Departments of 1Medical Laboratory Sciences, Faculty of Allied Health Sciences and 3Pathology and 4Research & Biostatistics Unit, Faculty of Medicine, Kuwait University, Kuwait; 2Cytology Laboratory, Mubarak Al-Kabeer Hospital, Kuwait *Corresponding Author’s e-mail: r.al-awadhi@hsc.edu.kw دراسة مدى انتشار العدوى امليكروبية يف مسحات عنق الرحم يف مستشفى مبارك الكبري، الكويت يف الفرتة مابني 2014–1997 رنا العو�شي، عزة ال�شاهني، اأحالم اجلوي�رس، �شارا �شرييل جورج، برم �شارما، كو�شوم كابيال abstract: Objectives: This study aimed to examine gynaecological infectious agents observed in conventional and modified Papanicolaou cervical smears (CS) at a tertiary care hospital in Kuwait. Methods: This retrospective study analysed 121,443 satisfactory CS samples collected between 1997–2014 at the Mubarak Al-Kabeer Hospital, Kuwait. Conventional CS samples were obtained between 1997–2005, while modified CS were obtained between 2006–2014 following the introduction of ThinPrep® testing (Hologic Corp., Bedford, Massachusetts, USA). All samples were initially screened by cytoscreeners before being analysed by cytopathologists to determine the presence of specific infectious agents. Results: Overall, 8,836 (7.28%) of the cervical samples had infectious agents; of these, 62.48% were conventional and 37.52% were modified CS samples. The most frequently observed infectious agents were Candida species (76.05%), Trichomonas vaginalis (9.72%), human papillomavirus (HPV; 9.3%), Actinomyces-like organisms (3.23%), Chlamydia trachomatis (1.27%) and the herpes simplex virus (HSV; 0.43%). There were significantly more cases of Candida species, HPV-associated changes, C. trachomatis, T. vaginalis and Actinomyces-like organisms detected in conventional compared to modified CS samples (P <0.050 each). However, there was no statistically significant difference in the frequency of HSV-associated changes (P = 0.938). The presence of two infectious agents in the same sample was identified in 0.87% of samples. Conclusion: Among CS samples collected during an 18-year period, Candida species were most frequently detected, followed by T. vaginalis and HPV. The identification of potential infectious agents is a valuable additional benefit of Papanicolaou smear testing. Keywords: Cervical Smears; Papanicolaou Test; Infection; Candida; Trichomonas vaginalis; Human Papilloma Virus; Cytology; Kuwait. امللخ�ص: الهدف: هدفت هذه الدرا�شة اإىل قيا�ص مدى انت�شار العدوى امليكروبية عند الن�شاء يف املسحات الإعتيادية لعنق الرحم مقارنة بعينات اللطخات امل�شبوغة ب�شبغة البابانيكولو واملاأخوذة بطريقة م�شتحدثة يف م�شت�شفى ثالثي املرجع يف دولة الكويت. الطريقة: مت جمع معلومات تتعلق بعينات للطاخات ماأخوذة �شابقًا يف الفرتة مابني 2014–1997، يبلغ عددها 121,443 عينة لعنق الرحم يف م�شت�شفى مبارك الكبري، الكويت، حيث اأخذت اللطاخات بالطريقة الإعتيادية من عام 1997 اإىل عام 2005 يف حني اأخذت العينات بالطريقة امل�شتحدثة يف الفرتة من 2006 اإىل 2014، وذلك بعد اإدخال اختبار اللطاخات ب�رسائح ®ThinPrep، مت فح�ص العينات مبدئيًا بوا�شطة فنيني خمت�شني باخلاليا ويف نهاية الأمر اأعد التقارير اأخ�شائيي علم الأمرا�ص واخلاليا للك�شف عن وجود عدوى ميكروبات حمددة يف عينات عنق الرحم امل�شببة لأمرا�ص عند الن�شاء. النتائج: ب�شكل عام، مت ك�شف وجود عوامل ميكروبية معدية يف 8,836 عينة لعنق الرحم )%7.28(، من هذه العينات كان هناك ن�شبة %62.48 من لطاخات الطريقة الإعتيادية ون�شبة %37.52 من عينات الطريق امل�شتحدثة، وكانت حالت العدوى امللحوظة والأكرث �شيوعًا هي من اأنواع فطريات امُلبي�شة )%76.05( وجرثومة امل�شعرات املهبلية )%9.72( وفريو�ص الورم احلليمي الب�رسي )%9.30( والكائن الدقيق امل�شابه جلرثومة ال�ُشعاعي )%3.23(، وجرثومة املتدثرة احلرثية )%1.27( وفريو�ص الهرب�ص الب�شيط )%0.43(. وقد لوحظ اأن هناك حالت عدوى بعوامل فطريات امُلبي�شة وفريو�ص الورم احلليمي الب�رسي وجرثومية امل�شعرات املهبلية والكائنات امل�شابهة جلرثومة ال�ُشعاعي اأكرث ب�شكل ملحوظ يف العينات امل�شتخرجة بالطرق العتيادية مقارنة بالطريقة امل�شتحدثة )P >0.050 لكل منها(، بينما ،)P = 0.938( ل يوجد فرق ملحوظ يف عدد حالت التي تظهر تغيريات تتعلق بفريو�ص الهرب�ص الب�شيط بني طريقتي ا�شتخال�ص املسحات من بني املسحات التي مت جمعها نف�ص العينة هي%0.87. اخلال�صة: ن�شبة ازدواجية نوعني من العدوية امليكروبية يف اإ�شافة لذلك فاإن خالل مدة 18 عامًا، كانت وجود فطريات امُلبي�شة هو الأكرث �شيوعًا من بني العوامل امليكروبية املعدية الأخرى، ويليها جرثومة امل�شعرات املهبلية ثم فريو�ص الورم احلليمي الب�رسي، كما اأن ك�شف هذه العوامل امليكروبية املعدية هي اأحد الإ�شافات املهمة التي ميكن اأن ت�شاف با�شتخدام مسحات ب�شبغة البابانيكولو. احلليمي الورم فريو�ص املهبلية؛ امل�شعرات جرثومة املبي�شة؛ فطر عدوى؛ البابانيكولو؛ فح�ص الرحم؛ عنق مسحات املفتاحية: الكلمات الب�رسي؛ علم اأمرا�ص اخلاليا؛ دولة الكويت. Prevalence of Infectious Organisms Observed in Cervical Smears Between 1997–2014 at Mubarak Al-Kabeer Hospital, Kuwait *Rana Al-Awadhi,1 Azza Al-Shaheen,2 Ahlam Al-Juwaiser,2 Sara S. George,3 Prem Sharma,4 Kusum Kapila3 clinical & basic research Sultan Qaboos University Med J, August 2018, Vol. 18, Iss. 3, pp. e324–328, Epub. 19 Dec 18 Submitted 30 Oct 17 Revisions Req. 28 Dec 17, 18 Feb & 18 Mar 18; Revisions Recd. 24 Jan, 21 Feb & 22 Mar 18 Accepted 25 Mar 18 doi: 10.18295/squmj.2018.18.03.010 Rana Al-Awadhi, Azza Al-Shaheen, Ahlam Al-Juwaiser, Sara S. George, Prem Sharma and Kusum Kapila Clinical and Basic Research | e325 Worldwide, most cervical screening programmes aim to detect cervical cancer at a pre-invasive stage. However, the Bethesda System used to report gynaecological abnormalities also discloses other microscopic changes in cervical smears (CS), including inflammatory changes in epithelial cells caused by specific infectious agents.1 As such, the doc- umentation of cervical organisms represents a valuable additional benefit of cervical cancer screening using Papanicolaou (Pap) smear tests. In Kuwait, there is unfortunately no formal cervical cancer screening programme. In addition, the results of Pap smears are not well studied, with most previous research originating from one centre, the Mubarak Al- Kabeer Hospital, a tertiary care hospital which provides cytological diagnostic services to 15 hospitals, 27 clinics and multiple practitioners in Kuwait.2–5 The purpose of this study was to determine and compare the prevalence of specific infectious agents in conventional and modified CS samples received over an 18-year period at the cytology laboratory of the Mubarak Al-Kabeer Hospital. Methods This retrospective study reviewed 121,433 conventional and modified Pap CS samples received between 1997–2014 at the cytology laboratory of the Mubarak Al-Kabeer Hospital. Between 1997–2005, conventional CS samples were obtained, while modified CS samples were collected between 2006–2014 following the intro- duction of ThinPrep® testing (Hologic Corp., Bedford, Massachusetts, USA). The cervical samples were obtained from women attending the outpatient obstetrics and gynaecology departments of general hospitals and clinics in Kuwait with a wide spectrum of gynaecological complaints. All CS samples were screened and assessed for abnormalities according to the 2001 Bethesda System guidelines.1 The CS slides were initially screened by cyto- screeners before being analysed for specific infectious agents or benign or reactive cellular changes associated with inflammation by cytopathologists. Specific infectious agents included the Candida species, Trichomonas vagi- nalis, Actinomyces-like organisms, Chlamydia trach- omatis and changes associated with herpes simplex virus (HSV) and human papilloma-virus (HPV) infections. In addition, the CS samples were reported as either neg- ative for intraepithelial lesions or malignancy (NILM) or positive for atypical squamous cells, atypical glandular cells, low-grade squamous intra-epithelial lesions (LSILs) or high-grade squamous intra-epithelial lesions (HSILs).1 The presence of normal vaginal flora (long rods or Lactobacilli) or shifts in the overgrowth of mixed flora (i.e. bacterial vaginosis) were not evaluated. Data were analysed using the Statistical Package for the Social Sciences (SPSS), Version 16.0 (IBM Corp., Armonk, New York, USA). Chi-squared or Fisher’s exact tests were used to compare the proportions of infectious agents observed in the CS samples. A P value of <0.050 was considered statistically significant. Ethical approval for this study was provided by the Health Science Center of Mubarak Al-Kabeer Hospital (#VDR/EC/2310). All study procedures were performed in compliance with the ethical standards of the revised Declaration of Helsinki of 2008. Results A total of 121,443 satisfactory CS samples were received during the study period. Of these, 65,338 (53.8%) samples were conventional CS samples collected between 1997–2005 and 56,105 (46.2%) were modified Thin- Prep® CS samples (Hologic Corp.) collected between 2006–2014. Specific infectious agents were detected in 5,521 (8.45%) conventional and 3,315 (5.91%) modified CS samples, resulting in a total of 8,836 (7.28%) CS samples with infectious agents, of which 62.48% were conventional and 37.52% were modified CS samples. Overall, fewer infectious agents were detected in modified CS samples compared to conventional CS samples [Figure 1]. The most frequently identified infect- ious organisms were Candida species (76.05%), T. vaginalis (9.72%), HPV (9.3%), Actinomyces-like organ- isms (3.23%), C. trachomatis (1.27%) and HSV (0.43%). In addition, 88.16% of CS samples with infectious agents were reported to be NILM. Significantly more Candida species, HPV-associated morphological changes, C. trach- omatis, T. vaginalis and Actinomyces-like organisms Advances in Knowledge - This study identified potential infectious agents in Papanicolaou cervical smear samples obtained using two different preparatory techniques. Identifying potential infectious agents represents a valuable additional benefit of cervical smear testing. - Very few similar studies have been conducted in the Gulf Cooperative Council (GCC) region, despite the relatively high incidence of low cervical neoplasia and human papillomavirus infections. Application to Patient Care - The results of this study may impact future gynaecological care in Kuwait and other GCC countries, particularly in view of the relatively low rate of gynaecological examinations. Prevalence of Infectious Organisms Observed in Cervical Smears Between 1997–2014 at Mubarak Al-Kabeer Hospital, Kuwait e326 | SQU Medical Journal, August 2018, Volume 18, Issue 3 Table 1: Gynaecological infectious agents observed in conventional and modified cervical smears received from 1997–2014 at the Mubarak Al-Kabeer Hospital, Kuwait (N = 8,836) Cytology diagnosis Infectious organism, n (%) Total Candida species HPV Chlamydia trachomatis Trichomonas vaginalis Actinomyces-like organisms HSV NILM 7,790 (88.16) 6,536 (97.26) 0 (0) 107 (95.54) 829 (96.51) 282 (98.95) 36 (94.74) Conventional CS 4,915 (63.09) 4,041 (61.83) 0 (0) 87 (81.31) 565 (68.15) 200 (70.92) 22 (61.11) Modified CS 2,875 (36.91) 2,495 (38.26) 0 (0) 20 (18.69) 264 (31.85) 82 (29.08) 14 (38.89) P value <0.001 <0.001 - <0.001 0.002 0.007 0.944 AGCs 19 (0.22) 15 (0.22) 0 (0) 0 (0) 3 (0.35) 1 (0.35) 0 (0) Conventional CS 13 (68.42) 10 (66.67) 0 (0) 0 (0) 2 (66.67) 1 (100) 0 (0) Modified CS 6 (31.58) 5 (33.33) 0 (0) 0 (0) 1 (33.33) 0 (0) 0 (0) P value 0.379 >0.999 - - 0.585 - - ASCs 139 (1.57) 117 (1.74) 0 (0) 3 (2.68) 18 (2.10) 1 (0.35) 0 (0) Conventional CS 88 (63.31) 71 (60.68) 0 (0) 3 (100) 13 (72.22) 1 (100) 0 (0) Modified CS 51 (36.69) 46 (39.32) 0 (0) 0 (0) 5 (27.78) 0 (0) 0 (0) P value 0.007 0.267 - - 0.546 - - LSILs 832 (9.42) 50 (0.74) 773 (94.04) 0 (0) 7 (0.81) 0 (0) 2 (5.26) Conventional CS 467 (56.13) 34 (68) 428 (55.37) 0 (0) 4 (57.14) 0 (0) 1 (50) Modified CS 365 (43.87) 16 (32) 345 (44.63) 0 (0) 3 (42.86) 0 (0) 1 (50) P value 0.686 0.101 0.196 - 0.755 - 0.584 HSILs 56 (0.63) 2 (0.03) 49 (5.96) 2 (1.79) 2 (0.23) 1 (0.35) 0 (0) Conventional CS 38 (67.86) 2 (100) 33 (67.35) 2 (100) 1 (50) 0 (0) 0 (0) Modified CS 18 (32.14) 0 (0) 16 (32.65) 0 (0) 1 (50) 1 (100) 0 (0) P value 0.014 - 0.669 - 0.812 - - Total 8,836 (100) 6,720 (76.05) 822 (9.3) 112 (1.27) 859 (9.72) 285 (3.23) 38 (0.43) Conventional CS 5,521 (62.48) 4,158 (61.88) 461 (56.08) 92 (82.14) 585 (68.10) 202 (70.88) 23 (0.03) Modified CS 3,315 (37.52) 2,562 (38.13) 361 (43.92) 20 (17.86) 274 (31.90) 83 (29.12) 15 (0.02) P value <0.001 0.046 <0.001 <0.001 <0.001 0.003 0.938 HPV = human papillomavirus; HSV = herpes simplex virus; NILM = negative for intraepithelial lesions and malignancy; CS = cervical smears; AGCs = atypical glandular cells; ASCs = atypical squamous cells; LSILs = low-grade squamous intraepithelial lesions; HSILs = high-grade squamous intraepithelial lesions. Figure 1: Prevalence of infectious agents observed in conventional and modified cervical smears received from 1997–2014 at the Mubarak Al-Kabeer Hospital, Kuwait (N = 8,836). CS = cervical smear. Rana Al-Awadhi, Azza Al-Shaheen, Ahlam Al-Juwaiser, Sara S. George, Prem Sharma and Kusum Kapila Clinical and Basic Research | e327 were detected in conventional compared to modified CS samples (P <0.050). No statistically significant difference was found between the two types of CS samples in relation to HSV (P = 0.938). A greater number of cases with HPV-associated morphological changes were detected in LSIL samples than HSIL samples (94.04% versus 5.96%); however, this difference was not significant (P = 0.196 and 0.669, respectively). Nevertheless, when the number of cases with HPV-associated morpholog- ical changes in the LSIL and HSIL categories were comb- ined, there was a significant difference between modified and conventional CS samples (P <0.001) [Table 1]. A combination of two infectious agents was observed in 77 cases (0.87%), of which 67.53% were conventional and 32.47% were modified CS samples. Among the conv- entional CS samples, 84.62% involved a combination of Candida species and another organism. Overall, two infectious agents were most frequently detected in either NILM (49.35%) or LSIL (48.05%) samples [Table 2]. Discussion In this study, common gynaecological infectious agents were encountered in 7.28% of CS samples collected between 1997–2014 at the Mubarak Al-Kabeer Hospital. In comparison, a previous study at the same hospital identified specific infectious agents in 15.2% of satisf- actory CS samples collected between 2002–2007.4 These findings therefore indicate a 52.11% decrease in the number of specific organisms detected. This may be due to the implementation of the ThinPrep® technique (Hologic Corp.), which was only fully achieved in the last nine years of the study period. This assumption is supported by the results of the current study which indicated a drop in the number of specific infectious agents detected in modified compared to conventional CS samples (37.52% versus 62.48%). Previous research has indicated that the incidence of infectious organisms in Kuwait is 4.4% for samples that show cervical cancer or precancerous changes.5 This rate is similar to that of the low invasive cervical carcinoma risk estimate (4/100,000 cases annually) for Kuwait and elsewhere in Asia.6 Additionally, Malkawi et al. reported specific inflammation in only 4.8% of CS samples in Jordan.7 In the current study, the most commonly identified infectious agents were Candida species, followed by T. vaginalis, HPV, Actinomyces-like organisms, C. trachom- atis and HSV. A similar pattern was noted in other studies, wherein fungal agents were most prevalent, followed by Trichomonas species.8–12 As mentioned earlier, the number of specific infectious agents detected was lower in modified compared to conventional CS samples; this reduction was noted in almost all infectious agents, except HSV. This finding has been supported by other researchers.8,13 At the Mubarak Al-Kabeer Hospital, the cytology laboratory employs in-house trained primary screeners whose work is monitored by senior checkers and a chief technician and all slides are signed off by medical practitioners, regardless of abnormalities. As such, differ- ences in the detection rate of infectious agents in the present study were probably not due to the experience Table 2: Samples with a combination of two infectious agents observed in conventional and modified cervical smears rec- eived from 1997–2014 at the Mubarak Al-Kabeer Hospital, Kuwait (N = 77) Cytology diagnosis Combination of infectious organisms, n (%) Total Conventional CS (n = 52) Modified CS (n = 25) NILM 38 (49.35) 26 (50) 12 (48) Candida species and Trichomonas vaginalis 13 (34.21) 9 (34.62) 4 (33.33) Candida species and Actinomyces- like organisms 13 (34.21) 8 (30.77) 5 (41.67) Candida species and Chlamydia trachomatis 4 (10.53) 4 (15.38) 0 (0) Candida species and HSV 4 (10.53) 3 (11.54) 1 (8.33) Trichomonas vaginalis and Actinomyces- like organisms 3 (7.89) 2 (7.69) 1 (8.33) Trichomonas vaginalis and HSV 1 (2.63) 0 (0) 1 (8.33) ASCs 1 (1.30) 1 (1.92) 0 (0) Candida species and Trichomonas vaginalis 1 (100) 1 (100) 0 (0) LSILs 37 (48.05) 24 (46.15) 13 (52) HPV and Candida species 31 (83.78) 20 (83.33) 11 (84.62) HPV and Trichomonas vaginalis 4 (10.81) 2 (8.33) 2 (15.38) HPV and Actinomyces-like organisms 1 (2.7) 1 (4.17) 0 (0) HPV and HSV 1 (2.7) 1 (4.17) 0 (0) HSILs 1 (1.3) 1 (1.92) 0 (0) HPV and Trichomonas vaginalis 1 (100) 1 (100) 0 (0) CS = cervical smears; NILM = negative for intraepithelial lesions and malign- ancy; HSV = herpes simplex virus; ASCs = atypical squamous cells; LSILs = low -grade squamous intraepithelial lesions; HPV = human papillomavirus; HSILs = high-grade squamous intraepithelial lesions. Prevalence of Infectious Organisms Observed in Cervical Smears Between 1997–2014 at Mubarak Al-Kabeer Hospital, Kuwait e328 | SQU Medical Journal, August 2018, Volume 18, Issue 3 of the screeners. In addition, the cost of preparation was unlikely to have influenced the results as both convent- ional and modified samples were collected and examined free of charge. Furthermore, the number of hospitals and clinics providing conventional or modified CS services has remained the same for over 20 years, with all centres utilising both techniques. Nevertheless, the difference in the number of infectious agents detected in convent- ional and modified CS samples could be due to technical aspects related to the fixative used or the preparation of the modified samples, which may have caused the screener to overlook infectious agents. The fixative could cause shrinkage and therefore the inaccurate identif- ication of organisms in the sample. In addition, filtration could result in a cleaner background and a reduction in inflammatory cell features.13 Few studies have focused on HPV distribution in Middle Eastern countries. In the current study, most HPV infections were detected in LSIL samples. In a prev- ious study of modified CS samples collected from women with abnormal cervical cytology in Kuwait, 89% and 67% of samples diagnosed as LSIL and HSIL, respectively, were infected with HPV type 16, the most common high- risk genotype.14 Another study in Kuwait also showed high-risk HPV DNA in women with squamous intra- epithelial lesions, indicating that the viral load was directly related to the severity of the cervical lesions.15 Conclusion This study described the prevalence of specific infectious agents identified in conventional and modified CS samples collected over an 18-year period at the Mubarak Al-Kabeer Hospital. The identification of potential infectious agents represents a valuable additional benefit of cervical sampling using Pap smear tests; however, it cannot substitute other definitive diagnostic methods. c o n f l i c t o f i n t e r e s t The authors declare no conflicts of interest. f u n d i n g No funding was received for this study. References 1. Solomon D, Davey D, Kurman R, Moriarty A, O’Connor D, Prey M, et al. The 2001 Bethesda System: Terminology for reporting res- ults of cervical cytology. JAMA 2002; 287:2114–19. doi: 10.1001/ jama.287.16.2114. 2. Luthra UK, Chishti M, Dey P, Jolly SV, Abdulla M, Das DK, et al. Performance of monolayered cervical smears in a gynecology outpatient setting in Kuwait. Acta Cytol 2002; 46:303–10. doi: 10.11 59/000326726. 3. Kapila K, George SS, Al-Shaheen A, Al-Ottibi MS, Pathan SK, Sheikh ZA, et al. Changing spectrum of squamous cell abnorm- alities observed on Papanicolaou smears in Mubarak Al-Kabeer Hospital, Kuwait, over a 13-year period. 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