For almost a decade, researchers have studied why a vaccine for adolescents that could prevent tens of thousands of cancers every year is so unpopular.

Turns out it's not so much the cost, or safety worries, or the antivaccine movement.

The biggest obstacle, studies show, is that doctors aren't recommending the HPV vaccine because they're uncomfortable talking to parents and tweens about a virus spread by S-E-X.

But a blitzkrieg against the doctor deterrent is underway. The U.S. Centers for Disease Control and Prevention and other public-health agencies have major campaigns designed to educate doctors about why and how to recommend the HPV shots. A primary theme: It's about cancer, not sex, so don't even imply it's controversial.

A Bryn Mawr start-up firm is trying to boost vaccine uptake with an educational iPad application that parents use while they wait in the doctor's exam room. And health insurers face economic pressure to get doctors to champion the vaccine.

Philadelphia is a case study in what happens when doctors do so, said Caroline Johnson, director of disease control at the city Department of Public Health. Last year, 60 percent of Philadelphia girls and 35 percent of boys ages 13 to 17 were fully vaccinated against HPV - compared to just 37 percent of girls and 13 percent of boys nationally.

"It's not the parents who are the block," Johnson said. "Parents are very accepting of the vaccine when doctors strongly recommend it."

Genital strains of the human papillomavirus, HPV, are so ubiquitous that almost all sexually active people - not just promiscuous ones - will be infected at some point.

Fortunately, most HPV infections are readily wiped out by the immune system.

But not all.

The annual HPV toll: about 12,000 cervical cancers; about 300,000 severe precancerous cervical lesions, which can be detected and treated early through Pap screening; about 14,000 cancers of the vagina, vulva, penis, anus, head, and neck, for which there are no early-detection methods; plus 300,000 cases of genital warts, which can spread and recur and require laser therapy or freezing. (Warts are prevented by Merck's nine-year-old Gardasil brand, but not GlaxoSmithKline's six-year-old Cervarix.)

For more than a decade, head and neck cancers in men and anal cancers in women have been increasing; witness the ordeals of actors Michael Douglas and the late Farrah Fawcett.

The vaccine's full impact on cancer may take another generation to emerge, given that persistent infections take years or decades to progress to malignancy. But already, the shots are yielding benefits, despite underuse. Federal data show dramatic declines in HPV infection rates and genital warts among vaccinated age groups.

No wonder that last year, the President's Cancer Panel called boosting HPV immunization "one of the most profound opportunities in cancer prevention today."

The panel's annual report concluded that getting doctors to stop missing that opportunity was "goal one."

The three-shot vaccine is usually administered by pediatricians and family physicians - not the gynecologists and oncologists who treat HPV disease. Guidelines say to give the vaccine to girls and boys ages 11 and 12, although "catch-up" shots can be given into the 20s.

Why target tweens?

Because the vaccine can prevent cancer only if given before the patient is exposed to the virus - that is, before becoming sexually active.

For all their medical training, many doctors who treat kids don't appreciate the nature of HPV, or their role in preventing adult disease.

"I know a strong recommendation is the most important predictor of vaccination; I'm not sure physicians know that," said Mandi Pratt-Chapman, director of the George Washington Cancer Institute, which produced a handbook for teaching doctors about the vaccine. "There's some education that needs to happen."

Doctors heartily recommend the other two adolescent vaccines, which protect against tetanus, diphtheria, pertussis, and meningococcal disease. CDC data show 80 percent to 90 percent of teens are immunized.

But none of those illnesses is sexually transmitted.

The latest study to explore physicians' bashfulness was published last month. In the Harvard-led national survey of pediatricians and family doctors, a third said they were uncomfortable talking about the HPV vaccine because of the sex aspect. About 60 percent selectively recommended the shots based on whether they perceived adolescents to be at high risk of infection - in other words, having sex.

"You have an 11-year-old girl sitting in front of you. It's hard for physicians to bring up the notion that the vaccine protects against sexually transmitted disease," said pediatrician Paul Offit, director of the vaccine-education center at Children's Hospital of Philadelphia.

Offit riffed on that reluctance in a New York Times op-ed piece titled "Let's Not Talk About Sex," arguing that doctors need not get hung up on how HPV is spread.

Teaching communication strategies that avoid hang-ups is a big part of doctor-education efforts. What parents want, studies show, is reassurance and clarity. The CDC's campaign, called "You are the key to cancer prevention," offers "tips and time-savers for talking with parents," such as this answer if parents ask why vaccinate so young:

"We vaccinate people well before they are exposed to an infection, as is the case with measles. Similarly, we want to vaccinate children well before they get exposed to HPV."

If parents worry the vaccine will be perceived by the child as permission to have sex, the tip sheet suggests this response:

"Research has shown that getting the HPV vaccine does not make kids more likely to be sexually active or start having sex at a younger age."

Doctors are taught to seize opportunities and presume parents won't push back.

"The presumptive approach calls for providers to 'announce' that it is time for the HPV shots, as opposed to 'asking' if the patient wants to get the vaccine," says the GW Cancer Institute's handbook.

But the Harvard-led survey, published in Cancer Epidemiology, Biomarkers & Prevention, found that half of respondents did not capitalize on visits by recommending same-day HPV vaccination. And more than a quarter considered the vaccine relatively unimportant, echoing previous studies in which doctors framed it as optional.

Philadelphia, where many vaccines were developed, has long been a standout in childhood immunization. The city Health Department used a $1 million CDC grant to collaborate with medical schools and other expert advisers on getting HPV vaccine rates up. Over the last two years, facilitators have gone into the offices of more than 730 pediatricians, family physicians, nurses, and medical assistants to share communication strategies and set up patient reminder systems.

That ongoing initiative is complemented by "Three for Me," which uses ads, social media, and postcards to inform parents about all three adolescent vaccines. Meanwhile, Children's Hospital is studying Noble.MD's iPad app, called Theo, to see whether the video and question-and-answer format can prime parents to say yes to the vaccine while making use of otherwise wasted waiting time in the exam room.

"This mode of communication seems to be well-received," said Children's pediatrician Kristen Feemster, leader of the Theo study. "We're such a tablet-smartphone culture."

Health-care economics are also driving change. The National Committee for Quality Assurance (NCQA), a nonprofit that evaluates and accredits health plans, last year added HPV vaccination rates as a measure of the quality of care delivered by the plans' doctors.

"Health plans and the government are moving toward incentive payments - that you have to perform well to get the better payments," said committee spokesman Matt Brock. "It sometimes comes down to the dollar."