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Lozano-Sánchez FS, Muñoz A, las Heras JA, González-Sarmiento R, García-Cenador MB (2020) Carotid Paragangliomas Related to Form Involving Multiple Systems (Syndromes and Diseases): A Systematic Literature Review. Int J Rare Dis Disord 3:024. doi.org/10.23937/2643-4571/1710024

Review Article | OPEN ACCESS DOI: 10.23937/2643-4571/1710024

Carotid Paragangliomas Related to Form Involving Multiple Systems (Syndromes and Diseases): A Systematic Literature Review

Francisco S Lozano-Sánchez MD, PhD1,2,3, Angel Muñoz MD, PhD1,4, José A de las Heras MD, PhD5,6, Rogelio González-Sarmiento, MD, PhD3,7 and M Begoña García-Cenador MD, PhD1,3*

1Department of Surgery, School of Medicine, University of Salamanca, Spain

2Service of Angiology and Vascular Surgery, University Hospital, Spain

3Salamanca Institute of Biomedical Research (IBSAL), Spain

4Service of Otorhinolaryngology, School of Medicine, University of Salamanca, Spain

5Department of Biomedical and Diagnostic Sciences, School of Medicine, University of Salamanca, Spain

6Service of Radiology, School of Medicine, University of Salamanca, Spain

7Department of Medicine, School of Medicine, University of Salamanca, Spain

Abstract

Carotid paragangliomas are infrequent tumours, generally single, non-functional and benign. Nevertheless, the biology of these tumours occasionally means they are bilateral, multicentric, functional and malignant. Such infrequency and the different ways they manifest themselves pose a diagnostic/therapeutic challenge that is reflected in the final outcomes.

According to the Shamblin classification, 75% of carotid paragangliomas are either Type I (tumour smaller than 4 cm, weakly attached to the carotid arteries, and can be surgically excised in a straightforward manner) or Type II (tumour larger than 4 cm, partially surrounding the carotid arteries, and attached to the vascular adventitia), and 25% of cases are Type III, completely surrounding the carotid bifurcation, firmly attached, so vessel replacement may be considered.

Fewer than 5% of carotid paragangliomas are associated with syndromes (e.g., von Hippel-Lindau disease and Carney triad) or diseases (e.g., thyroid cancer and thymoma), which further complicate their treatment. Morbidity and mortality rates in these cases are clearly different.

This review sets out to address carotid paragangliomas related to syndromes and diseases, with their references being very widely distributed in the literature, with the aim being to highlight their idiosyncrasies of clinical, diagnostic and therapeutic interest. This has involved a systematic literature review of the Medline and Cochrane Library databases up to 1 November 2019, locating 26 articles involving a total of 37 patients.

Conclusions

1) Patients with these exceptional combinations present major clinical complexity; 2) They pose a medical challenge, with the diagnostic strategy being vitally important (search for associated synchronous and metachronous tumours) together with the therapeutic process (surgical times and priorities); and 3) There must be interdisciplinary cooperation across the different medical specialisms involved.

Keywords

Carotid body tumour, Carotid paraganglioma, Carotid paraganglioma complex, Hereditary tumour syndrome, Inherited syndromes

Abbreviations

PG: Paraganglioma; PHEO: Pheochromocytoma; CPG: Carotid Paraganglioma; JPG: Jugular Paraganglioma; HLD: vonHippel-Lindau Disease; MEN-2: Multiple Endocrine Neoplasia-type 2; NF-1: Neurofibromatosis-type 1; CSS: Carney-Stratakis Syndrome; GIST: Gastrointestinal Stroma Tumour; PCH: Pulmonary Chondroma; HPT: Hyperplasia Parathyroid

Introduction

Although pheochromocytomas (PHEOs) and paragangliomas (PGs) share a common origin (neural crest-derived chromaffin cells), they are clearly different in terms of location (PHEOs - intra-adrenal paragangliomas (PGs) versus extra-adrenal ones) and biological behaviour. The term paragangliomais used for tumours that arise from the sympathetic ganglia in the thorax, abdomen and pelvis, as well as the parasympathetic paraganglia in the head and neck. PGs account for 0.012% of all the tumours in the body, and for 0.6% of those located in the head and neck (80% affect the carotid body, 15% involve the glomus-jugular bulb and tympanic nerve, and the remaining 5% affect the vagus nerve) [1,2].

The rate of carotid paragangliomas (CPGs) is estimated to be between 1/30,000 and 1/100,000 people [3,4], affecting more women (ratio of 2:1) in their fifties (age range 18-94). The tumours are usually single ones measuring < 4 cm in diameter, delimited (not attached to the carotids), with slow growth, non-secretary, and benign [5-7].

According to the Shamblin classification [8], 75% of CPGs are either Type I (tumour smaller than 4 cm, weakly attached to the carotid arteries, and can be surgically excised in a straight forward manner) or Type II (tumour larger than 4 cm, partially surrounding the carotid arteries and attached to the vascular adventitia), and Type III with a frequency of 25% of cases, which completely surround the carotid bifurcation and are firmly attached, so vessel replacement may be considered.

Nevertheless, these tumours' unpredictable biological behaviour and natural history lead to atypical forms (e.g., bilateral, multi-centric, functional, and malignant). Within these, there is a sub-group of CPGs related to different syndromes (von Hippel-Lindau disease, Carney triad, etc) and diseases (thyroid cancer, thymoma, etc), [9-12]. In most cases, these manifestations involve different systems, and present two major characteristics: a) A low rate, which means medical-surgical teams have little experience of them, and b) Diagnostic and therapeutic complexity; with both situations posing a challenge for doctors and surgeons.

This review seeks to adopt a unitary approach to these rare situations that are widely distributed throughout the literature on CPGs, with the aim being to understand and highlight their idiosyncrasies of clinical, diagnostic and therapeutic interest.

Systematic Literature Review

This review involved methodological aspects of the PRISMA statement [13] for a systematic approach.

Search methods: Two researchers (FSL and BGC) and a librarian (MMB) conducted a search in Medline (through PubMed) and the Cochrane Library (through Wiley) from their first records through to the end of the search (1 November 2019). No language restrictions have been applied, nor in terms of type of publication or date of the same. The search was conducted in English.

Inclusion criteria: The following keywords (MESH terms) were used: "Carotid Body Tumour", "Carotid Paraganglioma", "von Hippel-Lindau disease", "Multiple Endocrine Neoplasia-type 2", "Neurofibromatosis-type 1", "Carney triad", "Hereditary tumor syndrome", "Inherited syndromes", "Parathyroid adenoma", "Astrocytoma", "Thyroid carcinoma", "Papillary thyroid carcinoma", "Pituitary tumours", "Acromegaly", and "Thymoma".

Exclusion criteria: a) Sporadic form to PGs, as these are the most frequent cases; b) Familiar form to PGs, relatively frequent cases, and related to PGL syndromes (PGL1 to PGL4). Our experience of the sporadic and familiar forms of CPG has recently been reported [14]; c) CPGs detected in infancy or during pregnancy, as there are recent reviews on the matter [15-19]; and d) CPGs associated with another extracranial ipsilateral carotid pathology (stenosis or aneurisms), as a recent review has been conducted by our group [20].

Data collection and analysis: A search has been made for CPGs related to form involving multiple systems - syndromes and diseases, which are to be found throughout the corresponding literature, with the aim being to highlight and understand their clinical, diagnostic and therapeutic interest.

The search found 457 potential publications, of which 229 were duplications. A reading of the titles and abstracts of the remaining 228 publications, examined separately by two researchers (FSL and BGC), led to 194 references being discarded. This meant that only 34 articles were considered relevant for our review. Following a reading of the full manuscripts, a further eight articles were discarded because they dealt with aspects that were collateral to the search's core purpose. Finally, this review considered 26 publications (Figure 1). This low number, which is in turn spread across different syndromes and pathologies, does not permit the application of criteria of meta-analysis.

Figure 1: Literature review flowchart. View Figure 1

Results

The 26 articles selected [21-46] involve a total of 37 patients with a CPG associated with different syndromes and diseases (Table 1).

Table 1: Carotid paragangliomas (CPG) related to syndromes and diseases. Literature review. View Table 1

The articles included are basically reports on individual cases (12 in Europe, 10 in the US, and one in China), and short series (one in the US, and two in Mexico). Except for two written in German and Spanish, all the others are in English. The article in German was translated in full into English.

This review is divided into two main groups: a) CPGs related to syndromes (n = 17): Five to HLD, one to MEN-2, one to NF-1, nine to the Carney triad, and one to the CSS; and b) CPGs related to other diseases/no syndromes (n = 20): Two to parathyroid adenomas, one to astrocytomas, nine to thyroid cancer, six to pituitary tumours, and two to thymomas.

Table 2 describes the characteristics by groups as follows:

Table 2: Density grades in female group. View Table 2

• Gender: Nine males/15 females. This aspect was not reported in any of the other cases (13 patients).

• Patients' average age at the time of the report: 41.9, with the younger ones in the syndromes group (29.5 vs. 46.1) (p = 0.012). No differences between genders.

• Characteristics of the CPGs: 10 bilateral cases (27%), a malignant one (2.7%) and one catecholamine secretor (2.7%).

• Synchronous or metachronous PG/PHEO (not including bilateral CPGs): 11 patients (29.7%); eight PHEOs (three of them bilateral) and 14 PGs with a different location in six patients (one patient with seven PGs and a bilateral PHEO). Greater frequency in syndromes (35.3% vs. 25%).

• Other tumours unrelated to the disease itself: Nine patients (45%), all in the group unrelated to syndromes; there were mostly adenomas, with different locations.

• Genetic study: 10 positive cases out of the 12 reported.

• Resection of the CPG: This was performed in 19 of the 22 cases reported (the three unoperated cases were as follows: One rejection of surgery, one surgery under way, and one patient deceased before surgery). The surgery performed on tumours associated with the CPG was usually sequential before or after the CPG (there are numerous cases of 3-4 sequential surgical procedures). There are only two reported cases of simultaneous surgery (CPG and thyroids).

• Mortality: Recorded in only two cases. All other cases being monitored/not reported.

Table 3 shows the high number of patients with tumours unrelated to these syndromes/diseases; including bilateral CPGs and other PGs/PHEOs and other tumours (e.g., adenomas, leiomyomas, etc). There is a difference between the two groups (p < 0.001).

Table 3: Average range ratio of high frequency and low frequency in male group. View Table 3

Discussion

PGs in general and CPGs in particular are infrequent tumours; in fact, the number of CPGs reported in Medline/PubMed does not exceed 5,000 patients [5,47]. However, despite their low rate, the PGs that affect the carotid body are the most common among those in the head and neck.

The majority of CPGs are single tumours, Types I or II of the Shamblin classification (and therefore resectable without affecting the carotid axis), non-secretory and benign; with expert treatment, this normal presentation leads to excellent results. According to Al-Mefty and Teixeira [48], the remaining CPGs are complex, with one or more of the following characteristics: Very large, attached to the carotid arteries (non-resectable or requiring vascular repair) (i.e., Shamblin's Type III), secretory (functional), multiple (including bilateral CPGs), malign, residual/recurrent, treated by radiotherapy, with adverse effects with embolization, etc. Morbidity and mortality rates are clearly different in complex CPGs compared to simple ones. This latter group includes CPGs associated with syndromes (e.g., HLD), and other pathologies (e.g. thyroid cancer), which inform this review.

While the different forms of manifestation of complex CPGs account for 1/4 of all CPGs, those associated with syndromes and diseases are so rare that they involve only a handful of individual cases or, exceptionally, short series; an estimate of their frequency could be around 0.8% of overall CPGs (the 37 cases in this review out of the 5,000 CPGs reported in the literature) or the 3% of complex CPGs (37 out of 1,250 complex CPGs).

The embryological origin of PGs is the neural crest, involving tumours in the diffuse neuroendocrine system (formerly APUD). For this reason, and although many are exceptional cases, and somewhat fewer among familiar forms, CPGs have been described associated with diverse clinical situations. The latest way of classifying head and neck PGs, which logically include CPGs, is conducted from an etiological/molecular perspective [9,12] with our interest focusing on those forms that involve multiple systems, and which are exceptionally associated with a PG (Table 4).

Table 4: Average range ratio of high frequency and low frequency in female group. View Table 4

There are, in this sense, several syndromes (HLD, MEN-2B, NF1, Carney triad and CSS) related to PG/PHEO in general and PGC in particular, whose more salient aspects are shown in Table 5. Although these syndromes cannot be grouped, it may be said that they are all rare and the majority are hereditary, and a genetic mutation has been identified as their mechanism. It may also be affirmed that clinically speaking they are defined by the appearance of different tumours, which appear in different organs, at an early stage and throughout a patient's lifetime (metachronous).

Table 5: Average value of energy in male group. View Table 5

CPGs very rarely occur in these syndromes. HLD [30,32,35,41,45] and the Carney triad [27,28,43] are the least rare situations (five and nine cases, respectively). They reflect the complexity of these associations, which prompt the need to detect the different tumours, establish therapeutic priorities, and always make joint treatment decisions with other specialisms.

A second group of pathologies associated with CPGs contains parathyroid adenomas, astrocytomas, thyroid carcinomas and pituitary tumours. These situations also involve multiple systems, although they are not associated with syndromes such as the aforementioned ones. There is currently no evidence whatsoever regarding the possible existence of some form of genetic mechanism.

The most frequent situation is the association between a CPG and thyroid papillary cancer - the most common anatomopathological form of thyroid cancer. We have found nine, with highlights being the major personal pathological antecedents (multicentric CPGs, simultaneous PHEO, tumours in other locations, etc.) which logically further complicate these patients' treatment [21,22,26,31,34,38,46]. Simultaneous surgery (thyroids and CPG) has been performed successfully on two occasions [22,24]; the resection of a CPG and a full thyroidectomy in the same successful surgical procedure has also been reported in situations involving a benign pathology of the thyroids [52]. Nevertheless, the decision to perform concomitant or sequential surgery on these patients should always be made on a case-by-case basis.

Finally, when the first mention was made in 2000 of the coexistence of a CPG and a thymoma, a situation that had not been described before, the authors wondered whether it was a random finding [40]; nevertheless, a possible common neuroectodermic origin may explain the coexistence of the CPG and multiple endocrine tumours. Despite the scant existing experience, both tumours can be successfully removed [24].

The low frequency and highly varied clinical manifestation of CPGs (biology and natural history) render these associations extremely unusual, and they clearly pose a diagnostic and therapeutic challenge for doctors. This is reflected in the experience of the Mayo Clinic (Rochester, Minnesota), which in one of the broadest PG series in the literature (236 patients, including 117 CPGs) records the following casuistry: Five PGs associated with HLD (2.1%), one PG associated with MEN-2B (0.4%), and four PGs forming part of the Carney triad (1.5%) [29].

In short, CPGs are infrequent tumours, of which approximately 25% are complex cases; they include situations that are even more exceptional (the syndromes and pathologies described in this article) with around 1% of the CPGs (3% of the complex CPGs).

The diagnostic and therapeutic strategy is crucial in these cases. The complexity of these associations, sometimes multiple and rare, means there is no diagnostic-therapeutic consensus in the literature, and decisions need to be taken on a case-by-case basis. Table 6 presents some general criteria accordingly: The mandatory need to find functional and supposedly malignant tumours, prioritising the treatment of functional tumours, and the need for interdisciplinary approaches and monitoring because of the possibility of metachronous tumours.

Table 6: Average value of energy in female group. View Table 6

Acknowledgments

To María Jesús Marcos Blázquez, from the Library of the Faculty of Medicine (University of Salamanca). Only her professionalism has allowed me to obtain hard-to-find articles in the shortest possible time.

Declarations

Consent for publication

All authors concur with the submission.

Competing interests

All authors declare no potential conflicts of interest and none of the data have been previously reported or are under consideration for publication elsewhere.

Authors' Contributions

Conception and design: FSLS, AM, JAH, RGS, MBGC.

Data collection: FSLS, MBGC.

Analysis and interpretation of results: FSLS, AM, JAH, MBGC.

Writing up article (text, tables and figures): FSLS, MBGC.

Final approval of the article: FSLS, AM, JAH, RGS, MBGC.

References

  1. Gonzalez-Orus Alvarez-Morujo RJ, Aristegui Ruiz MA, da Costa Belisario J, Martinez Guirado T, Scola Yurrita B (2015) Head and neck paragangliomas: Experience in 126 patients with 162 tumours. Acta Otorrinolaringol Esp 66: 332-341.
  2. Sevilla Garcia MA, Llorente Pendas JL, Rodrigo Tapia JP, Garcia Rostan G, Suarez Fente V, et al. (2007) Head and neck paragangliomas: Revision of 89 cases in 73 patients. Acta Otorrinolaringol Esp. 58: 94-100.
  3. Bikhazi PH, Roeder E, Attaie A, Lalwani AK (1999) Familial paragangliomas: The emerging impact of molecular genetics on evaluation and management. Am J Otol 20: 639-643.
  4. Maxwell JG, Jones SW, Wilson E, Kotwall CA, Hall T, et al. (2004) Carotid body tumor excisions: Adverse outcomes of adding carotid endarterectomy. J Am Coll Surg 198: 36-41.
  5. Robertson V, Poli F, Hobson B, Saratzis A, Ross Naylor A (2019) A systematic review and meta-analysis of the presentation and surgical management of patients with carotid body tumours. Eur J Vasc Endovasc Surg 57: 477-486.
  6. Sajid MS, Hamilton G, Baker DM (2007) A multicenter review of carotid body tumour management. Eur J Vasc Endovasc Surg 34: 127-130.
  7. Suarez C, Rodrigo JP, Mendenhall WM, Hamoir M, Silver CE, et al. (2014) Carotid body paragangliomas: A systematic study on management with surgery and radiotherapy. Eur Arch Otorhinolaryngol 271: 23-34.
  8. Shamblin WR, ReMine WH, Sheps SG, Harrison EG Jr (1971) Carotid body tumor (chemodectoma). Clinicopathologic analysis of ninety cases. Am J Surg 122: 732-739.
  9. Baysal BE (2001) Genetics of familial paragangliomas: Past, present, and future. Otolaryngol Clin North Am 34: 863-879.
  10. Baysal BE (2002) Hereditary paraganglioma targets diverse paraganglia. J Med Genet 39: 617-622.
  11. Koch CA, Vortmeyer AO, Zhuang Z, Brouwers FM, Pacak K (2002) New insights into the genetics of familial chromaffin cell tumors. Ann N Y Acad Sci 970: 11-28.
  12. Offergeld C, Brase C, Yaremchuk S, Mader I, Rischke HC, et al. (2012) Head and neck paragangliomas: Clinical and molecular genetic classification. Clinics (Sao Paulo) 67: 19-28.
  13. Hutton B, Catala-Lopez F, Moher D (2016) The PRISMA statement extension for systematic reviews incorporating network meta-analysis: PRISMA-NMA. Med Clin 147: 262-266.
  14. Lozano FS, Muñoz A, de las Heras JA, González-Porras JR (2020) Simple and complex carotid paragangliomas. Three decades of experience and literature review. Head Neck 1-13.
  15. Georgiadis GS, Lazarides MK, Tsalkidis A, Argyropoulou P, Giatromanolaki A (2008) Carotid body tumor in a 13-year-old child: Case report and review of the literature. J Vasc Surg 47: 874-880.
  16. Ifeoluwa A, Lazar I, Szovordi E, Karosi T (2017) Management of carotid body tumor in pediatric patients: A case report and review of the literature. Int J Pediatr Otorhinolaryngol 93: 47-52.
  17. Kotsis T, Christoforou P, Nastos C (2019) Carotid paraganglioma in adolescence-clinical picture-surgical technique and review of the literature. Case Rep Vasc Med 2019.
  18. Kuchakulla M, Shah AH, Armstrong V, Jernigan S, Bhatia S, (2018) Multimodal management of pediatric carotid body tumors: A systematic review and case illustrations. J Neurosurg Pediatr 23: 325-332.
  19. Wing LA, Conaglen JV, Meyer-Rochow GY, Elston MS (2015) Paraganglioma in pregnancy: A case series and review of the literature. J Clin Endocrinol Metab 100: 3202-3209.
  20. Lozano-Sanchez FS, Muñoz A, de las Heras JA, Taboada CR, García-Cenador MB (2020) Carotid paraganglioma synchronous with another Ipsilateral carotid disease: A systematic literature review. World J Vasc Surg 3.
  21. Albores-Saavedra J, Cuevas A, Luna-Olivares A, Brandt H, Rodriguez-Cuevas H (1968) Sindromes carcinoma papilar-quimiodectoma y carcinoma-rnedular-feocromocitoma. Estudio comparative Prensa Med Mex 34: 334-342.
  22. Albores-Saavedra J, Duran ME (1968) Association of thyroid carcinoma and chemodectoma. Am J Surg 116: 887-890.
  23. Ali IM, Graham C, Sanalla B, Bell D (1994) Carotid body tumor associated with hyperparathyroidism. Ann Vasc Surg 8: 595-598.
  24. Bano G, Sennik D, Kenchaiah M, Kyaw Y, Snape K, et al. (2015) A case of co-existing paraganglioma and thymoma. Springerplus 4: 632.
  25. Berg B, Biörklund A, Grimelius L, Ingemansson S, Larsson LI, et al. (1976) A new pattern of multiple endocrine adenomatosis: Chemodectoma, bronchial carcinoid, GH-producing pituitary adenoma, and hyperplasia of the parathyroid glands, and antral and duodenal gastrin cells. Acta Med Scand 200: 321-326.
  26. Bugalho MJ, Silva AL, Domingues R (2015) Coexistence of paraganglioma/pheochromocytoma and papillary thyroid carcinoma: A four-case series analysis. Fam Cancer 14: 603-607.
  27. Carney JA (1999) Gastric stromal sarcoma, pulmonary chondroma, and extra-adrenal paraganglioma (Carney Triad): Natural history, adrenocortical component, and possible familial occurrence. Mayo Clin Proc 74: 543-552.
  28. Carney JA, Sheps SG, Go VL, Gordon H (1977) The triad of gastric leiomyosarcoma, functioning extra-adrenal paraganglioma and pulmonary chondroma. N Engl J Med 296: 1517-1518.
  29. Erickson D, Kudva YC, Ebersold MJ, Thompson GB, Grant CS, et al. (2001) Benign paragangliomas: Clinical presentation and treatment outcomes in 236 patients. J Clin Endocrinol Metab 86: 5210-5216.
  30. Gross DJ, Avishai N, Meiner V, Filon D, Zbar B, et al. (1996) Familial pheochromocytoma associated with a novel mutation in the von Hippel-Lindau gene. J Clin Endocrinol Metab 81: 147-149.
  31. Huguet I, Walker L, Karavitaki N, Byrne J, Grossman AB (2013) Dandy-Walker malformation, papillary thyroid carcinoma, and SDHD-associated paraganglioma syndrome. J Clin Endocrinol Metab 98: 4595-4596.
  32. Hull MT, Roth LM, Glover JL, Walker PD (1982) Metastatic carotid body paraganglioma in von Hippel-Lindau disease. An electron microscopic study. Arch Pathol Lab Med 106: 235-239.
  33. Larraza-Hernandez O, Albores-Saavedra J, Benavides G, Krause LG, Perez-Merizaldi C, et al. (1982) Multiple endocrine neoplasia: Pituitary adenoma, multicentric papillary thyroid carcinoma, bilateral carotid body paraganglioma, parathyroid hyperplasia, gastric leiomyoma, and systemic amyloidosis. Am J Clin Pathol 78: 527-532.
  34. Lin B, Yang HY, Yang HJ, Shen SY (2019) Concomitant paraganglioma and thyroid carcinoma: A case report. World J Clin Cases 7: 656-662.
  35. Majchrzak K, Cybulski C, Bobek-Billewicz B, Majchrzak H, Lubinski J (2011) A case of carotid body paraganglioma and haemangioblastoma of the spinal cord in a patient with the N131K missense mutation in the VHL gene. Neurol Sci 32: 491-496.
  36. Nicholas RS, Quddus A, Topham C, Baker D (2015) Resection of a large carotid paraganglioma in Carney-Stratakis syndrome: A multidisciplinary feat. BMJ Case Rep 2015.
  37. Ophir D (1991) Familial multicentric paragangliomas in a child. J Laryngol Otol 105: 376-380.
  38. Papathomas TG, Gaal J, Corssmit EP, Oudijk L, Korpershoek E, et al. (2014) Non-pheochromocytoma (PCC)/paraganglioma (PGL) tumors in patients with succinate dehydrogenase-related PCC-PGL syndromes: A clinicopathological and molecular analysis. Eur J Endocrinol 170: 1-12.
  39. Petr EJ, Else T (2018) Pheochromocytoma and Paraganglioma in Neurofibromatosis type 1: Frequent surgeries and cardiovascular crises indicate the need for screening. Clin Diabetes Endocrinol 4: 15.
  40. Refior M, Mees K (2000) Coexistence of bilateral paraganglioma of the A. carotis, thymoma and thyroid adenoma: A chance finding? Laryngo-rhino-otologie 79: 337-340.
  41. Schimke RN, Collins DL, Rothberg PG (1998) Functioning carotid paraganglioma in the von Hippel-Lindau syndrome. Am J Med Genet 80: 533-534.
  42. Steely WM, Davies RS, Brigham RA (1987) Carotid body tumor and hyperparathyroidism. A case report and review of the literature. Am Surg 53: 337-338.
  43. Wintermark P, Boubaker A, Gebhard S, Meuli R, Bettschart V, et al. (2001) Adrenal mass in carney triad. International Journal on Disability and Human Development 2: 229-240.
  44. Xekouki P, Pacak K, Almeida M, Wassif CA, Rustin P, Nesterova M, et al. (2012) Succinate dehydrogenase (SDH) D subunit (SDHD) inactivation in a growth-hormone-producing pituitary tumor: A new association for SDH? The J Clin Endocrinol Metab 97: E357-E366.
  45. Zanelli M, van der Walt JD (1996) Carotid body paraganglioma in von Hippel-Lindau disease: A rare association. Histopathology 29: 178-181.
  46. Zbuk KM, Patocs A, Shealy A, Sylvester H, Miesfeldt S, et al. (2007) Germline mutations in PTEN and SDHC in a woman with epithelial thyroid cancer and carotid paraganglioma. Nat Clin Pract Oncol 4: 608-612.
  47. Lozano Sanchez FS, Munoz Herrera A (2009) Surgical treatment of carotid paragangliomas. Acta Otorrinolaringol Esp 1: 80-96.
  48. Al-Mefty O, Teixeira A (2002) Complex tumors of the glomus jugulare: Criteria, treatment, and outcome. J Neurosurg 97: 1356-1366.
  49. Gruber LM, Erickson D, Babovic-Vuksanovic D, Thompson GB, Young Jr WF, et al. (2017) Pheochromocytoma and paraganglioma in patients with neurofibromatosis type 1. Clin Endocrinol (Oxf) 86: 141-149.
  50. Carney JA (2009) Carney triad: A syndrome featuring paraganglionic, adrenocortical, and possibly other endocrine tumors. J Clin Endocrinol Metab 94: 3656-3662.
  51. Stratakis C, Carney J (2009) The triad of paragangliomas, gastric stromal tumours and pulmonary chondromas (Carney triad), and the dyad of paragangliomas and gastric stromal sarcomas (Carney-Stratakis syndrome): Molecular genetics and clinical implications. J Intern Med 266: 43-52.
  52. Garcia Alva R, Bobadilla Rosado LO, Arzola LH, Escobar Preciado M, Anaya Ayala JE, et al. (2018) A case report of a concomitant total thyroidectomy and carotid body tumor resection in a 43 year old female. Int J Surg Case Rep 53: 17-20.

Citation

Lozano-Sánchez FS, Muñoz A, las Heras JA, González-Sarmiento R, García-Cenador MB (2020) Carotid Paragangliomas Related to Form Involving Multiple Systems (Syndromes and Diseases): A Systematic Literature Review. Int J Rare Dis Disord 3:024. doi.org/10.23937/2643-4571/1710024