Human Papillomavirus Genotype Distribution in Low-Grade Cervical Lesions: Comparison by Geographic Region and with Cervical Cancer

Gary M. Clifford; Rashida K. Rana; Silvia Franceschi; Jennifer S. Smith; Gerald Gough; Jeanne M. Pimenta

doi:10.1158/1055-9965.EPI-04-0812

DOI: 10.1158/1055-9965.EPI-04-0812 Published May 2005

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Figure 1.
Prevalence of the 15 most common HPV genotypes in 5,910 HPV-positive LSILs by region. *, Denominators of HPV-positive LSIL vary by HPV type, from 2,516 to 5,910 for all regions, from 268 to 2,746 for Europe, from 1,640 to 1,943 for North America, from 466 to 874 for South/Central America, from 62 to 178 for Africa, and from 160 to 169 for Asia. ^†, In Asia, upper 95% CI for HPV16 is 39.6%, and HPV53 is not shown because the denominator was 33 cases only.
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Figure 2.
ORs and corresponding 95% FCIs for infection with HPV16 and HPV18 in HPV-positive LSILs by region.

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Table 1.

Regional distribution and overall HPV prevalence among 8,308 LSILs

Region	Studies, n	Countries represented	LSIL cases, n	HPV positive, n (%)
Europe	21	Belgium, Croatia, Czech Republic, France, Germany, Greece, Holland, Italy, Portugal, Sweden, United Kingdom	4,051	2,746 (67.8)
North America	13	Canada, United States	2,425	1,943 (80.1)
South/Central America	13	Argentina, Brazil, Colombia, Costa Rica, Honduras, Jamaica, Mexico, Paraguay	1,279	874 (68.3)
Africa	4	Ivory Coast, Kenya, Nigeria, Senegal	301	178 (59.1)
Asia	4	China, Korea, Thailand	252	169 (67.1)
Total	55		8,308	5,910 (71.1)

Table 2.

Prevalence of 15 most common HPV genotypes in HPV-positive LSILs and comparison with that in SCC

HPV genotype	HPV-positive LSIL*			SCC^†^,^‡
	Tested, n	HPV positive, %	Tested, n	HPV positive, %	Prevalence ratio (95% CI)
HPV16	5,910	26.6	8,594	54.3	2.06 (2.02-2.11)
HPV18	5,910	8.6	8,502	12.6	1.47 (1.39-1.54)
HPV45	3,545	4.9	5,174	4.2	0.85 (0.77-0.94)
HPV33	5,744	7.6	8,449	4.3	0.58 (0.54-0.62)
HPV31	5,801	11.7	7,204	4.2	0.36 (0.34-0.39)
HPV58	3,380	8.5	5,646	3.0	0.36 (0.32-0.39)
HPV52	3,262	8.8	5,304	2.5	0.28 (0.25-0.31)
HPV35	4,754	5.9	6,223	1.0	0.17 (0.15-0.20)
HPV59	3,232	6.0	4,488	0.8	0.13 (0.11-0.16)
HPV6	3,638	8.1	6,569	0.6	0.08 (0.06-0.09)
HPV56	3,348	9.7	4,493	0.7	0.07 (0.06-0.09)
HPV51	3,566	10.9	4,580	0.6	0.06 (0.05-0.07)
HPV39	3,251	7.8	3,899	0.4	0.05 (0.04-0.07)
HPV66	3,132	8.5	4,799	0.2	0.02 (0.02-0.04)
HPV53	2,516	10.1	3,053	0.1	0.01 (0.01-0.02)

↵* Regional distribution of included cases: Europe 46.5%, North America 32.9%, South/Central America 14.8%, Africa 3.0%, and Asia 2.9%.
↵† Data from Clifford et al. (32).
↵‡ Regional distribution of included cases: Europe 32.0%, North America 13.0%, South/Central America 16.5%, Africa 6.9%, and Asia 31.7%.

First author	Reference	Country	HPV DNA source	PCR primers	Cases n	LSIL/CIN1	HPV prevalence (% of all LSILs tested)
							Any	16	31	51	53	56	52	66	58	6	18	39	33	59	35	45
Africa
de Vuyst H	Sex Transm Dis (2002)	Kenya	Cells	SPF10	30	0/30	60.0	13.3	3.3	3.3	10.0	3.3	13.3	3.3	6.7	0.0	6.7	0.0	0.0	0.0	23.3	3.3
La Ruche G	Int J Cancer (1998)	Ivory Coast	Cells	MY09/11	151	151/0	68.2	10.6	5.3	0.0	—	2.6	2.6	—	3.3	3.3	6.0	2.0	5.3	1.3	1.3	2.0
Thomas JO	Br J Cancer (2003)	Nigeria	Cells	GP5+/6+	34	34/0	38.2	5.9	2.9	2.9	—	2.9	2.9	0.0	5.9	2.9	2.9	0.0	0.0	0.0	0.0	0.0
Xi LF	Int J Cancer (2003)	Senegal	Cells	MY09/11	86	86/0	51.2	8.1	1.2	1.2	3.5	1.2	3.5	1.2	9.3	2.3	4.7	0.0	2.3	2.3	2.3	0.0
Africa subtotal					301	271/30	59.1	9.6	3.6	1.0	5.2	2.3	4.0	1.3	5.6	2.7	5.3	1.0	3.3	1.3	3.7	1.3
Asia
Bhattarakosol P	J Med Assoc Thai (2002)	Thailand	Biopsies	MY09/11	27	0/27	33.3	0.0		—	—	—	—	—	—	0.0	3.7	—	0.0	—	—	—
Chan PKS	J Med Virol (1999)	China	Cells	MY09/11	51	0/51	64.7	21.6	7.8	0.0	0.0	2.0	5.9	0.0	15.7	2.0	9.8	0.0	2.0	0.0	0.0	0.0
Chan PKS	J Med Virol (1999)	China	Cells	MY09/11	51	0/51	64.7	21.6	7.8	0.0	0.0	2.0	5.9	0.0	15.7	2.0	9.8	0.0	2.0	0.0	0.0	0.0
Cho NH	Am J Obstet Gynecol (2003)	Korea	Cells	GP5+/6+	150	150/0	73.3	26.7	1.3	5.3	—	6.0	2.7	0.7	10.0	0.7	7.3	4.0	0.7	0.0	2.0	1.3
Hwang TS	Gynecol Oncol (2003)	Korea	Cells	GP5+/6+	24	0/24	70.8	16.7	0.0	4.2	—	4.2	4.2	4.2	0.0	0.0	16.7	8.4	0.0	0.0	4.2	0.0
Asia subtotal					252	150/102	67.1	21.8	2.7	4.0	0.0	4.9	3.6	2.2	10.2	0.8	7.1	3.6	0.8	0.0	1.8	0.9
Europe
Astori G	Virus Res (1997)	Italy	Cells	MY09/11	111	111/0	77.5	24.3	5.4	0.0	7.2	0.9	0.0	0.0	7.2	10.8	5.4	0.9	0.0	0.9	1.8	0.0
Baay MFD	Eur J Gynaecol Oncol (2001)	Belgium	Biopsies	GP5+/6+	58	0/58	69.0	24.1	1.7	3.4	—	5.2	1.7	1.7	0.0	0.0	19.0	0.0	0.0	0.0	0.0	5.2
Cuschieri KS	J Clin Pathol (2004)	United Kingdom	Cells	GP5+/6+	243	243/0	90.9	28.0	12.8	17.3	—	9.9	12.3	11.9	5.0	0.0	9.5	9.1	7.4	8.6	2.1	5.3
Cuzick J	Br J Cancer (1999)	United Kingdom	Cells	MY09/11	50	0/50	42.0	12.0	0.0	2.0	—	4.0	12.0	—	2.0	—	10.0	—	2.0	—	0.0	—
Giannoudis A	Int J Cancer (1999)	United Kingdom	Biopsies	GP5+/6+	118	118/0	100.0	12.7	5.1	7.6	—	5.9	—	11.9	7.6	15.3	7.6	0.8	0.8	2.5	14.4	2.5
Grce M	Eur J Epidemiol (1997)	Croatia	Cells	MY09/11	183	183/0	35.5	6.0	8.7	—	—	—	—	—	—	—	2.2	—	1.6	—	—	—
Grce M	Anticancer Res (2001)	Croatia	Cells	MY09/11	1,028	1,028/0	54.5	11.6	5.8	—	—	—	—	—	—	—	2.9	—	3.1	—	—	—
Humbey O	Eur J Obstet Gynecol Reprod Biol (2002)	France	Cells	MY09/11	40	40/0	60.0	30.0	—	5.0	—	—	5.0	—	7.5	2.5	10.0	—	7.5	—	2.5	2.5
Kalantari M	Hum Pathol (1997)	Sweden	Cells	MY09/11	141	0/141	70.9	17.7	5.7	—	—	—	—	—	—	—	12.1	—	5.0	—	—	—
Labropoulou V	Sex Transm Dis (1997)	Greece	Biopsies/cells	MY09/11	51	0/51	90.2	11.8	9.8	0.0	2.0	—	—	2.0	—	11.8	11.8	—	9.8	—	—	—
Laconi S	Pathologica (2000)	Italy	Biopsies	GP5+/6+	20	0/20	95.0	30.0	0.0	20.0	—	0.0	0.0	—	0.0	10.0	0.0	0.0	0.0	—	0.0	—
Medeiros R	Int Meet Gynecol Oncol (1997)	Portugal	Biopsies	MY09/11	31	0/31	74.2	35.5	—	—	—	—	—	—	—	—	3.2	—	0.0	—	—	—
Meyer T	Int J Gynecol Cancer (2001)	Germany	Biopsies/cells	MY09/11	130	130/0	69.2	13.1	13.1	3.1	2.3	0.8	3.1	3.8	5.4	3.1	2.3	1.5	5.4	0.0	3.1	0.8
Nindl I	J Clin Pathol (1999)	Germany	Cells	GP5+/6+	49	0/49	53.1	12.2	2.0	4.1	—	4.1	0.0	2.0	8.2	—	0.0	2.0	6.1	0.0	0.0	4.1
Reesink-Peters N	Eur J Obstet Gynecol Reprod Biol (2001)	Netherlands	Cells	SPF10	35	0/35	97.1	28.6	31.4	—	—	11.4	—	—	—	—	31.4	—	17.1	—	—	—
Southern S	Hum Pathol (2001)	United Kingdom	Biopsies	GP5+/6+	49	0/49	100.0	10.2	2.0	4.1	—	2.0	6.1	6.1	10.2	24.5	8.2	4.1	2.0	0.0	0.0	0.0
Tachezy R	J Med Virol (1999)	Czech Republic	Cells	MY09/11	87	87/0	52.9	34.5	2.3	1.1	2.3	0.0	1.1	0.0	5.7	—	4.6	0.0	2.3	0.0	2.3	1.1
Venturoli S	J Clin Virol (2002)	Italy	Cells	MY09/11	40	40/0	47.5	7.5	10.0	—	—	—	—	—	—	5.0	2.5	—	2.5	—	—	0.0
Voglino G	Pathologica (2000)	Italy	Biopsies	MY09/11	1,499	0/1,499	73.0	24.7	15.9	—	—	—	—	—	—	—	4.2	—	8.9	—	4.3	—
Zehbe I	Virchows Arch (1996)	Sweden	Biopsies	GP5+/6+	45	0/45	93.3	40.0	11.1	—	—	6.7	2.2	—	6.7	6.7	6.7	—	2.2	—	2.2	0.0
Zerbini M	J Clin Pathol (2001)	Italy	Cells	MY09/11	43	43/0	53.5	14.0	4.7	—	—	—	—	—	—	9.3	0.0	—	9.3	—	—	2.3
Europe subtotal					4,051	2,023/2,028	67.8	19.4	10.4	6.9	3.7	4.8	5.4	6.0	5.7	6.8	5.1	3.4	5.7	3.0	3.8	2.5
North America
Adam E	Am J Obstet Gynecol (2000)	United States	Cells	MY09/11	161	0/161	72.7	45.3	3.1	—	—	—	—	—	—	—	23.6	—	6.2	—	17.4	—
ASCUS-LSIL Triage Study Group	Am J Obstet Gynecol (2003)	United States	Cells	PGMY09/11	1,242	1,242/0	92.4	21.5	9.0	16.1	11.1	12.8	11.7	10.9	7.6	6.8	10.5	11.0	4.4	10.0	7.0	6.0
Brown DR	Sex Transm Dis (2002)	United States	Cells	MY09/11	25	25/0	88.0	40.0	12.0	4.0	4.0	20.0	12.0	24.0	4.0	4.0	0.0	8.0	4.0	8.0	12.0	0.0
Evans MF	Mod Pathol (2002)	United States	Biopsies	GP5+/6+	26	0/28	100.0	7.1	7.1	10.7	0.0	3.6	7.1	10.7	0.0	7.1	3.6	10.7	3.6	10.7	3.6	3.6
Jarboe EA	Hum Pathol (2004)	United States	Cells	PGMY09/11	95	0/95	55.8	7.4	3.2	4.2	8.4	3.2	9.5	5.3	2.1	2.1	3.2	1.1	0.0	10.5	2.1	5.3
Kulasingam S	JAMA (2002)	United States	Cells	MY09/11	166	166/0	79.0	15.7	3.6	15.0	11.4	7.2	8.4	9.0	5.4	10.2	3.6	7.8	3.0	3.6	4.2	2.4
Liaw K	J Natl Cancer Inst (1999)	United States	Cells	MY09/11	173	173/0	42.2	7.5	4.0	6.4	4.6	4.6	1.7	1.2	3.5	—	1.7	2.9	1.7	0.0	1.7	1.2
Richardson H	Cancer Epidemiol Biomarkers Prev (2003)	Canada	Cells	MY09/11	44	44/0	88.6	18.2	2.3	18.2	18.2	20.5	4.5	9.1	6.8	0.0	9.1	6.8	0.0	2.3	2.3	0.0
Schiff M	Am J Epidemiol (2000)	United States	Cells	MY09/11	190	0/190	58.4	5.8	8.9	4.2	10.5	7.4	4.7	6.8	10.5	4.2	4.7	7.4	4.2	6.3	1.1	4.7
Sellors JW	CMAJ (2000)	Canada	Cells	MY09/11	22	22/0	90.9	50.0	4.5	0.0	0.0	4.5	0.0	—	0.0	4.5	4.5	4.5	0.0	0.0	0.0	0.0
Sellors JW	CMAJ (2000)	Canada	Cells	MY09/11	24	24/0	95.8	37.5	12.5	0.0	0.0	0.0	0.0	—	4.2	4.2	25.0	0.0	4.2	0.0	0.0	0.0
Tortolero-Luna	Cad Saude Publica (1998)	United States	Cells	MY09/11	175	175/0	64.6	12.6	6.9	—	—	—	—	—	—	—	8.0	—	—	—	4.0	9.1
Tran-Thanh D	Am J Obstet Gynecol (2003)	Canada	Biopsies	MY09/11	80	0/80	83.8	15.0	8.8	3.8	8.8	15.0	8.0	8.8	6.3	6.3	8.8	7.5	5.0	3.8	0.0	1.3
North America subtotal					2,425	1,872/554	80.2	19.4	7.4	12.6	10.1	10.7	9.3	9.3	6.8	6.3	9.2	8.8	3.9	7.6	5.8	5.0
South/Central America
Abba MC	Rev Argent Microbiol (2003)	Argentina	Cells	MY09/11	279	279/0	80.3	26.5	2.5	0.7	—	—	—	—	—	22.9	2.5	—	5.4	—	—	—
Ferrera A	Int J Cancer (1999)	Honduras	Cells	MY09/11	44	0/44	47.7	11.4	11.4	0.0	4.5	0.0	0.0	0.0	2.3	0.0	6.8	0.0	0.0	0.0	0.0	2.3
Franco E	Pan Am J Public Health (1999)	Brazil	Cells	MY09/11	27	27/0	81.5	26.0	11.0	14.8	14.8	3.7	11.1	0.0	11.1	0.0	0.0	3.7	3.7	3.7	3.7	0.0
Giuliano A	Cancer Epidemiol Biomarkers Prev (2001)	Mexico (some United States)	Cells	PGMY09/11	40	40/0	62.5	15.0	0.0	7.5	2.5	5.0	7.5	5.0	5.0	2.5	2.5	10.0	0.0	7.5	2.5	2.5
Gonzalez-Losa MdR	J Clin Virol (2004)	Mexico	Biopsies	MY09/11	104	104/0	28.8	5.8	2.9	1.9	2.9	1.0	1.9	1.9	6.7	3.8	3.8	1.0	1.0	1.9	0.0	1.0
Herrero R	J Natl Cancer Inst (2000)	Costa Rica	Cells	MY09/11	181	181/0	73.0	12.2	7.2	9.9	6.1	8.8	7.2	4.4	8.8	6.1	4.4	6.6	1.1	1.7	2.2	3.9
Illades-Aguiar B	Int Papillomarivus Conf Proc (2001)	Mexico	Biopsies	MY09/11	148	0/148	86.5	12.8	2.0	0.0	0.7	0.0	0.7	0.0	3.4	2.0	0.7	0.0	36.5	0.0	0.7	4.1
Lorenzato F	Int J Gynecol Cancer (2000)	Brazil	Cells	MY09/11	62	0/62	67.7	19.4	22.6	—	—	—	0.0	—	6.5	0.0	3.2	—	11.3	—	4.8	0.0
Molano J	Br J Cancer (2002)	Colombia	Cells	GP5+/6+	70	70/0	55.7	10.0	4.3	4.3	—	4.3	7.1	1.4	5.7	2.9	7.1	4.3	8.6	0.0	2.9	4.3
Rattray C	J Infect Dis (1996)	Jamaica	Cells	MY09/11	62	62/0	80.6	9.7	8.1	—	—	—	—	—	—	4.8	4.8	—	12.9	—	8.1	16.1
Strickler H	J Med Virol (1999)	Jamaica	Cells	MY09/11	186	186/0	54.3	4.3	1.6	1.6	2.7	1.6	2.7	2.2	2.2	2.2	2.7	1.6	1.6	0.5	2.2	0.5
Tonon SA	Infect Dis Obstet Gynecol (1999)	Argentina/Paraguay	Cells	GP5+/6+	55	55/0	96.4	74.5	—	—	—	—	—	—	—	5.5	12.7	—	—	—	—	—
Torroella-Kouri M	Gynecol Oncol (1998)	Mexico	Biopsies/cells	MY09/11	21	21/0	33.3	4.8	0.0	4.8	0.0	4.8	0.0	0.0	0.0	0.0	0.0	0.0	0.0	0.0	0.0	4.8
South/Central America subtotal					1,279	1,025/254	68.3	16.7	4.8	3.3	3.6	3.3	3.6	2.1	5.2	7.4	3.6	2.9	7.9	1.2	2.2	3.3
Total					8,308	5,341/2,967	71.2	18.7	8.2	8.0	7.6	7.2	6.7	6.5	6.3	6.2	6.1	5.8	5.3	4.6	4.3	3.7