Emily
Editor, Senior Moderator
Hart BL, Hart LA, Thigpen AP, Willits NH (2014) Long-Term Health Effects of Neutering Dogs: Comparison of Labrador Retrievers with Golden Retrievers. PLoS ONE 9(7): e102241. doi:10.1371/journal.pone.0102241 Editor: Roger A. Coulombe, Utah State University, United States of America
Received: March 5, 2014; Accepted: June 17, 2014; Published: July 14, 2014
Copyright: ? 2014 Hart et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by the Canine Health Foundation (#01488-A) and the Center for Companion Animal Health University of California, Davis (# 2009-54-F/M). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
[h=2]Introduction[/h] In the last three decades, the practice of spaying female dogs and castrating males (both referred to herein as neutering) has greatly increased. The current estimate is that in the U.S., 83 percent of all dogs are neutered [1] and, increasingly, neutering is being performed prior to 6 mo., as advocated by many veterinarians and animal activists. The impetus for this widespread practice is presumably pet population control, and the belief that mammary gland and prostate cancers are prevented and aggressive male behavior is markedly less likely than in those neutered later. This societal practice in the U.S. continues to contrast with the general attitudes in many European countries, where neutering is commonly avoided and not promoted by animal health authorities [2]?[4].
In the last decade or so, studies have pointed to some of the adverse effects of neutering in dogs on several long-term health parameters by looking at one disease syndrome in one breed or in pooling data from several breeds. With regard to cancers, a study on osteosarcoma (OSA) in several breeds found a 2-fold increase in neutered dogs relative to intact dogs [5], and in Rottweilers neutering prior to 1 year of age was associated with an increased occurrence of OSA to 3?4 times that of intact dogs [6].
A study of cardiac hemangiosarcoma (HSA) in spayed females found that the incidence of this cancer was 4 times greater than that of intact females [7] and another on splenic HSA in spayed females found rates 2 times greater than of intact females [8]. A study on lymphosarcoma (lymphoma, LSA) found that neutered females had a higher incidence of the disease than intact females [9]. Cutaneous mast cell tumors (MCT) were studied in several dog breeds revealing an increase in incidence in neutered females to 4 times that of intact females [10]. Another cancer of concern is prostate cancer that, in contrast to humans, is potentiated by the removal of testosterone. One extensive study found that this cancer occurred in neutered males 4 times as frequently as in intact males [11].
The most frequently mentioned advantage of early neutering of female dogs is protection against mammary cancer (MC) [12]. However, a recent meta-analysis of published studies on neutering females and MC found that the evidence linking neutering to a reduced risk of MC is weak [13].
Three very recent studies are particularly relevant in the discussion of neutering and cancers. One was a comprehensive study, from this center, on neutering in 759 Golden Retrievers where males were compared with females and effects of neutering were evaluated in early-neutered (<1 year), late-neutered (>1 year) and intact dogs [14]. Almost 10 percent of early-neutered males were diagnosed with LSA, 3 times more than intact males. There were no cases of MCT in intact females, but in late-neutered females the rate was nearly 6 percent. The incidence of HSA in late-neutered females was also higher than that of intact females. The occurrence of MC was very low and was only seen in a couple of late-neutered females.
A study utilizing the Veterinary Medical Database of over 40,000 dogs found that neutered males and females were more likely to die of cancer than intact dogs, especially of OSA, LSA and MCT [15]. This study included no information on age of neutering. The most recent publication in this area is a study of Vizslas utilizing owner-reported disease occurrence in an online survey, in which the incidence of cancers was reported higher in neutered dogs than in intact dogs [16]. The main cancers related to neutering were LSA, HSA and MCT. The occurrence of MC was very low in females left intact.
With regard to joint disorders, one study of effects of neutering in larger breeds documents a 3-fold increase in excessive tibial plateau angle ? a known risk factor for development of cranial cruciate ligament tears or rupture (CCL) [17]. Across several breeds, a study of CCL found that neutered males and females were 2 to 3 times more likely than intact dogs to have this disorder [18]. Neither study examined early versus late neutering with regard to this disorder. The study from this center of neutering in Golden Retrievers (mentioned above with regard to cancers [14]) included examination of joint disorders. Of the early-neutered males, 10 percent were diagnosed with hip dysplasia (HD), double the occurrence of that in intact males. There were no cases of CCL diagnosed in intact males or females, but in early-neutered males and females the occurrences were 5 percent and 8 percent, respectively.
One factor that merits attention with regard to the effects of neutering on joint disorders relates to documented effects of neutering in increasing body weight [19], as reflected in body condition score (BCS). Additional weight on the joints is considered to play a role in the onset of joint disorders [19], [20]. While neutering is expected to increase BCS, the issue of concern here is whether neutered dogs with a joint disorder have consistently higher BCSs at the time of diagnosis than do neutered dogs without the joint disorder in the same age range. In the previous analyses on Goldens [14] there was no consistent and major difference in BCS between early neutered dogs with and without a joint disorder. For dogs diagnosed with a joint disorder, some increase in BCS would be expected as a function of less activity due to discomfort from painful joints. Therefore, a modestly higher BCS was predicted for neutered dogs with a joint disorder than in the neutered counterparts without a joint disorder.
The above study on Golden Retrievers [14] raised a major question about breed differences in the effects of neutering, which are relevant for breeders and caregivers of puppies when deciding if, and when, to neuter. A more basic issue concerns insights into the possible pathogenic factors triggering the occurrence of the cancers under consideration. The present study, using the same veterinary hospital database, explored the effects of neutering on joint disorders and cancers in the popular Labrador Retriever to compare with the Golden Retriever, with an addition of several years to the database. The age periods of neutering were refined as <6 mo., 6?11 mo., 12?23 mo. (1 year), and 2 through 8 years to provide more detailed information on the effects of gonadal hormone removal. The Golden is known for being particularly vulnerable to cancers [21], so we expected some major differences from the Labrador where cancer-related deaths are less frequent than in Goldens [21].
In addition to reporting on the incidence of the individual joint disorders and cancers, a new slant on analyses in the present study combined the incidence of all three joint disorders that have shown evidence of being increased by neutering (HD, CCL, and elbow dysplasia, ED) for one data-point representing the incidence of dogs diagnosed with at least one of the joint disorders, after controlling for multiple diagnoses. This analysis was based on the perspective that for dog owners or breeders, avoidance of any of the debilitating joint disorders would be of prime interest. This analysis was also deemed logical for pathophysiological reasons because a disruption of the growth plate closure by gonadal hormone removal in the joint developmental stage would be expected to apply to all the joint disorders. The study also combined the incidence of dogs diagnosed with at least one of the cancers (LSA, HSA, MCT) for one data point, after controlling for multiple diagnoses, because for dog owners avoidance of any of the cancers would be important. This analysis seemed logical, as there may be a common factor involved in increasing these three particular cancers in neutered dogs because these cancers are repeatedly reported as being increased by neutering in several studies...
Full text at link.