A plane packed with hundreds of dogs landed in Canada. On board were 38 dead puppies

The Ukrainian International Airlines plane arrived in Toronto after what is usually a routine 10-hour flight. It was a typical commercial aircraft, but airport workers found a shocking scene on board.

Inside were 500 crated puppies, according to Canadian authorities. Many were dehydrated, weak and vomiting. Thirty-eight of them were dead in their crates.

The gruesome discovery on June 13 set off an investigation by the Canadian Food Inspection Agency. And it cast a spotlight on a growing international market for dogs that advocates and lawmakers say needs more restrictions - not only for the sake of imported dogs, but to protect the health of people and animals in North America.

"The number of dogs imported into the U.S. has skyrocketed in the past few years, and we are screening less than one percent of them," Rep. Ralph Abraham, R-La., a veterinarian who last month co-sponsored a bipartisan bill called the Healthy Dog Importation Act, said in an email. "We need to do more to protect these animals and those already in the country."

Much about the Ukrainian flight remains unknown, including whether Canadian authorities were aware so many puppies were headed to Toronto. The government, which says it has "rigorous standards" for animal imports, has released little information, citing the pending investigation. Ukraine International Airlines said in a statement Friday that it regretted the "tragic loss of animal life" and is working with local authorities to make "any changes necessary to prevent such a situation from occurring again."

Animal advocates said flying 500 dogs on a single plane is unusual, if not unprecedented. Dogs need water and other care when being crated on the tarmac and during flights, said Rebecca Aldworth, executive director of the Humane Society International in Canada.

"You're relying on the staff of the airport and the airline to do that care," she said. "If those animals are transported in those numbers, it would be physically impossible to provide that kind of care."

The puppies flown from Ukraine were French bulldogs, according to several Canadian news reports. The dogs are one of several brachycephalic, or snub-nosed, breeds so vulnerable to respiratory problems that some U.S. airlines refuse to transport them.

Despite their health problems, French bulldogs are among the most sought-after breeds in North America, ranking fourth on the American Kennel Club's most recent list of popular purebreds and fifth on the Canadian Kennel Club's list. Their popularity means "Frenchies" command high prices. On the sales website Puppyspot, French bulldog puppies are priced from $4,500 to $8,000. One U.S. nonprofit rescue has offered the dogs with adoption fees as high as $1,850, according to a Washington Post investigation.

The potential profits incentivize sellers and brokers to skimp on animal welfare, animal advocates and government officials say. The National Post reported that temperatures were approaching 90 degrees when the puppies were loaded onto the plane in Ukraine and that some of the puppies' crates were shrink-wrapped, which could cause suffocation.

How many French bulldogs, or dogs overall, are imported to Canada annually is unknown, Aldworth said. In the United States, more than 1 million dogs are imported each year, according to a 2019 report from the Department of Agriculture. The vast majority are assumed to be pets traveling with their owners, the report said; the USDA issued only about 2,900 permits for dogs destined to be resold to consumers. Some observers question that conclusion, including the American Kennel Club, which says it believes many are "actually destined for transfer."

Because a growing number of larger U.S. dog breeders are shutting and smaller-scale hobby breeders are retiring, some of "our breeding has been outsourced to other countries," said Patti Strand, founder of the Oregon-based National Animal Interest Alliance, which advocates for breeders and other animal businesses.

Some shipments have involved well over 40 dogs, often puppies too young to fly legally, according to a 2019 Centers for Disease Control and Prevention blog post that described surveillance of illegal puppy imports at New York's John F. Kennedy International Airport. Importers seek to skirt regulations by claiming the dogs are older or are "rescues" not intended for resale, because "the potential profit is exponential," the post said. French and English bulldogs are particularly common, it said.

In a 2019 report on puppy smuggling, the U.K. charity Dogs Trust said many dogs originate in Latvia, Lithuania, Poland, Hungary, Serbia, Romania and Bulgaria and are transported to other European countries without appropriate rest breaks, food or water. In her 2018 book "Designer Dogs," Madeleine Bernstein, president of the animal welfare group spcaLA, described a shipment of French bulldogs that landed in Los Angeles from Ukraine. The animals were "underage, not vaccinated against rabies, and in urgent need of care. The paperwork did not match the puppies in the container," she wrote.

Such incidents are evidence of a widespread problem, advocates say.

"The importation laws for pets have not kept pace with globalization anywhere in North America," Strand said.

The U.S. Department of Agriculture requires that dogs entering the United States for resale be at least 6 months old and vaccinated for rabies and other diseases.

But those criteria are not always met. In 2019, the CDC announced a temporary ban on dogs from Egypt following the imports of three rabid dogs, including one brought in by a Kansas City-area rescue group. And the minimum age requirements can eat into a puppy's most valuable weeks for marketing and sale, Aldworth said.

"It's only effective to administer rabies vaccines to puppies three months of age or older, so . . . that puppy should be 4 months old when it's transported," she said. "That's when you start to see forged paperwork, saying things like the animal is older than it actually is."

Humane Society International has been calling for a ban in Canada on imports of all commercially-bred dogs for resale. The approach would not stop international rescue imports, which the group sometimes organizes, Aldworth said.

"Governments and NGOs are trying so hard to eliminate puppy mills here in Canada," she said. "There is no reason to allow importation of dogs from the same kinds of facilities elsewhere."

In the United States, Abraham's legislation would target commercial and rescue importers alike, putting the focus on stopping disease no matter who is bringing in dogs. It would require importers to submit dogs' immunization records and allow U.S. customs agents to "more closely scrutinize importers from countries known to harbor traffickers," he said.

"Incidents like these are not only inhumane, but also a grave risk to public health," Abraham said of the flight to Toronto.

The bill is supported by the American Veterinary Medical Association, the American Kennel Club and Strand's group. She said a primary objective is ensuring that one U.S. agency takes the lead in overseeing dog imports and tracking their movement once they arrive.

"I think this legislation is going to lead to a public conversation," Strand said. "Once the public becomes aware of what's routinely going on, everyone will demand change."