By Carolyn Y. Johnson, Globe Staff

A squirrel monkey died of dehydration at a Harvard Medical School research facility in December -- the third monkey to die at the New England Primate Research Center in 19 months -- and animals there also suffered a fracture and other injuries over the past three months, according to a federal inspection report released today.

The US Department of Agriculture cited Harvard for three serious incidents, which occurred after the medical school had responded to a series of other problems by replacing the center’s leadership. Harvard could face fines or receive a warning because of the failures to comply with federal animal welfare regulations.

Harvard officials and the Agriculture Department report, posted on the agency’s website, attributed the December 27 death and the non-fatal dehydration of a second monkey to employees’ failure to check a water dispensing system that had malfunctioned sometime after both monkeys arrived at the center Dec. 7.

Another squirrel monkey’s leg was fractured in January, when it was caught under a door. And a group of rhesus macaques escaped from their pen in December, resulting in an injury to one monkey’s foot.

The Agriculture Department considers all three incidents “direct noncompliance” issues, meaning there is a direct, adverse impact on the welfare of animals, or the high potential of such an effect. In fiscal year 2011, there were 25 direct noncompliance issues at research facilities nationwide.

“They’ve had a tough stretch, and it’s certainly something that’s gotten our attention and we look forward to them correcting the situation,” said David Sacks, a USDA spokesman.

William W. Chin, executive dean for research at Harvard Medical School, acknowledged in an interview that “there have been deficiencies in what we’ve been doing, leading to a number of incidents. These are regrettable. ... I would say they’re frankly unacceptable.”

Chin discussed the new issues and broader problems at the primate center during a 45-minute interview earlier this month, on the condition that the Globe would not report his comments until the Agriculture Department posted the latest findings. It was the first time a medical school official had agreed to discuss the situation at the Southborough research center in depth.

He said problems with management systems and the implementation of basic procedures were discovered through a review launched in the summer of 2010, after the first monkey died. Those issues are being addressed, Chin said, through the change in the leadership team last September, disciplinary actions, new policies and procedures, and the formation of a six-member team that will perform continual reviews, training, and testing of staff, and conduct random audits. Harvard Medical School released a lengthy statement, describing some of the problems at the center, and its response.

“We, as part of this public trust, even though we’re doing great science, we have to be sure that the animals are treated in the best way possible. And we just haven’t done it, and now we are working so hard to continue to do better in this,” Chin said. He added that the recent incidents occurred because it will take time for the ongoing improvements in training, procedures, and oversight “to take hold.”

Sacks said that the agency was still investigating the October death of a monkey. A common marmoset escaped while it was being transferred for an imaging procedure, was caught with a net, and was found dead after undergoing imaging. Sacks said that investigation could expand to include new problems. If an investigation finds a violation of the Animal Welfare Act, consequences could include an official warning letter or a fine -- a maximum of $10,000 per violation.

The New England Primate Research Center houses 2,058 monkeys and has a staff of 231, including veterinarians, technicians, and scientists. It receives about $25 million annually in federal funding to support its research activities, which include developing a vaccine for HIV.

Chin said Harvard officials first became aware of problems at the center in June 2010, after a cage went through a washer with a monkey in it. The cotton-top tamarin was found dead on the floor of the cage. An autopsy determined the animal died of natural causes prior to the cleaning, but the Agriculture Department issued a warning letter to Harvard.

Harvard initiated a comprehensive review, involving outside veterinary experts and consultants, which revealed a lack of oversight and disturbing series of breaks in following procedures that govern the research.

The review found that in more than one case, procedures were being done on animals without the required approval of an institutional committee. Chin said the lapses “almost certainly” did not affect the scientific integrity of the experiments, but were not acceptable.

That led the investigators to examine animals’ medical records and to discover troubling omissions, including incomplete records of tuberculosis tests, which are supposed to be performed regularly to ensure the health of the large monkey colony.

“It was kind of a messy situation in terms of being able to know exactly what happened to each of the animals,” Chin said.

New experiments were suspended in summer 2011 while the health of the colony was tested. There were no cases of tuberculosis. But it had become clear that the problems were deeper than initially thought, Chin said.

Senior medical school officials decided to replace the key leaders at the center last September, including the director, associate director for administration, and veterinary leadership. Dr. Fred Wang, the interim director, was not made available for an interview. Disciplinary actions were also taken, Chin said, but he could not be specific about what actions were taken or how many individuals were involved, citing employee privacy reasons.

In addition to the three deaths since 2010 at the primate center, a monkey died at a separate Harvard Medical School facility in Feburary 2011, due to an anesthesia error.

Carolyn Y. Johnson can be reached at cjohnson@globe.com. Follow her on Twitter @carolynyjohnson.

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A third monkey death reported at Harvard’s New England Primate Research Center