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Asbestos exposure and malignant mesothelioma of the tunica vaginalis testis: a systematic review and the experience of the Apulia (southern Italy) mesothelioma register
Environmental Healthvolume 18, Article number: 78 (2019)
Malignant mesothelioma of the tunica vaginalis testis (MMTVT) is a rare disease with a poor prognosis. The diagnosis and management of these lesions are often difficult for pathologists, surgeons, oncologists and occupational physicians. A preoperative diagnosis of malignancy is rarely made, and there is no established effective therapy except orchidectomy.
A systematic literature review was conducted among the articles published in the English literature on primary MMTVT. Moreover four cases from the Apulia mesothelioma register are reported here.
Two hundred eighty-nine cases of MMTVT have been reported from 1943 to 2018. Overall asbestos exposure has been investigated only for 58% of all cases reported in this review, while in 41.8% this data are not available. Noteworthy is the fact that in many reports there is not an anamnestic reconstruction of any asbestos exposure. A history of direct occupational, environmental or familial asbestos exposure is found in 27.6% of the cases. The four cases from the Apulia mesothelioma register are all with ascertained occupational exposure to asbestos.
The true incidence of asbestos exposure in MMTVT is underestimated because of insufficient information reported in older literature. To establish a broad consensus on the causal relationship between asbestos and MMTVT in the scientific community its necessary to analyze the same variables in the epidemiological studies. In general it should be recommended that a positive history of exposure to asbestos or to asbestos–containing materials are at risk for the development of a MMTVT and should be monitored.
Malignant mesothelioma (MM) is a rare tumour that can occur in the body cavities covered by mesothelium, i.e., the pleura, peritoneum, pericardium and testicular vaginal tunica , with benign and malignant variants. Among MM cases, a very small percentage (< 3%)  arise in the tunica vaginalis testis. Malignant mesothelioma of the testicular vaginal tunica (MMTVT) is very rare with potentially aggressive behaviour, and it can invade the testicular parenchyma, spermatic cord, epididymis and subcutaneous tissue of the penis; therefore, it has also been classified with the term paratesticular mesothelioma , rather than adenomatoid tumours, malignant adenomatoid tumours, mixed mesoblastic tumours or other various diagnoses, which is how it has been misinterpreted in the past [4,5,6,7,8,9]. The confusion over nomenclature was due to the difficulty of histological classification .
Over the years, three groups of mesothelial tumours have been identified, defined and classified: well differentiated papillary mesothelioma (WDPM); an emerging diagnostic category of papillary mesothelioma with borderline features or localized mesothelioma of low grade malignancy, also called mesothelioma of uncertain malignant potential (MUMP); and mesothelioma of low malignancy potential (MLMP) [11, 12], representing a morphological continuum between WDPM and malignant mesothelioma (MM) [11, 13].
As reported by Rankin (1956)  and by Kossow (1981) , the first two cases of mesothelioma of the genital tract were reported in 1912 by Naegeli  and in 1916 by Sakaguchi , followed by Thompson (1936), Evans (1943), Golden and Ash (1945), Lee (1950), Bailey (1955) and Barbera (1957) [4, 17,18,19,20,21], although the last was actually classified as benign papillary mesothelioma (WDPM). These cases were described by various names until 1970, when Marcus and Lynn  demonstrated by electron microscopy that there were no differences between so-called adenomatoid tumours and malignant mesothelioma .
To date, the WHO(world health organization) classification of tumours of the urinary system and male genital organs , in the classification of tumours of the testis and paratesticular tissue, has reported MM and the WDPM, noting that the latter “may have a progression to malignant mesothelioma if the lesions are not completely excised”.
This review points out only case series and case reports of primary MM of the tunica vaginalis testis. We conducted a comprehensive review from Medline (National Library of Medicine database) and a PubMed database search of the English medical literature and on the references lists of published articles. Nevertheless, the data are often incomplete or not comparable due to the long period covered by the scientific literature examined (1943-2018) and the relative evolution of diagnostic techniques and classifications of mesotheliomas, as well as knowledge about the risk factors related to the onset of the disease [5, 21, 25, 26]. Similarly, despite the rarity of this disease, all of the various reviews reported might not indicate the true incidence because of the relatively recent agreement about the definition of the clinicopathologic entity. In addition, we report four cases from the Apulia (Southern Italy) mesothelioma register.
A PubMed computerized search was performed using the following keywords: mesothelioma tunica vaginalis testis (127 articles), testicular (276 articles), paratesticular (50 articles), testis (179 articles), and scrotum (46 articles); and it was filtered for human patients and English language. The English literature search without time limits, from 1943 to 2018, the cut-off date was December 15, 2018, and were identified a total of more than 276 previously published scientific articles on MMTVT (MEDLINE-PUBMED National Library of Medicine, National Center for Biotechnology Information; available from URL: http://www.ncbi.nlm.nih.gov/pubmed).
We undertook a review using the following criteria: we excluded articles with the diagnosis of benign mesothelioma as stated by the authors on the basis of histopathological findings and cases of adenomatoid tumours and other benign tumours and WDPM , although some authors, such as Grove (1989) , suggested that these tumours should always be considered “borderline malignancy”. Similarly, cases with doubtful primary tumour origin or with concomitant pleural or peritoneal disease were excluded.
Using the above criteria, the review of the literature to date revealed 289 previously described cases in 165 published articles from PubMed and from the reference lists of the available publications in the English literature, which we considered bona fide malignant MTVT(Table 1) [4, 5, 9, 11,12,13,14, 23, 28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116,117,118,119,120,121,122,123,124,125,126,127,128,129,130,131,132,133,134,135,136,137,138,139,140,141,142,143,144,145,146,147,148,149,150,151,152,153,154,155,156,157,158,159,160,161,162,163,164,165,166,167,168,169,170,171,172,173,174,175,176,177,178,179,180,181,182,183,184].
Watenabe (1994))  and Ascoli (1996)  reported two cases of multifocal mesothelioma; the subjects both had occupational exposure as insulators. Individual data were not available in three papers: Spiess (2005) , Gemba (2012)  and Recabal (2017)  which present case series.
Our cases were retrieved from the Apulian malignant mesothelioma register Cor Apulia (Cor-operating centre regional), established in 1993 as a part of the ReNaM-Italian national mesothelioma register. The Apulia mesothelioma register collects data on all incident cases of mesothelioma (pleura, pericardium, peritoneum and tunica vaginalis testis) from 1993 to date.
The regional register according to the national guidelines , using a standardized questionnaire and with direct interviews with patients or their relatives, obtained occupational and residential-environmental histories, lifestyle habits and the hobbies of the patients. Similarly, the best evidence of histological diagnosis, follow-up data and vital status of each patient were recorded.
Since, in 1943, a confusing nomenclature arose, and in 1945 Golden and Ash  introduced the term “adenomatoid tumours”, De Klerk and Nime  reported in 1975 that, from 1912 to 1975, two hundred three cases of adenomatoid tumours (malignant adenomatoid tumours) of testicular and paratesticular tissues were reported in the English language literature. Therefore, Bisceglia (Bisceglia 2010)  reported fewer than 250 cases of testicular and paratesticular mesothelioma, Jankovichova reported approximately 250 cases, and Mrinakova reported approximately 300 cases [165, 171]. All of these cases comprised and could be categorized as MM, WDPM and MUMP or MLMP.
In our review, we found 289 cases of MMTVT (Table 1). The last four cases reported in Table 1 were cases currently found in the Apulia regional registry of the mesothelioma, so the total number of cases reported is here 293.
Among the 289 cases reported here from the literature, the main features are summarized in Table 2.
The characteristics of our cases are reported in Table 1 and summarized in Table 3; the age at diagnosis ranged from 63 to 78 years old, with an average age of 73.2 years old; the clinical onset was a mass, and only two cases also had hydroceles; all of the cases involved the left testicle. All of the patients underwent surgery (orchidectomy), and the histological types were epithelioid. IHC (immunohistochemistry) was always performed with calretinin, HBME1, CK AE1/AE3, EMA positive (Figs. 1, 2, and 3).
All of our cases were directly interviewed, and asbestos exposure was documented. Two patients had pleural plaques found on computerized axial tomography (CAT) examination. At the last date of follow-up, in September 2018, two patients were alive and two were dead: one died of disease metastasis, and the other died of cardiopathy. The median survival was 46.7 months (range 2-141), the latency period was a mean of 47.5 years (range 41-58), and the duration of asbestos exposure had a mean of 10.5 years (range 2-21).
MMTVT is a rare neoplasm that constitutes 0.3-5% of all mesothelioma cases with a mortality rate of 53% at 2 years following diagnosis .
The tunica vaginalis has a common embryological origin with the visceral pleura, peritoneum and pericardium . Relative to histogenesis in the past, four embryologic hypotheses have been considered: endothelium, epithelial, mesonephric and mesothelial hypotheses . Early writers believed that this tumour had a lymphangiomatous origin because the predominance of labyrinthine channels lined by seemingly flat endothelial cells embedded in a reticular stroma, subsequent microscopic investigations excluded the endothelial origin due to the presence of vacuolated cuboidal and columnar cells. .
The mesothelial character was supported by electron microscopic studies . The tunica vaginalis develops from evagination of the peritoneum during fetal life, and it is an embryonic extension of the peritoneal mesothelium, resulting from the descent of the testis through the abdominal wall via the inguinal canal into the scrotum . The epithelial lining of the urogenital tract has mesodermal (mesothelial) origin , and the mesothelium has the ability to differentiate into fibroblasts and mesonephric tubular structures, or rather, the mesothelial cells could have a multipotent evolution; they can differentiate in an epithelial or a fibroblastic direction [33, 192, 193]. The mesothelial hypothesis was also corroborated by the occurrence in a patient affected by Maffucci’s syndrome, a mesenchymal disease .
To date, there is agreement regarding some of the main features of this disease as shown below; moreover, it is difficult to diagnose preoperatively.
MMTVT can be asymptomatic for a long time. Hydrocele, scrotal mass, a lack of pain, inguinal hernia, spermatocele, testicular torsion, previous herniorrhaphy, and post-traumatic injury are all possible clinical manifestations of the disease . Long asymptomatic intervals from initial presentation to clinical recurrence have been reported , moreover, MMTVT might mimic epididymitis  .
Computed tomography, ultrasound, ultrasonography (colour Doppler sonography), and cytological examination of the hydrocele fluid by sonographically guided fine-needle aspiration (FNA) [128, 137, 164] have been performed, although some authors [169, 173] do not agree with these methods due to the low sensitivity of cytology and the potential risk of metastasis, instead using gross pathology images and magnetic resonance imaging.
Macroscopic appearance gross findings
A firm painless scrotal mass , numerous small papillary lesions or multiple nodules studded on the internal surface of the hydrocele sac, diffuse thickening of the tunica vaginalis , and a solid coat around the tunica vaginalis with variable features.
Microscopic appearance findings
Malignant character is demonstrated by the growth pattern, cytological alterations, extensive tissue invasion, and metastases to the lymph nodes; early diagnosis is by cytologic examination of the hydrocele fluid. Nuclear atypia, mitotic activity, with a stroma invasion infiltrative pattern. Cellular nuclear pleomorphism and papillary configuration are signs of lethal potential . An infiltrative pattern of growth with increased cellularity nuclear pleomorphism and high mitotic rate and stromal invasion [105, 195]. Large lymphoid cells with clear or slightly eosinophilic cytoplasm with large strongly atypical polymorphic nuclei and a great number of mitoses; epithelioid features with papillary growth, papillary tubules, and solid growth in invasive foci .
Histologically, it can be of three histologic types
Epithelial (papillary, tubuloalveolar-glandular or solid) , fibrosarcomatous or mesenchymal; biphasic; or mixed, associated with the papillary architecture with stromal invasion. Hallmarks of mesothelioma are epithelial cuboidal cells with microvilli, basement membranes, filaments and desmosomes .The criteria for malignancy are nuclear pleomorphism, mitotic activity and stromal invasion [13, 198, 199].
IHC (immunohistochemistry) shows the presence of both cytokeratin and vimentin, suggesting the diagnosis of mesothelioma. Positive staining for cytokeratin, vimentin and Ema (epithelial membrane antigen), with negative staining for Cea carcinoembryonic antigen, Leu–M1, and cytokeratin 20 CKL20. Epithelial membrane antigen and factor VIII are strongly suggestive for the diagnosis of MM; mesothelioma-related markers include calretinin, thrombomodulin, CK5/6 (pleural), WT1 (Wilms tumour antibody), D2-40, CK7 (tunica vaginalis) [120, 162, 188, 198], CD20 +, and calretinin + [196, 200].
The microvilli are elongated and develop complex throughout the tumour; there are well-defined, mature desmosomes through the interdigitating portions of the cytoplasmatic membrane, and numerous cytoplasmatic filaments are observed [104, 151, 188]. In 2009, the International Mesothelioma Interest Group (IMIG) ) recommended IHC as the gold standard for the diagnosis of MM, instead of electron microscopy.
The most common sonographic finding is the presence of heterogeneous nodular or papillary masses of the tunica vaginalis associated with a hydrocele or hypoechoic hydrocele with heterogeneous masses of increased echogenicity at the periphery [74, 115, 187, 202]. Lesions are closely related to the tunica vaginalis .
Most cases are unilateral on presentation, while only a few cases of bilateral MMTVT have been reported ; in the present review, we found only six cases (2.03%) with reported bilateral disease [50, 93, 97, 111, 175, 179].The case reported by Slaysman (1982)  occurred in a young man of 20 years old affected by Maffucci syndrome.
Distant spread usually occurs via lymphatics; the retroperitoneal nodes are the most common site of metastasis, while spinal metastasis was described by Mathew (1996)  and cutaneous metastasis has also been reported [34, 53, 61, 170].
The differential diagnosis includes mesothelial hyperplasia, adenomatoid tumour, benign papillary mesothelioma, borderline serous papillary tumours, serous carcinomas, carcinoma of the rete testis or epididymis and metastatic adenocarcinoma [26, 99, 188, 203]. Because of potential misdiagnosis, the best evidence for definitive diagnosis requires a panel of HIC markers [145, 198, 203].
The prognosis is poor. While MM of the pleura and peritoneum has an extremely poor prognosis, MMTVT has a better prognosis, but the natural history of this tumour suggests an aggressive behaviour, with a survival rate of less than 50% 2 years after diagnosis .Early diagnosis is of great importance for treatment and long-term survival, especially in young men [156, 160].
A multidisciplinary approach of radical orchiectomy and retroperitoneal node dissection is the best choice for cases of this disease. Chemotherapy can be useful for regression of disseminated disease, although to date, because of the rarity of this disease, no statistically significant studies or large series are available to assess the role of adjuvant therapy (chemo- and radiotherapy) . Long-term follow-up over 5 years is needed because late recurrence is not rare and, to date, an aggressive surgical approach is necessary to achieve a cure because of potential late recurrence or metastasis. Many authors have emphasized the importance of considering this tumour in men with scrotal masses and hydroceles , even in the absence of asbestos exposure [115, 122, 123]. Lifelong follow-up and management in a multidisciplinary setting are recommended [161, 168, 171].
Similarly, our review, which considered only malignant mesotheliomas in the English literature, as reported by the authors of the examined articles due to the temporal evolution of the histological classification of this pathology, as already noted, does not confirm the total number of cases as reported in previous reviews  including approximately 250 cases.
Another limitation of this review is that no best evidence of diagnosis from early articles and no best evidence of asbestos exposure are available.
The histologic prevalent pattern is epithelial (53.6%of all cases), followed by a mixed biphasic pattern in 15.5% and a fibrous sarcomatoid variant in 1.7%. The more frequent age at presentation ranges from 61 to 80 years old (38.7%). Hydrocele was present in 29.06% of the cases described and swelling in 27.3%. Two cases [79, 89] were not primary tumours but of multifocal origin, and the pleura and peritoneum were involved in two patients with heavy exposure to an insulator.
Only 4.4% of cases had a follow-up of over 8 years. Sixty-six patients died of disease progression with an average survival of 24.2 months (range1-76); two cases with a long duration of follow-up died after 132 and 564 months; ultimately, the prognosis remains poor with only rare long-term survivors. The overall recurrence rate (recurrence or metastasis) was 26.2%, predominantly within the first 2 years of follow-up. Both cases reported by Mathew (1996)  presented spinal metastasis, and the case reported by Hispan (2016)  presented cutaneous metastasis. Finally, in the papers by Spiess (2005) , Gemba (2012)  and Recabal (2017) , no individual data were reported. In previous reviews, a statistically significant correlation was reported between survival with age < 60 years old and organ-confined disease at diagnosis [74, 202]. Assessment of prognostic parameters revealed a significant correlation of the patient’s age with survival . Radical inguinal orchiectomy might contribute to a better prognosis . Due to the possibility of late tumour recurrence reported in 2.7% , lifelong follow-up can be recommended and should be offered to the patient because of the metastatic potential of the tumour; in fact, recurrence can occur as late as 15 years postoperatively [123, 205].
Regarding risk factors, the only causal factor so far ascertained is asbestos exposure, and exposure to different asbestos-containing materials is the only well-documented risk factor [87, 96], as stated by IARC (international agency on cancer research) (2012) , although information about exposure might not always have been adequate. Nevertheless, there are authors who do not agree with the absence, until today, of analytical case-control epidemiologic studies to test this relationship .
Asbestos is an ascertained carcinogen  in the development of mesotheliomas. It is necessary to bear in mind that it is ubiquitous not only in the workplace but also in the general environment . The first study reporting an MMTVT case, diagnosed in 1969, with asbestos exposure was published in 1976 by Fligiei and Kaneko  in a pipe insulator exposed for 40 years. In the same year, Pizzolato and Lamberty  reported a case in a sugar refinery worker. Since the first case of MMTVT described in 1976 by Fligiel and Kaneko (Fligiel 1976 , it has been supposed that the asbestos fibres from the lung can reach the tunica vaginalis by a lymphatic or bloodstream route [207, 208]. Mirabella (1991) , in his review of the literature, reported eleven cases with occupational asbestos exposure. In the review by Jones (1995)  of a total of 63 cases, 48% had histories of asbestos exposure, while in Mensi’s report (2012) , 61% of cases had asbestos exposure.
Overall, asbestos exposure was investigated only in 58% of all cases reported in this review, while in 41.8%, these data were not available. Notably, in many reports, there was no anamnestic reconstruction of any asbestos exposure.
A history of direct occupational, environmental or family asbestos exposure is found in 27.6% of these cases. Among these cases (80 cases) 12.5% reported generic occupational exposure the others 87.5% have a documented history of asbestos exposure. Among the latter there are insulators, dock workers, steel industry workers, farmers, shipyard workers and other different occupations in sectors known to involve asbestos exposure. To be noted there are four cases with environmental exposure, six with household, family or hobby exposure and five cases with or without declared exposure but with pleural plaques or asbestos bodies.
The duration of asbestos exposure is recorded in 108 articles of the 165 reviewed (65.45%). In these articles 50 ascertained the exposure (30.30%) while in 58 articles it was excluded (35.15%).
The duration of exposure is between 4 and 50 years, for occupational exposures only the range is 4-40 years. For the new employment cases presented here the range is 3-23 years.
The true incidence of asbestos exposure in these reported MMTVT cases is underestimated because of insufficient information, especially for the earlier cases and case series described until the beginning of the 2000s, when the scientific community became aware of the risk factors for this disease represented by asbestos exposure . Similarly, because of the long latency period, even over decades, poor patient recall in the reconstruction of asbestos exposure and occupational histories or the patient being unaware of using materials containing asbestos , until now, the quality of these data was quite unclear, which might have caused the majority of MMTVT cases to date appearing to be idiopathic, and there is no accurate assessment of asbestos exposure association. However, latency in Antman’s (1984))  case series ranged from 16 to 40 years. The higher incidence of MMTVT among older patients is related to longer exposure to asbestos with a latency range of 10-40 years. A positive history of asbestos exposure or asbestos-containing materials constitutes a risk for the development of an MMTVT and should be monitored .
The Apulia mesothelioma registry recorded 4 cases of MMTVT from 1993 to 2018, accounting for 0.3% of all MM cases reported in the regional register during this period. This percentage is consistent with the national Renam data (0.28%) from the national Italian mesothelioma registry . The age at diagnosis was an average of 73 years old, and the mean survival (46 months) was consistent with that reported in the literature . The family histories and clinical-medical histories of the patients were unremarkable. None of our patients underwent chemotherapy or radiotherapy cycles after orchidectomy. The Renam data  showed that more than 59% of MMTVT cases had asbestos exposure. Our four cases, all with occupational exposure, had a latency of 47 years and an exposure length of 10.5 years, and these data are concordant with the descriptions in the literature of the aetiological role of asbestos in the pathogenesis of MM [3, 13, 206]. The accurate diagnosis of primary malignant MMTVT and occupational anamnesis are helpful for medicolegal compensation considerations, especially for the cases associated with asbestos exposure . The case described here was referred to the Italian workers’ compensation authority (Inail - National Insurance Institution for Occupational Accidents).
Recently, many studies have demonstrated molecular changes in MM with multiple chromosomal alterations [184, 210,211,212,213,214]. Chromosomal abnormalities in cases of MMTVT were described for the first time by Serio (Serio 2016) in two cases with comparative genomic hybridization (CGH) findings. The two cases showed several gains and losses, in particular, identical lost regions at 1p13.3 → q21.1; 19q13.42; 21q22.2; and 22q12.2 (tumour suppressor gene NF2). Jean (Jean 2012)  hypothesized that NF2 regulates cell growth function, and its inactivation could be related to tumour progression and patient survival. We are deepening the study of these new cases, all with ascertained exposure to asbestos, to understand whether there are specific DNA copy number changes in MMTVT and investigating the relative genes involved to define whether they are or are not the same as those reported in pleural MM, particularly in relation to asbestos exposure, and whether they might be useful in elucidating tumorigenesis and predicting prognosis.
Although this systematic review shows that only 27.6% of the cases reported in this long period of time (1943-2018) had asbestos exposure must be underlined that in 41.8% of the cases in the literature exposure to asbestos is not investigated. In our opinion, to establish a broad consensus on the causal relationship between asbestos and MMTVT in the scientific community, we will need to analyze these relationships with analytical epidemiological studies. A case control study on the data from the national mesothelioma registry is under way in Italy, together with molecular epidemiological studies.
Availability of data and materials
The dataset and articles used and analyzed during the study are available from the corresponding author on reasonable request.
Computerized axial tomography
Comparative genomic hybridization
Operating centre regional
Fine needle aspiration
International agency on cancer research
International mesothelioma interest group
Mesothelioma low malignant potential
Malignant mesothelioma tunica vaginalis testis
Mesothelioma uncertain malignant potential
National mesothelioma register
Well differentiated papillary mesotheloma
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The authors thank Mr. Alberto Amenduni for his help in retrieving articles.
This work was supported with the ordinary funds of the University Aldo Moro of Bari.
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