Published reports of neoplasia of the caprine tubular genital tract (ie, vagina, cervix, and uterus) are rare. In one of the first reports,1 federal meat inspectors reported a higher prevalence of tubular genital tract neoplasia in goats than in cattle and sheep. A review2 of caprine biopsy and necropsy samples submitted to the Oregon State University Veterinary Diagnostic Laboratory revealed that 100 of 1,146 (8.7%) submissions for goats included lesions diagnosed as neoplasia, and of the 102 tumors identified (2 goats had 2 types of tumors), 4 (4%) were attributed to the tubular genital tract. The latter lesions included uterine leiomyoma (n = 2) and cervical or vaginal adenocarcinoma (2). Various clinical reports have described the diagnosis of cervical leiomyoma,3,4 uterine leiomyoma,5 and uterine adenocarcinoma6 in living goats or at necropsy. Investigators of a retrospective case series7 found that the overall prevalence of leiomyosarcoma among necropsy submissions for goats at a veterinary teaching hospital was 7 of 1,344 (0.52%), with a higher prevalence of genital leiomyosarcoma in the Saanen breed, compared with the Pygmy goat breed and Pygmy-crossbred goats. Although sheep and goats are similar in many ways, a literature search identified only 2 clinical reports8,9 of tubular genital tract neoplasia in sheep. The prevalence of tubular genital tract neoplasia in the general goat population is presently unknown. Considering that goats are more commonly being kept as pets and that goats kept as pets are likely to live to an older age than goats kept for production purposes, the prevalence of neoplasia of the reproductive tract in these animals may be higher than previously reported.7
The described clinical signs of neoplasia of the uterus, cervix, or both in does include bloody vulvar discharge, abdominal straining, perineal swelling, pollakiuria, hemorrhage, and death.3–7 There have been sporadic reports6,7 of antemortem diagnosis of these conditions by manual or visual vaginal examination and laparotomy, but to the authors’ knowledge there are no current reports detailing a diagnostic protocol for antemortem diagnosis of genital tract neoplasia in does or exploring the efficacy of available diagnostic methods. Additionally, information regarding prognosis after partial or complete tumor resection is not readily available.
The aim of the study reported here was to determine the prevalence of tubular genital tract tumors in does at 2 veterinary teaching hospitals; describe the main clinical, surgical, histopathologic, and necropsy findings in affected goats; and assess factors potentially associated with short-term prognosis (ie, survival to discharge vs death or euthanasia) for these animals.
Materials and Methods
Case selection criteria
The study was designed as a multicenter, retrospective cohort study. Hardcopy and electronic medical records of does evaluated at the University of California-Davis Veterinary Medical Teaching Hospital (facility 1) from January 1, 1992, through December 31, 2011, and the University of Pennsylvania George D. Widener Hospital for Large Animals (facility 2) from January 1, 2007, through August 31, 2015, were reviewed to identify does with a histopathologic diagnosis of neoplasia of the tubular genital tract on the basis of biopsy, exploratory laparotomy, or necropsy findings. Does were excluded if a histopathologic diagnosis was not made.
Medical records review
Keywords for electronic searches at facilities 1 and 2 included uterine tumor, uterine neoplasia, cervical tumor, cervical neoplasia, vaginal tumor, vaginal neoplasia, leiomyoma, leiomyosarcoma, and hematuria. Records were reviewed and data were collected by 1 observer at each site (including one of the study authors [JKL]), and information was recorded in a standardized spreadsheet.
Information gathered from the medical records included the breed, age at hospital admission, reasons for evaluation, breeding history, abnormalities detected on physical examination, and diagnostic procedures performed for each doe in the study. Diagnostic imaging findings were obtained from the medical records without retrospective review of stored images; imaging was performed by a veterinarian with specialty training in ultrasonography or internal medicine (transabdominal imaging) or reproduction (transrectal imaging) or by a resident or fellow under direct oversight of a specialist. For does that underwent exploratory celiotomy, surgical findings and procedures were recorded. Results of histologic evaluation of biopsy specimens, gross and histologic findings on necropsy, and presence or absence of metastasis were collected from the records when available; histologic diagnoses were made by faculty veterinary pathologists at facilities 1 and 2. Short-term outcome for each animal in the study was classified as discharge from the hospital, spontaneous death, or euthanasia. No additional follow-up information was recorded for animals that survived to hospital discharge.
Statistical analysis
For continuous variables (age and body temperature), normality was assessed with a Tukey ladder of powers. Descriptive statistics were calculated; normally distributed data (body temperature) were reported as mean ± SD, and nonnormally distributed data (age) were reported as median and IQR. Comparison between categorical variables was performed with a χ2 analysis. A Kruskal-Wallis equality-of-populations rank test was used to compare the ages of does in the study sample with the ages of does for the overall hospital populations during the time periods for which data were collected (January 1, 1992, through December 31, 2011, at facility 1 and January 1, 2007, through August 31, 2015, at facility 2).
Univariate logistic regression analysis was performed to explore associations between a diagnosis of adenocarcinoma and the following variables: breed, hospital where the animal was seen, selected clinical signs on admission, and other examination data (hemorrhagic vulvar discharge at any point during hospitalization, whether vaginal examination was performed, and detection of a mass on vaginal examination), ultrasonographic factors (whether ultrasonography was performed, detection of a mass on ultrasound, mass traced to the uterus on ultrasound, presence of a heterogenous mass, presence of a hyperechoic mass, detection of a fluid-filled uterus, and urinary bladder involvement), surgical or necropsy findings (bladder or cervical involvement, tumor adhesions or local invasion, tumor location [uterus, cervix, or vagina], distant metastasis of the tubular genital tract tumor, and presence of other neoplasia), treatment (surgery [excluding animals euthanized intraoperatively], euthanasia [at any time], or none [spontaneous death]), and survival to hospital discharge (yes vs no). Univariate logistic regression analysis was also performed to explore associations of the outcome of euthanasia with the same variables (except for treatment type and survival to hospital discharge) and with tumor type. All variables that showed an association with the outcome of interest at a value of P < 0.2 were included in subsequent analysis. A stepwise backward and forward algorithm was conducted to identify the subset of independent variables that together were significantly associated with the main outcome of euthanasia. Only the combination of variables that showed a significant association with the outcome of interest, euthanasia, was reported as part of the final logistic multivariable inference model. Statistical analysis was performed with commercially available software.a For all comparisons, values of P < 0.05 were considered significant.
Results
A total of 2,737 does were evaluated at the 2 study facilities (2,092 at facility 1 and 645 at facility 2) during the respective study periods. Forty-two does (25 and 17 at facilities 1 and 2, respectively) met the inclusion criteria. The prevalence of neoplasia of the tubular genital tract among adult does was 1.2% and 2.6% in the populations of facilities 1 and 2, respectively. The median age of study does was 10 years (IQR, 8 to 11 years); the ages of study does did not differ significantly (P = 0.65) between facilities 1 (median, 10 years; IQR, 9 to 11 years) and 2 (median, 9 years; IQR, 7 to 11 years). The sample of does with tubular genital tract neoplasia was significantly (P < 0.001) older than the combined general hospital population (median age, 2 years; IQR, 5 to 9 years). The most commonly represented breeds were Pygmy goats (n = 22) and Nubians (7). Other breeds included Toggenberg (n = 2), Boer (2), Alpine (1), Angora (1), Tennessee Fainting Goat (1), LaMancha (1), and Nigerian Dwarf (1), with 2 does described as crossbred goats and 2 of unknown breeding. Pygmy goats were overrepresented in the study sample (22/42 [52%]), compared with the combined general hospital population (742/2,737 [27%]; P = 0.047). Thirteen of 42 (31%) survived to hospital discharge, 3 (7%) died, and 26 (62%) were euthanized (10 during surgery). One goat was dead on evaluation at the hospital, and no examinations or diagnostic tests had been performed prior to death.
The reasons for evaluation included bloody vaginal discharge or hematuria (n = 21), abdominal straining (9), weak rumen contractions (8), abdominal distension or bloat (5), signs of abdominal pain (5), pale mucous membranes (4), and anorexia (3); 22 of 42 goats had multiple clinical signs. Previous breeding history was available for 17 (40%) does, of which 13 had never been bred or had been bred but were never confirmed pregnant. The other 4 does had produced ≥ 1 live offspring.
Vulvar discharge was noted during the initial examination in 20 of 42 (48%) does; discharge was hemorrhagic in 10 (50%) animals and mucoid or purulent in 10 (50%). One other doe was noted to have hemorrhagic vulvar discharge detected at another time during hospitalization. Other common physical examination findings detected at this time included subjectively weak rumen contractions (n = 8), udder development (6), abdominal distension (5), signs of abdominal pain (5), and pale mucous membranes (4). Digital vaginal examination or visual examination by use of a vaginal speculum was performed in 6 of 42 (14%) animals, and a mass was detected in 3 animals (2 vaginal masses and 1 cervical mass) by these methods.
Ultrasonography was performed in 34 of 42 (81%) does (transabdominally in 30 and transrectally in 4). A discrete mass or thickening was identified in the caudal abdominal region in 31 of 34 (91%) does; these included 28 of 30 (93%) and 3 of 4 animals that underwent transabdominal and transrectal ultrasonography, respectively (Figure 1). The origin of the mass was identified as uterine in 24 of 31 (77%) does and could not be determined ultrasonographically in the remaining 7. Of these 24, 23 (96%) were confirmed at surgery or necropsy to have a primary uterine neoplasia, and 1 had cranial extension of a cervical mass. The uterine mass was described as heterogenous in 13 of 24 (54%) does, echogenic in 2 (8%) does, and other (no descriptor, mottled, irregular, thickened, or anechoic) in 9 (38%). Intrauterine fluid was detected in 13 of 34 (38%) does that underwent ultrasonographic examination and in 12 of 24 (50%) does in which a tubular genital tract mass was identified. Urinary bladder involvement was suspected in 5 patients evaluated with this method and was confirmed during surgery in 3 patients and not found in 2 (1 that underwent surgery and 1 that underwent necropsy). No screening for metastatic disease was performed.
Ultrasonographic images of masses of the tubular reproductive tract in 2 of 42 does in a retrospective study to assess the prevalence of tubular genital tract neoplasia in does evaluated at 2 veterinary teaching hospitals; describe the main clinical, surgical, and histopathologic or necropsy findings in affected does; and assess potential prognostic indicators in these animals. A—Image obtained with the ultrasound probe placed in the nonhaired region of the abdomen just dorsal to the udder and the ultrasound beam oriented toward the tail in a 9-year-old Pygmy goat doe (the dorsal aspect of the animal is at the bottom of the image). The urinary bladder (white arrow) is compressed ventrally by the large, fluid-filled uterus (outlined arrow). B—Image obtained for a 6-year-old Nubian doe (with the probe placement and beam orientation similar to that in panel A). The urinary bladder (white arrow) is compressed ventrally by a uterine mass (outlined arrows). Markings on the right edge of each image indicate depth (largest dashes = 1 cm).
Citation: Journal of the American Veterinary Medical Association 256, 7; 10.2460/javma.256.7.808
Twenty-three of 42 (55%) does underwent surgery. Ten of 23 (43%) does were euthanized during surgery because of poor prognosis; findings in these patients included local adhesions (n = 6), extension of the primary uterine mass caudally into the cervix or vagina (3), and obvious metastasis (1). Adhesions to the jejunum (n = 1), dorsal body wall and aorta (1), and ascending colon and body wall (1) also resulted in intraoperative euthanasia; some animals had > 1 finding that contributed to election of euthanasia. Carcinomatosis with involvement of the cecum, omasum, and uterus was identified in 1 doe that was euthanized during surgery. Of the remaining 13 does, a complete hysterectomy was performed in 6 and a partial ovariohysterectomy was performed in 7 because of local adhesions to the bladder (n = 1) or suspected extension of the mass caudally into the cervix or vagina (6). Of 6 patients with suspected cervical involvement that had partial ovariohysterectomy, 5 had evidence of neoplastic cells at the resection site on histologic examination, indicating the possibility for local recurrence. Sixteen does were euthanized without surgical intervention, and the 2 does that died spontaneously during hospitalization did not undergo surgery. All study does that were euthanized (n = 26) or died (3; including the animal that was dead on arrival at the hospital) underwent a full necropsy, and all tissue removed during surgery was submitted for histologic examination.
A histopathologic diagnosis was made for 13 of 42 does by evaluation of a biopsy sample and for 29 does by evaluation of necropsy submissions. Common diagnoses included leiomyoma (n = 13 does [4 that survived to discharge, 8 that were euthanized, and 1 that died spontaneously]), adenocarcinoma (13 [4 that survived, 8 that were euthanized, and 1 that died spontaneously]), and leiomyosarcoma (11 [3 that survived and 8 that were euthanized]). Two does (1 that survived and 1 that was euthanized) had a diagnosis of sarcoma. The remaining does had diagnoses of anaplastic carcinoma, fibrosarcoma, and adenoma (1 each); the doe with adenoma survived, the doe with anaplastic carcinoma died, and the doe with fibrosarcoma was euthanized.
During surgery or necropsy, most (34/42 [81%]) tumors were found to be uterine in origin, and the remainder had origins attributed to multiple parts of the tubular genital tract (5 [12%]), the vagina (2 [5%]), or the cervix (1 [2%]). Twenty of 29 (69%) does that were necropsied had evidence of neoplasia in other organs, with metastasis of the primary genital tumor to distant sites (ie, organs other than the uterus, cervix, vagina, bladder; n = 10; these included metastasis to multiple organs [6], the lungs [2], or the liver [1] and carcinomatosis [1]), a tumor type that differed from the primary genital tumor (6), or both (4). Other tumor types found included thymoma (n = 2), mesothelioma (1), ovarian adenocarcinoma (1), mammary adenocarcinoma (1), and anaplastic transitional cell carcinoma (1). Histologic examination of the uterus revealed CEH in 9 of 42 (21%) samples; this was detected in does with adenocarcinoma (n = 5), leiomyoma (2), leiomyosarcoma (1), and adenoma (1).
The odds of a diagnosis of adenocarcinoma were significantly (P = 0.006) greater for does that had metastasis of the primary tumor to distant organs (9/10) than for those that did not have metastatic disease (5/32; OR, 40.5). Neither the diagnosis of adenocarcinoma nor the outcome of euthanasia was significantly associated with the following variables by univariate analysis: breed (compared with Pygmy as a referent, including Nubian, Boer, Toggenberg, mixed, or other), vulvar discharge at admission, hemorrhagic discharge at admission, hemorrhagic discharge at any point during hospitalization, and straining. Undergoing ultrasonographic examination, detection of a mass on ultrasound, presence of a heterogenous mass, presence of a hyperechoic mass, and presence of a fluid-filled uterus were also not associated with either of these outcomes. Finally, undergoing vaginal examination, having a mass appreciated on vaginal examination, presence of udder development, tumor location (uterine, cervical, or vaginal), presence of another type of neoplasia, and facility where the animal was seen were not associated with either outcome. Treatment type (euthanasia, surgery, or none [spontaneous death]), a finding of tumor adhesions or local invasion at surgery, and survival to hospital discharge were not associated with a diagnosis of adenocarcinoma. Tumor type (compared with a referent of leiomyoma; leiomyosarcoma, adenocarcinoma, sarcoma, and other) and metastasis were not associated with the outcome of euthanasia. However, the odds of euthanasia for does with adhesions or local invasion found at the time of surgery were significantly (P = 0.007) greater than those for does that did not have adhesions or local invasion (9/9 vs 1/13; OR, 56.5).
On the basis of multivariable logistic modeling that included straining and hemorrhagic bleeding, when adjusted for hemorrhagic discharge, does with straining had greater odds of euthanasia (OR = 13; P = 0.026), compared with does without straining. Furthermore, when the model was adjusted for straining status, does with hemorrhagic discharge had greater odds of euthanasia (OR = 6.5; P = 0.04) than did does without this finding.
Discussion
The present study provided information regarding diagnosis and potential short-term prognostic factors for does with neoplasia of the tubular genital tract. In this retrospective study of 42 does evaluated at 2 veterinary medical teaching hospitals, metastasis of the primary tumor to distant organs was associated with significantly greater odds of a diagnosis of adenocarcinoma, compared with the odds for animals without distant metastasis. Metastases to the lungs, liver, kidney, and other tissues were previously found in an investigation of domestic rabbits with primary genital tract tumors, and metastasis was most commonly detected when the primary tumor was adenocarcinoma.10 In another report,11 a rabbit that had undergone ovariohysterectomy for treatment of uterine adenocarcinoma was identified as having intrathoracic metastatic disease and hypertrophic osteopathy 9 months after the surgery, and necropsy examination revealed that the lung nodules were consistent with metastatic uterine adenocarcinoma. In women, MRI has been used to estimate the risk of metastasis to lymph nodes, and myometrial and cervical invasion can be assessed with MRI or ultrasonography performed by an experienced practitioner.12–14 In the present study, transabdominal ultrasonography was the diagnostic tool most commonly used to identify the presence of a tumor (with a mass or thickening detected in 28/30 [93%] does examined); successful detection by the less frequently used methods of transrectal ultrasonography (3/4) and direct vaginal examination (3/6) was less common. Ultrasonographic imaging, whether transabdominal or transrectal, was successfully used in this study to detect the presence of a uterine mass in most of the does evaluated with this method, and further studies to determine whether a similar approach could be used to evaluate the extent of uterine invasion of such masses in does should be pursued. Screening of animals with suspected genital tract neoplasia should also include radiographic evaluation of the thorax prior to ovariohysterectomy.
Pygmy goat does were overrepresented in the study sample, compared with overall hospital admissions in the present study. A previous report7 indicated that Saanen does were more likely to have a diagnosis of uterine leiomyosarcoma than other breeds; however, to the authors’ knowledge, there are currently no published reports that detail the frequency of this diagnosis in Pygmy goat does. In a retrospective study2 of 102 tumors of various types and anatomic sites found in 100 female and male goats, dwarf-type (including Pygmy and Pygora), Nubian, and Saanen breeds were overrepresented, possibly because of a predisposition to neoplastic processes associated with the older ages of pet or dairy goats, compared with meat goat breeds. In women, the prevalence and malignancy of uterine tumors as well as prognosis for affected patients have been linked to ethnicity and race and may be influenced by genetics, exposure, or other factors.15–17 Additionally, in a study18 of women with abnormal uterine bleeding who underwent endometrial biopsy, the likelihood of a diagnosis of complex hyperplasia or cancer for those with a body mass index ≥ 30 kg/m2 was 4 times that for women with a lower body mass index. Body weights but not body condition scores were available in the present study, so a potential association between obesity and tumor development could not be evaluated. Further exploration is warranted to determine whether a link may exist between body condition score and neoplasia of the tubular genital tract in goats.
In the present study sample, among does for which reproductive history was known (17/42 [40%]), only 4 had a history of previous pregnancy, and these data were not statistically analyzed. Nulliparous women are at increased risk of developing endometrial cancer relative to women who have ≥ 1 child, and this is most likely associated with more frequent increases in local and circulating estrogen concentrations that occur with normal reproductive cycles.19 There are very few reports linking parity with neoplasia of the reproductive tract in the veterinary literature. Of 1,445 parous (mean parity, 6.8) production sows, only 12 (0.8%) were found to have a tumor of the tubular genital tract,20 whereas in an investigation of nulliparous miniature pigs 4 months to 19 years of age, 20 of 32 (63%) animals were found to have a uterine tumor.21 Although there are multiple other differences between production and miniature sows, it is possible that parity can influence the prevalence of tubular genital tract neoplasia in these animals; however, further investigation is necessary.
Cystic endometrial hyperplasia was reported in 9 of 42 (21%) uterine samples submitted for histopathologic examination in the present study, and this condition was most commonly found in patients with adenocarcinoma (5/13 does vs 2/13 and 1/11 does with leiomyoma and leiomyosarcoma, respectively; the only doe in the study with a diagnosis of adenoma also had CEH). These results were not analyzed statistically because of the low numbers; however, it is interesting to note that concomitant adenocarcinoma is estimated to be present in 30% to 40% of women with atypical CEH.22 The presence of CEH has also been reported in sows and does but, to our knowledge, associations with subsequent endometrial neoplasia in these species have not been reported. Histologic examination performed for 4-month to 18-year-old miniature pigs revealed CEH in 24 of 32 (75%) patients, and CEH concurrent with smooth muscle tumors and endometrial masses was seen in 14 (44%) and 10 (31%), respectively.21 Presence of CEH was also reported in a 2-year-old Boer goat with 2 irregular, nonneoplastic cystic masses found in the uterus during a caesarean section23; among 950 does at a single slaughter facility in India, the prevalence of CEH was 0.211%.24 Currently, the potential link between CEH and adenocarcinoma is not thoroughly understood in does. To the authors’ knowledge, the present study was the first to detail multiple cases of uterine, rather than cervical or vaginal, adenocarcinoma in does.
In total, 13 of 42 (31%) does of the present study survived to discharge from the hospital after surgical resection of the primary tumor, and extension of neoplastic tissue across the surgical margin was detected on histologic examination in 5 patients. However, no follow-up information was available for further assessment of outcomes. Adenocarcinoma of the uterine stump of an ovariohysterectomized cat has been described.25 In women with endometrial carcinoma, tumor recurrence occurs in 15% to 20% of women after surgical resection and systemic treatments, with one-third of recurrences developing locally (in the vagina or other pelvic tissues).26 Although, to the authors’ knowledge, the recurrence rates for neoplasia of the tubular genital tract in does remain unknown, these data suggest that ovariohysterectomy in affected does should include complete resection of the uterine body, if possible. Follow-up care of such patients after surgery should include monitoring for local recurrence and distant metastasis.
The present study had multiple limitations. These included its retrospective nature with reliance on records, a small sample size, and lack of follow-up after hospital discharge.
Antemortem diagnosis of tubular genital tract neoplasia in female goats currently relies on histologic examination of samples obtained by excisional biopsy, although endoscopy-guided biopsy or advanced imaging such as MRI may also provide useful information. Studies that include further evaluation of histologic samples for endometrial hyperplasia, whether simple or atypical, may help to characterize the impact of estrogen on development of endometrial cancer in goats.
Acknowledgments
No third-party funding or support was received in connection with this study or the writing or publication of this manuscript. The authors declare that there were no conflicts of interest.
The authors thank Betsy Vaughan and Katherine Watson for their assistance in case selection and data collection.
ABBREVIATIONS
| CEH | Cystic endometrial hyperplasia |
| IQR | Interquartile (25th to 75th percentile) range |
Footnotes
STATA/MP, version 15, StataCorp, College Station, Tex.
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