diagnostics

Article Azygos Lobe: Prevalence of an Anatomical Variant and Its Recognition among Postgraduate Physicians

Asma’a Al-Mnayyis 1,* , Zina Al-Alami 2, Neveen Altamimi 3, Khaled Z. Alawneh 4 and Abdelwahab Aleshawi 3 1 Department of Clinical Sciences, Faculty of Medicine, Yarmouk University, Irbid 21163, Jordan 2 Department of Medical Laboratory Sciences, Faculty of Allied Medical Sciences, Al-Ahliyya Amman University, Amman 19328, Jordan; [email protected] 3 King Abdullah University Hospital, Irbid 22110, Jordan; [email protected] (N.A.); [email protected] (A.A.) 4 Department of Diagnostic Radiology and Nuclear Medicine, Faculty of Medicine, Jordan University of Science and technology, Irbid 22110, Jordan; [email protected] * Correspondence: [email protected]; Tel.: +962-2-7211111; Fax: +962-2-7211162

 Received: 5 June 2020; Accepted: 7 July 2020; Published: 10 July 2020 

Abstract: The right azygos lobe is a rare anatomical variant of the upper lobe that can be misdiagnosed as a neoplasm, a lung abscess, or a bulla. The aim of this study was to assess the prevalence of right azygos lobe and to evaluate the ability of postgraduate doctors to correctly identify right azygos lobe. We analyzed a total of 1709 axial thoracic multi-detector computed tomography (CT) images for the presence of an azygos lobe. Additionally, a paper-based survey was distributed among a sample of intern doctors and radiology and surgery residents, asking them to identify the right azygos lobe in a CT image and in an anatomy figure. Results showed that the prevalence of the right azygos lobe in the study sample was 0.88%. Men have more right azygos lobes than women. None of the intern doctors or surgery residents identified the right azygos lobe correctly, whereas more than half (57.1%) of the radiology residents did. Most of the incorrect answers about the CT scan were related to the bronchi (25.0%). The apex of the lung (17.7%) and the (17.7%) were the most common incorrect answers about the anatomy figure. In conclusion, the prevalence of the right azygos lobe in the current study is within the range of previously published literature. More education should be given for the identification of the right azygos lobe during anatomy and clinical teaching.

Keywords: azygos lobe; prevalence; misdiagnosis; computed tomography; Jordan

1. Introduction The right azygos lobe (lobus venae azygos) is an anatomical variant present in the upper lobe of the right lung, separated from the rest of the lung by a deep groove called an azygos fissure, which consists of the azygos vein and four layers of pleura (two parietal layers and two visceral layers). The right azygos lobe is formed during the development of the when the precursor to the upper thoracic segment of the azygos vein, called the right posterior cardinal vein, penetrates the apex of the right lung, carrying along the pleural layers instead of arcing forward above the as to enter the superior vena cava. The right azygos lobe is detected by conventional chest radiographs and by computed tomography (CT) scans [1–3]. It does not correspond to a specific , and it does not have its own [4]. The prevalence of the azygos lobe is 1.0% in anatomic specimens, about 0.4% in chest radiographs, and 1.2% in high-resolution CT scans [5,6]. Clinicians, anatomists, surgeons, and imaging practitioners should be aware of the possibility of the presence of a right azygos lobe. Since it is usually asymptomatic, its recognition is essential to prevent

Diagnostics 2020, 10, 470; doi:10.3390/diagnostics10070470 www.mdpi.com/journal/diagnostics Diagnostics 2020, 10, 470 2 of 8 misdiagnosis, and to be prepared for the technical implications on surgical procedures. It is important to be able to recognize the presence of a right azygos lobe to prevent the wrong interpretation during studying and reading various chest radiologic images, since it might appear as a mass, a lung abscess, or a bulla [5,7]. It could also be misidentified in AIDS patients with tuberculosis, when a fistula between a large lymph node and the esophagus is seen [8]. Furthermore, it might change the normal location of the superior vena cava [9] or cause right paratracheal opacity [5]. The presence of a right azygos lobe might also be associated with other anomalies, such as intrapulmonary right brachiocephalic veins [10] or esophageal atresia [11]. Clinically, surgeons should be ready for different surgical procedures if they encounter the right azygos lobe, since its presence makes surgery using a thoracoscope more difficult, increasing the probability of bleeding throughout the thoracic surgery [12,13] and particularly during sympathectomies [14]. As there are few studies about the azygos lobe compared to other anatomical variants, and since many anatomy textbooks and radiology atlases do not mention the right azygos lobe [15], this study will enrich the existing literature with new data about the prevalence of the right azygos lobe in a sample of the Jordanian population. No previous work studied the prevalence of this anatomical variant either in the Jordanian or Arab populations. Moreover, the findings showcase the common misconceptions and potential incorrect answers that could be given by postgraduate doctors upon attempting to identify the right azygos lobe. The aims of this study were to assess the prevalence of the right azygos lobe in a sample of the Jordanian population, and to evaluate postgraduate doctors’ ability to identify it correctly. The questions to be answered by our study were: (a) is the right azygos lobe present in the Jordanian population, (b) what is its prevalence in the study sample, (c) can postgraduate Jordanian physicians identify the right azygos lobe using CT and anatomy images correctly, and (d) what incorrect answers will the doctors provide when attempting to identify the right azygos lobe?

2. Materials and Methods

2.1. Prevalence of Right Azygos Lobe Two of the authors, who are consultant radiologists with more than 10 years of experience in thoracic imaging, studied 1709 axial thoracic multi-detector CT scans of 801 women and 908 men. The sample size was calculated using the Kish formula [16]. For sample size estimation at a 95% significance level with a 5% margin of error, the minimum representative sample size was 386. The anonymous images were chosen randomly from the Picture Archiving and Communication System (PACS) at King Abdullah University Hospital, located in Al-Ramtha in the north of Jordan. A serial number was assigned to each examined scan, and sex and date of birth were also recorded. Every CT scan was analyzed axially for presence or absence of the right azygos lobe. Sagittal and coronal planes were assessed when needed. Our inclusion criterium was that the CT scan was for a patient who was recorded as Jordanian according to their identity card, and our exclusion criteria were that the scans were for (a) non-Jordanian patients and (b) patients with pulmonary parenchymal distortion as a result of pulmonary or pleural diseases or due to previous thoracic surgery.

2.2. Description of the Right Azygos Lobe The right azygos lobe is seen in CT images of the right lung using the lung and mediastinal windows. It causes changes in the standard anatomy of the right lung-mediastinal relations. It is identified in the immediate right pre-, para-, and retro-tracheal locations by first identifying the azygos vein and arch (which is shifted superiorly in the case of an azygos lobe) and its drainage in the superior vena cava, with the azygos lobe seen in Figure1 being inseparable from the postero-medial wall of superior vena cava. The azygos lobe is seen medial to the azygos vein, with its posterior part seen to the right of the esophagus. Diagnostics 2020, 10, 470 3 of 8 Diagnostics 2020, 10, x FOR PEER REVIEW 3 of 8

Diagnostics 2020, 10, x FOR PEER REVIEW 3 of 8

Figure 1. Axial computed tomog tomographyraphy ( (CT)CT) cuts showing the right azygos lobe (white arrows) in the Figure 1. Axial computed tomography (CT) cuts showing the right azygos lobe (white arrows) in the same patient in a lung window (a)) andand inin aa mediastinalmediastinal windowwindow ((bb).). Scale barbar== 1010 cm cm. same patient in a lung window (a) and in a mediastinal window (b). Scale bar= 10 cm 2.3. Identifying the R Rightight A Azygoszygos L Lobeobe U Usingsing CT and A Anatomynatomy ImagesImages 2.3. Identifying the Right Azygos Lobe Using CT and Anatomy Images A paper-based evaluating survey was prepared (Figure2), which included two images of the A Apaper paper-based-based evaluating evaluating survey survey waswas preparedprepared (Figure(Figure 2),2), whichwhich included included two two images images of ofthe the right azygos lobe: an axial CT image from our current study and an anatomy figure used with rightright azygos azygos lobe lobe: an: an axial axial CT CT image image from from our current study study and and an an anatomy anatomy figure figure used used with with permission [17]. permissionpermission [17 [17]. ].

FigureFigure 2.2. The evaluati evaluatingng survey. survey. Figure 2. The evaluating survey. ThisThis part part of of the the study study was was performed performed inin a 700-bed700-bed teaching teaching hospital hospital in in the the north north of ofJordan, Jordan, which which waswas selectedThis selected part randomly. of randomly. the study A A was random random performed convenient convenient in a 700 sample-bed ofteaching of 22 2277 postgraduate postgraduate hospital in physicians the physicians north ofwas wasJordan, recruited recruited, which, includingwasincluding selected 173 173 randomly. intern intern doctors, doctors A random which, which convenient was was 56.0%56.0% sample ofof the total of 22 number number7 postgraduate of of intern intern doctors physicians doctors in in the thewas hospital hospital recruited of of, choice;includingchoice 26; 26 173 surgery surgery intern residents, residentsdoctors, which,which which was waswas 66.7%;56.0%66.7% ;of andand the 28 total radiology number residents residents, of intern, 90.3%. 90.3%.doctors Intern Intern in the doctors doctorshospital are are of postgraduatechoicepostgraduate; 26 surgery physicians physicians residents who who, which must must complete was complete 66.7% ayear ;a and year of 28 postgraduateof radiology postgraduate residents training training, (called90.3%. (called anIntern internshipan internship doctors year) are year) to be able to practice medicine inside Jordan. They were recruited because they are fresh topostgraduate be able to practice physicians medicine who insidemust Jordan.complete They a year were of recruited postgraduate because training they are (called fresh graduatesan internship and graduates and are expected to have a good background in anatomy. Surgery and radiology residents areyear) expected to be able to have to practicea good background medicine inside in anatomy. Jordan. Surgery They and were radiology recruited residents because are they trained are freshto be graduatesare trained and to are be expected specialists to in have surgery a good or backgroundradiology, respectively. in anatomy. They Surgery should and be radiology able to pass residents the arenecessary trained toexit be exams specialists after completing in surgery the or 4 radiology–5 year long, respectively. residency period. They We should recruited be able them to because pass the necessary exit exams after completing the 4–5 year long residency period. We recruited them because

Diagnostics 2020, 10, 470 4 of 8 specialists in surgery or radiology, respectively. They should be able to pass the necessary exit exams after completing the 4–5 year long residency period. We recruited them because they are expected to have better knowledge of anatomy and radiology than intern doctors or other residents. The evaluating survey was distributed in person and collected by one of the authors, after asking the physicians orally if they agree to answer the provided questions for research purposes. All distributed surveys were evaluated by one of the authors. Answers other than azygos lobe or right azygos lobe were considered incorrect. Our inclusion criteria were that participants were (a) physicians who were either intern doctors, or surgery or radiology residents at the time of conducting this part of the study (December 2019), and (b) physicians working in the chosen teaching hospital in the north of Jordan. Our exclusion criteria were that they were radiology or surgery specialists. The methodologies used in this work fulfill the ethical standards of the Helsinki Declaration. An institutional review board numbered 13/2/3496 was obtained.

3. Results

3.1. The Prevalence of the Right Azygos Lobe The prevalence of the right azygos lobe in the Jordanian population was found to be 0.88%. The prevalence in men was almost double that in women (Table1).

Table 1. Prevalence of the right azygos lobe in a sample of the Jordanian population represented as percentages.

Men Women Total Total number of patients (n) 908 801 1709 Cases with an azygos lobe (n) 10 5 15 Prevalence (%) 1.01 0.62 0.88

3.2. Knowledge of Postgraduate Physicians about the Right Azygos Lobe None of intern doctors or surgery residents answered the questions identifying the right azygos lobe in CT and anatomy images correctly. However, more than half (57.1%) of the radiology residents identified the right azygos lobe correctly (Table2).

Table 2. Summary of the results identifying the right azygos lobe represented as numbers and percentages.

Intern Surgery Radiology Type Doctors Residents Residents Total number of physicians in the teaching 309 39 31 hospital (n) Total number of physicians who responded to the 173 (56.0) 26 (66.7) 28 (90.3) survey n (%) a Correct answer CT scan 0 (0.0) 0 (0.0) 16 (57.1) n (%) b Anatomy 0 (0.0) 0 (0.0) 16 (57.1) Incorrect answer CT scan 18 (10.4) 12 (46.2) 6 (21.4) n (%) b Anatomy 7 (4.05) 7 (26.9) 3 (10.7) No answer CT scan 155 (89.6) 14 (53.8) 6 (21.4) n (%) b Anatomy 166 (96.0) 19 (73.1) 9 (32.1) a Percentages are calculated as a proportion of the total number of intern doctors or surgery or radiology residents in the hospital of choice. b Percentages are calculated as a proportion of the number of intern doctors or surgery or radiology residents who participated in the survey. Diagnostics 2020, 10, 470 5 of 8

Most of the incorrect answers identifying the right azygos lobe using the radiological CT image were related to the bronchi (25.0%). The apex of the lung (17.7%) and the superior vena cava (17.7%) were the most common incorrect answers in the anatomy image (Table3).

Table 3. A list of incorrect answers identifying the right azygos lobe represented as numbers and percentages. The percentages in the table are calculated as proportions of incorrect answers, not the total number of answers.

Incorrect Answers about the CT Image Incorrect Answers about the Anatomy Figure Structure N % Structure N % Bronchus/right bronchus/right Apex of the lung or right 9 25.0 3 17.7 pulmonary bronchus/right main bronchus lung apex Aortic arch 4 11.1 Superior vena cava 3 17.7 Pulmonary trunk 4 11.1 Avascular ring 2 11.8 Superior vena cava 3 8.33 Pleura 1 5.88 Esophagus 3 8.33 Azygous fissure 1 5.88 Inferior vena cava 3 8.33 Apical lung 1 5.88 Bronchus/right bronchus/right 2 5.56 pulmonary bronchus/right 1 5.88 main bronchus Lung 2 5.56 Aortic arch 1 5.88 Avascular ring 2 5.56 Right upper lobe 1 5.88 Apex of the lung or right lung apex 1 2.78 Lingula 1 5.88 Azygous fissure 1 2.78 Right lung 1 5.88 Apical lung 1 2.78 Circulating aorta 1 5.88 Right upper lobe 1 2.78 Total 36 100.00 17 100.00

4. Discussion The right azygos lobe is a rare anatomical variant in the superior lobe of the right lung. A search for the terms azygos and/or azygous lobe in the scientific literature revealed that the azygos lobe was never studied in the Jordanian or Arab populations, neither on cadavers nor on any imaging modality. Here, we studied the prevalence of the right azygos lobe in a sample of the Jordanian population and recorded the potential incorrect answers that were provided by a sample of postgraduate doctors when asked to identify the right azygos lobe using anatomy and CT images. Rauf et al. (2012) explored the prevalence of the right azygos lobe in various cadaveric populations in their literature review and discovered that it varied from 0.11–1.06%, and from 0.11%–0.2% in radiographic studies [14]. After examining axial CT images, we found that the prevalence of the right azygos lobe in the Jordanian population is 0.88%, which is comparable with the previously reported percentages on cadaveric populations. However, this might be considered a new record because it represents only about half of the previously recorded prevalence in Turkey (1.54%) using thoracic CT scans [18]. We chose CT scans because they provided a clearer and more reliable diagnosis than plain radiographs. Previously, CT scans proved that a group of patients had no pulmonary diseases or mediastinal masses after their X-rays showed abnormal opaque azygos lobes [1]. In patients with , chest X-rays overlook the right azygos lobe [19]. The literature also showed that no previous studies were published on the misconceptions about and misidentifications of the right azygos lobe. As our results showed, the structures that the sample of recruited doctors thought was the azygos lobe, both in the CT scan and in the anatomy image, were ambiguous and bizarre. Figure3 is the same figure used in the survey, fully labeled. Table4 summarizes CT-based descriptions for the structures that were recorded as answers when attempting to identify the azygos lobe. Diagnostics 2020, 10, x FOR PEER REVIEW 6 of 8

DiagnosticsTable2020 4 ,summarizes10, 470 CT-based descriptions for the structures that were recorded as answers6 of 8 when attempting to identify the azygos lobe.

Figure 3. Axial CT scan used in the survey, fully labeled. Scale bar= 10 cm Figure 3. Axial CT scan used in the survey, fully labeled. Scale bar = 10 cm.

Table 4.4. The structures that were provided as incorrect answers when attempting to identify the right azygos lobe using a CT scan, with authors’ remarks.remarks.

StructureStructure CT-Based CT-Based Description Description

BronchusBronchus For its location For its location,, please please refer refer to the to the labeling labeling in in Figure3 3 In the providedIn the providedimage, it image, is not it isseen not seenas a as complete a complete arch, arch, asas the the level level of thisof this Aortic archAortic arch image isimage at its is atmost its most inferior inferior aspect aspect PulmonaryPulmonary trunk Not seen, as it is just above the level of the provided CT image Not seen, as it is just above the level of the provided CT image trunkSuperior vena cava For its location, please refer to the labeling in Figure3 A posterior mediastinal structure; for its location, please refer to the labeling in Superior venaEsophagus For its location, please referFigure to the3 labeling in Figure 3 cavaInferior vena cava Cannot be in the same image; seen at the level of diaphragm TracheaA posterior mediastinal For its structure location, please; for its refer location to the labeling, please in Figurerefer 3to the labeling Esophagus This answer is correct, but because it was not specific, it was considered an Lung in Figure 3 Inferior vena incorrect answer CanTherenot is be no in such the anatomical same image term;; one seen possibility at the couldlevel beof that diaphragm the doctor meant cavaAvascular ring a vascular ring, which is a vascular anomaly of the aortic arch system; vascular Trachea For its location, plringsease are refer not presentto the labeling in Figure3 in Figure 3 Apex of the rightTh lungis answer is correct, Thebut apexbecause of the it lung was is notnot shown specific in Figure, it was3 considered an Lung Azygous fissure For its location,incorrect please refer answer to the labeling in Figure3 There is no such anatomical term; it seems that the doctor meant the apex of the Apical lung There is no such anatomical term; one possibility could be that the doctor lung, which is not shown in Figure3 Avascular ring meant aThis vascular answer ring, is correct, which but becauseis a vascular it was not anomaly specific, itof was the considered aortic arch an Right upper lobe system; vascular ringsincorrect are not answer present in Figure 3 Apex of the The apex of the lung is not shown in Figure 3 Regardingright lung the anatomy figure [17], Figure4 represents the same image used in the survey, fully Azygous labeled. A full record of the incorrectFor its answers location with, please our refer notes to and the remarkslabeling isin presented Figure 3 in Table5. fissure There is no such anatomical term; it seems that the doctor meant the apex of Apical lung the lung, which is not shown in Figure 3 Right upper This answer is correct, but because it was not specific, it was considered an lobe incorrect answer

Diagnostics 2020, 10, x FOR PEER REVIEW 7 of 8

Regarding the anatomy figure [17], Figure 4 represents the same image used in the survey, fully Diagnostics 2020, 10, 470 7 of 8 labeled. A full record of the incorrect answers with our notes and remarks is presented in Table 5.

FigureFigure 4. 4.Right Right azygos azygos lobe lobe used used in in the the survey, survey, fully fully labeled. labeled. (The (The original original figure figure was was adopted adopted after after a a writtenwritten permission permission from from [ 17[17]]).).

Table 5. The structures that were written as incorrect answers when attempting to identify the right Table 5. The structures that were written as incorrect answers when attempting to identify the right azygos lobe using an anatomy figure, with authors’ remarks. azygos lobe using an anatomy figure, with authors’ remarks. Structure Anatomy Figure-Based Description Structure Anatomy Figure-Based Description Apex ofApex the of the lung For its usual location, please refer to the labeling in Figure4. For its usual location, please refer to the labeling in Figure 4. lungSuperior vena cava The superior vena cava is not shown in Figure4 There is no such anatomical term; one possibility could be that the doctor meant Superior vena Avascular ring aThe vascular superior ring, which vena is cava the vascular is not anomalyshown in of theFigure aortic 4 arch system; cava vascular rings are not shown in Figure4 PleuraThere is no such anatomical For its usual term location,; one pleasepossibility refer to could the labeling be that in Figure the doctor4 meant Avascular Azygous fissurea vascular ring, which For its usual is the location, vascular please anomaly refer to the of labelingthe aortic in Figure arch4 system; ring There no such anatomical term; it seems that the doctor meant the apex of the Apical lung vascular rings are not shown in Figure 4 lung, which is labeled in Figure4 Pleura BronchusFor its usual For location, its usual location, please please refer referto the to thelabeling labeling in in Figure 4 4 Azygous Aortic archFor its usual location, The aorticplease arch refer is not to shown the labeling in Figure 4in Figure 4 fissure This answer is correct, but because it was not specific, it was considered an Right upper lobe There no such anatomicalincorrect term answer;; it seems please referthat tothe the doctor labeling mean in Figuret the4 apex of the Apical lung The ligula is a tongue-like structure near the base of the left lung; Figure4 is an Lingula lung, which is labeled in Figure 4 image of a right lung Bronchus For itsThe usual answer location, is correct, please but because refer it wasto the not labeling specific, it in was Figure considered 4 an Right lung Aortic arch The aortic arch is incorrectnot shown answer in Figure 4 Right upperCirculating aortaThis answer is correct, but because The aorta it is was not shownnot specific in Figure, 4it was considered an lobe incorrect answer; please refer to the labeling in Figure 4 The ligula is a tongue-like structure near the base of the left lung; Figure 4 is an InLingula this study, we documented a new reading for the prevalence of the right azygos lobe in a sample of Jordanians. The findings can also helpimage anatomy of a and right medicine lung teaching staff to draw their The answer is correct, but because it was not specific, it was considered an students’Right attentionlung toward various misconceptions about the right azygos lobe, which will improve their anatomical background and their skills in readingincorrect CT scans. answer Circulating The limitations of our study are two-fold:The aorta the is sample not shown of patients in Figure was 4 only from the north of Jordan,aorta and the sample of doctors for the evaluation of postgraduate doctors’ knowledge about the azygosIn lobe this was study only, we from document one teachinged a new hospital. reading Future for workthe prevalence might use aof more the representativeright azygos lobe sample in a ofsample the Jordanian of Jordanians population,. The findings recruit can more also doctors help anatomy to answer and the medicine survey, andteaching analyze staff anatomy to draw andtheir radiologystudents’ syllabiattention involving toward clinicallyvarious misconceptions important anatomic about variants. the right Weazygos conclude lobe, thatwhich more will attention improve shouldtheir anatomical be given to background the right azygos and their lobe duringskills in anatomy reading andCT scans. clinical teaching, since it is present in the JordanianThe population.limitations of our study are two-fold: the sample of patients was only from the north of Jordan, and the sample of doctors for the evaluation of postgraduate doctors’ knowledge about the Authorazygos Contributions: lobe was onlyConceptualization: from one teaching A.A.-M. hospital. and Z.A.-A.; Future Data work curation: might A.A.-M., use a N.A. more and representative K.Z.A.; Formal analysis: A.A.-M. and Z.A.; Investigation: A.A.-M. and N.A.; Methodology: A.A.-M.; Project administration: A.A.-M.sample and of the Z.A.-A.; Jordanian Resources: population, A.A.-M., N.A.recrui andt more K.Z.A.; doctors Supervision: to answer A.A.-M. the andsurvey, Z.A.-A.; and Validation: analyze anatomy A.A.-M., Z.A.-A.and radiology and A.A.; Writing—originalsyllabi involving draft: clinically Z.A.-A.; important Writing—review anatomic & editing: variants. A.A.-M., We conclude Z.A.-A., N.A., that K.Z.A. more and A.A. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Diagnostics 2020, 10, 470 8 of 8

Conflicts of Interest: The authors declare no conflict of interest.

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