability organizations” include: an ongoing preoccupation with failure and the factors that contribute to failure (i.e., humans make mistakes, and we need to learn about the factors that contribute to non-adherence); a reluctance to over-simplify the factors that contribute to adherence and non-adherence; attention to the details of processes and how the processes actually function (i.e., appreciating the human factors that influence the processes); a commitment to resilience (learning from adverse events and bouncing back) and redundancy in process design and management; and a deference to expertise (one has to pay attention to both the experts as well as individuals at the local level, as those working with the process on a daily basis often know best). Application of these characteristics to the hand-hygiene enigma may afford another avenue for cultural change.(12-13)
Several factors have aligned that may open the door to cultural change. First, healthcare-associated infections are incredibly expensive at a time when the economy is not as robust as it has been, healthcare costs are receiving increased scrutiny, and hospitals are no longer being reimbursed for certain healthcare-associated infections. In 2009, Centers for Disease Control and Prevention (CDC) estimated that the costs associated with healthcare-associated infections in the U.S. ranged between $28.4 and $33.8 billion, and further estimated that appropriate prevention activities, including effective hand hygiene, might reduce these costs by as much as 70 percent.(14)
Secondly, hand hygiene has become a focus of the burgeoning patient safety industry and, is, without any doubt, a significant patient safety matter. The engagement of our patient safety colleagues in this fight provides insightful reinforcements. Their knowledge of behavioral modification and human factors issues will likely provide novel approaches to this longstanding problem.
Third, healthcare regulators, from the Joint Commission to the Centers for Medicare and Medicaid Services (CMS) and beyond, are beginning to focus on prevention activities in healthcare-delivery settings. Hospitals and other healthcare delivery sites are now expected to utilize precise metrics for adherence and to develop improvement strategies and interventions when the data are less than optimal. Accreditation and funding decisions may rest on institutions’ abilities to meet these goals.
Fourth, the continuing pressure for public reporting of healthcare-associated infection rates (with all of its unfortunate and, sometimes inappropriate accompanying baggage) will likely focus healthcare institutions’ energy on any and all interventions that may decrease healthcare-associated infection rates. The details of infection control protocols, including meticulous attention to the appropriate performance of hand hygiene, are obvious areas for emphasis.
Fifth, for some of the very highly resistant organisms (e.g., the carbapenem--resistant Enterobacteriaceae) that are increasingly being transmitted in hospitals and longterm care facilities, prevention activities are all we have to protect patients. These pathogens are resistant to most, if not all, available antimicrobials. When severely immunocompromised patients develop healthcare-associated infections caused by these organisms, we have no adequate antimicrobial therapy to cure their infections. Attention to the details of infection control protocols becomes incredibly critical in such settings and effective hand hygiene is a mandatory part of those protocols.
New technologies that make monitoring of adherence to prevention strategies more practical are rapidly becoming available. All of us have suffered with the challenges of direct observation as a mechanism for measuring adherence. With some of these newer devices we may get the opportunity to see data – perhaps for the first time –that are unencumbered by reporter bias or by the Hawthorne effect associated with direct observation.
Nonetheless, direct observation can offer substantial benefit. In our own institution, when multidrug-resistant organisms were being transmitted, we hired contract nursing assistants to serve as adherence monitors and placed them directly outside patient rooms 24 hours a day to assure that all personnel and visitors entering and leaving patients’ rooms adhered to infection control protocol, including the use of appropriate hand hygiene. Although costly, implementing this intervention was temporally associated with termination of two MDRO outbreaks.(15-17)
Finally, and perhaps most importantly, for many of the reasons noted above, the problems brought about by less-than-optimal hand hygiene almost certainly are going to attract the attention of both the physician and executive leadership in healthcare institutions. If the physicians and executive leadership of institutions can be convinced (in the manner of Holmes and Semmelweis) that hand hygiene is a critical preventive strategy, we may find the single best opportunity in history to effect cultural change.
With any luck, this constellation of factors may provide the impetus to move our industry from its current, longstanding, and perhaps somewhat stagnant culture to one in which the reliability with which healthcare professionals follow appropriate protocol for patient interactions approaches that in other high-reliability organizations.(18) Should that happen, we are certain that the work of the historical trailblazers characterized above will finally be placed in appropriate context.
The authors are affiliated with the Office of the Deputy Director for Clinical Care and the Hospital Epidemiology Service Clinical Center. National Institutes of Health in Bethesda, Md.
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2. De Costa C.M. The contagiousness of childbed fever: a short history of puerperal sepsis and its treatment. M Med J Aust 2002; 177 (11): 668-671.
3. Holmes OW. On the contagiousness of puerperal fever. New England Quarterly Journal of Medicine. 1842-3;1:503-30. Reprinted in Vol. XXXVIII, Part 5. The Harvard Classics. New York: P.F. Collier & Son, 1909–14.
4. Meigs, Charles Delucena. On the Nature, Signs, and Treatment of Childbed Fevers. Philadelphia: Blanchard and Lea, 1854: 104.
5. Balint P, Balint G. The Semmelweis-reflex. Orv Hetil. 2009;150(30):1430.
6. Pasteur, Louis (1880) [May 1880]. "(translated from French)" [On the extension of the germ theory to the etiology of certain common diseases]. Comptes rendus, de l’Academie des Sciences XC. Ernst, H.C. (trans). pp. 1033–44.
7. Semmelweis IP. Die aetiologie, der begriff und die prophylaxis des kindbettfiebers (The Etiology, Concept, and Prophylaxis of Childbed Fever). Pest, Wein, und Leipzig: Harleben's Verlags-Expedition 1861.
8. Albert RK, Condie F. Hand-washing patterns in medical intensive-care units. N Engl J Med. 1981;304(24):1465-6.
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11. Bischoff WE, Reynolds TM, Sessler CN, Edmond MB, Wenzel RP. Handwashing compliance by health care workers: The impact of introducing an accessible, alcohol-based hand antiseptic. Arch Intern Med. 2000;160(7):1017-21.
12. Chassin, MR, Loeb, JM. The ongoing quality improvement journey: next stop, high reliability. Health Affairs 2011; 30(4):559–568.
13. Carrol, JS, Rudolph, JW. Design of high reliability organizations in health care. Qual Saf Health Care 2006;15(Suppl I):i4–i9.
14. Scott II, R.D. The direct medical costs of healthcare-associated infections in U.S. Hospitals and the benefits of prevention. – Centers for Disease Control and Prevention. Atlanta, GA. March 2009. Accessed 3-10-2014, at http://www.cdc.gov/hai/pdfs/hai/scott_costpaper.pdf p 1-16.
15. Palmore TN, Michelin A, Bordner M, Odom R, Stock F, Fedorko D, Murray PR, Henderson DK. Use of adherence monitors as part of a team approach to control clonal spread of multidrug-resistant Acinetobacter baumannii in a research hospital. Infect Control Hosp Epidemiol. 2011; 32(12): 1166-72.
16. Snitkin ES, Zelazny AM, Thomas PJ, Stock F, National Institutes of Health Intramural Sequencing Center Comparative Sequencing Program, Henderson DK, Palmore TN, Segre JA. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole genome sequencing. Science Translat Med 2012; 4(148)ra116 (1-9).
17. Palmore TN, Henderson DK. Managing transmission of carbapenem-resistant Enterobacteriaceae in healthcare settings: A view from the trenches. Clin Infect Dis. (2013) 57 (11):1593-1599.
18. Palmore TN, Henderson DK. Carbapenem-resistant Enterobacteriaceae: a call for cultural change. Ann Intern Med. 2014; in press.