Pulmonary influences on early post-operative recovery in patients after cytoreductive surgery and hyperthermic intraperitoneal chemotherapy treatment: a retrospective study
© Arakelian et al.; licensee BioMed Central Ltd. 2012
Received: 17 July 2012
Accepted: 31 October 2012
Published: 27 November 2012
The combination of cytoreductive surgery (CRS) and hyperthermic intraperitoneal chemotherapy (HIPEC) is a curative treatment option for peritoneal carcinomatosis (PC). There have been few studies on the pulmonary adverse events (AEs) affecting patient recovery after this treatment, thus this study investigated these factors.
Between January 2005 and December 2006, clinical data on all pulmonary AEs and the recovery progress were reviewed for 76 patients with after CRS and HIPEC. Patients with pulmonary interventions (thoracocenthesis and chest tubes) were compared with the non-intervention patients. Two senior radiologists, blinded to the post-operative clinical course, separately graded the occurrence of pulmonary AEs.
Of the 76 patients, 6 had needed thoracocentesis and another 6 needed chest tubes. There were no differences in post-operative recovery between the intervention and non-intervention groups. The total number of days on mechanical ventilation, the length of stay in the intensive care unit, total length of hospital stay, tumor burden, and an American Society of Anesthesiologists (ASA) grade of greater than 2 were correlated with the occurrence of atelectasis and pleural effusion. Extensive atelectasis (grade 3 or higher) was seen in six patients, major pleural effusion (grade 3) in seven patients, and signs of heart failure (grade 1–2) in nine patients.
Clinical and radiological post-operative pulmonary AEs are common after CRS and HIPEC. However, most of the pulmonary AEs did not affect post-operative recovery.
KeywordsPeritoneal carcinomatosis CRS HIPEC Post-operative recovery Pulmonary influences Radiological assessment
Acute Respiratory Distress Syndrome
American Society of Anaesthesiologists
Body Mass Index
Completeness of cytoreduction
Congestive heart failure
Continuous positive airway pressure
Hyperthermic intraperitoneal chemotherapy
Intensive care unit
Peritoneal Cancer Index.
Peritoneal carcinomatosis (PC) can arise from various tissues, including the appendix, colorectal, abdominal mesothelioma and the ovaries. It is considered a terminal disease, and patients with this diagnosis usually have a poor prognosis despite treatment with systemic chemotherapy . Cytoreductive surgery (CRS) combined with hyperthermic intraperitoneal chemotherapy (HIPEC) is a relatively recent treatment, and can be curative in selected patients with PC [1, 2]. However, this treatment combination is a complex and time-consuming procedure. During CRS, tumor cells on the surface of intra-abdominal organs and the peritoneum are carbonized and destroyed with high voltage electrosurgical diathermy, which produces heat [3, 4]. This results in a large intra-abdominal burn area, and may cause fluid loss. Furthermore, to avoid a critical rise in body temperature during HIPEC, systemic hypothermia is usually required before HIPEC [1, 5–7]. CRS and HIPEC may result in hemodynamic changes as a result of moderate blood loss, peripheral vasodilatation, and massive fluid shift [5, 7–9]. Thus, the patient’s general condition and their respiratory, cardiovascular, metabolic status, and electrolytic balance are significantly affected [8, 9]. Large abdominal incisions, in addition to a long surgery and the particular operating technique used  may lead to a fluid deficit. Therefore, to maintain adequate circulating volume and urine output, large amounts of intravenous fluids are given during surgery [9–11].
As was reported previously, the initial post-operative care is recommended to take place in the intensive care unit (ICU) because of the hemodynamic and respiratory challenges for the patient after surgery, and the total hospital stay lasts about 3 weeks . The post-operative recovery process may be influenced by several factors before, during and after the operation, and one of these factors is the incidence of pulmonary adverse events (AEs) . However, there are few reports in the literature on pulmonary AEs occurring after CRS and HIPEC. Acute respiratory distress syndrome (ARDS)was reported in two case studies after CRS and HIPEC, with systemic inflammatory response or multiple transfusions during major surgery suggested as possible etiologies [10, 14].
The primary aim of this study was to investigate the factors related to pulmonary AEs. In addition, we aimed to describe the effect of pulmonary AEs on the post-operative recovery process after CRS and HIPEC, and to compare patients who received an intervention with those who did not.
The study was approved by the regional ethics committee, and was performed in accordance with the Declaration of Helsinki . Informed consent was obtained from each patient.
Between January 2005 and December 2006, 76 patients with PC (42 women) with a mean age of 54 years (range 24–75 years) and mean BMI of 25 (range 17–33) underwent primary CRS and HIPEC at Uppsala University Hospital, Uppsala, Sweden.
Patient characteristics a
Chronic obstructive lung disease
Cardiovascular diseases or diabetes
ASA: classification grade n
Malignant abdominal mesothelioma
ICU stay, hours
Missing data, n
Total hospital stay, days
Data were collected on admission, progress, and discharge, operating room, ICU and post-operative ward stay, previous medical history, primary diagnosis, surgical procedures performed, tumor burden (Peritoneal Cancer Index; PCI), chemotherapy received before and after the operation, stoma formation, duration of surgery, ASA grade, peri-operative blood loss and fluid therapy, total time on mechanical ventilation, need for treatment with continuous positive airway pressure (CPAP), post-operative recovery progress, duration of stay in the ICU, and total hospital stay. All pulmonary AEs of grades II to V were documented in accordance with the Common Terminology Criteria (version 3.0) of the National Cancer Institute . In addition, all available radiological images of the lungs taken during the first post-operative week were reviewed separately by two senior radiologists, who were blinded to all clinical data. The radiological imaging was performed when indicated by the clinical symptoms. Only two of the patients had any history of lung disease prior to surgery, and these had asthma and chronic obstructive pulmonary disease respectively.
All 74 patients had a thoracic epidural catheter inserted between the Th8 and Th10 level before induction of anesthesia. For medical reasons, two of the patients had patient-controlled analgesia instead of epidural anesthesia (EDA). Patients were given EDA (bupivacain and sufentanil) before surgery began, and this was continued up to 8 days postoperatively. Anesthesia was induced by fentanyl and sodium thiopental, and after administration of rocuronium and fentanyl, the trachea was intubated and mechanical ventilation started. Anasthesia was maintained with isoflurane and intermittent doses of fentanyl.
Peri-operative and post-operative fluid therapy a,b
Duration of surgery, hr: m
9:51 (3:20 to 16:40)
3,350 (150 to 11,000)
2,384 (50 to 14,000)
Total mechanical ventilation time, hr:m:s
00:22:52 (00:06:50 to 02:04:15)
Length of CPAP use, days
4.1 (1.0 to 10.0)
Fluids during surgery, ml
12,220(5,000 to 23,100)
4,791 (550 to 21,150)
Sum of crystalloid and colloids
17,012 (5,900 to 35,150)
Intraoperative blood transfusion
1,130 (300 to 3,300)
Fresh frozen plasma
1,877300 to 8,400)
Total crystalloid balance, ml
On the day of surgery
10,502 (1,455 to 20,820)
Post-op day 1
−77 (−3,982 to 4,498)
Post-op day 2
−937 (−4,450 to 2,615)
Post-op day 5
−405 (−3,800 to 3,277)
From day of surgery until post-op day 5
7,292 (−4,790 to 22, 507)
Pre-op and post-op weight differences, kg
73.1 (45.3 to 110.0)
Post-op day 1
Post-op day 5
Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy
CRS was performed as described by Sugarbaker, and HIPEC was given by means of the Coliseum technique [6, 17]. The selection of drugs for HIPEC was based on previous studies  patients with PMP received mitomycin C and patients with colorectal cancer received oxaliplatin, while patients with ovarian cancer, gastric cancer, or mesothelioma were treated with a combination of cisplatinand doxorubicin. The duration of perfusion with oxaliplatin was 30 minutes, and for all other drugs it was 90 minutes. Tumor load and completeness of cytoreduction (CC) for peritoneal carcinomatosis were recorded using the PCI and the CC score directly after surgery, as described previously [1, 17]. Of the 76 patients, 20 patients received pre-operative chemotherapy, and the mean PCIfor the patients was 23 (range 3–39, PCIwas missing for 13 patients). Diaphragm stripping was performed in 52 patients, and a stoma was created for 44 patients.
Classifications of the operating site
The operating site
Upper abdomen (n = 58)
1 to 3
Right upper quadrant, epigastrium, and left upper quadrant
Middle abdomen (n = 75)
0, 4, 8 to 12
Right flank, central, left flank, and small bowel
Lower abdomen (n = 68)
5 to 7
Right lower quadrant, pelvis, and left lower quadrant
Post-operative recovery of patients in this study was defined as mobilization  (patients standing up, sitting down on a chair, washing themselves, and walking for the first time after surgery), and drinking, eating, and having bowel movements or flatulence . Patients were mobilized in accordance with a specially designed mobilization schedule after surgery .
Radiological assessment of the thoracic organs and grading of pulmonary adverse events
Gradation of pulmonary adverse events made for the purpose of this study a
More extensive than one lobe
Minimal amounts defined as blunted pleural sinus
Moderate amounts defined as extension to two pleural sinuses but not reaching the level of lung hilum
Large amounts up to and > the level of lung hilum
Signs indicative of heart failure
No signs of heart failure
Enlargement of pulmonary vessels in the absence of other congestive signs (pulmonary effusion and/or cardiac enlargement) was interpreted as suggestive of congestion
Congestive heart failure was diagnosed when dilatation or congestion of pulmonary vessels were present, combined with pleural effusion and/or cardiac enlargement
The intervention group
With respect to progress in their recovery process, patients who had an invasive intervention as a result of their pulmonary AE(s) were compared with those who received no intervention. Invasive intervention (thoracocentesis and chest tubes) was performed if there was presence of respiratory distress, including dyspnea, tachypnea, or poor saturation.
Inter-rater analysis between the two radiologists’ gradations of atelectasis, pleural effusion, and heart failure was performed using Cohen’s κ-value. To test the probability of association between the effects of pulmonary AE on recovery variables, the Mann–Whitney U-test or Kruskal–Wallis test was performed. To test the probability of association between clinical data on post-operative recovery variables, univariate analysis of each clinical and post-operative recovery variables was tested using the χ 2 or Fishers’ exact test for categorical data, and the Mann–Whitney U-test or Kruskal–Wallis test for continuous data. A general linear model in a multivariate analysis was used for correlation analysis between post-operative recovery variables and pulmonary AEs with a 95% confidence interval (CI). Correlation analysis between different variables was tested using Spearman’s rank correlation. P < 0.05 was considered significant.
Pulmonary adverse events occurring in 62 patients (60 radiographs and 2 computed tomography scans) during post-surgery week 1, and comparison between gradations performed by radiologist 1 and 2
Cohen’s weighted κ value
None (grade 0)
Lamellar atelectasis (grade 1)
Segmental atelectasis (grade 2)
Lobar and larger than lobar (≥ grade 3)
Pleural effusion (n)
None (grade 0)
Minimal (grade 1)
Moderate (grade 2)
Large (grade 3)
Signs suggestive of CHF (grade 1)
CHF (grade 2a)
The presence of atelectasis, pleural effusion, and heart failure showed no correlation with gender, age (<65 vs. ≥65 years), BMI, different types of primary tumor, duration of surgery, stoma formation, pre-operative chemotherapy, presence of AEs (surgical, infectious, or medical); type of surgical procedure (upper, middle, or lower abdominal) or presence of diaphragm stripping. Pulmonary AEs were not correlated with mobilization (as defined in the Methods section).
Factors influencing the occurrence of atelectasis and pleural effusion
Effect of pulmonary adverse events (AEs) on recovery time and parameters of62 patients
MV time, days
0 to 1
1.2 to 3.1
2 to 3
2.4 to 4.2
ICU stay, days
0 to 1
1.4 to 2.5
2 to 3
0.9 to 1.3
Total hospital stay, days
0 to 1
18.0 to 24.2
2 to 3
20.3 to 25.3
ICU stay, days
0.9 to 1.2
1.3 to 2.6
13 to 24
1 to 2
23 to 36
In a multivariate analysis, pleural effusion correlated with PCI and ASA classification grade. Patients with pleural effusion of grades 1 to 2had higher PCI (>24) than those who had no pleural effusion, and there was a correlation between ASA classification grade and pleural effusion. The duration of stay in the ICU also correlated with pleural effusion, and a post hoc test showed that patients with a moderate amount of pleural effusion (grade 2) had a mean stay of approximately 23 hourslongerin the ICU than the patients with no effusion.
The occurrence of heart failure in nine patients correlated with oral intake (r 0.33, P 0.02), bowel movement (r 0.26, P 0.03), length of ICU stay (r 0.38, P 0.03) and length of total hospital stay (r 0.30, P 0.02).
Early post-operative recovery and volume of peri-operative fluids
Patients received a mean of approximately 17 liters of combined crystalloids and colloids during surgery, which resulted in a positive fluid balance on the day of surgery. No correlations were found between the peri-operative fluid therapy used (crystalloids, colloids, and the sum of both) and the occurrence of post-operative pulmonary AEs or whether upper or lower abdominal surgery had been performed. Patients’ pre-operative fluid balance decreased gradually during the 5 days after surgery, while weight, increased on post-operative day 1, but decreased before discharge to below the baseline level (P < 0.005).
Recovery comparison between pulmonary intervention and non-intervention groups
In total, 12 patients needed an invasive intervention to treat pulmonary AEs; 6 patients underwent thoracocentesis and 6 others received chest tubes. None of the patients was re-intubated as a result of a pulmonary AE. For patients in the intervention group, eating, drinking, and bowel functions were restored within a mean of 14 days, and it took a mean of 6 days for patients to stand up, sit down on a chair, wash themselves, and walk independently after the surgery.
Comparisons in recovery process of the 12 patients in the intervention group with 64 non-intervention patients a
Peri-operative and post-operative parameters
Intervention group, mean (95% CI)
Non-intervention group, mean (95% CI)
Use of CPAP days
6.8 (3.2 to 10.3)
3.1(1.4 to 4.8)
Peri-operative crystalloids, ml
14,842 (12,100 to 17,582)
11,671 (10,677 to 12,665)
Sum of peri-operativecrystalloids and colloids, ml
20,629 (16,790 to 24,469)
16,255 (14,702 to 17,808)
Pulmonary complications after cytoreductive surgery and hyperthermic intraperitoneal chemotherapy
In this study, we found that pulmonary AEs are common after CRS and HIPEC; however, despite this, only a limited number of patients (16%) needed thoracocentesis or chest tubes. This may be a result of the strict patient selection (good performance status) for this treatment , as most of the study patients (91%) were ASA grade 1 or 2, and only two patients with pulmonary AEs had co-morbidities prior to surgery.
Patients after CRS and HIPEC treatment, usually required early post-operative ICU treatment due to influence on thoracic organs. However, the extent of treatment influence on thoracic organs is unknown. In the literature, pulmonary AEs after CRS and HIPEC have been reported previously in only two case reports, which both described the occurrence of ARDS after CRS and HIPEC [10, 14].
Peri-operative fluids and other clinical factors
To study the effect of peri-operative trauma and its effects on thoracic organs, we divided the abdomen into three surgical sites: upper, middle, and lower abdomen. We considered that the surgical trauma and the surgical site closest to the diaphragm (upper abdomen), the large amount of fluids administered during surgery, and the length of time that patients were kept on a respirator might have an influence on the development of pulmonary AEs [20, 21]. However, despite stripping of the diaphragm, the patients included in this study did not have any of the factors associated with pulmonary AEs. Therefore, insertion of a chest tube after surgery on the diaphragm should be based on individual patient signs and symptoms of AEs rather than the procedure.
Formation of atelectasis may be affected by several factors, including type and duration of anesthesia, patient position, inhaled fraction of oxygen , lack of positive end-expiratory pressure, and presence of paralysis caused by muscle relaxants [20, 22]. One study also showed that extubation failure may occur due to generous fluid treatment [23, 24]. Conversely, we did not find that the amount of fluid therapy received correlated with the occurrence of atelectasis, pleural effusion, or heart failure. However, the patients who had thoracocentesis or who had chest tubes implanted received larger amounts of crystalloids and the combination of crystalloids and colloids during surgery. None of the study patients had any signs of heart failure prior to surgery, and most of the study patients (70%) developed no signs of CHFpostoperatively. In this study, there was a weak correlation between oral intake, bowel movement, and ICU stay with the occurrence of heart failure grade 1 or 2. However, because of small number of patients with post-operative signs of congestion or CHF, it is not possible to draw any reliable conclusions.
Pulmonary AEs were not correlated with recovery parameters (restoring gastrointestinal functions and mobilization). Nevertheless, it seems that atelectasis might influence the length of post-operative hospitalization and ICU stay. Although all the patients (from our previous cohort ) were supposed to follow the same post-operative mobilization schedule  regardless of the grade of their pulmonary AE, it is possible that patients with larger atelectasis had more extensive physical therapy and mobilization than the other patients and thus stayed in the ICU for a shorter time period than patients with less atelectasis.
In our study, patients with segmental and larger atelectasis were extubated later than other groups, and patients with moderate pleural effusion had the longest hospital stay, a finding that has also been suggested in earlier studies . Conversely, good pain relief can result in patients being easier to mobilize and this might thereby result in smaller or less atelectasis. In this study, the number of patients with severe atelectasis may have been underestimated, and therefore having a larger number of patients with consecutive CT scans would have been preferable to allow us study the causality closely.
Patients in the intervention group, received larger amounts of crystalloids and the combination of colloids and crystalloids during surgery than the non-intervention group. A weight increase was seen in the entire patient population on post-operative day 1. Nevertheless, our centre’s policy is to give restricted fluid therapy during HIPEC, which is in line with other studies [6, 8, 11]. Despite good performance status, patients with higher PCI were more likely to develop pleural effusion, and this might reflect the extent of surgery. However, in this study there were no significant differences in PCI between the intervention and the non-intervention group. The intervention group also did not differ from the non-intervention group with respect to the restoration of gastrointestinal functions and mobilization.
Issues concerning radiological imaging
Radiological imaging was not routinely carried out in this study, but was performed whenever the patients status required it, for example in cases of pulmonary AE. Images were taken of only 82% of the patients, and therefore some information about the pulmonary AEs may be lacking. However, this study reflects the real-life situation, because it describes the daily care of patients with PC at our hospital. Most of the images were bedside chest radiographs, and only two CT scans were performed. It is difficult to compare the two types of image because CT scans may show more detailed findings than chest radiographs [20, 25, 26], and this could influence the findings in this study. In the future, it would be preferable to perform radiologic examinations (such as ultrasonography, CT, and chest radiography) on predetermined dates in order to be able to draw better conclusions about pulmonary AEs after CRS and HIPEC. The benefits of these two imaging methods for patients undergoing major surgery could not be addressed in the current study.
This study, assessed the incidence of pulmonary AEs after CRS and HIPEC and their effect on early recovery. Although the gradations of atelectasis, pleural effusion and heart failure have not been established, we found similar results in the literature [20, 27]. However, the radiologists who performed the gradations were blinded to the post-operative course of the study, and Cohen’s weighted κ score indicated only a moderate level of agreement between the two radiologists, which is a weakness in the study, but still demonstrates that the grading process was rigorous.
In conclusion, clinical and radiological post-operative pulmonary AEs are common after CRS and HIPEC; however, most have no effect on post-operative recovery.
This work was supported by the University Hospital’s Clinical Research Support (sådd-ALF).
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