Anal Cancer and Anal Intraepithelial Neoplasia Risk among Patients Treated for HPV-Related Gynecological Diseases—A Systematic Review
Abstract
:1. Introduction
2. Materials and Methods
2.1. Search Strategy and Information Sources
2.2. Study Selection
2.3. Inclusion and Exclusion Criteria
2.4. Data Extraction and Synthesis
2.5. Risk of Bias
3. Results
3.1. Search Results
3.2. Study Characteristics
3.3. Data Extraction and Synthesis Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
AC | Anal cancer |
AIN | Anal intraepithelial neoplasia |
CC | Cervical cancer |
CIN | Cervical intraepithelial neoplasia |
Cl | Confidence level |
HPV | Human papillomavirus |
HPV-RGD | HPV-related gynecological diseases |
IR | Incidence risk |
OR | Odds ratio |
PY | Person–years |
SD | Standard deviation |
SIR | Standardized incidence ratio |
VaC | Vaginal cancer |
VaIN | Vaginal intraepithelial neoplasia |
VIN | Vulvar intraepithelial neoplasia |
VC | Vulvar cancer |
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No. | Authors and Year of Publication | Geographic Location | Study Design | Sample Size | Period of Time Analyzed | The Type of Primary Cancer/Precancer Lesion | Median Age of Participants | Number of AIN/AC | Increased Risk | Risk of Bias |
---|---|---|---|---|---|---|---|---|---|---|
1. | Acevedo-Fontánez et al. (2018) [16] | Puerto Rico | Retrospective, population-based cohort study | 9489 | 1987–2013 | 8039 CC 1378 VC 773 VaC | 46, CC 70, VC 67, VaC | 14 AC after CC 3 AC after VC 1 AC after VaC | AC after CC: SIR = 1.8 (95% Cl: 0.9–3.4) AC after VC and VaC: SIR = 2.9 (95% Cl: 0.8–7.5) | L |
2. | Chaturvedi et al. (2007) [17] | Denmark, Finland, Norway, Sweden, and USA * | Retrospective, population-based cohort study | 27,466 | 1973–2001 | 27,466 CC ** | 48.6 | NI | AC after CC: SIR = 3.12 (95% Cl: 1.88–4.88) | L |
3. | Ebisch et al. (2017) [18] | Netherlands | Retrospective, population-based cohort study | 89,018 | 1990–2015 | 89,018 CIN 3 | 36 | 73 AC 80 AIN 3 | AC after CIN 3: SIR = 3.85 (95% CI: 2.32–6.37) AIN 3 after CIN 3: SIR= 6.68 (95% CI: 3.64–12.25) | L |
4. | Edgren et al. (2007) [19] | Sweden | Retrospective, population-based cohort study | 125,292 | 1968–2004 | 125,292 CIN 3 | 35 | 131 AC | AC after CIN 3: SIR = 4.68 (95% Cl: 3.87–5.62) | L |
5. | ElNaggar et al. (2013) [20] | Memphis, Tennessee (USA) | Prospective, cross-sectional study | 272 | 2006–2010 | CIN 1 29 CIN 2 16 CIN 3/CIS 41 VIN 1 46 VIN 2 16 VIN 3/CIS 69 VaIN 1 34 VaIN 2 13 VaIN 3/CIS 8 = 272 | 39 | 64 AIN (36 stage 1, 6 stage 2, 22 stage 3) | 48 (36.4%) had VIN, 10 (18.2%) had VaIN, and 13 (14.4%) had CIN | H |
6. | Evans et al. (2003) [21] | Southeast England | Retrospective, population-based cohort study | 81,124 | 1960–1999 | 59,519 CIN 3 21,605 CC | NI | 23 AC after CIN 3 18 AC after CC | AC after CIN 3: SIR = 5.9 AC after CC: SIR = 6.3 | L |
7. | Gaudet et al. (2014) [22] | British Columbia (Canada) | Retrospective, population-based cohort study | 54,320 | 1985–2005 | 54,320 CIN 2 and CIN 3 *** | 35 | 4 AC after CIN 2 16 AC after CIN 3 | AC after CIN 2: SIR = 0.89 (95% Cl: 0.09–3.35) AC after CIN 3: SIR = 2.28 (95% Cl: 0.71–5.42) | L |
8. | Hemminki et al. (2001) [23] | Sweden | Retrospective, population-based cohort study | 17,234 | 1958–1996 | 17,234 CC | NI | 16 AC | AC after CC: SIR = 4.22 (95% Cl: 2.41–6.55) | L |
9. | Hemminki et al. (2000) [24] | Sweden | Retrospective, population-based cohort study | 135,386 | 1958–1996 | 117,830 CIN 3 17,556 CC | NI | 68 AC after CIN 3 17 AC after CC | AC after CIN 3: SIR = 3.75 (95% Cl: 2.91–4.69) AC after CC: SIR = 3.92 (95% Cl: 2.28–6.00) | L |
10. | Heráclio et al. (2018) [25] | Recife (Brazil) | Prospective, cross-sectional study | 324 | 2008–2009 | 200 CIN 1, 97 CIN 2 or CIN 3, 27 CC | 33 | 37 AIN | AIN after CIN 1: IR = 7% AIN after CIN 2/3: IR = 18.5% | L |
11. | Jakobsson et al. (2011) [26] | Finland | Retrospective, population-based cohort study | 26,876 | 1987–2006 | 26,876 CIN (unknown grade) | NI | 3 AC | AC after CIN: SIR = 3.56 (95% Cl: 0.73–10.4) | H |
12. | Jiménez et al. (2009) [27] | Ontario (Canada) | Retrospective, population-based cohort study | 674 | 1992–2005 | 7 CCs, 3 VaC, and 1 VC | 61 | 674 AC | AC after HPV-RGD: OR = 10.5 (95% CI: 3.6–30.3) AC after CC: OR = 6.84 (95% CI: 2.16–21.61) | H |
13. | Kalliala et al. (2005) [28] | Helsinki (Finland) | Retrospective cohort study | 7564 | 1974–2003 | 2446 CIN 1 1543 CIN 2 1334 CIN 3 2241 CIN “not otherwise specified” | NI | 3 AC | AC after CIN: SIR = 5.7 (95% Cl: 1.2 to 17.0) | L |
14. | Matsuo et al. (2018) [29] | USA * | Retrospective, population-based cohort study | 79,050 | 1973–2013 | 79,050 CC | 63 | 49 AC | 10-, 20-, 30-year cumulative incidence for AC after CC: 0.04%, 0.16%, and 0.38% | H |
15. | Neumann et al. (2016) [30] | France **** | Retrospective, population-based cohort study | 4808 | 1989–2007 | 4234 CC 339 VC 235 VaC | NI | 5 AC after CC 1 AC after VC 0 AC after VaC | AC after CC: SIR = 5.42 (95% Cl: 1.75–12.64) AC after VC: SIR = 11.7 (95% Cl: 0.15–65.51) | L |
16. | Pan et al. (2019) [31] | Scotland | Retrospective, population-based cohort study | NI | 1989–2015 | 69,714 CIN 3 | 30 | 37 AC after CIN 3 | AC after CIN 3: SIR = 2.6 (95% Cl: 1.9–3.6) | L |
17. | Papatla et al. (2019) [32] | USA * | Retrospective, population-based cohort study | 21,060 | 1973–2014 | 21,060 CC | 61.73 | 17 AC | AC after CC: SIR = 2.20 (95% Cl: 1.28–3.52) | L |
18. | Preti et al. (2020) [33] | Piedmont (Italy) | Retrospective, population-based cohort study | 3184 | 1992–2004 | 3184 CIN 2 or 3 | NI | 1 AC | AC after CIN 2 or 3: SIR = 1.8 (95% Cl: 0.04–10.0) | H |
19. | Rabkin et al. (1992) [34] | USA * | Retrospective, population-based cohort study | 25,295 | 1935–1988 | 25,295 CC | NI | 12 AC | AC after CC: SIR = 4.6 (95% Cl: 2.4–8.1) | H |
20. | Saleem et al. (2011) [35] | USA * | Retrospective, population-based cohort study | 189,206 | 1973–2007 | 124,075 CIN 3 6792 VIN 3 1463 VaIN 3 43,669 CC 9950 VC 3257 VaC | NI | 255 AC | AC after CIN 3: SIR = 16.4 (95% CI: 13.7–19.2) AC after CC: SIR = 6.2 (95% CI: 4.1–8.7) AC after VIN 3: SIR = 22.2 (95% CI: 16.7–28.4) AC after VC: SIR = 17.4 (95% CI: 11.5–24.4) AC after VaIN 3: SIR = 7.6 (95% CI: 2.4–15.6) AC after VaC: SIR = 1.8 (95% CI: 0.2–5.3) | L |
21. | Sand et al. (2016) [36] | Denmark | Retrospective, population-based cohort study | 156,290 | 1978–2012 | 52,135 CIN 2 104,155 CIN 3 | 33.8 for CIN 2 34.0 for CIN 3 | 32 AC after CIN 2 125 AC after CIN 3 | AC after CIN 2: SIR = 2.9 (2.0–4.1) AC after CIN 3: SIR = 4.2 (3.4–5.0) | L |
22. | Suk et al. (2018) [37] | USA * | Retrospective, population-based cohort study | 52,589 | 1973–2014 | 44,011 CC 6905 VC 1673 VaC | 63 for CC, 61 for VC, 95 for VaC | 34 AC after CC 31 AC after VC 1 AC after VaC | AC after CC: SIR = 2.3 (95% CI: 1.6–3.2) AC after VC: SIR = 13.2 (95% CI: 8.9–18.7) AC after VaC: SIR = 2.3 (95% CI: 0.1–12.8) | L |
23. | Tatti et al. (2012) [38] | Buenos Aires (Argentina) | Prospective, cross-sectional study | 481 | 2005–2011 | 121 CIN 1 114 CIN 2/3 188 VIN 1 39 VIN 2/3 70 VaIN 1 22 VaIN 2/3 | 35 | 28 AIN 2/3 106 AIN 1 | No information (AIN after CIN 2/3 comparted to AIN after CIN 1: OR = 1.91) | H |
24. | Tomassi et al. (2018) [39] | Southern California (USA) | Retrospective, population-based cohort study | 221,511 | 2005–2015 | 1168 CC 15,711 CIN 2/3 109,893 CIN 1 94,739 genital warts | 63.8 | 1 AC after CC 5 AC after CIN 2/3 14 AC after CIN 1 14 AC after genital warts | AC after CC: IR = 0.09% AC after CIN 2/3: IR = 0.03% AC after CIN 1: IR = 0.01% AC after genital warts: IR = 0.01% | H |
25. | Wang et al. (2020) [40] | USA * | Retrospective, population-based cohort study | 56,127 | 2000–2015 | 46,550 CC 7855 VC 1722 VaC | NI | 50 AC after CC 9 AC after VC 1 AC after VaC | AC after CC: SIR = 1.63 (95% Cl: 1.21–2.14) AC after VC: SIR = 1.10 (95% Cl: 0.50–2.09) AC after VaC: SIR = 0.62 (95% Cl: 0.01–3.47) | L |
No. | Authors and Year of Publication | Number of Secondary AIN or AC/Number of Primary HPV-RGD | Person–Years | Incidence Rate of AIN or AC | IR per 100,000 Person–Years | Comment |
---|---|---|---|---|---|---|
1. | Acevedo-Fontánez et al. (2018) [16] | 10 AC/8039 CC 3 AC/1378 VC 1 AC/773 VaC | 119,617 14,631 6554 | 0.124% 0.217% 0.129% | 8.36 20.5 15.26 | |
2. | Chaturvedi et al. (2007) [17] | - | - | - | - | No information about the number of AC cases. |
3. | Ebisch et al. (2017) [18] | 73 AC/89,018 CIN 3 80 AIN 3/89,018 CIN 3 | 1,261,804 1,261,804 | 0.082% 0.090% | 5.79 6.34 | |
4. | Edgren et al. (2007) [19] | 131 AC/125,292 CIN 3 | 2,193,409 | 0.105% | 5.97 | |
5. | ElNaggar et al. (2013) [20] | 13 AIN/90 CIN 48 AIN/132 VIN 10 AIN/55 VaIN | - - - | 14.4% 36.4% 18.2% | - - - | 1 AIN out of 3 CC, but not included because of the small number of cases. |
6. | Evans et al. (2003) [21] | 23 AC/59,519 CIN 3 18 AC/21,605 CC | 477,069 145,621 | 0.039% 0.083% | 4.82 12.36 | |
7. | Gaudet et al. (2014) [22] | 20 AC/54,320 CIN 2 and CIN 3 | 545,945 | 0.037% | 3.66 | |
8. | Hemminki et al. (2001) [23] | 16 AC/17,234 CC | - | 0.093% | - | |
9. | Hemminki et al. (2000) [24] | 68 AC/117,830 CIN 3 17 AC/17,556 CC | - | 0.058% 0.097% | - | |
10. | Heráclio et al. (2018) [25] | 14 AIN/200 CIN 1 23 AIN/124 CIN 2 and 3 | - | 7% 18.5% | - | |
11. | Jakobsson et al. (2011) [26] | 3 AC/26,876 CIN | 226,510 | 0.011% | 1.32 | |
12. | Jiménez et al. (2009) [27] | - | - | - | - | No information about the total number of CC, VC, or VaC cases. |
13. | Kalliala et al. (2005) [28] | 3 AC/7564 CIN | 97,556 | 0.040% | 3.08 | |
14. | Matsuo et al. (2018) [29] | 49 AC/79,050 CC | - | 0.062% | - | |
15. | Neumann et al. (2016) [30] | 3 AC/4234 CC 1 AC/339 VC | 28,122 1533 | 0.071% 0.295% | 10.67 65.23 | |
16. | Pan et al. (2019) [31] | 37 AC/69,714 CIN 3 | 893,622 | 0.053% | 4.14 | |
17. | Papatla et al. (2019) [32] | 17 AC/21,060 CC | - | 0.081% | - | |
18. | Preti et al. (2020) [33] | 1 AC/3184 CIN 2 and 3 | 20,022 | 0.031% | 4.99 | |
19. | Rabkin et al. (1992) [34] | 12 AC/25,295 CC | 156,838 | 0.047% | 7.65 | |
20. | Saleem et al. (2011) [35] | 137 AC/124,075 CIN 3 28 AC/43,669 CC 5 AC/1463 VaIN 3 2 AC/3257 VaC 55 AC/6792 VIN 3 28 AC/9950 VC | - | 0.110% 0.064% 0.342% 0.061% 0.810% 0.281% | - | |
21. | Sand et al. (2016) [36] | 32 AC/52,135 CIN 2 125 AC/104,155 CIN 3 | 597,467 1,529,564 | 0.061% 0.120% | 5.36 8.17 | |
22. | Suk et al. (2018) [37] | 34 AC/44,011 CC 31 AC/6905 VC 1 AC/1673 VaC | 473,820 48,373 9057 | 0.077% 0.449% 0.060% | 7.18 64.09 11.04 | |
23. | Tatti et al. (2012) [38] | 20 AIN/114 CIN 2 and 3 35 AIN/121 CIN 1 18 AIN/39 VIN 7 AIN/22 VaIN 2 and 3 27 AIN/70 VaIN 1 | - | 17.544% 28.926% 46.154% 31.818% 38.571% | - | Results without dividing AIN into HSIL (AIN 2/3) and LSIL (AIN 1). |
24. | Tomassi et al. (2018) [39] | 1 AC/1168 CC 14 AC/109,893 CIN 1 5 AC/15,711 CIN 2 and 3 | 10,359 708,690 114,031 | 0.086% 0.013% 0.032% | 9.65 1.98 4.38 | |
25. | Wang et al. (2020) [40] | 50 AC/46,550 CC 9 AC/7855 VC 1 AC/1722 VaC | - - - | 0.107% 0.115% 0.058% | 7.6 2.1 8.3 | No information about PY. IR per 100,000 PY as provided by the authors of the publication. |
Type of HPV-Related Gynecological Disease |
Risk of AC Mean SIR (95% Cl) 1 |
Risk of AC Mean IR (95% Cl) 2 | Risk of AC Mean IR per 100,000 PY (95% Cl) 3 |
Risk of AIN Mean SIR (95% Cl) 1 |
Risk of AIN Mean IR (95% Cl) 2 | Risk of AIN Mean IR per 100,000 PY (95% Cl) 3 |
---|---|---|---|---|---|---|
Cervical cancer | 3.814 (1.21–6.41) | 0.086% (0.07–0.102) | 9.73 (8.03–11.43) | |||
Vulvar cancer | 14.55 (0.15–24.4) | 0.265% (0.17–0.36) | 37.98 (22.64–53.32) | |||
Vaginal cancer | 1.8 (0.2–5.3) | 0.096% (0.009–0.183) | 11.78 (0–29.15) | |||
CIN 3 | 5.701 (2.23–19.2) | 0.084% (0.076–0.092) | 5.78 (4.85–5.89) | 6.68 (3.64–12.25) | 6.34 (5.10–7.90) | |
CIN (1–3) | 4.563 (0.12–19.2) | 0.066% (0.06–0.072) | 5.37 (4.85–5.89) | 16.45% (13.25–19.65) | ||
VIN 3 | 0.810% (0.59–1.03) | |||||
VIN (1–3) | 36.4% (28–44.8) | |||||
VaIN 3 | 0.342% (0.037–0.647) | |||||
VaIN (1–3) | 18.2% (7.8–28.6) |
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Brzeziński, M.; Stukan, M. Anal Cancer and Anal Intraepithelial Neoplasia Risk among Patients Treated for HPV-Related Gynecological Diseases—A Systematic Review. J. Clin. Med. 2023, 12, 4216. https://doi.org/10.3390/jcm12134216
Brzeziński M, Stukan M. Anal Cancer and Anal Intraepithelial Neoplasia Risk among Patients Treated for HPV-Related Gynecological Diseases—A Systematic Review. Journal of Clinical Medicine. 2023; 12(13):4216. https://doi.org/10.3390/jcm12134216
Chicago/Turabian StyleBrzeziński, Michał, and Maciej Stukan. 2023. "Anal Cancer and Anal Intraepithelial Neoplasia Risk among Patients Treated for HPV-Related Gynecological Diseases—A Systematic Review" Journal of Clinical Medicine 12, no. 13: 4216. https://doi.org/10.3390/jcm12134216