Post-traumatic stress disorder (PTSD) is a severe anxiety disorder.1 This syndrome has been described to occur after exposure to any event, resulting in psychological trauma. This event may encompass the threat of death or the loss of physical, sexual, or psychological integrity. By definition, the symptoms of PTSD last more than 1 month and produce significant deficiency in social, occupational, or other important fields of performance. The early detection of PTSD is critical because its occurrence is correlated to a reduced quality of life.2 PTSD and mood disorders have been found to frequently occur together. Mood disorders can include major depression, bipolar disorder, and seasonal affective disorder. They are common in the population and much more common among certain groups of patients, such as those with PTSD. We sought to assess postoperative burden by a dimension that can help the clinicians to document the disease. PTSD has been described in a wide number of circumstances, including physical assault, procedural pain, or intensive care management.3–5 PTSD is a debilitating psychological condition triggered by a major traumatic event, such as rape, war, a terrorist act, death of a loved one, a natural disaster, or a catastrophic accident. It is marked by upsetting memories or thoughts of the ordeal, blunting of emotions, increased arousal, and sometimes severe personality changes.
PTSD symptoms include hyperalertness, fear and anxiety, nightmares and flashbacks, sight, sound, and smell recollection, avoidance of recall situations, anger and irritability, guilt, depression, increased substance abuse, negative world view, and decreased sexual activity.
Symptoms usually begin within 3 months of the trauma. For a diagnosis of PTSD, symptoms must include: intrusive symptoms (flashbacks, sleep disorders: nightmares or night terrors, intense distress when exposed to events that are associated with the trauma) and at least three of the following avoidance symptoms that affect interactions with others (trying to avoid thinking or feeling about the trauma, inability to remember the event, inability to experience emotion, as well as a loss of interest in former pleasures—psychic numbing or blunting—and a sense of a shortened future), and evidence of increased arousal, including at least two of the following (problems falling asleep, startle reactions: hyperalertness and strong reactions to unexpected noises, memory problems, concentration problems, moodiness, or violence). The use of the validated impact of event scale revised (IES-R) has also the major strength of exploring these three domains distinctly.
After hospital stay, symptoms of PTSD are found in 27% of survivors of intensive care unit (ICU) stay,3 16% of survivors of myocardial infarction,4 and 11% of survivors of cardiac surgery.5 Predictors of development of symptoms of PTSD include female sex, young age, memories of events, and use of benzodiazepines in ICU patients,6,7 whereas only cognitive impairments are identified in cardiac surgery patients.8
The specific role of cancer diagnosis should be considered. After gynecological surgery, the diagnosis of cancer and the stage of the disease increase the prevalence of PTSD-related symptoms.9 Lung cancer is the most frequent cancer in male patients.10 The literature about quality of life in lung cancer survivors is abundant. About half of the patients with advanced cancer encounter criteria for a psychiatric disorder.11 The initial patient-rated quality of life affects the subsequent survival. For instance, being married seems to be a strong factor to an improved survival.12,13
To the best of our knowledge, there are no data available on the prevalence of PTSD-related symptoms in patients undergoing lung surgery for cancer. Our hypothesis was that the prevalence of PTSD-related symptoms should be high in this population. We sought to determine prevalence and risk factors for PTSD-related symptoms after lung cancer resection.
PATIENTS AND METHODS
This is a single-center observational study carried out in a thoracic surgery department of a university hospital of 923 beds. From January 3, 2011 to June 30, 2011, all patients over the age of 17 years, with a telephone, receiving social security, and scheduled to undergo surgical resection for suspected lung cancer were eligible for inclusion. Those excluded from the study were patients with progressive neurological disease with known cognitive impairment (Alzheimer’s, Parkinson’s, multiple sclerosis), patients scheduled for pneumonectomy, patients who refused to consent to their participation, patients with decompensated somatic or psychiatric illness recently, patients who died before follow-up of 3 months, patients who could not read or speak French properly, and those with criteria of inoperability intraoperatively. The study was approved by the Ethics Committee of the French Society for Thoracic Surgery and Cardiovascular Surgery (reference: CERC-SFCTV-2010-12-11-17-12-23-LeMa) and written informed consent was obtained from participating patients.
Course of Patients
The patients were included by the thoracic surgery anesthesiologist team during the preoperative consultation. This consultation was scheduled after the surgical consultation for a pulmonary resection for suspected cancer. After inclusion, the typical course of a patient consists of a preanesthetic visit the day before the surgical intervention. Then, the patient undergoes the surgical resection. Next, the patient is first monitored for a short duration in the recovery room and then is transferred to the surgical ward before being discharged home or to a rehabilitation center. Of note, the surgical unit has a full-time clinical psychologist who can meet patients on their requests.
The surgery is indicated in accordance with existing guidelines for pulmonary resection.14 With regard to surgical techniques, open thoracotomy and videothoracoscopy were used as required. In those patients in whom the cancer diagnosis was not achieved preoperatively, the nature of the tumor was confirmed either by frozen section and/or conventional pathologic analysis of the resection specimen. In the last case, the diagnosis of cancer was confirmed to the patients at the first outpatient clinical consultation, usually 1 month after the operation. In any case, the patient was informed at the first meeting with the surgeon of the high probability of cancer. All the surgical procedures consisted of anatomical lung resection (segmentectomy, lobectomy) or wedge resection combined with mediastinal lymphadenectomy. These procedures were performed under general anesthesia after premedication with hydroxyzine 1 mg/kg.
When discharged from the recovery room, patients were managed in the thoracic surgery ward unless there were complications that required their admission to the polyvalent ICU. Postoperative pain control differed depending on the type of surgical procedure. With regard to videothoracoscopy, a morphine pump with patient control was used. With regard to open thoracotomy, an epidural catheter was placed before induction. Epidural analgesia was delivered for 5 days after surgery using local anesthetics. In case of failure of epidural placement, a paravertebral block was placed after surgery. The paravertebral block analgesia was based on a continuous infusion of local anesthetics associated with the use of intravenous morphine delivered by a pump. The choice of analgesic technique was made by an agreement between the anesthesiologist, surgeon, and patient preference. All patients had an active program of physiotherapy, including deep-breathing exercises and incentive spirometry in the postoperative period.
Demographic and Clinical Characteristics
We collected age, sex, marital status, education level, and occupation. From the medical records were identified: body mass index, American Society of Anesthesiology class, New York Heart Association functional class, medical history (coronary diseases, arrhythmias, diabetes, chronic renal failure, chronic obstructive pulmonary disease, preoperative use of noninvasive ventilation, alcohol consumption, smoking, psychiatric history, which was considered positive if patients had already have a follow-up), oncologic status (history of cancer, cancer surgery, radio, and/or chemotherapy), ongoing treatment (β-blocker, antidepressants, benzodiazepines). Then, we collected the prospective data related to: the surgical procedure (incision, side, extent of pulmonary resection, length of stay), the underlying disease (malignancy, primary, secondary, nonmalignant disease), the anesthesia (maximal visual analogic score (VAS) within the first 48 hours after surgery, type of analgesia), and the postoperative complications (pneumonia, clots, leaks, reoperation, renal failure, need for chemotherapy or radiotherapy). Postoperative treatments such as β-blockers, antidepressants, and use of psychotropic drugs (sedatives, hypnotics) were identified.
The Psychological Well-Being Index (PGWBI) was used preoperatively and at 3 months. This general instrument measures the quality of life. This self-administered questionnaire was initially validated in healthy subjects to assess the psychological well-being. It includes 22 questions divided into six distinct dimensions of quality of life: anxiety, depressed mood, well-being, self-control, overall health, and vitality. This tool has an excellent internal consistency, reliability, and validity in several diseases. Preoperative assessment of PGWBI predicts the postoperative quality of life for patients with non–small-cell lung cancer managed with thoracic surgery.13
The Hospital Anxiety and Depression Scale (HADS) was used preoperatively and at 3 months. This self-administered questionnaire consists of two subscales of seven items each, one for anxiety and one for depression, which can be traded independently of one another. Each question is scored from 0 to 3 points, making a maximum of 21 points for each subscale. The HADS takes only 2 to 5 minutes to complete. An analysis of scores on both subscales showed that the scores of 0 to 7 are normal whereas anxiety scores greater than or equal to 8 indicate the possibility of anxiety or depressive disorders. Subscales anxiety and depression were found to be independent of each other. The HADS is considered as a reliable screening tool to detect states of depression and anxiety in outpatients.15–17 The elements of the HADS are relevant in terms of either generalized anxiety or depression, it excludes symptoms that may occur from physical illness, such as insomnia, fatigue, or anergy. The HADS has been translated into and validated in French language. It is an acceptable, reliable, valid, and easy tool to use, convenient for identifying and quantifying depression and anxiety.15–17
The IES-R includes 22 items measuring symptoms of intrusion, avoidance, and hyperarousal symptoms of post-traumatic stress. Each item is rated from 0 to 4. This is a benchmark in the international literature to assess the subjective distress caused by traumatic events. The French version has been validated. We used it preoperatively to control pre-existing PTSD-related symptoms before the announcement of a cancerous disease or other pre-existing traumatic events. The IES-R is a self-assessment questionnaire. It can be completed easily by a telephone interview. Respondents are asked to identify a stressful life event and a specific one (the thoracic surgery–related event) and to indicate how often they experienced each of the 22 items in 7 days (0, not at all; 1, rarely; 3, sometimes; 4 often). Thus, the score ranges from 0 to 88. In general, the IES-R is not used to diagnose PTSD, but the cutoff scores for a preliminary diagnosis of PTSD-related symptoms have been reported in the literature. Although there is no threshold for the IES-R, after review of the literature, we chose a cutoff at 22 as the best value to be more specific in detecting patients at risk of developing PTSD-related symptoms. The IES-R was translated into French language.18–20
VAS score was used for pain assessment after surgery. A VAS is a measurement tool attempting to measure a characteristic or attitude that is believed to range across a continuum of values and cannot easily be directly measured. The goal of analgesia was to obtain a VAS score max less than 40. For the purpose of our study, we collected the mean and maximal VAS scores during the first 24 hours after surgery.
The three questionnaires assessing preoperative symptoms of post-traumatic stress, anxiety, and depression, and quality of life were distributed at the time of the anesthesia consultation. Patients had the option to complete the questionnaires at home and then bring them back to the hospital or complete it directly before or after the anesthesia consultation, with the help of a physician or nurse. After discharge from the thoracic ward, patients completed the questionnaires again for the symptoms of PTSD. Three months later, the patients were contacted again by mail and the questionnaires had to be returned with a prestamped envelope.
Statistics were performed using SPSS version 17.0. Quantitative data are expressed as mean ± standard deviation or median (lower and upper quartiles). Percentages were calculated for qualitative data. The comparisons of medians were performed using the Mann–Whitney U test. The comparisons of means were performed using the two-sample t-test. Comparisons of proportions were performed with a Fisher’s exact test.
After univariate analysis, the variables with significance less than 0.1 were included in the logistic regression model, also taking into account their clinical relevance. The covariates highly correlating with each other were not included in the same multivariate model together. The final level of significance was 0.05.
Homer-Lemeshow test is used to test the goodness-of-fit of the logistic regression model.21 The χ2 test was applied by separating the population into homogeneous risk groups. A p value greater than 0.1 indicated a good calibration. The area under the receiver operating characteristic is presented for the multivariate logistic regression model.22
A total of 68 patients were enrolled in this study. Seventeen patients were lost to follow-up, and investigators were unable to collect all the data in another four patients. These 21 subjects were excluded from final analysis. As a result, 47 patients were included in the cohort (Table 1). Participants consisted of 26 male patients and 21 female patients with a mean age of 59 years (±13). They stayed an average of 9 days (±4) in the hospital. Open thoracotomy and minimally invasive resection (using videothoracoscopy) were used in 32 cases (68%) and 15 (32%) cases, respectively. Two patients spent 1 day in the ICU for unexpected complications. The diagnosis of lung cancer was confirmed in 41 patients. In six patients, the diagnosis was changed after pathological examination.
At the 3-month follow-up assessment, an IES-R score higher than 22 was found in 24 participants (51%) (Group A).18–20 In Group A, the mean score was 41 (±18), as compared with 9 (±8) in those with an IES-R score of 22 or lesser (Group B) (p < 0.001) (Table 1). With regard to social, demographic, and surgical characteristics, Group A did not significantly differ from those with Group B. Comorbidity, preoperative chemotherapy, preoperative radiotherapy, preoperative uses of β-adrenergic antagonist, benzodiazepines, and antidepressant drugs were not associated with the IES-R score (Table 1). At the 3-month follow-up assessment, anxiety-related symptoms (HADSanxiety score > 7) and depression-related symptoms (HADSdepression score > 7) were found in 15 (32%) and 12 (26%) patients, respectively (Table 2).16,17
In contrast, the factors related to the patient’s personality, preoperative quality of life and postoperative pain were associated with an IES-R score higher than 22 at the 3-month follow-up assessment (Table 2).18–20 Preoperative anxiety–related symptoms and depression-related symptoms were associated with an IES-R score higher than 22 at the 3-month follow-up assessment. The preoperative anxiety–related symptoms component of the HADS score were above eight of 15 participants (62%) of Group A and six participants (26%) of Group B, respectively (p = 0.03) (Table 2).16,17 The preoperative depression–related symptoms component of the HADS score was above 8 in seven patients (29%) of Group A, as compared with one patient (4.3%) of Group B (p = 0.05). The preoperative PGWBI scores were of 68 (±19) in the patients of Group A and 81 (±16) in those of Group B (p = 0.02). This reflected a reduced preoperative quality of life in the patients of Group A.
During the first 24 hours after surgery, a VASmax score higher than 40 was found in 18 patients of Group A, as compared with 10 patients of Group B (p = 0.05). The mean VAS scores over the 24 postoperative hours were 35 (±10) and 24 (±20) in the patients of Group A and those of Group B at the 3-month follow-up assessment (p = 0.004) (Table 3). The use of specific drugs or procedures did not differ between the patients according to their IES-R score. Among the patients with VAS higher than 40, 13 (46%), nine (32%), and seven (25%) received epidural analgesia, paravertebral block, or parenteral analgesics only (p = 0.6). The occurrence of postoperative complications did not affect the IES-R score.
Time between the first surgical consultation and the surgical procedure was similar in the two groups (32 days [±26 [Group A] and 26 days [±12] [Group B]; p = 0.93). No significant correlation was found between this time and the occurrence of PTSD (r = −0.11, p = 0.47). Metastatic cancer was diagnosed in 11 patients (46%) in Group A and 10 (43%) in Group B (p = 0.9).
Through a hierarchical linear regression we examined entering factors that were identified by the univariate analysis. Because of the size of our cohort, only selected factors were entered into the model: preoperative anxiety–related symptoms (HADSanxiety score > 7; p = 0.02), preoperative depression–related symptoms (HADSdepression > 7; p = 0.06), preoperative quality of life (PGWBI, global score; p = 0.06), and VASmax during the first 24 hours after surgery higher than 40 (p = 0.002).16,17 An IES-R score higher than 22 was predicted by preoperative HADSanxiety score higher than 8 and a VASmax higher than 40 during the first 24 hours. Patients with a preoperatorive HADSanxiety score higher than 7 and a maximal VAS score higher than 40 during the first 24 hours after surgery were more likely to develop PTSD-related symptoms at 3 months with odd ratios at 4.61 [1.20–17.73] (p = 0.03) and 1.34 [1.05–1.75] (p = 0.02), respectively (Table 4).18–20 The discrimination of these two variables was satisfactory with an area under the receiver operating characteristic curve estimated at 0.8 (95% confidence interval [0.7–0.9], p < 0.001) (Fig. 1). The calibration was adequate. The difference was not significant between the rates of the predicted cases and observed cases (p = 0.65 using Hosmer–Lemeshow test). The exclusion of patients with nonmalignant lesions did not change the significance of these results (Table 4).
Finally, the postoperative VAS scores were 40 [2–50] in the patients with preoperative anxiety–related symptoms (HADSanxiety score > 7), as compared with 45 [15–65] in those without preoperative anxiety–related symptoms (HADSanxiety score ≤ 7) (p = 0.46).16,17
In our cohort, 3 months after lung cancer resection, the prevalence of PTSD-related symptoms was 51%. Preoperative anxiety–related symptoms and postoperative pain seem to trigger the development of PTSD-related symptoms at the 3-month follow-up assessment. Hence, to prevent the development of PTSD-related symptoms, one may hypothesize the need for an aggressive pain management and an early identification of anxiety-related symptoms. The prevalence of PTSD-related symptoms was evaluated using the IES-R score with a cutoff at 22.18–20,23 The high prevalence that we found can be explained by the nature of the underlying disease of our patients. Lung cancer can serve as model of aggression at the intersection between three causes of stress symptoms.
The stress symptoms can be because of the lung resection itself. This surgical procedure is associated with a high lethal related risk observed in elective surgery. Previous studies showed that PTSD-related symptoms were found in 32%, 25%, and 15% of patients undergoing abdominal aortic repair or coronary artery bypass, secondary peritonitis, and native valve replacement, respectively.24–26 In patients undergoing coronary artery bypass grafting procedures, depression and PTSD were associated with an increase of risk of death by a magnitude comparable with well-established physical health risk factors after coronary artery bypass grafting surgery.27 Thus, the surgical procedure itself may generate the reported stress symptoms.
The stress symptoms can be related to impaired functional outcomes after the lung surgery. Lung cancer resection is associated with a worsening of short-form-36 subscales for physical functioning, role-physical, bodily pain, and mental health, as compared with the preoperative values.28 In breast cancer, a reduced physical functioning at 3 months was identified as an independent risk factor for PTSD-related symptoms.29 We used the PGWBI score to assess the quality of life. The high PTSD-related scores in the patients suggests that they developed feelings of anxiety, depressed mood, distress, loss of self-control, and lack of vitality.13 Our study did not explore the long-term effect of PTSD on outcomes. In trauma patients, a previous study showed that the median time to remission was around 25 months, and in more than one third of cases PTSD persisted for more than 60 months.30 Hence, the reported stress symptoms can be because of impaired functional outcomes.
The diagnosis of cancer itself may be associated with the development of PTSD-related symptoms. In female patients undergoing gynecological surgery, a diagnosis of cancer was associated with a 34% prevalence of PTSD-related symptoms, whereas that of a nonmalignant disease was associated with a 15% prevalence.31 Similarly, the prevalence of PTSD-related symptoms increased in male patients undergoing radical prostatectomy if the diagnosis was prostate cancer.32 Thus, lung cancer resection seems to generate stress because of various factors that act synergistically between themselves.
A VAS score higher than 40 after surgery was an independent factor of PTSD-related symptoms. We did not identify an independent relation between PTSD-related symptoms and drugs used to relieve pain. Elsewhere, the use of morphine was associated with a reduced development of PTSD symptoms.33,34 Ketamine has also been identified as protective in burned patients.35 All our patients had a dedicated protocol for pain relief using a multimodal approach. Of note, patient-controlled analgesia or epidural analgesia had no specific effect on the development of PTSD-related symptoms. This underlines the fact that the critical point is the global management of pain rather than a specific procedure. This finding is in line with the concept of “sensitivity to pain traumatization,” which is strongly correlated with the development of PTSD-related symptoms.36 However, the use of analgesics by itself may affect the long-term outcomes of the patients.37
The preoperative screening of patients with anxiety symptoms can serve to identify those at high risk of developing PTSD-related symptoms after lung cancer resection. The hallmark of PTSD-related symptoms is the persistence of severe, disabling anxiety after a life-threatening event. In cancer, the operation passes but the threat does not resolve. Thus, as shown by our results, anxiety remains a persistent cause and the threat of annihilation is not lifted until much later, if at all.38 This finding has already been reported after various procedures.39,40 We confirmed here the negative impact of anxiety on the quality of life after lung surgery, which was suggested in a previous study.
Anxiety-related symptoms should be screened with attention. They are correlated to the rate of readmission after coronary artery bypass graft.41 As previous studies showed a protective role for β-adrenergic antagonist in women or preoperative use of a stress dose of hydrocortisone,42,43 one can expect future studies to test an antianxiety drug in patients undergoing lung cancer surgery. Elsewhere, PTSD-related symptoms were successfully reduced by the use of serotonin inhibitor medication.44,45 Similarly, early psychological interventions can reduce acute stress symptoms.46 Then, the screening of these patients can result in an effective management, improving their outcomes. Of note, we clearly show that pain and anxiety are not related because the two variables are independently identified in our multivariate analysis. In addition, no difference in pain intensity was found between the anxious and nonanxious participants.
Our study has several limitations that deserve to be discussed. The number of patients is relatively small. In addition, it is a single-center study. However, the size of our cohort is in agreement with that of previous studies on this topic.39,47–49 Because ICU admission is an independent cause of PTSD,35 we excluded from our analysis the patients undergoing pneumonectomy. Indeed, in our institution, these patients were admitted to ICU after surgery. However, to avoid secondary exclusion, two patients admitted to the ICU for unexpected complications were included in the analysis. One can suggest that considering only anatomical resections may be misleading by creating a bias excluding more compromised patients. Another potential bias was the stage of the disease process. First, the baseline of the patient was obtained the day before surgery. Then, we assessed our patients 3 months after the surgical procedure. For several patients, the disease was probably diagnosed several weeks before this event. This may not be the best baseline given the nature of the disease. Thus, the course of the disease was actually longer than our 3-month measure. The trigger of the PTSD-related symptoms may be independent of the surgical procedure. This can perhaps explain the high prevalence of PTSD-related symptoms that is reported in the present study. However, we did not find a correlation between the first surgical consultation and the surgical procedure. This indirectly suggests that this factor is not critical. The least bias was the interview (IES-R), which assesses symptoms of PTSD but not confirmed diagnosis. On the basis of current literature, the structured interview remains the definitive standard in the diagnosis of PTSD.50,51 Some studies have used the IES-R as a screening tool, but the cutoff changes by study and has not been validated, and an IES-R score does not make a diagnosis of PTSD. Our study looks at patients having symptoms associated with PTSD, using a cutoff in the IES-R found in other studies but not validated. As such, these symptoms are also associated with other non-PTSD diagnoses.
In conclusion, our study shows that PTSD-related symptoms are frequent after lung cancer resection. This is the first study to highlight a clear relation between postoperative pain and the development of PTSD-related symptoms in lung cancer patients. In addition, preoperative anxiety–related symptoms should be carefully screened for detecting the patients at risk of PTSD-related symptoms. These are preliminary findings, and need replications with larger sample size. Also, future studies should focus on interventions aimed at altering these factors and measure the use of postoperative morphine, which has not been possible here. Our future studies should also focus on structured interviews with paired blind experts to identify patients with confirmed diagnoses of PTSD, and then conduct the analysis on that cohort.
The work is attributed to the department of anesthesiology and critical care medicine, Nord Hospital, Assistance Publique-Hôpitaux de Marseille, Marseille, France.
The work was funded by the Department of Anesthesiology and Critical Care medicine, Nord Hospital, Marseille, France.
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Post-traumatic stress disorder; Thoracic surgery; Lung resection; Postoperative pain
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