Staff members at the National Zoo fretted early last year over Kisangali, a female lion who was sick for weeks. She was lethargic and had bouts of vomiting and frequent thirst. Having ruled out digestive and kidney problems, a zoo veterinarian wrote in case notes that the troubles might be psychological.
Three weeks later, in February 2004, a raging infection in Kisangali's reproductive tract ruptured and spilled gallons of pus into her abdomen. Despite surgery, she died.
Veterinarians not affiliated with the zoo, who reviewed records at the request of The Washington Post, said the lion was showing classic symptoms of pyometra, a uterine infection. They maintained that the zoo, which is part of the Smithsonian Institution, missed an obvious diagnosis and failed to take surgical action early enough to save the 13-year-old animal.
"From the moment I started reading the medical history, my brain was screaming 'pyometra,' " said Peggy Larson, a former veterinary inspector for the U.S. Department of Agriculture.
Pyometra is "a very well-known condition that could account for all the signs noted in the record," said Gary Kuehn, a retired zoo veterinarian in California. "At least five veterinarians attended Kisangali, yet there is no record that any of them considered the possibility of pyometra."
The case is one of five deaths between December 2003 and December 2004 that raise new concerns about animal care at the National Zoo, according to three veterinarians and two other animal experts. A fourth veterinarian called the deaths "regrettable" but said he did not believe they reflected the overall care of animals at the zoo. The outside experts reviewed records, including medical notes and pathology reports, that the zoo provided to The Post.
In the other cases, zoo records and interviews show:
* A newly arrived emu, a large, flightless bird native to Australia, stopped breathing and died while veterinarians struggled to hold it to get a routine blood sample.
* A ring-tailed lemur, a small primate native to Madagascar, was not treated for a serious lung problem for nearly three months, until the animal had trouble breathing. The weakened lemur died five weeks later of a leg hemorrhage.
* An orangutan from the zoo's Think Tank exhibit was euthanized six weeks after being lent to a primate center in Iowa when veterinarians found a small hole in its inflamed bladder. The ape had suffered for two years from a rectal area abscess that appears to have spread infection to the bladder, according to veterinarians consulted by The Post.
* A Komodo dragon, a member of the largest lizard species in the world, died when an egg follicle and a blood vessel ruptured in an ovary. The animal, prone to reproductive tract infections, had not had a recommended internal ultrasound exam in nearly four years.
Zoo veterinarians said they failed to diagnose the lion's uterine infection but gave good care to the four other animals. They questioned the ability of outsiders to second-guess them.
The cases "represent less than 1 percent of our entire collection of 2,400 animals" and "less than 1 percent of the 701 individual animals we treated in some way last year," the veterinarians declared in a written statement. "While we have all been trained in a variety of species, we cannot be perfect in every diagnosis and treatment, nor can we be expected to know everything about all species."
David L. Evans, the Smithsonian's undersecretary for science and the zoo's interim director, said in an interview that he is confident that the zoo provides proper care.
"We have a terrific group of veterinarians," he said. "They are better-trained, higher-quality vets than you would find probably at any other zoo, but certainly at most other zoos in the country."
Suzan Murray, the zoo's head veterinarian, said in an interview that veterinarians, curators, keepers, a nutritionist and other experts successfully use a teamwork approach to animal care, adding, "I really do feel we have a very strong, caring, dedicated team."
Murray, associate veterinarian Sharon Deem and senior veterinary trainee Carlos Sanchez issued the statement as part of their written response to questions about animal care.
Sanchez, who provided much of the care for the five animals, has worked at the zoo for nearly five years. Zoo officials said he has lectured throughout the world on subjects involving wild animal populations. He received his veterinary degree in Mexico in 1992 and was a licensed staff veterinarian at the Zoological Parks of Mexico City. He has a master's degree in wild animal health from the Royal Veterinary College in London.
Sanchez, who is not licensed to practice in the United States, works under the supervision of other veterinarians, officials said. The Smithsonian said the federal laws that govern its veterinarians do not require them to have a local license to practice. Sanchez is the only National Zoo veterinarian without a U.S. license.
Evans said Sanchez's cases are reviewed "every single day" by one of the zoo's licensed veterinarians. He said Sanchez is scheduled to take his licensing exam this winter.
The 116-year-old zoo attracts 2 million visitors a year. Its operations came under scrutiny in 2003 after the deaths of several animals, including two red pandas that ate rat poison. The National Academy of Sciences, asked to review those deaths for Congress, concluded in January that most of the animals whose records it examined received acceptable care.
Evans, pointing to the academy's 18-month review and final report, said that "experts have passed judgment on us, and they've said we are providing appropriate care."
The report, however, was criticized by the Humane Society of the United States and by Donald K. Nichols, a former associate pathologist at the zoo, who said the academy ignored or glossed over veterinary mistakes that had fatal consequences. Nichols had given the academy packets of documents alleging numerous instances of poor veterinary care.
Nichols called the more recent deaths "among the worst cases" he knows about and said they were particularly troubling because they occurred while the zoo was under scrutiny by the science academy.
Kuehn and Larson also criticized the zoo's animal care practices.
"Every vet has really embarrassing screw-ups; I've had mine," said Kuehn, who worked at the San Diego and Los Angeles zoos before retiring in 1997. But the deaths, he said, suggest that the National Zoo sometimes has "deficiencies of basic clinical judgment and caring."
Edward C. Ramsay, a veterinarian at the Knoxville Zoo who teaches at the University of Tennessee's veterinary school, expressed concern about the care of the lion, lemur and orangutan. He stressed, however, that he believes the problems were aberrations and that the National Zoo treats hundreds of other animals "competently and with care about their welfare."
Kisangali came to the zoo in August 2003 from an animal sanctuary in California. Three months later, the lion began looking and acting ill. Blood work indicated that she had an infection.
Sanchez, according to medical records, did an ultrasound exam on several organs but did not look at the uterus. In his case notes of Jan. 29, 2004, with the lion showing no sign of kidney or other trouble, Sanchez wondered why the illness persisted. "Psychological factors cannot be ruled out," he wrote.
Kisangali's condition worsened in February. During surgery Feb. 23, veterinarians discovered the pus-filled abdomen. They spayed the animal and tried to clean out the infection. The lion died that night.
Ramsay said the zoo "certainly paid attention to this animal." Still, he said, "when somebody says pyometra is Vet Medicine 101, I think they're right." The zoo's veterinarians, he said, "set their minds to a different direction and never came back."
The zoo's veterinarians, in their written response, said pyometra should have been "high on the list" of possible conditions. They said they focused on kidney and digestive problems because older cats are prone to kidney disease and because Kisangali had a history of gastrointestinal troubles.
The 8-year-old bird was sold to the zoo in late November 2003 by Ed and Rhonda Keeling, who breed emus in Upper Marlboro. A private veterinarian had recently examined it and taken a blood sample. The Keelings said they were stunned when the emu died while zoo veterinarians tried to draw blood during a routine exam about two weeks later.
The emu had been kept in the zoo's quarantine area, where animals are examined before joining the collection. When she delivered the bird, Rhonda Keeling said, the staff told her that they didn't know much about emus and asked her to demonstrate how to handle it.
"They are very docile animals, as long as you treat them gently and don't move too quickly," she said.
At the Dec. 9 exam, Sanchez put a hood over the emu's head to make it easier to restrain. Keeling said the bird had never been hooded and probably panicked. Sanchez and a keeper struggled to hold the bird down, according to medical records, while another veterinarian tried twice to draw blood. The emu stopped breathing, and attempts to revive it failed.
A pathology report said the emu died of the stress of the restraint and possible trauma to a neck nerve.
The zoo's veterinarians said Sanchez used a hood because it often has a calming effect on large birds and other animals. According to several veterinary texts, hooding is strongly recommended for ostriches but not standard for emus because they are deemed easier to restrain. If a hood causes a bird to become agitated, experts say, it should be removed.
The Ring-Tailed Lemur
Priam, donated to the zoo in 2001 by Duke University, had an incomplete quarantine exam. Medical records said the blood sample was unsatisfactory. The lemur went more than 21/2 years before getting another physical examination.
On May 24, 2004, Sanchez examined the lemur and, in X-rays, saw indications of a lung problem. He sent the X-rays to outside specialists, who on June 20 provided their conclusions: The lemur had a lung tumor, pneumonia or, possibly, tuberculosis, and more tests were needed for a firm diagnosis.
The zoo did not do any further tests or start any treatment.
On Aug. 18, the lemur began struggling to breathe and was moved to the zoo's hospital and put in an incubator with oxygen. Sanchez waited another day -- until an ultrasound consultant had diagnosed pneumonia and a lung abscess -- to start antibiotics.
"To delay treatment prolongs the animal's discomfort and often makes treatment progressively more difficult," Kuehn said. "A serious medical problem was not attended to for nearly three months. . . . She deserved better."
The zoo's veterinarians said that they often use outside volunteer experts and that they planned to schedule a follow-up exam to firm up a diagnosis. They said they wanted to know what was wrong before starting treatment. But they did not rush to do the tests, they said, because of concerns about anesthetizing the lemur again when it did not appear to be in discomfort.
"We must weigh the considerable risks of repeat anesthetic exams when the animal is showing no signs of illness," they said. "Not everything needs immediate, emergency treatment."
Kuehn, Nichols and Larson said that because exotic animals hide their symptoms, looking ill should not be a criterion for treatment.
"Why do physical exams at all if you're not going to act on what you find?" Nichols said.
The lemur remained in the hospital. On Sept. 27, it was found lying on its side, taking shallow breaths. Deem anesthetized the lemur and drew "blood-tinged" fluid from its lungs. She also noted a new problem: The lemur's right hind leg was swollen two to three times its normal size.
The zoo's veterinarians said Deem concentrated on the lemur's breathing problem but also applied a pressure bandage to the leg. A pathology report said the animal, already weakened by its respiratory condition, died that morning of shock caused by the leg hemorrhage. It was 4 years old.
Indah, a star attraction at the zoo's Think Tank, developed an abscess near her rectum in November 2002. The zoo's veterinarians treated it with antibiotics and warm compresses, but the abscess infection did not heal.
Nearly a year later, according to medical records, the abscess was an open wound the size of a half dollar. An outside surgeon examined the abscess Nov. 25, 2003, during a sterilization procedure and found that it did not appear very extensive. There was no sign of a fistula, or draining tract, carrying infection to other organs.
On March 9, 2004, the records state, the abscess was "still exuding thick yellow [pus] material." That month, the veterinarians discontinued antibiotic treatment, saying it did not seem to be working.
By then, a zoo biologist who did language research with Indah and another orangutan, Azy, had moved to the Great Ape Trust of Iowa. The zoo agreed to lend him the pair so the studies could continue.
During a pre-shipment exam Sept. 7, 2004, Sanchez noted that the "fistula/abscess" was draining "mild amounts" of pus but was "not very extensive or deep." When he squeezed it, the anesthetized animal moved. "Appears painful," he wrote in his notes.
On Sept. 28, Indah was shipped to the primate center in Des Moines. On Nov. 11, veterinarians in Iowa found a tiny hole in the bladder, through which urine was seeping into surrounding tissue. The animal was euthanized immediately.
The pathology report said that the abscess and bladder infections had existed for some time and that it was possible the abscess spread infection to the bladder.
Nichols said he would "stake my reputation" that the abscess caused the deadly bladder problem. He, Kuehn and Larson said the abscess should have been surgically explored and removed before the zoo shipped Indah to Iowa.
Ramsay said he would have been "more aggressive" with the abscess, squirting dye into the draining tract to see, in X-rays, how far it went.
Even superficial abscesses "can be lethal," Kuehn said. Yet the zoo, he said, seemed to regard the abscess as "a nuisance," leaving Indah "with a painful, chronic, dangerous problem."
The zoo's veterinarians said they took the 24-year-old animal's case very seriously and determined through several probes that the abscess and fistula were not deep. Indah, they said, was not in any discomfort. They said the abscess did not require surgery, which might have caused permanent injury or, if the animal picked at the sutures, worsened the infection.
"We would never ship an animal with a life-threatening condition," Murray said. She added, "We had no indication that there was any problem."
The Komodo Dragon
Kraken was one of more than a dozen Komodo dragons hatched at the zoo in 1992. The births made history as the first group of this endangered species born outside Indonesia.
Trooper Walsh, who was a biologist at the zoo's Department of Herpetology, helped pioneer the breeding and management of the huge lizards. He said he worked with the zoo's veterinarians to do physicals on Kraken at least every six months, with internal ultrasound exams, given under anesthesia, that probed the reptile's reproductive system. The female, which weighed nearly 80 pounds, was prone to reproductive tract infections, which have killed 18 captive Komodo dragons worldwide.
Kraken was last given an internal ultrasound exam in April 2001. Walsh said the exams lapsed after he left the zoo in 2000. He said Reptile House curator Mike Davenport unfairly forced him out on disability retirement. Davenport declined to be interviewed.
The zoo later began doing external ultrasounds while the animal was awake but confined to a box. Walsh said the external exam does not provide the same detail.
Nichols said the lizard did not have any type of ultrasound for the last 23 months of its life and that the zoo's staff "should have paid extra attention to this animal."
Late last year, Kraken became lethargic and had a distended abdomen, according to medical records. Sanchez wrote on Dec. 22 that Davenport was not concerned because the animal had shown similar behavior during previous breeding seasons. The 12-year-old lizard was found dead three days later after an egg follicle and a blood vessel ruptured in an ovary, causing severe blood loss.
The zoo's veterinarians said an ultrasound exam would not have prevented the death.
"I firmly disagree," said Walsh, a member of the Species Survival Program for Komodo dragons, who described himself as "heartsick" over Kraken's death. "It could have helped save this animal . . . and would have been the best way to detect the problem."
Staff researcher Bobbye Pratt contributed to this report.