Introduction

Nipple-areola reconstruction is the final, important, and essential process of breast reconstruction. Patients with nipple reconstruction after breast reconstruction have higher general and esthetic satisfaction rates than those who had undergone breast reconstruction alone [1,2,3,4]. Nipple-areola reconstruction has been reported to make a psychological contribution and to significantly improve the patients’ overall satisfaction and sexual sensation as well as nude appearance in the reconstructed breast [5]. Nipple-areola reconstruction using nipple and labia minora grafts began in the 1940s, as reported by Adams [6]. Subsequently, areola reconstruction using split and full-thickness skin grafts from the inner thigh [7] and contralateral areola [8, 9] combined with nipple reconstruction was reported. The skin graft from the contralateral areola is good in terms of color tone; however, the size of the reconstructed areola that can be made is limited, and it is not an option for bilateral reconstruction cases. In addition, many patients do not want the skin removed from the normal areola [9].

Studies on nipple-areola tattooing have been published since the 1970s [10,11,12,13,14,15,16,17]. Nipple-areola tattooing is combined with various types of nipples reconstructed with a local flap, as described elsewhere [18]. The major advantages of the nipple-areola tattooing are the thorough control of the shape, position, and color without the need for donors. On the other hand, it has the disadvantage of imposing a large financial burden, as it is not covered by insurance and the tattoo fades over time.

Furthermore, tattooing is not common in Japan and carries some stigma. In addition, nipple-areola tattooing is considered to be a medical practice and must be performed at a medical institution; however, few medical facilities perform such procedures.

Although nipple-areolar tattooing is a well-accepted step in breast reconstruction [2, 3], medical data on the safety of and patient satisfaction with this treatment are insufficient. Thus, we aimed to evaluate the complications of and satisfaction with nipple-areola tattoos in post-mastectomy breast reconstruction patients in Japan.

Material and Methods

This study was ethically approved by the institutional review board (approval number H30-14), and informed consent was obtained from the participants before the questionnaires were provided. Patients who visited our institution’s outpatient clinic (Tokyo, Japan) after undergoing nipple-areola tattooing from January 2017 to March 2020 were provided an unmarked questionnaire with basic questions on age, nipple reconstruction method, date of tattooing, and pigment used for the tattoo. The questionnaire also included a survey of possible complications, based on previous reports [13, 19,20,21,22], after tattooing, including infection and allergic reactions, such as persistent redness, swelling, itch and rash, granuloma, lichenoid reaction, and pseudolymphoma. In a previous survey [23], 60% of the patients cited psychological reasons and 44% cited going to hot springs or public baths as the reason for the breast reconstruction. Consequently, we included patients’ subjective evaluation of their nipple-areola appearance based on a visual analog scale, a 5-point Likert scale, and a free-text section about the contribution of the nipple-areola tattoo to their daily lives.

The questionnaires were completed outside the examination room or at the patients’ homes after a single plastic surgeon explained the purpose of the questionnaire. The questionnaires were collected in a collection box at the entrance of the outpatient clinic (if they were filled in at home, they were collected at the next visit). The survey was not conducted by mail.

Nipple-areola tattooing was performed by a single plastic surgeon, using a tattooing machine (Biotouch, CA, USA, or Ink Machines, Växjö, Sweden) and flesh-toned sterilized pigments (Biotouch), under local anesthesia. The new areola was marked while the patient was standing to make a mirror image of the contralateral side. The colors were mixed manually and made slightly yellowish as compared to the color of the normal side, as recommended in a previous report [24] (Fig. 1).

Fig. 1
figure 1

Breast reconstruction with latissimus dorsi myocutaneous flap and nipple reconstruction with modified C-V flap. a First, trace the contralateral areola with a clear film with a hole in the center and make a mirror image. b Second, mix the pigments manually and make it slightly yellowish as compared to the normal side. c Tattoo was performed with 7 needle tattoo machine. d The patient before nipple-areola tattoo. e The color is slightly darker immediately after the tattoo

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Patients who were followed up within 6 months after getting a tattoo and those who did not fully respond to questions about complications, VAS scale of nipple-areola appearance, and overall satisfaction by Likert scale were excluded. We also excluded patients with unknown basic information, such as age, method of nipple reconstruction, tattoo date, and pigment used.

Statistical Analysis

All statistical analyses including the determination of means and standard deviations were performed using Stata, version 10.1 (Lightstone, Tokyo, Japan).

Results

Sixty-two patients were included in this study. The average age of the patients was 49.7 ± 9.8 years, and the post-tattooing period was 21.2 ± 10.5 months. Of the 62 patients enrolled in our study, 22 needed a second tattoo. As tattoo color duration depends on its darkness, additional tattoos were performed 7.1 ± 6.5 months after the first tattoo was applied. For nipple reconstruction, a modified C-V flap was used in 59 cases, two cases had a nipple transplant, and one patient had a 3D tattoo. The patients’ characteristics are detailed in Table 1. In this series, an average of 3.2 ± 0.9 colorants (five colors maximum) was used per person, from a total of nine colorants. The nine colorants were a mixture of the following four metal particles: three iron oxides and one titanium dioxide. An ocher color, “toffee,” was used in 60 cases (96.8%), and a reddish color, “pink brick,” was used in 43 cases (69.4%) (Table 2).

Table 1. Clinical patient characteristics
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Table 2. Colorants used for tattoo.
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The average visual analog scale score for the subjective evaluation of the nipple-areola appearance was high (8.5 ± 1.5). Regarding the patients’ overall satisfaction, the average score on the 5-point Likert scale was also high (4.5 ± 0.6). Fifty-nine of the 62 patients (95.3%) answered that they were satisfied (Figs. 2,3). The majority of patients reported high esthetic and overall satisfaction after undergoing nipple-areola tattooing. Fifty-eight of 62 patients responded to the question of whether the tattoo had an impact on their daily life; of these, 49 patients (79.0%) stated that their lives were changed by the tattoo. In the free-text section, 25 patients answered that they could now go to the hot springs, and 19 patients reported that their mental health has improved, as they felt happier and unbothered (Table 3). Although this part of the questionnaire was open-ended, the answers tended to be grouped into the two aforementioned categories.

Fig. 2
figure 2

Patient nipple-areola appearance before a and 8 months after b tattoo application. This patient had breast implant and nipple reconstruction with modified C-V flap. Four pigments were used for her tattoo. This patient still had a good color match 8 months after the tattoo. The VAS for the nipple-areola appearance was 8 and she was very satisfied with her tattoo

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Fig. 3
figure 3

Patient nipple-areola appearance before a and 25 months after b tattoo application. This patient had free transverse rectus abdominis myocutaneous flap and nipple reconstruction with modified C-V flap. Two pigments were used for her tattoo. This patient still had a good color match 25 months after the tattoo. The VAS for the nipple-areola appearance was 10 and was very satisfied with her tattoo

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Table 3. Post-tattoo questionnaire findings.
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Discussion

This study investigated the safety of and patient satisfaction with nipple-areola tattooing in Japanese patients who underwent breast reconstruction. None of the patients experienced any of the major complications of tattooing. Moreover, the majority of patients reported high esthetic and overall satisfaction after the procedure. These results show that nipple-areola tattooing is a safe and satisfying procedure, which should be recommended to post-breast reconstruction patients.

There have been a few reports summarizing the complications of nipple-areola tattooing. Spear et al. [13] conducted a retrospective study of 151 patients with a mean follow-up period of 25.2 months and reported that five patients (3.3%) developed an infection. Infections, including bacterial and viral infections, are among the major complications after tattooing [21, 25]. As a general post-tattoo infection rate, in a cross-sectional survey of 501 participants in the United States, Liszewski et al. [26] reported that 3.2% of their subjects had a history of an infected tattoo and 21.2% had a history of a pruritic tattoo. Kluger [27] assessed the prevalence of cutaneous complications of tattooing among a cohort of 448 French tattooists. They reported that 6.2% had an infection after getting one of their tattoos.

In contrast, no infections occurred in the study participants. A nipple-areola tattoo is smaller than the regular tattoos, and the risk of infection is considered to be low. Patients who have undergone breast reconstruction may need to be particularly aware of the signs and symptoms of infections because they may have breast implants or may have undergone post-mastectomy radiation. We consider that the use of a clean procedure, equivalent to surgery, and the use of sterile equipment and pigments led to the absence of infection cases in our study. In addition, we recommend an outpatient visit at 2 days, 1 week, and 1 month after the tattoo procedure, to ensure proper wound management and to prevent the development of infections.

Another complication of concern after tattooing is allergy. We could not find any previous reports on allergy after nipple-areola tattooing. As a general post-tattoo allergy rate, Kluger [27] reported that 8.5% of 448 French tattooists had an allergic reaction to at least one of their tattoos. In addition, 94% of these were colored tattoos. Serup et al. [28] reported that 85% of the patients who came to their hospital with the chief complaint of allergy after tattooing had used a reddish pigment. Until recently, inorganic compounds, including cadmium and mercury compounds, were used as red tattoo pigments [29]; however, as these compounds have been reported as being carcinogenic, they are now less commonly used [30]. Instead, azo compounds, which are organic compounds, are now the mainstream tattoo pigments. Azo compounds are cheap and allow the generation of various colors. However, aromatic amines, which are the decomposition products of azo compounds, have been suggested to pose a risk for tattoo allergies [20, 25, 31,32,33].

The red pigment is essential for a nipple-areola tattoo, and thus, it is important to choose safe ingredients. In this study, we chose a red pigment made of iron oxide. This red iron oxide is used not only for cosmetics and food additives but also as a contrast agent for magnetic resonance imaging. Although it has a rusty color, we consider it to be safer than organic pigments, as reported by Spear et al. [13] and Serup et al. [34]. Spear et al. [13] conducted a cohort study of 151 nipple-areola tattoos and reported no allergies in many patients who were tattooed using the pigments, from various manufacturers, that contained iron oxide or titanium dioxide. In all patients in our survey, the pigment used contained red iron oxide. Although the minimum follow-up period was 6 months (mean, 21.2 months), no patient reported any allergic tattoo reaction. Nevertheless, further long-term follow-up is warranted.

Nipple reconstruction has been reported to significantly improve the esthetics and overall satisfaction after breast reconstruction [1,2,3,4]. To date, no studies have quantitatively compared patient satisfaction before and after tattooing. Smallman et al. [35] performed a quantitative assessment before and at 2 weeks after nipple-areola tattooing, using BREAST-Q, and concluded that tattoos significantly improved patient satisfaction. Similarly, in the present survey, those with a nipple-areola tattoo had high esthetic and overall satisfaction. In particular, 95.3% of the respondents reported high overall satisfaction using the 5-point Likert scale. However, it is also likely that patients who are satisfied with their breast reconstruction may also be likely to undergo nipple reconstruction. Therefore, we think it necessary to evaluate the esthetic and overall satisfaction of patients before and after the nipple-areola reconstruction.

According to the National Database of Health Insurance Claims and Specific Health Checkups of Japan (NDB open data) [36], compared with 7993 breast reconstructions performed in 2018, only 2077 nipple reconstructions were performed, equating to 26.0% of the number of breast reconstructions. In 2017, breast reconstructions were performed in 8162 cases, and 1857 nipple reconstructions were performed, equating to 22.8% of the number of breast reconstructions. For Japanese individuals who have a culture of bathing with others, such as in public baths and hot springs, we recommend that the nipple-areola reconstruction be performed. Based on our study and previous reports, there is a high level of satisfaction with nipple-areola reconstruction and tattooing; therefore, we urge more patients who had undergone breast reconstruction to consider nipple-areola reconstruction and tattooing.

There may be several reasons why nipple reconstruction is not widespread in Japan. First, it is not easy to ensure a good color for the areola, such as when using a skin graft from another region. Second, tattooing procedures providing a suitable color is expensive, because they are not covered by insurance. Third, not many clinics perform nipple-areola tattooing. Finally, the tattooing rates are low in Japan, as compared to elsewhere [37, 38], and tattoos tend to be stigmatized. However, the esthetic and psychological satisfaction after nipple-areola tattooing in Japanese breast cancer patients was high in our study. Additionally, patients were able to enjoy the unique Japanese culture of visiting hot springs and public baths.

In many countries, including the United States and Europe, tattooing and permanent makeup are performed by qualified tattooists, not doctors. Japan is unique in that it is required that doctors and nurses perform tattooing to patients. Therefore, in Japan, the treatment of complications is often performed at the same hospital, making it easy to investigate the causes of complications. We will continue to conduct research on safe treatments and pigments in the future.

Limitations

This study had some limitations. First, the sample size of this cohort study was small. Second, there is a potential for selection bias given that patients were recruited from only one medical center. Third, as a single population was studied, the results may not be generalizable to different populations.

Conclusion

Our study concluded that nipple-areola tattooing after breast reconstruction could achieve highly satisfactory esthetics, without serious complications, when provided as a medical treatment. Even though tattoos are somewhat stigmatized in Japan, nipple-areola tattoos are useful for patients who have undergone breast reconstruction. It is particularly recommended for Japanese individuals with a culture of visiting hot springs and public baths.