History
A 13-month-old virgin Holstein heifer housed at the University of Florida Institute of Food and Agricultural Sciences Dairy Research Unit was evaluated for enlargement of the rear mammary glands (Figure 1). She was the only heifer in a group displaying signs of abnormal mammary gland development and lactation.
Photograph of the developing rear quarters of the mammary gland and teats that secreted milk in a nonpregnant, 13-month-old virgin Holstein heifer.
Citation: Journal of the American Veterinary Medical Association 260, 13; 10.2460/javma.22.03.0148
On physical exam, all measurable parameters were found to be within the physiological range of normal limits. The left and right rear quarters of the mammary gland were distended, soft on palpation, and leaking a small amount of milk-like secretions. Samples from both rear quarters were collected by use of aseptic technique for analysis. The mammary secretions appeared like normal milk on visual inspection with no evidence of clinical mastitis. On rectal examination, a nonpregnant uterus with symmetrical uterine horns and normal ovaries were palpated.
A pooled sample of the secretions collected from the rear quarters was submitted to Quality Milk Production Services at Cornell University for composition testing and culture. Composition testing confirmed that it was milk and revealed 2.99% butterfat, 3.50% protein, 2.49% lactose, and 5,400,000 cells/mL elevated somatic cell count (SCC). Culture results revealed gram-positive Bacillus and Staphylococcus spp (not Staphylococcus aureus). Culture for Mycoplasma spp was negative.
Diagnostic Imaging Findings and Interpretation
Ninety days after the initial evaluation of the mammary gland and 55 days after insemination, Doppler ultrasonography (MyLab; Esaote SPA) was performed to confirm the normality of blood flow within the heifer’s reproductive tract and the current pregnancy. The right ovary (Figure 2) presented multiple follicles (< 5 mm) and a corpus luteum (CL) (23.0 mm in diameter and an area of 398.5 mm2). The left ovary (Figure 3) presented a 12.9-mm follicle and multiple small follicles (< 5 mm). A healthy pregnancy was reconfirmed in the right horn of the uterus (Figure 4).
Transrectal Doppler ultrasound image of the right ovary and 23.0-mm CL present with more than 25% of blood flow on the basis of the difference of total colored pixel area in the largest CL diameter/total CL area.
Citation: Journal of the American Veterinary Medical Association 260, 13; 10.2460/javma.22.03.0148
Transrectal ultrasound image of the left ovary and 12.9-mm follicle.
Citation: Journal of the American Veterinary Medical Association 260, 13; 10.2460/javma.22.03.0148
Transrectal Doppler ultrasound image of the fetus and cross section of the thoracic cavity. The area with colored pixels represents the location of the heart indicating the presence of a viable fetus.
Citation: Journal of the American Veterinary Medical Association 260, 13; 10.2460/javma.22.03.0148
Luteal blood flow was recorded by use of the color Doppler mode function. The percentage of irrigation calculated was 26% (ImageJ version 1.62; NIH), which is considered a functional CL.1 No additional relevant findings were observed in the uterus or ovaries.
Blood serum was collected and submitted to the University of California-Davis Clinical Endocrinology Laboratory for anti-Müllerian hormone (AMH) testing. The results revealed 0.07 ng/mL AMH present.
Treatment and Outcome
Both quarters were infused with 1 tube of a nonantimicrobial intramammary teat sealant (Orbeseal). No abnormal findings were observed in the front quarters. Following pregnancy confirmation, the heifer remained in the herd as a replacement heifer. The distended rear mammary glands did not require any antimicrobial treatment. She calved without assistance at 271 days of gestation and gave birth to a healthy female Holstein calf. In early lactation, mild ketosis was her only health issue of concern. All 4 quarters remained patent throughout her lactation. Her average milk yield was 28.6 kg of milk/d for the first 1 to 40 days and 35.4 kg of milk/d for 41 to 100 days. This is comparable to her first lactation cohorts on this farm, which had an average yield of 31.3 kg of milk/d for the first 1 to 40 days and 35.8 kg of milk/d for 41 to 100 days.
Following the 70-day voluntary waiting period, the double Ovsynch synchronization protocol2 was begun and the heifer was confirmed pregnant following her first service with conventional Holstein semen.
Comments
The development of precocious lactation has previously been described in virgin Holstein dairy heifers with granulosa-theca cell tumor (GTCT) or persistently exposed to elevated concentrations of estradiol. The presence of excessive estrogenic compounds could come from feed, cystic ovaries, or lymphatic and neoplastic anomalies. In small ruminants, precocious udder development and lactation have been previously described as “inappropriate lactation syndrome,” in which some of the possible etiologies may include pituitary adenoma, adrenal pheochromocytoma, cystic ovaries, and cystic endometrial hyperplasia3 and GTCT.
This heifer was the only individual displaying signs of abnormal mammary gland development and lactation within her cohort. There was no evidence of estrogenic plant compounds in the pasture, nor in the total mixed ration being fed. Our results indicated the absence of GTCT as the AMH concentrations were lower than the suggested cutoff of 0.36 ng/mL.4,5 A recent study6 found that Holstein heifers had an average AMH concentration of 0.149 ± 0.013 ng/mL.
In the present case, premature udder development and milk production were not associated with estrogen toxicosis, a GTCT, or abnormal ovarian structures. Although the cause remains unknown and we cannot completely rule out pituitary or adrenal tumors, the heifer conceived in her second breeding, calved normally, and is currently lactating and pregnant. Even though her milk production was slightly below herd average, it was not possible to establish whether this was associated with the udder development or other factors such as genetics or heat stress.
Given that this heifer had Bacillus and Staphylococcus spp isolated from her milk secretions, in addition to an SCC higher than that of normal prepubertal heifers, the evidence of subclinical mastitis cannot be ruled out. However, the presence of mastitis in heifers has not been previously associated with the presence of precocious lactation.
The recommended close monitoring of the heifer, absence of udder manipulation, and use of teat sealants may have prevented the development of clinical mastitis and further inappropriate development of the mammary gland during gestation and therefore may have favored the normal lactation. This case supports the decision to maintain heifers in the herd that present with premature udder development; however, this is difficult to validate as the phenomenon is not commonly seen.
Acknowledgments
The authors declare that there were no conflicts of interest.
The authors thank the University of Florida Institute of Food and Agricultural Sciences Dairy Research Unit for their willingness to facilitate additional evaluations of the heifer.
References
- 1. ↑
Acosta TJ, Yoshizawa N, Ohtani M, Miyamoto A. Local changes in blood flow within the early and midcycle corpus luteum after prostaglandin F(2 alpha) injection in the cow. Biol Reprod 2002;66(3):651–658.
- 2. ↑
Souza AH, Ayres H, Ferreira RM, Wiltbank MC. A new presynchronization system (Double-Ovsynch) increases fertility at first postpartum timed AI in lactating dairy cows. Theriogenology. 2008;70(2):208–215.
- 3. ↑
Miller CC, Williamson LH, Miller-Liebl DM, Thompson FN. Lactation associated with acidophilic pituitary adenoma, pheochromocytoma, and cystic endometrial hyperplasia in two goats. J Am Vet Med Assoc. 1997;210(3):378–381.
- 4. ↑
El-Sheikh Ali H, Kitahara G, Nibe K, et al. Plasma anti-Müllerian hormone as a biomarker for bovine granulosa-theca cell tumors: comparison with immunoreactive inhibin and ovarian steroid concentrations. Theriogenology. 2013;80(8):940–949.
- 5. ↑
Roberts JN, Carleton CL, Conley AJ, Agnew DW. Theriogenology Question of the Month. Enlarged ovary due to granulosa theca cell tumor. J Am Vet Med Assoc. 2015;247(2):153–155.
- 6. ↑
Sabuncu A, Evkuran Dal G, Enginler SO, Kocak O, Arici R. Association of anti-Müllerian hormone concentrations between the pregnancy rates and pregnancy continuity of cows in different age groups. Vet Med (Praha). 2019;64:302–308.
