ABSTRACT
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f o r d i a g n o si s o f p a r o t i d g l a n d m a sses: a
clinicopat hological st udy of 114 pat ient s
Jens Kristjan GUDMUNDSSON2, Aida AJAN1, Jahan ABTAHI1
1- Linköping University Hospital, Department of Oral and Maxillofacial Surgery, Linköping, Sweden. 2- Eskilstuna Hospital, Department of Otorhinolaryngology, Eskilstuna, Sweden.
Corresponding address: Jahan Abtahi - Department of Oral and Maxillofacial Surgery - Linköping University Hospital - Linköping - Sweden - phone: +46 (0)70 756 69 97 - e-mail: jahan.linkoping@gmail.com - e-mail: jahan.abtahi@regionostergotland.se
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bj ect ive: Fine- needle aspirat ion cyt ology is a valuable m et hod for preoperat ive assessm ent of head and neck t um ors. However, it s accuracy in det ect ion of salivary gland m asses is cont roversial com pared wit h ot her m et hods. The aim of t his work was WRHYDOXDWHWKHHIIHFWLYHQHVVDQGDFFXUDF\RI¿QHQHHGOHDVSLUDWLRQF\WRORJ\)1$&LQ t he diagnosis of parot id gland m asses. Mat erial and Met hods: Over a 10-year period, 126 parot id gland m asses were resect ed. Ret rospect ive chart reviews of 114 pat ient s ZHUHSHUIRUPHG7KHUHVXOWVRI)1$&DQG¿QDOKLVWRORJLFDOGLDJQRVLVZHUHFRPSDUHGDQG t he accuracy of FNAC was det erm ined. Result s: Final hist ological evaluat ion revealed 11 m alignant t um ors and 103 benign lesions. Pleom orphic adenom a was t he m ost com m on neoplasm ( 63% ) , followed by Warthin’s tum or ( 17.5% ) . The sensitivity of FNAC in detecting PDOLJQDQWWXPRUVZDVDQGWKHVSHFL¿FLW\ZDV3RVLWLYHSUHGLFWLYHYDOXH339 was 73% and negat ive predict ive value ( NPV) was 97% . The overall accuracy of FNAC in detecting parotid m asses was 95% . False- negative diagnosis was found in m ucoepiderm oid carcinom a, acinic cell carcinom a, and epithelial- m yoepithelial carcinom a whereas there was false- posit ive diagnosis in cases of pleom orphic adenom a and norm al parot id gland t issue. Conclusion: FNAC is a reliable m inim ally invasive diagnost ic m et hod wit h a high sensit ivit y in diagnosis of lesions in parot id glands. The sensit ivit y of det ect ion of m alignant t um ors in parot id glands was low due t o t he biopsy t echnique used, and depended on t um or locat ion. 3RVWRSHUDWLYHFRPSOLFDWLRQVGHFUHDVHGDIWHUVXSHU¿FLDOSDURWLGHFWRP\Keywords: Fine- needle. Cit ology. Parot id disease. Diagnosis. Biopsy.
INTRODUCTION
Salivary gland tum ors are a m orphologically and clinically diverse group of neoplasm s, which m ay
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challenges. I n t he west ern world, t he est im at ed overall incidence is approxim at ely 2.53.0 cases
per 100,000 per year21. Malignant salivary gland
neoplasm s account for m or e t han 0. 5% of all m alignancies and approxim at ely 35% of all head and neck cancers21. I n Sweden, t he incidence of parot id gland t um ors is 0.77 cases per 100,000
w om en an d 1 . 1 6 cases p e r 1 0 0 , 0 0 0 m en . I n
com parison, t he overall incidence of salivary gland t um ors during t he sam e year was 0.99 in wom en
and 1.49 in m en7. Several im aging m odalit ies have
been used for diagnosis of parotid m asses, including magnet ic resonance im aging ( MRI ) and com put ed t om ography (CT)16,28. MRI pr ov ides anat om ical
inform at ion about parot id t um or locat ion and can be a useful t ool t o det erm ine whet her t he m ass is benign or m alignant16. Fine- needle aspirat ion
m icropart icles of t issue for m orphological analysis. Com pared with histological results, a concordance of
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a sensit ivit y of 84% , and a diagnost ic accuracy of 94%1. However, the value of FNAC for the diagnosis of parot id gland m asses. has been quest ioned due to its low sensitivity regarding m alignancy, variation in r epor t ed r esu lt s, an d t h e belief t h at m ost parot id m asses require surgery in any case17,20. Tum ors of t he parot id gland can be rem oved by
VXSHU¿FLDOSDURWLGHFWRP\DQGWRWDOSDURWLGHFWRP\10. Enucleat ion of parot id gland m asses is not t he
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risk of recurrence29. Several com plicat ions have been associat ed wit h parot id gland surgery, such as facial nerve dist urbance, Frey’s syndrom e, and great auricular nerve parest hesia9,27. Fact ors t hat affect facial nerve dysfunct ion include m alignant t um ors, lesion sizes, operat ing t im e, and t ype of
SDURWLGHFWRP\WRWDOYVVXSHU¿FLDO2,3,9,27. The aim of t his st udy was t o evaluat e t he diagnost ic value of FNAC in det ect ion of parot id gland t um ors at our clinic ( especially for det ect ion of m align lesions) .
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a ret rospect ive st udy. I n addit ion, clinical out com e of surgery and post operat ive param et ers were also evaluat ed.
MATERIAL AND METHODS
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Eskilst una Hospit al provides healt hcare t o m ore t han a quart er of a m illion inhabit ant s. Over a 10-year period ( January 2003 t o Decem ber 2014) , m asses in the salivary gland tum ors of 126 patients were resect ed. Pat ient s t reat ed bet ween January and Decem ber 2006 were excluded due t o an error in t he pat ient s’ elect ronic m edical records. The m edical records of 12 patients could not be located, so 114 pat ient s ( 61 m ales and 53 fem ales) wit h a m ean age of 56.4 years ( range 18-85 years) were included in t his st udy for furt her invest igat ion. Three surgeons perform ed the surgical procedures. I nt raoperat ive facial nerve m onit oring wit h a nerve st im ulat or was used in all cases. We used our depart m ent’VHOHFWURQLFGDWDEDVHDQGFOLQLFDO¿OHV
t o ident ify all pat ient s who were diagnosed wit h a m ass in t he parot id gland. The I CD- 10 codes D11.0, D11.9, C08.8, C08.9, and C07.9 were used t o ident ify subj ect s from t he dat abase; t his was
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t he diagnosis.
I nform at ion regarding pat ient dem ographics, FNAC r esu lt s, an d f in al h ist ological diagn osis result s was evaluat ed. The post operat ive out com e, including post operat ive infect ion and hem at om a,
facial nerve dist urbance, and Frey’s syndrom e was also regist ered. The pr eoperat ive FNAC r esult s
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from t he surgical specim ens. Dat a on age, gender, t u m or t y p e, an d p ost op er at iv e com p licat ion s ( facial nerve dist urbance, post operat ive infect ion, Frey’s syndrom e, and hem at om a) were collect ed from t he clinical records. Facial nerve dist urbance w as classified int o four cat egor ies: ( 1 ) none, ( 2) t ransient ( 02 m ont hs) , ( 3) less t ransient ( 212 m ont hs) , and ( 4) perm anent . Pat ient s wit h radiologically v er ified and FNAC- v er ified cy st s in par ot id glands w er e excluded. Pat ient s w it h inconclusive FNAC result s were also excluded.
Fine-needle aspiration cytology technique
FNAC was perform ed using a 22- gauge needle at t ached t o a 10- m L plast ic syringe m ount ed on a syringe holder for a single hand grip. The aspirat ed
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w it hout using local anest hesia. The num ber of aspirat ions varied bet ween 2 and 3, depending on the accessibility of the tum or. FNAC air-dried sm ears were st ained wit h Giem sa st ain and t he slides were t hen exam ined under a light m icroscope ( Olym pus Cx 31, Nishi Shinj uk u 2- chom e, Tok yo, Japan) , and result s were report ed according t o t he World Healt h Organizat ion guidelines regarding parot id gland neoplasm .
Al l FNAC sa m p l e s a n d t u m o r sp e ci m e n s w e r e a n a l y z e d b y t h e s a m e l a b o r a t o r y ( Unilabs Laborat or iem edicin at Mälarsjuk huset , diagnost ikcent rum Eskilst una, Sweden) . Pat ient s
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t o t he head and neck cancer cent er at Örebro Universit y Hospit al for furt her cancer t reat m ent .
The cyt ology laborat ory provided t hree t ypes of hist ological result s: ( 1) benign aspirat ion cyt ology, ( 2) suspicious or m alignant aspirat ion cyt ology, an d ( 3 ) n on - con t r ib u t or y asp ir at ion cy t olog y ( indet erm inat e or inconclusive) .
Statistics
FNAC- based diagnoses w er e com par ed w it h d i a g n o ses f r o m h i st o l o g i ca l ex a m i n a t i o n o f specim ens. We calculat ed t he sensit ivit y regarding t he presence of m alignancy ( t rue posit ive/ t rue
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absence of m alignancy (true negative/ true negative + false posit ive) , posit ive predict ive value ( PPV) ( t r u e posit iv e/ t r u e posit iv e + f alse posit iv e) , negat ive predict ive value ( NPV) ( t rue negat ive/ t r ue negat ive + false negat ive) , and accuracy of FNAC ( t r ue posit ive + t r ue negat ive/ t ot al) .
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t he agreem ent bet ween t he FNAC- based diagnosis
and the biopsy- based diagnosis. Statistical analysis
was carried out using SPSS ( version 12.0) .
RESULTS
Demographic and histological outcome
One hundr ed four t een pat ient s w it h par ot id m asses (61 m ales and 53 fem ales) with a m ean age of 56.4 years ( range 1885 years) were included in t he st udy. Mean durat ion of follow- up was 66 m onths (range 3132 m onths). The fem ale-to-m ale rat io was approxim at ely 1 t o 1.1. Tum ors were
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cases, 76% ), but 27 tum ors (24% ) were in the deep parot id lobe. FNAC of t he deep port ion of parot id m ass was conduct ed in 7 cases ( 6% ) , whereas in 20 cases ( 17.5% ) t his procedure was perform ed using ult rasound- guided biopsy.
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parotidectom y (n= 91; 79.8% ). Total parotidectom y
was perform ed in 18 cases wit h deep- lobe t um ors
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parot idect om y was perform ed in 2 cases ( 1.7% ) . Final hist ological evaluat ion revealed 11 m alignant t um ors ( 9.6% ) and 103 benign lesions ( 90.3% ) . Pleom or ph ic aden om a w as t h e m ost com m on neoplasm ( 72 cases; 63% ) , followed by Wart hin’s t um or ( 20 cases; 17.5% ) .
Accuracy oI¿ne-needle aspiration cytology
FNAC was perform ed in 94 pat ient s ( 4 t um ors in deep por t ions and 90 t um or s in super ficial parot id glands) . I n 20 cases ( 21% ) wit h t um ors locat ed in deep par t s of par ot id glands, FNAC was com plem ent ed w it h ult rasound. I n 108 of
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overall accuracy of FNAC for parot id m asses was est im at ed t o be 95% . False- negat ive diagnoses were found in m ucoepiderm oid carcinom a ( n= 1; 1.4% ) , acinic cell carcinom a ( n= 1; 1.4% ) , and
Accuracy of FNAC vs. FHD
Location S/D
Method FNAC/UGB
Diagnosed as cancer (false positive)
Correctly diagnosed (as benign)
Total
FHD Benign
No. No. No. % No. % No.
Pleomorphic adenoma 6,4 8,25 2 2.7 72 97.3 74 Warthin’s tumor 19/1 19/1 0 0 20 100 100 Normal parotid tissue 2 3/0 1 1.4 2 66.6 20 Basal cell adenoma 2 2 0 0 3 100 3
Sialoadenitis 1/0 1/0 0 0 1 100 1
Benign oncocytoma 0/1 0/1 0 0 1 100 1 Lymphatic tissue 1/0 1/0 0 0 1 100 1
Total 89/14 92/11 3 100 103
Location S/D
Method FNAC/UGB
Diagnosed as benign (false negative)
Correctly diagnosed (as malignant)
Total
FHD Malignant
No. No. No. % No. % No.
0DOLJQL¿HG 0/2 0/2 0 0 2 100 2
pleomorphic adenoma
Acinic cell carcinoma 0/1 1/0 1 1.4 0 0 1 Mucoepidermoid carcinoma 0,5 2 1 1.4 2 66.6 3
Lymphoma 1/0 1/0 0 0 1 100 1
Epithelial-myoepithelial 0/1 1/0 1 1.4 0 0 1 Carcinoma
Adenocarcinoma 0/3 0/3 0 0 3 100 3
Total 3 8 11
All cases 2/9 5/6 6 108 114
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epit helial- m yoepit helial carcinom a ( n= 1; 1.4% ) whereas t here were false- posit ive diagnoses in cases of pleom orphic adenom a ( n= 2; 2.7% ) and in norm al parot id t issue ( n= 1; 1.4% ) ( Table 1) .
FNAC result s did not correlat e wit h hist ology in 6 specim ens ( 6.4% ) , 3 of which were benign ( 3% ) and 3 m alignant ( 3% ) . Final hist ological evaluat ion show ed 11 m alignant t um or s ( 8 t um or s w er e
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as benign) . Thus, FNAC failed t o give a correct cytological result in 3 cases ( 27.3% ) . The sum m ary
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73% ( 95% CI 3994) and 97% ( 95% CI 9299) , respect ively. The PPV was 73% and t he NPV was 97% ( Table 2) . The kappa st at ist ic for t he degree of agreem ent between FNAC and histological results was 0.94.
I n sum m ary, the study showed low sensitivity for m alignant t um ors. However, regarding t he locat ion of t um ors, t hese t hree false- negat ive cases were locat ed in t he deep port ion of t he parot id gland and t hey were diagnosed by FNAC wit hout ult rasound-guided biopsy.
Surgical outcome and postoperative complications
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lobe ( 87 cases, 76% ) , but 27 ( 24% ) were in t he deep lobe of t he parot id gland. The m ost com m on com plication of parotid gland surgery was transient facial nerve palsy. Of 114 pat ient s, 39 ( 34% ) had a m ild t ransient palsy, 9 ( 7.9% ) had a t ransient palsy last ing m ore t han 2 m ont hs, and only one pat ient ( 0.9% ) had perm anent facial nerve palsy at 1-year follow- up. Of 39 pat ient s wit h short- t erm
facial nerve weakness ( last ing 02 m ont hs) , 21 ( 53.8% ) had t um ors locat ed in t he deep parot id lobe. Post operat ive infect ion was found in 7 cases ( 5.8% ) . Nine pat ient s ( 7.5% ) had a recurrence of t he t um or, 1 pat ient ( 0.8% ) had hem orrhage, and 3 pat ient s ( 2.5% ) developed Frey’s syndrom e.
DISCUSSION
FNAC is a sim ple, inexpensive, and at raum at ic m et hod for preoperat ive assessm ent of t um ors, lym ph nodes, and other lesions in the head and neck. I t is a safe procedure requiring m inim al equipm ent, wit h a very low risk of cancer cell im plant at ion11,25. Fine- needle aspirat ion of parot id glands m ay lead
WRKHPRUUKDJHIDFLDOQHUYHLQMXU\DQG¿EURVLV5. I nfarct ion or m et aplast ic t ransform at ion of benign t um or has also been m ent ioned in t he lit erat ure8. I n t his st udy, t here were a few cases of infect ion ( 5.8% ) , hem orrhage ( 0.8% ) , and Frey’s syndrom e ( 2.5% ) as a result of FNAC of t he parot id m ass lesions. No long- t erm facial nerve dysfunct ion was observed 1 year aft er surgery.
Several im aging m odalit ies have been used for diagnost ics of parot id m asses, including CT-scan, MRI , and ult rasound- guided cor e needle biopsy ( USCB)15,16,28. CT- scan and MRI pr ov ide
inform at ion about size and locat ion of t he t um or. However, com paring t hese t wo m et hods, CT- scan accurately assesses parotid lesions while MRI shows t he relat ionship t o adj acent st ruct ures bet t er16,28. I n a clinical st udy by I nohara, et al.16 ( 1993) , t he relat ive value of FNAC and MRI in relat ion t o t he differ ent ial diagnosis of benign and m alignant parot id m ass lesions was invest igat ed. Eight y- one
Reliability of FNAC
Kappa Value (%) FRQ¿GHQFHLQWHUYDO
Lower limit Upper limit
Sensitivity 73% 39% 94% 0.947
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Positive predictive value 73% 39% 94% Negative predictive value 97% 92% 99%
Correlation between FNAC and FHD
Final histological diagnosis, FHD
Cytological diagnosis, FNAC Malignant Benign Total
Malignant 8 (TP) 3 (FP) 11
Benign 3 (FN) 100 (TN) 103
Total 11 103 114
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positive; FN, false negative.
pat ient s wit h parot id m ass lesions ( 60 benign and 21 m alignant ) who had undergone FNAC and MRI preoperat ively were ret rospect ively reviewed. The
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MRI were 90% / 95% / 94% and 81% / 92% / 89% , respect ively, and t he com binat ion of FNAC and MRI conferred no diagnost ic advant age over eit her m odality alone14. Haldar, et al.13 (2015) reported the largest series of patients with parotid neoplasm who underwent USCB. One hundred t wenty specim ens were analyzed wit h FNAC, 313 were analyzed wit h USCB, and 259 surgical specim ens were analyzed
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of FNAC were 70% and 89% , respect ively, and
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by ot hers15.
Th e im p or t an ce of FNAC in d ist in g u ish in g m alignant parot id m ass lesions from benign ones h as b een in v est ig at ed b y sev er al au t h or s1 , 1 9. Despit e t he sim plicit y of t he m et hod, t he accuracy of FNAC varies depending on t he precision and experience of pat hologist s2'LDJQRVWLFGLI¿FXOWLHV
wit h FNAC are m ost com m on in lesions involving pleom orphic adenom a, basal cell adenom a, low-grade m ucoepiderm oid carcinom a, and acinic cell carcinom a30RUHRYHUWKHGLDJQRVLVLVPRUHGLI¿FXOW in low- grade m ucoepiderm oid carcinom as where thick m ucinous liquid is seen in the background with a paucicellular sm ear3.I n such cases, m alignant t um ors are m ist akenly report ed as benign lesions3. This occurred wit h one of our pat ient s wit h a t um or in t he deep port ion of t he parot id gland ( Figure 1) . The m alignant t um or was assessed t o be a benign t um or. Pleom orphic adenom a was one of t he m ost com m on benign t um ors in t his st udy. Figure 2 shows cyt ological im ages of pleom orphic adenom a wit h it s charact erist ic biphasic pat t ern, com p r isin g ep it h elial/ m y oep it h elial cells an d
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I n t his st udy, of 103 cases of benign t um or, 100 cases w er e diagnosed using FNAC; of 11 m alignant cases, 8 were diagnosed wit h FNAC. The overall accuracy of FNAC for parot id m asses was est im at ed t o be 95% , which is in t he sam e range as in pr ev ious st udies4, 12, 22- 24, 30. False- negat iv e
Figure 1- A low-grade mucoepidermoid carcinoma with thick mucinous material, intermediate cells, and only rare mitotic
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Figure 2- Patient with a pleomorphic adenoma with an epithelial cell component, a myoepithelial cell component, and a
diagnosis was found in m ucoepiderm oid carcinom a ( n= 1; 1.4% ) , acinic cell carcinom a ( n= 1; 1.4% ) , an d epit h elial- m y oepit h elial car cin om a ( n = 1 ; 1.4% ) , and t here was false- posit ive diagnosis in cases of pleom orphic adenom a ( n= 2; 2.7% ) and in norm al parot id t issue ( n= 1; 1.4% ) . Diagnosis of
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due t o it s ext rem e m orphological het erogeneity; it m ay be m isdiagnosed as Warthin’s tum or or m ucous ret ent ion cyst s.
A r ev iew of t h e lit er at u r e sh ow ed a FNAC sen sit iv it y r an g in g f r om 5 4 % t o 9 2 % an d a
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t um ors account for approxim at ely 3% of head and neck t um ors and 80% of salivary gland t um ors7,21. I n this study, the incidence of pleom orphic adenom a and Wart hin’s t um or was est im at ed t o be 65%
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h ist ological diagn osis in 9 8 % of pleom or ph ic adenom as and in 100% of Wart hin’s t um ors.
CONCLUSION
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m alignant parot id gland t um ors, and provides t he surgeon wit h valuable inform at ion in preoperat ive diagnost ics. I n t his st udy, t he sensit ivit y of FNAC in det ect ion of m alignant t um ors was low due t o t he biopsy t echnique used, which depended on t he locat ion of t he t um or. However, in cases where ultrasound guidance was used, 100% accuracy was achieved.
ACKNOWLEDGEMENTS
This st udy was support ed by t he Depart m ent of Or al an d Max illof acial Su r g er y, Lin k öp in g University Hospital, Sweden and the Departm ent of Ot orhinolaryngology, Eskilst una Hospit al, Sweden.
Funding
There was no funding.
ConÀicts oI interests
Non e of t h e au t h or s h av e any fin an cial or
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dat a and conclusions present ed in t his m anuscript .
Ethical approval
Th e st u d y w as ap p r ov ed b y t h e Reg ion al Com m it t ee f or Et h ics in St ock h olm , Sw ed en ( 2015/ 1028- 31/ 1) . We also received perm ission by t he aut horit ies t o review t he pat ient s’ m edical records.
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Al Khafaji, et al.2 (1998) 154 82 86 Stewart, et al.26 (2000) 341 92 100
Zbaren, et al.30 (2001) 228 64 95
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