Examniatino of Changes in Oxytocin Levels by Cassie Gonce

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An Examination of Changes in Oxytocin Levels in Men and Women Before and After Interaction with a Bonded Dog Suzanne C. Miller,* Cathy Kennedy,* Dale DeVoe,* Matthew Hickey,* Tracy Nelson* and Lori Kogan†

ABSTRACT Oxytocin (OT) is a neuropeptide increasingly recognized for its role in bonding, socialization, and stress relief. Previous research has demonstrated participants’ OT levels increased after interacting with or petting a dog, suggesting OT is at least partially responsible for the calm, relaxing feeling that participants experienced during this intervention. The purpose of our study was to more closely examine changes in oxytocin levels in men and women in response to interaction with their own dog after being separated from the dog while at work all day. This condition was compared with a reading control condition, without the presence of the dog. Because the workplace is a common stressor, participants were examined after work to evaluate how interacting with a pet may help decrease stress, as evidenced by increases in serum oxytocin levels. Ten men and ten women participated in the study. Serum oxytocin levels were obtained before the participants had contact with their dogs and then again after 25 minutes of interaction with their dog. The same protocol was followed for the reading condition except that instead of interacting with their dog, participants read nonfiction materials selected by the researchers. Serum oxytocin levels increased statistically more for women who interacted with their dog when compared with women in the reading condition (p = 0.003). There was no significant increase in oxytocin level in men after interaction with the bonded dog compared with the reading condition; in fact, male oxytocin levels decreased after both the dog and reading conditions. These results suggest that men and women may have different hormonal responses to interaction with their dogs. It is unclear to what degree OT reactivity was affected by hormones, personality traits, or interpersonal relationships; factors which warrant further research. Keywords: bonded dog, oxytocin, workplace stress

Address for correspondence: Lori Kogan, Ph.D., 104 Physiology Building, Colorado State University, Fort Collins, CO 80523, USA. E-mail: Lori.Kogan@colostate.edu

Anthrozoös DOI: 10.2752/175303708X390455

* Department of Health and Exercise Science, Colorado State University, USA † Department of Clinical Sciences, Colorado State University, USA

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For many years, researchers have hypothesized about the influence pets may have on their owners’ health, specifically in regard to loneliness, stress, and anxiety. Most information regarding the health benefits of companion animals was anecdotal until the early 1980s, when scientific research into the human–animal bond began in earnest. Evidence of an increased one-year survival rate for pet-owning cardiac patients was discovered (Friedmann et al. 1980) and subsequent research has expanded to explore the neuroendocrine pathways that may account for the positive psychosocial health benefits of pet ownership. Pets may have a positive psychological effect on humans in that they help attenuate emotional responses to stress-producing situations by decreasing sympathetic nervous system arousal and anxiety (Friedmann 1990). Pets may also have a positive effect on depression and loneliness by providing companionship and something to nurture. For example, cat owners have demonstrated fewer psychiatric disturbances than non-cat owners (Straede and Gates 1993). In addition, pets can attenuate the loneliness felt when living alone and may partially compensate for the lack of a human companion (Zasloff and Kidd 1994). Other studies have found positive associations between pet ownership and increased psychosocial functioning in men and women of all ages, including those with cancer and AIDS (Levinson 1983; Garrity et al. 1989; Lago et al. 1989; Wilson 1991; Folse et al. 1994; Holcomb et al. 1997; Norris et al. 1999; Siegel et al. 1999; Johnson et al. 2003). The neurochemical oxytocin may be responsible for the positive feelings people report when interacting with a companion animal (Odendaal and Meintjes 2003). OT facilitates bonding and attachment and has the potential ability to decrease stress and anxiety. When released centrally, OT acts as a neuromodulator of maternal and affiliative behavior, social memory, and the stress response (Pedersen and Prange 1979; Gibbs 1984; Carter et al. 1992; Witt, Winslow and Insel 1992; Windle et al. 1997; Ferguson et al. 2000). Oxytocin levels may change after “feel good” activities such as massage and petting a dog. In one study, increased plasma OT levels were found in women after massage (Turner et al. 1999; Uvnäs-Moberg 2004). In another study, OT levels were measured in both humans and dogs before and after a 30-minute interaction between the humans and dogs. Participants sat quietly on the laboratory floor and spoke softly or petted a dog gently during the intervention. Participants interacted with either their own dog or a dog provided by the researchers. Results demonstrated a significant increase in OT in participants who interacted with their own dog. OT also increased in participants who interacted with an unfamiliar dog, but not to a significant level. Both men and women participated; however, the effect of the participants’ sex on the responses was not reported (Odendaal and Meintjes 2003). This is an important limitation to this study, as there may be different stimuli that affect oxytocin secretion among men and women (Jezova et al. 1996; Petersson, Lundeberg and Uvnäs-Moberg 1999). The purpose of our study was to elaborate on the previous research of Odendaal and Meintjes (2003), by examining how oxytocin levels may change in men and women in response to interaction with their own bonded dog, as compared with a control (reading) condition.

Methods Approval for the study was obtained from the University Regulatory Compliance Committee.

Recruitment We sought to recruit 10 male and 10 female pet owners (all over 18 years of age), who had been employed at least 30 hours a week for the previous 6 months and had owned their dogs

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for at least 6 months. Exclusionary criteria for the study included being pregnant or lactating, taking medication for anxiety or depression, expressing fear of having blood drawn, or expressing a lack of affection for dogs or animals. Participants were recruited in several ways: posting flyers in the community, setting up a booth at a local pet fair, and word-of-mouth. Twenty-eight people expressed interest in the study. Eight volunteers were excluded; seven because they did not meet the inclusion/exclusion criteria and one because she did not have adequate time for the study.

Participants Ten men and ten women participated in the study. All participants were Caucasian. Women ranged in age from 22 to 50 years, with a mean age of 35.9 (SD =10.53). Three women were married and seven were single. Men ranged in age from 22 to 58 years, with a mean age of 38.3 (SD =12.51). Two men were married and eight were single. Number of dogs owned by participants ranged from one to three for women and from one to four for men. All participants were considered primary caregivers of their dogs. All participants lived and worked on the Front Range of eastern Colorado in a variety of occupations such as construction, computer work, and education. All participants provided written informed consent prior to beginning the study.

Procedure This study used a cross-over design, where each participant acted as his/her own control. We met with participants three different times, including an initial interview followed by two testing days (dog intervention and reading/control intervention). Testing occurred at the participants’ homes on two separate occasions, about 1–2 weeks apart, on the same day of the week. Tuesdays, Wednesdays, or Thursdays were designated testing days; Mondays, Fridays, and weekends were excluded because they were not viewed as “average” work days. On testing days, participants were required to have worked all day without contact with their dogs.

Protocol for Dog Intervention: Immediately upon arriving home and before going inside the house, the participant had a baseline serum OT level drawn. The participant did not have contact (visual, auditory, or tactile) with their dog until after baseline measurements were taken. The participants then went into their houses to interact with their dogs as they would normally after returning home from work. This included talking to, petting, and/or playing with their dogs. A maximum time limit for interaction was set at 25 minutes, to minimize potential for boredom or annoyance. We were in another room or outside the home while the participants and dogs were interacting. To help prevent distractions, caution was taken to minimize chances that the dogs were aware of our presence. No other people were present during the intervention and no radios or televisions were on. After 25 minutes had passed, a second blood draw was conducted in the presence of the dogs.

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Initial Interview: The initial interview was scheduled with participants at their home to the discuss procedures that would take place on testing days. This meeting was designed to ensure that study procedures were understood, so that on testing days minimal conversation would take place between researchers and participants. A human–animal bond questionnaire based on the Lexington Attachment to Pets Scale (Johnson, Garrity and Stallones 1992) was completed by each participant. Order of intervention (dog or reading intervention) was randomized. To eliminate a possible order effect, half of the participants completed the dog intervention first and the other half completed the reading intervention first.

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Protocol for the Reading (Control) Intervention: The protocol for the reading intervention was the same as the dog intervention except that the dogs were not present. A baseline OT level was drawn when the participant arrived home and before they went inside the house. Arrangements were made at the initial meeting for someone to take the dogs prior to the participants arriving home. A choice of three neutral books (pertaining to local or state history presented in a factual manner) was offered to each participant, who were then asked to read for 25 minutes. After the reading intervention, a second blood draw was conducted and participants were asked to answer one question regarding their interest in the reading material.

Instruments The blood samples were taken to the Human Performance Clinical Research Lab at Colorado State University for processing and analysis. At the participants’ homes, laboratory samples were collected in serum-separator tubes and placed on ice after 500 KIU/ml aprotinin (SigmaAldrich, St. Louis, MO) was added to the sample. At the laboratory, blood was centrifuged at 5 ˚C for 15 minutes at 3,200 RPM. Serum was removed and frozen at –80 ˚C until all samples were collected. An oxytocin enzyme immunoassay was used (R & D Systems, Minneapolis, MN) to analyze the serum. Sensitivity of the oxytocin assay was less than 4.68 pg/ml. Samples were run in duplicate and then averaged. The Lexington Attachment to Pets Scale (Johnson, Garrity and Stallones 1992) was used to evaluate participant attachment to their dog. This 23-item questionnaire has demonstrated construct validity, as evidenced by a strong correlation between scores on the scale and subjective ratings of pet attachment made by researchers. The scale has high content validity, evidenced by the fact that all items on the scale represent some level of attachment to the pet, as well as high internal consistency (coefficient alpha = 0.93). Examples of questions include, “My pet and I have a very close relationship” and “I feel that my pet is a part of my family.” For our study, we altered the response scale from its original design (0 = strongly disagree to 3 = strongly agree) to a 5-point scale (1 = strongly agree to 5 = strongly disagree, with 3 = neutral) to allow a “neutral” response, so that participants did not feel obligated to agree or disagree with each statement. A score of 23 on the scale represents a person who is maximally bonded to their dog, while a score of 115 indicates a person who is minimally bonded to their dog. Several questions are reverse scaled, so reverse scoring was done with those questions prior to totaling the final score. We created one question for the participants to answer regarding their interest in the reading material. This Reading Question asked the participants to rate their interest in the reading material on a scale of 1 to 5. A score of 1 indicated no interest in the reading material and a score of 5 indicated that the reading material was very interesting.

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Statistical Analysis Given the physiologic and metabolic differences in oxytocin levels between females and males, planned comparisons (a priori) were used to test the specific research hypotheses. These planned comparisons were that there would be differences in change of oxytocin level between 1) dog and reading condition for females and 2) dog and reading condition for males. Statistical analyses were restricted to these differences. A priori simple main effects tests were used to test the specific research hypotheses instead of performing an omnibus F test (Keppel, Saufley and Tokunaga 1992, pp. 140–141). The dependent variable was change in oxytocin level. The statistical program used was SAS 9.1 (SAS Institute Inc., Cary, NC, USA).

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Results A priori simple main effects tests were used to evaluate the effects differences in OT between the two conditions for women and men. Percent changes in OT for men and women from before to after each condition are shown in Figure 1. Means, standard deviations, and ranges of OT for men and women before and after each condition are shown in Table 1.

Figure 1. Percent change in oxytocin level between women and men and between the dog and reading conditions. Table 1. Means, standard deviations, and ranges of raw OT scores in pg/ml.

Men

Post-Book

33.5 ± 37.7

45.2 ± 45.2

54.6 ± 57.6

29.1 ± 21

(8.1–137.9)

(8.2–169.6)

(7.6–202.3)

(4.5–77.8)

77.7 ± 93

61.5 ± 70

131.5 ± 140.7

54.3 ± 78.8

(16.6–334.9)

(13.4–237.9)

(32.2–490)

(12.2–276.2)

For women, the change in OT based on condition (dog or reading) was significant (F(1, 17) = 9.86, p = 0.003), with women having a 58.4% increase in oxytocin level after interacting with their bonded dogs compared with a 26% decrease in oxytocin level after the reading condition. The mean change in OT for women in the dog condition was 11.7 pg/ml (SD = 16.1). The mean change in OT for women in the reading condition was 25.5 pg/ml (SD = 40.3). For men , the change in OT based on condition (dog or reading) was significant (F(1, 17) = 4.71, p = 0.045), with men having a 21.5% decrease in oxytocin level after interacting with their dogs compared with a 56.3% decrease in oxytocin level after the reading condition. The mean change in OT for men in the dog condition was 16.2 pg/ml (SD = 35). The mean change in OT for men in the reading condition was 77.2 pg/ml (SD = 72.8). Individual variability of OT levels is shown in Figures 2–5, which clearly demonstrates the wide range of OT levels in both men and women. Specifically, eight out of ten women demonstrated

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Women

Mean ± SD (range) Post-Dog Pre-Book

Pre-Dog

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increases in serum OT levels after interaction with their dogs. In men, there was no overall significant increase in OT level after interacting with their dogs; in fact, there was an overall decrease in OT level. Interestingly, though, two out of ten men did demonstrate increases in OT level after interaction with their dogs. When individual responses were examined, one woman and one man were found to be greater than 2 SDs from the respective means. When results were recalculated without these two participants, results were the same; the only overall increases in OT were found in women interacting with their dogs. On closer examination of the two outlying participants, the woman had the most dogs in the study (four), while the male outlier was the only participant in the study who had small children. Whether these facts account for why these two participants had much higher OT levels than the other participants is unclear. In general, men had higher OT levels overall compared with women.

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Figure 2. Oxytocin levels in women before and after interaction with bonded dog. Each line represents one person. Increases are shown with a ▲ and decreases are shown with a ■.

Figure 3. Oxytocin levels in women before and after the reading condition. Each line represents one person. Increases are shown with a ▲ and decreases are shown with a ■.

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Figure 4. Oxytocin levels in men before and after interaction with bonded dog. Each line represents one person. Increases are shown with a ▲ and decreases are shown with a ■.

Analysis of the scores on the Lexington Attachment to Pets Scale demonstrated scores for women ranged from 26 to 51 (mean = 37.2, SD = 9.39). Scores for men ranged from 25 to 52 (mean = 39, SD = 9.24). Thus, participants were considered well-bonded to their dogs (based on the possible range of 23 to 115; 23 being most bonded and 115 being least bonded). Further analysis demonstrated no correlation between reported attachment to pets and changes in oxytocin levels when men interacted with their dogs (r = 0.31, p = 0.37) or when women interacted with their dogs (r = 0.26, p = 0.45). Results of the Reading Question showed that 19 out of 20 participants scored between 3 and 5, indicating those participants had some degree of interest in the reading material. Only one participant rated the material a 2, indicating some disinterest in the material. Thus, the vast majority of participants rated the material similarly. This is important for consistency of the control condition.

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Figure 5. Oxytocin levels in men before and after reading condition. Each line represents one person. Increases are shown with a ▲ and decreases are shown with a ■.

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Discussion In our study, we found that serum OT levels rose significantly in women when interacting with their dogs compared with the reading condition; in fact, OT levels dropped for women with the reading condition. In men, OT levels dropped when they interacted with their dogs; however, not nearly as much as the OT level dropped during the reading condition. The responses of the women in our study were similar to responses in previously mentioned studies involving stimulation by massage in female participants (Turner et al. 1999; Uvnäs-Moberg 2004). In these studies, OT levels rose in response to the non-noxious stimulation. In Odendaal and Meintjes (2003), OT levels in men and women participants rose overall in response to petting a dog; however, the authors did not report results for men and women separately. The first conclusion one might draw from these results is that interacting with a bonded dog leads to more relaxation for women than for men. However, close examination of the physiology of OT may change the conclusions we make about the study results. One explanation for these results may be related to the sex hormones estrogen and testosterone. Estrogen is a strong stimulus for OT production and secretion and maintains longer lasting effects in women compared with men (Petersson, Lundeberg and Uvnäs-Moberg 1999). In addition, OT release tends to be greater in women than men, with androgens actually inhibiting release of OT (Jezova et al. 1996). Interestingly, it may be a lack of OT that contributes to menopausal symptoms such as anxiety, depression, and insomnia (Petersson et al. 1998). Shukovski, Healy and Findlay (1989) found that OT levels dropped as progesterone rose during the second half of the menstrual cycle. These authors suggested progesterone may inhibit estrogen-stimulated OT secretion. This raises the question of whether decreased OT levels may contribute to symptoms of pre-menstrual syndrome (PMS), such as irritability, anxiety, trouble concentrating, and mood swings. It should be noted that, even though menstrual cycle was not considered when interventions were scheduled in our study, OT levels were still significantly increased for women when interacting with the dog. In addition to hormones, another issue that makes research in the area of OT reactivity challenging is the complexity of how personality traits and states may affect OT levels. Our results support the hypothesis that increases in OT are related to a calm and relaxed state. This is in contrast to Taylor et al. (2006), who studied post-menopausal women, aged 56–75 years, some who were on hormone replacement therapy and some who were not. They concluded that higher basal levels of OT were related to interpersonal stress, not laboratory stress challenges or recovery. Turner et al. (1999) found basal OT levels also correlated with unhealthy personality traits, such as anxiety, intrusiveness, and coldness. However, OT reactivity was associated with healthy personality traits in this case. The quality of interpersonal relationships may also affect OT levels. Frequent hugs between significant others are associated with higher OT levels (Light, Grewen and Amico 2005). Our study did not examine personality traits or health of interpersonal relationships, so any correlation with the results is not possible. Several major differences in research design between our study and Taylor et al. (2006) may have contributed to differences in findings. The women in our study were 50 years old or younger; none were post-menopausal or on hormone replacement therapy, which could influence OT response. All participants were employed and worked at least 30 hours/week as part of inclusionary criteria, whereas in Taylor et al. (2006) employment status was not controlled. Finally, participants were exposed to the positive experience of interacting with their dog, rather than being exposed to a negative stressor. Thus, research suggests that

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the relationship between OT and stress is not entirely clear. Clarification on whether increases in OT aid in stress reduction or whether they are a reflection of stress is at the forefront of ongoing research. The way in which the participants greeted and interacted with their dogs may also have affected the results. Women are more likely to “tend and befriend,” which may be due to the effects of OT (Taylor et al. 2000). “Calm and connection” is also a phrase that has been used to describe female-specific behaviors that are mediated by OT (Uvnäs-Moberg 2003, pp. 21–26). In contrast, men tend to interact more in a rough-and-tumble fashion due to higher levels of androgens (Collaer and Hines 1995). Observation of how participants interacted with their dogs was not recorded, as the researcher was outside the home when interaction occurred. Since OT levels were drawn only once after interaction with the dog began, there is no way of knowing whether the greatest changes in OT occurred when the participant initially greeted the dog or whether the changes occurred gradually over the 25-minute interaction time. The phenomenon of the “greeting response” has been documented as a significant increase in blood pressure when a research participant initially greeted their own dog (Baun et al. 1984); however, there are no studies of this nature that measured changes in OT before and after the initial greeting of the dog. Different results may have been seen if the interaction time was shorter or longer or if an indwelling catheter had been placed prior to the intervention in order to obtain blood samples more frequently throughout the intervention. However, this would change the methods significantly, in that a researcher would need to be in close proximity to the participants and dogs in order to accomplish this, which may affect the external validity of the project. The half-life of OT is approximately 15 minutes (Amico, Ulbrecht and Robinson 1987), so blood samples were drawn immediately upon termination of the intervention to accurately portray OT activity. Finally, stressors, responses to stressors, and methods of relieving stress are different for men and women (Earle, Linden and Weinberg 1999; Stroud, Salovey and Epel 2002). In our study, we specifically studied the impact of interaction with the dog on stress reduction after a day at work because the workplace is a potential source of stress in today’s society. The National Institute for Occupational Safety and Health indicates that at least 25% of workers report their jobs as extremely stressful (NIOSH 2005). In addition, the amount of work stress correlates with cardiovascular, musculoskeletal, and psychological illnesses and results in significant loss of productive work days (Toppinen et al. 2005). Unlike the Odendaal and Meintjes study, our interventions were conducted in participants’ homes, to better simulate real-life situations (greeting and interacting with their dogs upon arriving home from work). Participants were required to be away from their dogs all day in order to clearly separate the potentially stressful work environment and the potential stress reducing effects of interaction with the dog, making interpretation of OT results more clear. Employment status and separation from the dog prior to study interventions were not controlled by Odendaal and Meintjes (2003). Finally, the study protocol required numerous needle sticks and this cannot be overlooked as a source of stress, even though participants were screened for fear of needle sticks. Even so, it is possible that some anxiety existed in this regard and cannot be dismissed as something that could have affected OT levels. Limitations of our study include that we did not control for the menstrual cycle nor did we evaluate psychosocial background, personality traits, and workplace stress of the participants. Including this information in a follow-up study would allow more information to be gleaned

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about how these conditions might modify or clarify the results. Simultaneous measurement of OT along with other biomarkers of the stress response, such as cortisol, may provide more information on the relationship of OT and stress in future studies. Odendaal and Meintjes (2003) did measure cortisol, along with OT, in their study and found that levels decreased in participants after interaction with the dog, at the same time that OT levels increased.

Conclusion The focus of our study was to examine the potential health benefit of interacting with bonded dogs compared with a reading condition, as measured by serum OT levels in men and women. That women demonstrated increases in OT when interacting with their dogs and decreases when reading alone may be due to the social nature of interacting with a dog that is happy to see you at the end of the day. OT is often referred to as the “affiliation” hormone because of its role in attachment and social interaction (Carter et al. 1992; Winslow and Insel 2002). In addition, OT reactivity in women may be greater due to the influence of estrogen. Given this influence of estrogen on OT, it is important to note that this in no way suggests that dogs do not offer health benefits to men. OT is only one measurable biomarker and may be sex-specific to women. There are other biomarkers that may be more reflective of the health benefits for males. Our study combines the research done in the area of OT with research completed in the human–animal bond arena to study the impact of positive interaction with companion animals on OT levels. Our research evaluates OT as it relates to the attachment that occurs between humans and their pet dogs. In today’s society, it is important to explore ways to reduce stressors. In light of research that examines OT levels with respect to personality traits, interpersonal relationships, menstrual cycles, and stress reduction, our results add to the existing information in this important research area.

Acknowledgement In memory of Popo, King of the Huskies, and to Orizaba, the next generation…

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