The impact of smoking on neurosurgical outcomes

A review

Free access

Cigarette smoking is a common health risk behavior among the general adult population, and is the leading preventable cause of morbidity and mortality in the US. The surgical literature shows that active tobacco smoking is a major risk factor for perioperative morbidity and complications, and that preoperative smoking cessation is an effective measure to lower these risks associated with active smoking. However, few studies have examined the effects of smoking and perioperative complications following neurosurgical procedures. The goal of this review was to highlight the scientific data that do exist regarding the impact of smoking on neurosurgical outcomes, to promote awareness of the need for further work in the specific neurosurgical context, and to suggest ways that neurosurgeons can promote smoking cessation in their patients and lead efforts nationally to emphasize the importance of preoperative smoking cessation. This review indicates that there is limited but good evidence that smoking is associated with higher rates of perioperative complications following neurosurgical intervention. Specific research is needed to understand the effects of smoking and perioperative complications. Neurosurgeons should encourage preoperative smoking cessation as part of their clinical practice to mitigate perioperative morbidity associated with active smoking.

Abbreviation used in this paper:SAH = subarachnoid hemorrhage.

Abstract

Cigarette smoking is a common health risk behavior among the general adult population, and is the leading preventable cause of morbidity and mortality in the US. The surgical literature shows that active tobacco smoking is a major risk factor for perioperative morbidity and complications, and that preoperative smoking cessation is an effective measure to lower these risks associated with active smoking. However, few studies have examined the effects of smoking and perioperative complications following neurosurgical procedures. The goal of this review was to highlight the scientific data that do exist regarding the impact of smoking on neurosurgical outcomes, to promote awareness of the need for further work in the specific neurosurgical context, and to suggest ways that neurosurgeons can promote smoking cessation in their patients and lead efforts nationally to emphasize the importance of preoperative smoking cessation. This review indicates that there is limited but good evidence that smoking is associated with higher rates of perioperative complications following neurosurgical intervention. Specific research is needed to understand the effects of smoking and perioperative complications. Neurosurgeons should encourage preoperative smoking cessation as part of their clinical practice to mitigate perioperative morbidity associated with active smoking.

Cigarette smoking is the leading preventable cause of morbidity and mortality in the US. Even at low levels, tobacco smoke has been shown to be detrimental to overall health,9 and is associated with cancer, coronary artery disease, chronic obstructive pulmonary disease, cerebrovascular disease, peripheral vascular disease, and birth defects.1,26,44,47,85 One in 5 deaths in the US is attributed to tobacco use, which translates to nearly half a million deaths annually.86 In addition, the tobacco-related burden of morbidity and mortality is a significant strain on medical expenditures and health care systems.12 Despite the push for tobacco cessation and the advances in tobacco control, an estimated 44 million Americans continue to smoke and the prevalence continues to rise, making this an ever more important issue.73,86

Smoking has long been identified as a risk factor for chronic disease, but expanding evidence in the surgical literature demonstrates that tobacco smoking is also a risk factor for perioperative morbidity and complications.42,93,97 Active smoking has been clearly linked to increased risk of perioperative cardiovascular complications, pulmonary complications, and wound healing complications (including infections, anastomotic dehiscence, reintubation, and respiratory failure).42 These complications in turn result in longer hospital stays, higher rates of ICU admission, greater need for repeat surgery, and higher overall costs of care.42 The impact of smoking on perioperative outcomes is relatively well defined in general surgery,96 cardiac surgery,23,35,97 plastic surgery,50,78,79,84,105 orthopedic surgery,6,72,83,89 and pediatric surgery.25,60,70,88

Among the neurosurgical subspecialties, it is generally well accepted that smoking leads to increased risk for intracranial aneurysm formation,17,28,32,36,39,75,77 aneurysmal SAH,8,36–38,57,76 and decreased bone healing and fusion after spine surgery.21,34,61 However, the effects of smoking on perioperative morbidity following neurosurgical procedures are less well defined. In this review, we sought to highlight the existing scientific data regarding the impact of smoking on neurosurgical outcomes, identify where additional studies are needed, and suggest ways that neurosurgeons can lead the efforts nationally to emphasize the importance of preoperative smoking cessation.

Methods

The words “smoking and neurosurgery” or “tobacco and neurosurgery” were used as search terms in PubMed (for the years 1950–2012) to identify all articles that included at least one of these terms or phrases. The references lists of the relevant articles and systematic reviews were scanned for additional sources.

Results

How Smoking Increases Perioperative Complications

Cigarette smoking is associated with numerous toxic effects to the body, even at the cellular level: cellular damage secondary to free radical release,33 tissue hypoxia,14 compromised immune cell function,107 and microvascular injury leading to dysfunction and thrombogenesis.50 Each of these mechanisms can contribute to the multitude of smoking-related complications seen in the perioperative period. The increased perioperative morbidity risk that smoking poses for patients is probably related to both the acute and long-term consequences of tobacco use.

Cellular Injury and Vascular Dysfunction

One of the best-understood mechanisms of the way that smoking can lead to perioperative complications relates to the pathophysiological effects of smoking that cause tissue hypoxia, thrombogenesis, and vasoconstriction. Tissue hypoxia is thought to be secondary to direct damage of the microvasculature that results in detachment of endothelial cells from the lumen of small vessels. The loss of endothelial protection results in exposure of a prothrombogenic/procoagulant basement membrane, increased platelet activation, and activation of the coagulation cascade.50 In addition, as endothelial cells are injured and detached from the microvasculature, there is an intrinsic deficiency in endothelial-derived relaxing factor, which leads to a decrease in anticoagulation and antispasmodic factors.50 The end result of this process is hypercoagulability and vasoconstriction, and both mechanisms can lead to cellular and tissue hypoxia.

Tissue hypoxia is further exacerbated by the systemic effects of nicotine and carbon monoxide. Residual nicotine in the blood can activate the sympathetic nervous system, induce release of epinephrine and norepinephrine from the adrenal glands,98 and increase leukotriene and thromboxane levels.2,15 The increase of these metabolites leads to additional vasoconstriction of microvasculature.14,46 Carbon monoxide is found in high concentrations as a toxic byproduct of tobacco smoke. Its pathophysiological mechanism involves the competitive binding of hemoglobin and consequent decrease in the oxygen-carrying capacity of blood. A chronic hypoxic state (due to binding of carbon monoxide to hemoglobin) can stimulate a physiological erythropoietic response as a compensatory mechanism. Increased blood cell count and mass can lead to the consequences of red cell aggregation, increased blood viscosity, and thrombogenicity.79

These cumulative effects of tobacco smoking effectively result in the Virchow triad for thrombosis as well: endovascular injury/dysfunction, hemostasis (increased viscosity), and stasis (especially for procedures with associated postoperative immobility).27

Wound Healing and Infection

Wound healing is highly dependent on the ability of the vasculature to provide essential nutrients, oxygen, growth factors, and immune cells. Therefore dysfunction of the microvasculature can lead to significantly impaired wound healing.107 Tobacco smoking results in significant injury and dysfunction of the vasculature, and therefore may cause decreased oxygen, nutrients, and immune cells at the site of incision, which are essential for wound healing.65 In addition, tobacco may stimulate a stress response mediated by enhanced fibroblast activity, resulting in decreased cell migration and increased cell adhesion. The net consequence is inappropriate connective tissue deposition at the surgical site, delayed wound healing, and increased risks of wound infection.53,107

Intraoperative Blood Loss

In the neurosurgical literature, 2 retrospective clinical studies suggest that active smokers tend to have higher intraoperative blood loss following craniotomy for tumor resection and lumbar spine surgery.20,53 The exact underlying mechanism has yet to be defined. In the literature regarding craniotomy for tumor resection, there is evidence that cigarette smoking can lead to an acute hyperemia response and long-term morphological changes within the cerebral vasculature.2,22,95 Acute hyperemia is a result of a buildup of transient vasodilating metabolites in blood vessels2,95 and causes increased blood flow within the cerebral vasculature, which can potentially contribute to an increase in blood loss during craniotomy. With regard to long-term plastic changes, smoking causes permanent structural changes of vessels such as vessel wall thickening, which can result in the dysfunction and/or inhibition of vessel accommodation during bleeding.45 These correlate with a Doppler ultrasonography study that showed impairment of the cerebral vasculature even after smoking cessation.11 In addition, tumor vascularity probably plays a role in blood loss intraoperatively. There is evidence that cigarette smoking is associated with increased proliferation and angiogenesis of blood vessels, leading to larger and more vascularized tumors, which may further contribute to intraoperative blood loss during resection.62,109

Cardiopulmonary Effects

Although pulmonary complications can result from poor lung function and/or exacerbation of chronic smoking-related diseases, even smokers without chronic disease are at increased risk for perioperative morbidity.101 There are many mechanisms for which tobacco smoking increases the risk for pulmonary complications in the perioperative period. Oxidative damage following smoke exposure can result in mucosal damage, goblet cell hyperplasia, ciliary dysfunction, and impaired bronchial function, which leads to the inability to expel mucus.4,82 This can further translate the respiratory environment into a favorable nidus for pathogenic organisms and lead to infection and possibly respiratory failure. In fact, smokers tend to have delayed bacterial clearance and increased bacterial load compared with their nonsmoking counterparts.24 In addition, smoking alters the respiratory immune response: it leads to increased airway inflammation resulting in bronchial hyperreactivity,30 and impaired alveolar macrophage function, further contributing to higher rates of postoperative pneumonia.56

As with pulmonary complications, the adverse perioperative cardiovascular effects of smoking are thought to have both chronic and acute contributions. Long-term tobacco smoking promotes systemic atherosclerosis, alteration of lipid metabolism via increased lipolysis and lipotoxicity, and insulin resistance.31 The most devastating sequelae from these systemic abnormalities are macrovascular complications such as perioperative myocardial infarct, pulmonary embolus, and even stroke. But even short-term smoking exposure poses a significant perioperative morbidity risk through mechanisms of increased coagulability, increased sympathetic tone, and reduced oxygen-carrying capacity.101 In smokers the reduced oxygen-carrying capacity is an additional risk factor for decreased oxygen supply to the heart, which places these patients at even higher risk for myocardial ischemia and/or infarct.

The Evidence: Smoking and the Risks in Neurosurgery

Cranial Surgery

Only a few studies have examined how smoking affects perioperative morbidity and mortality following neurosurgical intervention (Table 1). The most robust studies of tobacco smoking and its association with morbidity in neurosurgery are in the cerebrovascular literature. Abundant evidence demonstrates that smoking is highly associated with the risk for aneurysm formation17,28,32,36,39,75,77 and aneurysm rupture/SAH.8,36–38,57,76 In fact, smoking cessation has been suggested as an excellent alternate treatment for older patients with small intracranial aneurysms.38

TABLE 1:

Studies evaluating the effect of smoking on neurosurgical procedures

Authors & YearProcedure TypeNo. of PatientsResults
Lau et al., 2012craniotomy for tumor resection453smokers had higher rates of blood loss & complications; smokers who quit had reduced risk of postop complications & higher 1-yr survival rates compared to active smokers
Litvack et al., 2009collagen sponge dural graft implant following craniotomy475smoking did not affect risk of infection or CSF leak
Krishnamurthy et al., 2007clip &/or coil occlusion of aneurysmal SAH320smokers more likely to experience delayed neurological deterioration
Dean et al., 2006lumbar spine surgery500smoking associated w/ increased blood loss & intraop transfusion

Several studies examining smoking and the treatment of cerebrovascular disorders provide good evidence that smoking is associated with greater perioperative morbidity and worse outcomes. A retrospective study of 320 patients with aneurysmal SAH who underwent surgical or endovascular treatment showed that current smokers (patients with at least a 10 pack-year history and who were still smoking during the past year) and patients with a 20 pack-year or longer history of tobacco use were more likely to experience neurological deterioration occurring at least 2 days after intervention.48 Other studies of postoperative outcomes of aneurysmal SAH have also shown that smokers have higher rates of pulmonary complications,66 greater need for ventilation,66 and greater risk for cerebral vasospasm.74,106 Smokers even have higher rates of complications following diagnostic cerebral angiography and neuroendovascular procedures.54 Altered wound healing has also been seen after superficial temporal artery–middle cerebral artery anastomosis; more specifically, it has been suggested that smokers have higher rates of cutaneous necrosis.41

Within the subspecialty of neurooncology, just one study has evaluated the association between tobacco smoking and perioperative outcome after craniotomy for tumors. It was a retrospective study of 453 patients in which it was found that current smoking status was an independent risk factor for higher intraoperative blood loss, postoperative complication risk, and lower 1-year survival following craniotomy for tumor resection.53 Another finding was t hat patients who quit smoking continued to have significantly higher mean blood loss, but did not carry a higher risk for postoperative complications and 1-year mortality. This may demonstrate that smoking cessation may be effective in mitigating the perioperative morbidity risks associated with active smoking after tumor resection.

Two studies examined the effects of smoking on specific cranial procedures. A single-center retrospective study of 475 patients found that smoking does not seem to affect the risk of infection and CSF leakage after the use of collagen sponge dural allografts.59 Similarly, smoking was not a risk factor for failure in tissue cranial reconstruction.69 The last study, however, was a retrospective review of only 21 patients.

Spine Surgery

The neurosurgical spine literature contains considerable evidence that smoking is associated with worse long-term outcomes, but there are few studies of smoking and its effects on perioperative morbidity and mortality. Most of the data pertaining to spine surgery demonstrates that smoking is associated with delayed spinal fusion,55 poor spinal fusion rates,21,34,61 and higher rates of pseudarthrosis following spinal instrumentation.108 Smoking has been identified as a risk factor for higher subsidence rates in the placement of carbon fiber cages following anterior cervical discectomy and fusion.7 The mechanism behind poor fusion and greater rates of subsidence in smokers is related to poor bone quality secondary to tobacco smoking. Nicotine exposure is associated with delayed vascularization and smaller areas of revascularization, which lead to reduced levels of osteogenesis and hypocellular fusion mass.19 There is also evidence that smokers have higher rates of recurrent lumbar disc herniation after surgery.16,43,92 The higher rates of recurrent disc herniation are possibly secondary to nicotine-induced vasoconstriction and decreased blood flow to the area of prior surgery.43 This results in the inhibition of the annular healing process and degeneration.

The only study that directly evaluated whether tobacco smoking affected perioperative outcomes was a retrospective review of 500 patients that demonstrated that smoking was associated with increased surgical blood loss and intraoperative transfusion following lumbar spine surgery.20

Peripheral Nerve Surgery

The neurosurgical literature contains no studies that directly examined the effects of smoking and perioperative outcomes after surgery for diseases of the peripheral nervous system.

Applicability of Studies From Other Surgical Specialties

Of the surgical literature on the association of smoking and perioperative complications, the most applicable to neurosurgery comes from the specialties of plastic surgery, orthopedic surgery, and vascular surgery. In plastic surgery, wound healing is of paramount importance because success is often judged largely on aesthetic appearance. Plastic surgery studies have shown that tobacco smokers have increased rates of wound infections, reduced skin flap survival, and increased risk for skin necrosis.5,13,49,50 Similar to procedures in plastic surgery, neurosurgical procedures often involve large incisions in readily visible areas, as are used when performing a craniotomy. Therefore, proper and optimal wound healing is important because this may have large implications for appearance and quality of life, especially in the pediatric population.

Because orthopedic surgery is often involved with the surgical management of the spine, studies from this discipline are clearly applicable to neurosurgical patients who are undergoing spine surgery. Two orthopedic studies have demonstrated that tobacco smoking is associated with poor fusion rates, supporting similar findings in the neurosurgical literature.87,108 In a retrospective study of 4555 patients, smoking cessation was associated with less residual back pain and less need for analgesic drugs.83

Carotid endarterectomy is performed both by general vascular surgeons and by neurosurgeons; therefore, findings from the vascular literature regarding smoking's effect on perioperative outcomes after endarterectomy are most likely to be applicable to neurosurgery as well. Among patients who experience perioperative stroke as a complication following endarterectomy, a significant portion are active smokers, and therefore it is suggested that active smoking status is a risk factor for perioperative stroke following this procedure.81 In addition, a randomized controlled trial showed that active smoking status is a risk factor for restenosis following carotid endarterectomy.52

Discussion

Our review of tobacco smoking and perioperative outcomes in neurosurgery indicates that the limited literature available provides evidence that smoking is associated with higher perioperative morbidity after neurosurgical intervention (Table 2). Most of the studies were done in the subspecialties of cerebrovascular surgery and spine surgery. Compared with studies from other surgical specialties, few in neurosurgery concentrate on the effects of smoking on perioperative rather than long-term outcomes. Although it may be appropriate to apply certain findings from other fields such as plastic surgery, orthopedics, and vascular surgery for the time being, further studies are needed to assess the effects of smoking and perioperative complications following specific neurosurgical procedures. Nevertheless, tobacco smoking is an overall detriment to patient health, and smoking cessation should be encouraged preoperatively to mitigate the associated risk for complications and to reap the long-term benefits of neurosurgical treatment.

TABLE 2:

Major smoking-related morbidities by neurosurgical subspecialty

SubspecialtyPerioperative MorbidityLong-Term Complications
neurooncologyintraop blood loss, postop complicationslower 1-yr survival
spine surgeryintraop blood loss, increased need for transfusiondelayed spine fusion, pseudarthrosis, higher subsidence rates, recurrent lumbar disc herniation
cerebrovascularneurological deterioration, stroke, altered wound healing/cutaneous necrosis, pulmonary complicationsaneurysm rupture, aneurysm formation

Evidence of the Effect of Smoking Cessation on Surgical Outcomes

Accumulating evidence indicates that smoking cessation can reduce the higher perioperative complications risk seen in active smokers and possibly improve long-term outcomes. A randomized clinical trial demonstrated that a 4-week smoking cessation program consisting of individual counseling and nicotine replacement provided a 49% relative risk reduction in postoperative complications among smokers.58 Another clinical trial showed a significant decrease in complication rates, especially wound healing, when patients abstained from smoking for 6–8 weeks.64 A third trial demonstrated a significant decrease in postoperative complications after repair of acute fractures.68 However, one randomized trial was an exception; it showed that 2-week preoperative smoking cessation did not change postoperative complication rates and risk following colorectal surgery.91 However, a major drawback to this study was that it was originally powered to 0.80 if 300 patients were included, but only 60 patients were included in the final analysis. This dramatically limits the ability to detect a potential benefit.

Because there is strong evidence from the other randomized clinical trials that smoking cessation is effective in decreasing perioperative morbidity risk, preoperative smoking cessation should be implemented to improve neurosurgical outcomes. The exact duration of abstinence required for these benefits to be observed is unclear.102,103 The benefit probably depends both on the duration of cessation and the neurosurgical complication of interest. The suggested durations of smoking cessation range from hours to days for cardiovascular complications,40,99 and even months for pulmonary complications, depending on the study.100 Most trials have found that 4–8 weeks of smoking abstinence significantly reduces perioperative complications and the need for repeat surgery.58,63,64 There are even trials that demonstrate that just 3 weeks of smoking cessation is beneficial.71

Although it may seem intuitive that smoking cessation should be encouraged whenever possible and even for brief periods, there has been controversy in the past that brief preoperative abstinence may actually increase the risk of pulmonary complications, and that cessation must occur at least 8 weeks before surgery.10,51 However, a meta-analysis demonstrated no suggestion of increased postoperative complications associated with brief durations of smoking cessation.67 In addition, there is no reliable evidence that abstinence of any duration increases the risk for complications.90,93 Therefore, neurosurgeons can confidently and safely encourage preoperative smoking cessation at any time before surgery.

Smoking Cessation: the “Teachable Moment” and Current Barriers

Encouraging patients to quit smoking may seem quite simple, but in actuality and in clinical practice this is not the case, because tobacco is highly addicting. In addition, undergoing surgery is very stressful for many patients and, stress being a common motivator for smoking, may make quitting even more difficult.18 However, the seriousness of surgery can be used to the advantage of the clinician in motivating patients to quit smoking successfully. This relates to the phenomenon of a “teachable moment,” in which an event such as disease diagnosis, hospitalization, or pregnancy motivates a patient to change a risky health behavior. During these times, patients may be more amenable to changing their habits and/or addiction because of the risk to self. In fact, it has been shown that patients tend to be more likely to quit smoking after hospitalization for serious illness.29,80 Therefore, not only does preoperative smoking cessation decrease perioperative morbidity, but scheduling surgery is a great opportunity to encourage permanent smoking cessation so the patient can reap the lifelong benefits of a tobacco-free life.

Despite the potential “teachable moment” that surgery presents for smoking cessation, neurosurgeons are currently not capitalizing on this event. Studies suggest that almost half of all surgeons do not routinely counsel their patients to stop smoking before an operation, and it is most likely that neurosurgeons are not an exception in this regard.104 In addition, smoking cessation counseling is practice dependent, and no set structures have been implemented to promote preoperative smoking cessation in the traditional neurosurgical practice. Brief counseling (less than 3 minutes) may increase rates of smoking cessation.40,64 However, even with appropriate counseling the failure rate of smoking cessation can remain high, and often multiple attempts are required.3 Therefore, methods need to be implemented to make sure patients remain successful in quitting their smoking habit. In one randomized trial of a perioperative smoking cessation intervention, high cessation rates were obtained—most likely because the intervention was intense and included repeated personal contact.58 More intensive smoking cessation programs are associated with higher quit rates and are effective in surgical settings, whereas other briefer and less intensive programs are less effective.94 Therefore, a strict smoking cessation program is likely to be the key to success for patients to stop smoking. Effective interventions that health care providers can use to help patients stop smoking include simple open dialog about the patient's motivation to quit smoking, individual counseling, group counseling, and repeated personal contact.

Policy Implications

There is considerable evidence that smoking is a major risk factor for perioperative complications, which points to a great opportunity to change policy and federal mandates regarding tobacco companies and the health care system. In 2009, landmark legislation that granted the FDA the authority to regulate tobacco was passed. However, in August of 2012, a US appeals court in Washington, DC, ruled that a requirement for graphic warning labels on cigarette boxes was unconstitutional and violated the First Amendment. The federal government subsequently asked for a further appeal of this ruling, but the US continues to lag behind other nations, which have implemented enhanced health warnings on cigarette packs. Therefore, alternative actions may be required to reduce smoking exposure: limits on the annual production of cigarettes by tobacco companies, an increase of taxes on the ingredients used to manufacture cigarettes, and restrictions on the height to which tobacco plants are allowed to grow.42 At a federal level, the creation of new policies that affect practicing neurosurgeons and medical care providers through the development and implementation of pay for performance mandates may be an effective incentive to further encourage patients to quit smoking preoperatively.

Conclusions

The surgical literature shows that active tobacco smoking is a major risk factor for perioperative morbidity and complications, and that preoperative smoking cessation is effective at lowering the risks associated with active smoking. The relatively few studies specifically in the neurosurgical literature do provide evidence that smoking is associated with higher rates of perioperative complications. Because one of the most powerful times to convince a smoker to quit is before a surgical procedure, neurosurgeons are encouraged to do so. On the policy level, neurosurgeons should take the lead in catalyzing constructive changes to minimize the impact of tobacco smoking in the perioperative setting.

Disclosure

Dr. Maa is vice chair of the University of California, Office of the President, Tobacco Related Disease Research Program's Scientific Advisory Committee. This is an unpaid position. The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author contributions to the study and manuscript preparation include the following. Conception and design: Maa, Berger. Acquisition of data: all authors. Analysis and interpretation of data: all authors. Drafting the article: Maa, Lau. Critically revising the article: all authors. Reviewed submitted version of manuscript: Maa, Lau. Approved the final version of the manuscript on behalf of all authors: Maa. Study supervision: Maa.

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    Lau DZiewacz JESiddiqi HKPelly ASullivan SEEl-Sayed AM: Cigarette smoking: a risk factor for postoperative morbidity and 1-year mortality following craniotomy for tumor resection. Clinical article. J Neurosurg 116:120412142012

  • 54

    Lawson MFVelat GJFargen KMMocco JHoh BL: Interventional neurovascular disease: avoidance and management of complications and review of the current literature. J Neurosurg Sci 55:2332422011

  • 55

    Lee TCUeng SWChen HHLu KHuang HYLiliang PC: The effect of acute smoking on spinal fusion: an experimental study among rabbits. J Trauma 59:4024082005

  • 56

    Lensmar CElmberger GSköld MEklund A: Smoking alters the phenotype of macrophages in induced sputum. Respir Med 92:4154201998

  • 57

    Lindekleiv HSandvei MSNjølstad ILøchen MLRomundstad PRVatten L: Sex differences in risk factors for aneurysmal subarachnoid hemorrhage: a cohort study. Neurology 76:6376432011

  • 58

    Lindström DSadr Azodi OWladis ATønnesen HLinder SNåsell H: Effects of a perioperative smoking cessation intervention on postoperative complications: a randomized trial. Ann Surg 248:7397452008

  • 59

    Litvack ZNWest GADelashaw JBBurchiel KJAnderson VC: Dural augmentation: part I-evaluation of collagen matrix allografts for dural defect after craniotomy. Neurosurgery 65:8908972009

  • 60

    Lyons BFrizelle HKirby FCasey W: The effect of passive smoking on the incidence of airway complications in children undergoing general anaesthesia. Anaesthesia 51:3243261996

  • 61

    Martin GJ JrHaid RW JrMacMillan MRodts GE JrBerkman R: Anterior cervical discectomy with freeze-dried fibula allograft. Overview of 317 cases and literature review. Spine (Phila Pa 1976) 24:8528591999

  • 62

    Martínez-García EIrigoyen MGonzález-Moreno OCorrales LTeijeira ASalvo E: Repetitive nicotine exposure leads to a more malignant and metastasis-prone phenotype of SCLC: a molecular insight into the importance of quitting smoking during treatment. Toxicol Sci 116:4674762010

  • 63

    Mason DPSubramanian SNowicki ERGrab JDMurthy SCRice TW: Impact of smoking cessation before resection of lung cancer: a Society of Thoracic Surgeons General Thoracic Surgery Database study. Ann Thorac Surg 88:3623712009

  • 64

    Møller AMVillebro NPedersen TTønnesen H: Effect of preoperative smoking intervention on postoperative complications: a randomised clinical trial. Lancet 359:1141172002

  • 65

    Monfrecola GRiccio GSavarese CPosteraro GProcaccini EM: The acute effect of smoking on cutaneous microcirculation blood flow in habitual smokers and nonsmokers. Dermatology 197:1151181998

  • 66

    Morris KMShaw MDFoy PM: Smoking and subarachnoid haemorrhage: a case control study. Br J Neurosurg 6:4294321992

  • 67

    Myers KHajek PHinds CMcRobbie H: Stopping smoking shortly before surgery and postoperative complications: a systematic review and meta-analysis. Arch Intern Med 171:9839892011

  • 68

    Nåsell HAdami JSamnegård ETønnesen HPonzer S: Effect of smoking cessation intervention on results of acute fracture surgery: a randomized controlled trial. J Bone Joint Surg Am 92:133513422010

  • 69

    Nassiri NCleary DRUeeck BA: Is cranial reconstruction with a hard-tissue replacement patient-matched implant as safe as previously reported? A 3-year experience and review of the literature. J Oral Maxillofac Surg 67:3233272009

  • 70

    O'Rourke JMKalish LAMcDaniel SLyons B: The effects of exposure to environmental tobacco smoke on pulmonary function in children undergoing anesthesia for minor surgery. Paediatr Anaesth 16:5605672006

  • 71

    Pearce ACJones RM: Smoking and anesthesia: preoperative abstinence and perioperative morbidity. Anesthesiology 61:5765841984

  • 72

    Peolsson AVavruch LOberg B: Predictive factors for arm pain, neck pain, neck specific disability and health after anterior cervical decompression and fusion. Acta Neurochir (Wien) 148:1671732006

  • 73

    Pleis JRLucas JWWard BW: Summary Health Statistics for US Adults: National Health Interview Survey 2008 National Center for Health Statistics2009. (http://www.cdc.gov/nchs/data/series/sr_10/sr10_242.pdf) [Accessed May 14 2013]

  • 74

    Pobereskin LH: Influence of premorbid factors on survival following subarachnoid hemorrhage. J Neurosurg 95:5555592001

  • 75

    Qureshi AISung GYSuri MFStraw RNGuterman LRHopkins LN: Factors associated with aneurysm size in patients with subarachnoid hemorrhage: effect of smoking and aneurysm location. Neurosurgery 46:44502000

  • 76

    Qureshi AISuri MFYahia AMSuarez JIGuterman LRHopkins LN: Risk factors for subarachnoid hemorrhage. Neurosurgery 49:6076132001

  • 77

    Rahme RJBatjer HHBendok BR: Multiplicative impact of smoking and genetic predisposition on intracranial aneurysm formation. Neurosurgery 67:N15N162010

  • 78

    Rees TDLiverett DMGuy CL: The effect of cigarette smoking on skin-flap survival in the face lift patient. Plast Reconstr Surg 73:9119151984

  • 79

    Riefkohl RWolfe JACox EBMcCarty KS Jr: Association between cutaneous occlusive vascular disease, cigarette smoking, and skin slough after rhytidectomy. Plast Reconstr Surg 77:5925951986

  • 80

    Rigotti NAMcKool KMShiffman S: Predictors of smoking cessation after coronary artery bypass graft surgery. Results of a randomized trial with 5-year follow-up. Ann Intern Med 120:2872931994

  • 81

    Rockman CBCappadona CRiles TSLamparello PJGiangola GAdelman MA: Causes of the increased stroke rate after carotid endarterectomy in patients with previous strokes. Ann Vasc Surg 11:28341997

  • 82

    Saetta MTGTurato GBaraldo SZanin ABraccioni FMapp CE: Goblet cell hyperplasia and epithelial inflammation in peripheral airways of smokers with both symptoms of chronic bronchitis and chronic airflow limitation. Am J Respir Crit Care Med 161:101610212000

  • 83

    Sandén BFPFörsth PMichaëlsson K: Smokers show less improvement than nonsmokers two years after surgery for lumbar spinal stenosis: a study of 4555 patients from the Swedish spine register. Spine (Phila Pa 1976) 36:105910642011

  • 84

    Sarin CLAustin JCNickel WO: Effects of smoking on digital blood-flow velocity. JAMA 229:132713281974

  • 85

    Sasco AJSecretan MBStraif K: Tobacco smoking and cancer: a brief review of recent epidemiological evidence. Lung Cancer 45:Suppl 2S3S92004

  • 86

    Schroeder SA: Tobacco control in the wake of the 1998 master settlement agreement. N Engl J Med 350:2933012004

  • 87

    Schwab FJNazarian DGMahmud FMichelsen CB: Effects of spinal instrumentation on fusion of the lumbosacral spine. Spine (Phila Pa 1976) 20:202320281995

  • 88

    Shi YWarner DO: Pediatric surgery and parental smoking behavior. Anesthesiology 115:12172011

  • 89

    Singh JAHTHouston TKPonce BAMaddox GBishop MJRichman J: Smoking as a risk factor for short-term outcomes following primary total hip and total knee replacement in veterans. Arthritis Care Res (Hoboken) 63:136513742011

  • 90

    Sørensen LT: Wound healing and infection in surgery. The clinical impact of smoking and smoking cessation: a systematic review and meta-analysis. Arch Surg 147:3733832012

  • 91

    Sørensen LTJørgensen T: Short-term pre-operative smoking cessation intervention does not affect postoperative complications in colorectal surgery: a randomized clinical trial. Colorectal Dis 5:3473522003

  • 92

    Swartz KRTrost GR: Recurrent lumbar disc herniation. Neurosurg Focus 15:3E102003

  • 93

    Theadom ACropley M: Effects of preoperative smoking cessation on the incidence and risk of intraoperative and postoperative complications in adult smokers: a systematic review. Tob Control 15:3523582006

  • 94

    Thomsen TVillebro NMøller AM: Interventions for preoperative smoking cessation. Cochrane Database Syst Rev 7CD0022942010

  • 95

    Tur EYosipovitch GOren-Vulfs S: Chronic and acute effects of cigarette smoking on skin blood flow. Angiology 43:3283351992

  • 96

    Turan AMascha EJRoberman DTurner PLYou JKurz A: Smoking and perioperative outcomes. Anesthesiology 114:8378462011

  • 97

    Underwood MJBailey JS: Coronary bypass surgery should not be offered to smokers. BMJ 306:104710481993

  • 98

    Wang WHWang DX: Role of sympathetic nerve and adrenal gland in the potentiation of hypoxic pulmonary vasoconstriction during cigarette smoking. J Tongji Med Univ 12:151992

  • 99

    Warner DO: Helping surgical patients quit smoking: why, when, and how. Anesth Analg 101:4814872005

  • 100

    Warner DO: Perioperative abstinence from cigarettes: physiologic and clinical consequences. Anesthesiology 104:3563672006

  • 101

    Warner DO: Preoperative smoking cessation: the role of the primary care provider. Mayo Clin Proc 80:2522582005

  • 102

    Warner DO: Tobacco dependence in surgical patients. Curr Opin Anaesthesiol 20:2792832007

  • 103

    Warner DOKlesges RCDale LCOfford KPSchroeder DRVickers KS: Telephone quitlines to help surgical patients quit smoking patient and provider attitudes. Am J Prev Med 35:6 SupplS486S4932008

  • 104

    Warner DOSarr MGOfford KPDale LC: Anesthesiologists, general surgeons, and tobacco interventions in the perioperative period. Anesth Analg 99:176617732004

  • 105

    Webster RCKazda GHamdan USFuleihan NSSmith RC: Cigarette smoking and face lift: conservative versus wide undermining. Plast Reconstr Surg 77:5966041986

  • 106

    Weir BKKongable GLKassell NFSchultz JRTruskowski LLSigrest A: Cigarette smoking as a cause of aneurysmal subarachnoid hemorrhage and risk for vasospasm: a report of the Cooperative Aneurysm Study. J Neurosurg 89:4054111998

  • 107

    Wong LSMartins-Green M: Firsthand cigarette smoke alters fibroblast migration and survival: implications for impaired healing. Wound Repair Regen 12:4714842004

  • 108

    Zdeblick TA: A prospective, randomized study of lumbar fusion. Preliminary results Spine (Phila Pa 1976) 18:9839911993

  • 109

    Zhang QTang XZhang ZFVelikina RShi SLe AD: Nicotine induces hypoxia-inducible factor-1alpha expression in human lung cancer cells via nicotinic acetylcholine receptor-mediated signaling pathways. Clin Cancer Res 13:468646942007

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Article Information

Address correspondence to: John Maa, M.D., 521 Parnassus Ave., C 341, San Francisco, CA 94131-0790. email: john.maa@ucsfmedctr.org.

Please include this information when citing this paper: published online June 18, 2013; DOI: 10.3171/2013.5.JNS122287.

© AANS, except where prohibited by US copyright law.

Headings

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Krueger JKRohrich RJ: Clearing the smoke: the scientific rationale for tobacco abstention with plastic surgery. Plast Reconstr Surg 108:106310772001

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Kuri MNakagawa MTanaka HHasuo SKishi Y: Determination of the duration of preoperative smoking cessation to improve wound healing after head and neck surgery. Anesthesiology 102:8928962005

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Lal BKBeach KWRoubin GSLutsep HLMoore WSMalas MB: Restenosis after carotid artery stenting and endarterectomy: a secondary analysis of CREST, a randomised controlled trial. Lancet Neurol 11:7557632012

53

Lau DZiewacz JESiddiqi HKPelly ASullivan SEEl-Sayed AM: Cigarette smoking: a risk factor for postoperative morbidity and 1-year mortality following craniotomy for tumor resection. Clinical article. J Neurosurg 116:120412142012

54

Lawson MFVelat GJFargen KMMocco JHoh BL: Interventional neurovascular disease: avoidance and management of complications and review of the current literature. J Neurosurg Sci 55:2332422011

55

Lee TCUeng SWChen HHLu KHuang HYLiliang PC: The effect of acute smoking on spinal fusion: an experimental study among rabbits. J Trauma 59:4024082005

56

Lensmar CElmberger GSköld MEklund A: Smoking alters the phenotype of macrophages in induced sputum. Respir Med 92:4154201998

57

Lindekleiv HSandvei MSNjølstad ILøchen MLRomundstad PRVatten L: Sex differences in risk factors for aneurysmal subarachnoid hemorrhage: a cohort study. Neurology 76:6376432011

58

Lindström DSadr Azodi OWladis ATønnesen HLinder SNåsell H: Effects of a perioperative smoking cessation intervention on postoperative complications: a randomized trial. Ann Surg 248:7397452008

59

Litvack ZNWest GADelashaw JBBurchiel KJAnderson VC: Dural augmentation: part I-evaluation of collagen matrix allografts for dural defect after craniotomy. Neurosurgery 65:8908972009

60

Lyons BFrizelle HKirby FCasey W: The effect of passive smoking on the incidence of airway complications in children undergoing general anaesthesia. Anaesthesia 51:3243261996

61

Martin GJ JrHaid RW JrMacMillan MRodts GE JrBerkman R: Anterior cervical discectomy with freeze-dried fibula allograft. Overview of 317 cases and literature review. Spine (Phila Pa 1976) 24:8528591999

62

Martínez-García EIrigoyen MGonzález-Moreno OCorrales LTeijeira ASalvo E: Repetitive nicotine exposure leads to a more malignant and metastasis-prone phenotype of SCLC: a molecular insight into the importance of quitting smoking during treatment. Toxicol Sci 116:4674762010

63

Mason DPSubramanian SNowicki ERGrab JDMurthy SCRice TW: Impact of smoking cessation before resection of lung cancer: a Society of Thoracic Surgeons General Thoracic Surgery Database study. Ann Thorac Surg 88:3623712009

64

Møller AMVillebro NPedersen TTønnesen H: Effect of preoperative smoking intervention on postoperative complications: a randomised clinical trial. Lancet 359:1141172002

65

Monfrecola GRiccio GSavarese CPosteraro GProcaccini EM: The acute effect of smoking on cutaneous microcirculation blood flow in habitual smokers and nonsmokers. Dermatology 197:1151181998

66

Morris KMShaw MDFoy PM: Smoking and subarachnoid haemorrhage: a case control study. Br J Neurosurg 6:4294321992

67

Myers KHajek PHinds CMcRobbie H: Stopping smoking shortly before surgery and postoperative complications: a systematic review and meta-analysis. Arch Intern Med 171:9839892011

68

Nåsell HAdami JSamnegård ETønnesen HPonzer S: Effect of smoking cessation intervention on results of acute fracture surgery: a randomized controlled trial. J Bone Joint Surg Am 92:133513422010

69

Nassiri NCleary DRUeeck BA: Is cranial reconstruction with a hard-tissue replacement patient-matched implant as safe as previously reported? A 3-year experience and review of the literature. J Oral Maxillofac Surg 67:3233272009

70

O'Rourke JMKalish LAMcDaniel SLyons B: The effects of exposure to environmental tobacco smoke on pulmonary function in children undergoing anesthesia for minor surgery. Paediatr Anaesth 16:5605672006

71

Pearce ACJones RM: Smoking and anesthesia: preoperative abstinence and perioperative morbidity. Anesthesiology 61:5765841984

72

Peolsson AVavruch LOberg B: Predictive factors for arm pain, neck pain, neck specific disability and health after anterior cervical decompression and fusion. Acta Neurochir (Wien) 148:1671732006

73

Pleis JRLucas JWWard BW: Summary Health Statistics for US Adults: National Health Interview Survey 2008 National Center for Health Statistics2009. (http://www.cdc.gov/nchs/data/series/sr_10/sr10_242.pdf) [Accessed May 14 2013]

74

Pobereskin LH: Influence of premorbid factors on survival following subarachnoid hemorrhage. J Neurosurg 95:5555592001

75

Qureshi AISung GYSuri MFStraw RNGuterman LRHopkins LN: Factors associated with aneurysm size in patients with subarachnoid hemorrhage: effect of smoking and aneurysm location. Neurosurgery 46:44502000

76

Qureshi AISuri MFYahia AMSuarez JIGuterman LRHopkins LN: Risk factors for subarachnoid hemorrhage. Neurosurgery 49:6076132001

77

Rahme RJBatjer HHBendok BR: Multiplicative impact of smoking and genetic predisposition on intracranial aneurysm formation. Neurosurgery 67:N15N162010

78

Rees TDLiverett DMGuy CL: The effect of cigarette smoking on skin-flap survival in the face lift patient. Plast Reconstr Surg 73:9119151984

79

Riefkohl RWolfe JACox EBMcCarty KS Jr: Association between cutaneous occlusive vascular disease, cigarette smoking, and skin slough after rhytidectomy. Plast Reconstr Surg 77:5925951986

80

Rigotti NAMcKool KMShiffman S: Predictors of smoking cessation after coronary artery bypass graft surgery. Results of a randomized trial with 5-year follow-up. Ann Intern Med 120:2872931994

81

Rockman CBCappadona CRiles TSLamparello PJGiangola GAdelman MA: Causes of the increased stroke rate after carotid endarterectomy in patients with previous strokes. Ann Vasc Surg 11:28341997

82

Saetta MTGTurato GBaraldo SZanin ABraccioni FMapp CE: Goblet cell hyperplasia and epithelial inflammation in peripheral airways of smokers with both symptoms of chronic bronchitis and chronic airflow limitation. Am J Respir Crit Care Med 161:101610212000

83

Sandén BFPFörsth PMichaëlsson K: Smokers show less improvement than nonsmokers two years after surgery for lumbar spinal stenosis: a study of 4555 patients from the Swedish spine register. Spine (Phila Pa 1976) 36:105910642011

84

Sarin CLAustin JCNickel WO: Effects of smoking on digital blood-flow velocity. JAMA 229:132713281974

85

Sasco AJSecretan MBStraif K: Tobacco smoking and cancer: a brief review of recent epidemiological evidence. Lung Cancer 45:Suppl 2S3S92004

86

Schroeder SA: Tobacco control in the wake of the 1998 master settlement agreement. N Engl J Med 350:2933012004

87

Schwab FJNazarian DGMahmud FMichelsen CB: Effects of spinal instrumentation on fusion of the lumbosacral spine. Spine (Phila Pa 1976) 20:202320281995

88

Shi YWarner DO: Pediatric surgery and parental smoking behavior. Anesthesiology 115:12172011

89

Singh JAHTHouston TKPonce BAMaddox GBishop MJRichman J: Smoking as a risk factor for short-term outcomes following primary total hip and total knee replacement in veterans. Arthritis Care Res (Hoboken) 63:136513742011

90

Sørensen LT: Wound healing and infection in surgery. The clinical impact of smoking and smoking cessation: a systematic review and meta-analysis. Arch Surg 147:3733832012

91

Sørensen LTJørgensen T: Short-term pre-operative smoking cessation intervention does not affect postoperative complications in colorectal surgery: a randomized clinical trial. Colorectal Dis 5:3473522003

92

Swartz KRTrost GR: Recurrent lumbar disc herniation. Neurosurg Focus 15:3E102003

93

Theadom ACropley M: Effects of preoperative smoking cessation on the incidence and risk of intraoperative and postoperative complications in adult smokers: a systematic review. Tob Control 15:3523582006

94

Thomsen TVillebro NMøller AM: Interventions for preoperative smoking cessation. Cochrane Database Syst Rev 7CD0022942010

95

Tur EYosipovitch GOren-Vulfs S: Chronic and acute effects of cigarette smoking on skin blood flow. Angiology 43:3283351992

96

Turan AMascha EJRoberman DTurner PLYou JKurz A: Smoking and perioperative outcomes. Anesthesiology 114:8378462011

97

Underwood MJBailey JS: Coronary bypass surgery should not be offered to smokers. BMJ 306:104710481993

98

Wang WHWang DX: Role of sympathetic nerve and adrenal gland in the potentiation of hypoxic pulmonary vasoconstriction during cigarette smoking. J Tongji Med Univ 12:151992

99

Warner DO: Helping surgical patients quit smoking: why, when, and how. Anesth Analg 101:4814872005

100

Warner DO: Perioperative abstinence from cigarettes: physiologic and clinical consequences. Anesthesiology 104:3563672006

101

Warner DO: Preoperative smoking cessation: the role of the primary care provider. Mayo Clin Proc 80:2522582005

102

Warner DO: Tobacco dependence in surgical patients. Curr Opin Anaesthesiol 20:2792832007

103

Warner DOKlesges RCDale LCOfford KPSchroeder DRVickers KS: Telephone quitlines to help surgical patients quit smoking patient and provider attitudes. Am J Prev Med 35:6 SupplS486S4932008

104

Warner DOSarr MGOfford KPDale LC: Anesthesiologists, general surgeons, and tobacco interventions in the perioperative period. Anesth Analg 99:176617732004

105

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