温泉科学（J. Hot Spring Sci.），70，50-60（2020）

原著

Initial Trials of Monochloramine Disinfection of
Circulating Bathtub Water at Public Hot Spring
Facilities and Determining its Efficacy
Yasunori Mori1）2）*, Keita Yanagimoto3）, Tetsuji Yamamoto4）, Yuki Nagai1）,
Hideki Yoshimura1）, Shigehiro Akachi1）**, Takaya Yamagami3）, Kosei Uematsu3）,
Yoshiko Hisada3）, Masaya Nishio4）, Jyurina Yagi4） and Shinji Izumiyama5）(Received May 1, 2020, Accepted Jun. 12, 2020)

温泉を用いた公衆浴場におけるモノクロラミン消毒の試行とその有用性
森 康則1）2）*，栁本恵太3），山本哲司4），永井佑樹1），吉村英基1），赤地重宏1）**，
山上隆也3），植松香星3），久田美子3），西尾正也4），八木樹里奈4），泉山信司5）要旨

本研究では，手投入による簡易的なモノクロラミン消毒による浴用水中のレジオネラ属菌をはじめとする微生物学的，理化学的モニタリングを行うことにより，その消毒効果の検証を行った．従来の消毒方法である次亜塩素酸ナトリウムによる消毒効果の減弱が指摘されている
高 pH と高濃度のアンモニア態窒素を含む温泉を利用する施設を対象とした．研究の結果，いずれの浴用水，配管内部からもレジオネラ属菌は検出されなかったことから，手投入の簡易的なモノクロラミン消毒であっても，レジオネラ属菌の殺菌に効果があるものと考えられた．本
研究の結果から，手投入による簡易型モノクロラミン消毒であっても，レジオネラ属菌の制御が可能となることが示唆された．今後，従来型の次亜塩素酸ナトリウム消毒に阻害要因を持つ
温泉水を利用している施設がモノクロラミン消毒の導入を検討する場合，初期投資を要しない
本方法でその試行を行うことが可能となる．
1)

Mie Prefecture Health and Environment Research Institute, 3684-11 Sakura-cho, Yokkaichi, Mie, 5121211, Japan. 1）三重県保健環境研究所 〒512-1211 三重県四日市市桜町 3684-11.
2)Graduate School of Bioresource, Mie University, 1577 Kurima-machiya-cho, Tsu, Mie 514-8507, Japan.
2）
三重大学大学院生物資源学研究科 〒514-8507 三重県津市栗真町屋町 1577.
3)
Yamanashi Institute of Public Health and Environment, 1-7-31 Fujimi, Kofu, Yamanashi, 400-0027,
Japan. 3）山梨県衛生環境研究所 〒400-0027 山梨県甲府市富士見 1-7-31.
4)Household Products Research, Kao Corporation, 1334 Minato, Wakayama, Wakayama 640-8580, Japan.
4）
花王ハウスホールド研究所 〒640-8580 和歌山県和歌山市湊 1334 番地．
5)
National Institute of Infectious Diseases, 1-23-1 Toyama, Shinjyuku-ku, Tokyo, 162-8640, Japan. 5）国立感染症研究所 〒162-8640 東京都新宿区戸山 1-23-1.
*Corresponding author：E-mail moriy04@pref.mie.lg.jp, TEL 059-329-2917, FAX 059-329-3004.
**Former institute.

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キーワード：レジオネラ属菌，モノクロラミン，高 pH，NH4-N，手投入，循環ろ過

Abstract
In this study, the effect of monochloramine disinfection by simple manual addition wasverified through the microbiological and chemical monitoring of bathtub water. The
research focuses on hot spring facilities that use hot spring waters containing high pH andhigh NH4-N concentrations, because these conditions diminish the effectiveness of sodium
hypochlorite disinfection. Using the manual application of monochloramine as a disinfectant,Legionella spp. was not detected in the bathtub water or inside the pipes. Therefore, thesimple manual disinfection using monochloramine was suggested to effectively control
Legionella spp. These results imply that monochloramine disinfection by simple manual
addition can control Legionella spp. Hot spring facilities using hot spring water unsuited tosodium hypochlorite disinfection that are considering the introduction of monochloramine
disinfection, can verify this method without upfront costs.
Key words : Legionella spp., monochloramine, high pH, NH4-N, manual addition, circulation
filtration system

1.

Introduction

In many hot spring facilities, sodium hypochlorite has been widely used as a method of
disinfecting bathtub water because of its low cost and the simplicity of handling. However, it
has been shown that sodium hypochlorite can be inhibited by the chemical qualities of hot
spring water, thereby reducing its disinfection effects. Therefore, sodium hypochlorite may notalways be appropriate as a disinfectant, depending on the chemical qualities and dissolved
components of the hot spring water (Yanagimoto et al., 2015).
Monochloramine is an effective disinfectant for controlling Legionella spp. (Jakubek et al.,2013). It is reported that biofilms adhering to pipes can be controlled using monochloramine(Kool et al., 2000 ; Flannery et al., 2006). In 2019, the Ministry of Health, Labor and Welfare
issued the “Guidelines for the Management of Environmental Health in Public Bath Facility”(Minister of Health, Labor and Welfare, Deputy Vice-Minister for Public Health and Food Safety,2019) and the “Manual for Prevention of Legionella Disease in Bath of Circulating Filtration
System” (Minister of Health, Labor and Welfare, Pharmaceutical Safety and Environmental
Health Bureau, Environmental Health Division, 2019), recommending the use of monochloramine
disinfection for hot spring water that has a high pH or contains high concentrations ofammonium ions, for which the disinfection effects of sodium hypochlorite are reduced.
Monochloramine is prepared from a formulation containing ammonium sulfate or ammonium
chloride, and a formulation containing sodium hypochlorite or calcium hypochlorite. These
formulations are necessary because monochloramine cannot be preserved.
In some public bath facilities, automatic addition equipment is installed before the filter inthe circulation filtration system to perform automatic monochloramine addition. However, installation of the automatic addition equipment requires an upfront cost, which appears to discourage
the usage of monochloramine disinfection.
However, monochloramine disinfection by manual addition does not involve an upfront cost.
51

森 康則，栁本恵太，山本哲司，永井佑樹，吉村英基，赤地重宏，山上隆也，植松香星，久田美子，西尾正也，八木樹里奈，泉山信司

温泉科学

It is considered that the effect of monochloramine disinfection on hot spring water can be experimentally verified. Therefore, in this study, we performed monochloramine disinfection by manual
addition and monitored Legionella spp. in the bathtub water to determine its disinfection effect.

2.
2. 1

Methods

Target facilities and characteristics of hot spring water quality
This study was carried out in cooperation with two hot spring facilities that have chemicalcompositions that affect the disinfection efficacy of sodium hypochlorite. In selecting thesetarget facilities, we focused on hot spring water that has a high pH and contains high ammonium
ion concentrations, which can significantly reduce the efficacy of sodium hypochlorite
disinfection.
Table 1 shows an overview of the hot spring water quality used in these targeted hot spring
facilities.
Station A is a hot spring facility located in Yamanashi Prefecture in Japan. It uses hot
spring water with an extremely high pH (i.e., exceeding 10). The concentration of dissolved
components in the hot spring water is low, and the concentrations of ammonium nitrogen andmetal components, which inhibit sodium hypochlorite disinfection, are also low.
Conversely, Station B is a hot spring facility located in Mie Prefecture in Japan. The hotspring water here is characterized by its high ammonium nitrogen concentration (NH4-N) of
3.3 mg/L.
In hot springs containing more than 1 mg/L of ammonium nitrogen, it is difficult to adjust
the sodium hypochlorite concentration on site, and problems, such as disinfecting odor anddisinfection by-products, can arise. This is further described in the “Manual for Prevention of
Legionella Disease in Bath of Circulating Filtration System” (Minister of Health, Labor andWelfare, Pharmaceutical Safety and Environmental Health Bureau, Environmental Health
Division, 2019). Therefore, it can be inferred that the ammonium nitrogen (3.3 mg/kg) in Station
B had slightly higher concentration for adequate sodium hypochlorite disinfection.
It is also rich in metal ions, with a total Fe ion (Fe2+＋Fe3+) concentration of 4.5 mg/L, and a
Mn ion (Mn2+) concentration of 2.3 mg/L. The hot spring water gradually becomes colored as
the metal ions are oxidized after emerging onto the ground surface. Neither hot spring contains
sulfur components such as hydrogen sulfide (H2S), hydrogen sulfide ions (HS－), or thiosulfate ions
(S2O32－), which contribute to total sulfur content.
In general, these facilities are disinfected using sodium hypochlorite ; however, disinfecting

Table 1

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Water quality parameters of targeted hot springs

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using this method can be difficult. As an evidence, in Station A, 100 CFU/100 mL of Legionella spp.
was detected in the bathtub water in a preliminary investigation prior to this study. Moreover,predominantly in Station B, several cases of Legionella spp. were detected in the past, and there
were cases of Legionella infection. Legionella spp. was tested at Station B at the time of theoutbreak and as a result, Legionella spp. in the bathtub water was detected to be 98-9,500
CFU/100 mL, and more than 30,000 CFU/100 mL Legionella spp. was detected in the hot springtank (Ohno et al., 2016). In this study, the effects of monochloramine disinfection in the hotspring facilities was verified with an aim to drastically improve these situations.
2. 2

Monochloramine disinfection method
Table 2 shows an overview of the bathtubs and circulation filtration system used in thisfield test.
For the purposes of this study, Station A selected an open-air bathtub (approximately 3 m3)and Station B selected an indoor bathtub (approximately 5.6 m3). At Station A, the bathtub
water was changed completely every day and the bathtub was cleaned each time.
Station B normally exchanged the bathtub water daily. However, at our request, during thetest period of this study, the bathtub water was not changed.
While both hot spring facilities normally use sodium hypochlorite as a disinfectant, they did
not during the test period. Notices that monochloramine disinfection was implemented wereshown near the bathtub at targeted facilities, out of consideration for the facility users.
The disinfectant to be added to the bathtub water for monochloramine disinfection was
prepared on-site at the time of use. Granules of ammonium chloride covered with a polyethylene
glycol and calcium hydroxide (hereafter referred to as “Agent A”) and granules of calcium
hypochlorite (hereafter referred to as “Agent B”) were prepared.

The weight ratios ofammonium chloride, polyethylene glycol, and calcium hydroxide of Agent A are 52.4%, 17.7%,
and 29.9%, respectively.
Tap water (5 L) was placed in a plastic container, and 24 g of Agent A and 14 g of Agent B
were added. The container was shaken to allow both agents to dissolve completely. This mixture was added manually to the bathtub water through the circulation filtration system. The
control standard monochloramine concentration was set at 3 ppm so as not to fall below the
Table 2

Details of targeted hot spring facilities and equipment during the test period※1

Only during the field test period. Station B normally exchanges the bathtub water daily. However, at ourrequest, during the test period of this study, the bathtub water was not changed.

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森 康則，栁本恵太，山本哲司，永井佑樹，吉村英基，赤地重宏，山上隆也，植松香星，久田美子，西尾正也，八木樹里奈，泉山信司

温泉科学

control standard.
Sugiyama (2019) reported that when the bathtub water was not disinfected, various bacteria
were detected on the first day, amoeba were detected on the second day, and Legionella spp. on
the third day. Based on this research, the examination period of monochloramine disinfection was
set to be 4 to 5 days longer than the period required for the appearance of Legionella spp. as thisstudy’s purpose was to verify whether the appearance of Legionella spp. could be suppressed bymonochloramine disinfection during the test period.
The frequency of addition was approximately once in the morning and once in the afternoon.
Meanwhile, monochloramine measurements were recorded once every 1-2 hours. If the measurement result was ＜ 3 ppm, a supplemental addition was performed.
2. 3

Sampling and analysis methods
Samples were collected at each facility by the methods described in 1). These samples wereimmediately transported to the laboratory and analyzed using the methods described in 2).
Monochloramine concentrations in the bathtub water were measured with a pocket colorimeter(HACH DR-300), using the indophenol method.
1)

Sampling method
Sample water :Water samples were collected from the bathtub outside operating hours.
Wiping sample (only Station A) :Wiping samples were collected by wiping the pipe inside the circulation filtration system (i.e.,
inside the hair catcher).
Transportation and storage :Samples were stored under refrigeration, except for the samples for amoeba culture, whichwere stored at room temperature, and were immediately brought into the laboratory for
analysis.

2)

Analysis method
pH :Glass electrode method.
NH4-N :
Indophenol method.
Total Organic Carbon (TOC) (only Station B) :Wet oxidation method.
Legionella spp. :Sample water (500 mL) was concentrated 100 times with a polycarbonate filter with a 0.2 µm
pore size. The concentrations and wiping samples were heat-treated or acid-treated andinoculated on a GVPC agar medium and a BCYEα agar medium and cultured at 36℃ for 7
days. If necessary, an identification test using PCR (polymerase chain reaction) was performed.
Viable bacteria :Sample water (1 mL) was diluted at an appropriate magnification. The diluted sample was
inoculated on a standard agar medium by a pour medium method and cultured at 36℃ for
24 h.

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Heterotrophic bacteria :Sample water (1 mL) was diluted at an appropriate magnification. The diluted sample was
inoculated on a R2A agar medium by a pour medium method and was cultured at 42℃ for
2 weeks.
Amoeba :Sample water (1 mL) was inoculated on an E. coli-coated nutrient agar medium and wascultured at 42℃ for 7 days.
Coliform group :Sample water (100 mL) was inoculated into a specific enzyme substrate medium (X-Gal MUG
medium supplemented with pyruvate) and was cultured at 36℃ for 24 h.

3.
3. 1

Results and Discussions

Monochloramine concentration
Figure 1 shows the variations of monochloramine concentration at Station A (A) and Station

B (B).
Monochloramine concentrations were measured on-site every 1-2 hours during operating
hours and remained stable at approximately 3 ppm or more.
3. 2

Microbiological and chemical feature
Table 3 lists the microbiological and chemical analysis results, including Legionella spp.

detection.
In Station A, which has a high pH hot spring water, Legionella spp. was not detected in thebathtub water during the test period. Similarly, Legionella spp. was not detected in any of thewiping samples collected inside the circulation filtration system of Station A. In addition, amoeba

Fig. 1 Changes in the monochloramine concentrations in bathtub water for Station A (A), andStation B (B).  Broken lines indicate the control standard of 3 ppm monochloramine.  The blankspace between the second and third days of (A) indicates the closing of the facility.   Monochloramine was added once in the morning and once in the afternoon.  As a result, the control
standard of the monochloramine concentration was almost satisfied.

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森 康則，栁本恵太，山本哲司，永井佑樹，吉村英基，赤地重宏，山上隆也，植松香星，久田美子，西尾正也，八木樹里奈，泉山信司
Table 3

温泉科学

Water quality investigation results※

CFU means “colony forming unit”.
N.D. means “not detected.”※
Sampling dates are 30/Jul/2018-3/Aug/2018 (Station A), and 11/Jun/2018-15/Jun/2018 (Station B).
※1“Viable bacteria” in this table shows the colony counts by standard agar medium, and “Heterotrophic
bacteria” in this table shows the colony counts by R2A agar medium.
※and the coliform group were not detected.
In Station B, which has hot spring water containing a high NH4-N concentration, no Legionella
spp. was detected in the bathtub water during the test period.
These results imply that monochloramine disinfection was effective in the selected facilities.
3. 3

Levels of viable and heterotrophic bacteria
Regarding Legionella spp., all samples were negative. However, all the viable bacteria

samples were positive in Station A and Station B except for one sample after a single day. This
result was the same for heterotrophic bacteria. In particular, in Station B, the number of viable
and heterotrophic bacteria gradually increased over the test period (Fig. 2).
Previous studies have reported that bacteria in bathtub water cannot be effectively disinfectedwith monochloramine (Mori et al., 2019) because some bacteria can be resistant to monochloramine
disinfection. The results in this study are consistent with these findings.
Watanabe et al. (2018) analyzed circulating bathtub water that underwent monochloramine
disinfection and found that the dominant species of heterotrophic bacteria detected was
Mycolibacterium phlei. (hereinafter referred to as “M. phlei.”). Furthermore, comparing theresistance of M. phlei. to monochloramine and sodium hypochlorite disinfectants, it was reported
that the number of bacteria increased under the monochloramine disinfection environment. As
M. phlei. uses ammonia as a substrate (Kuenen and Robertson, 1994), they found that excessammonia under monochloramine disinfection may have attributed to the growth of M. phlei.
Although heterotrophic bacteria were not identified in this study, it is highly possible thatheterotrophic bacteria, such as M. phlei., increased.
Analyzing the results further by each facility, both viable and heterotrophic bacteria weredetected at Station A, although the number of bacteria did not increase. Conversely, Station B
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Fig. 2 Changes of the number of viable and heterotrophic bacteria and totalorganic carbon (TOC) concentrations in bathtub water at Station B.  
“Viable bacteria”in this figure shows the colony counts of colony bystandard agar medium, and“Heterotrophic bacteria”in this figure shows
the colony counts by R2A agar medium (see text).

contained 1,080 CFU/mL for viable bacteria after 4 days, and 210 CFU/mL for heterotrophic
bacteria after 4 days. Based on these results, we determined that it was more difficult to control
the bacteria in Station B than Station A.
3. 4

Legionella spp. growth risk process inferred from chemical indicators
We explored the differences in the difficulty of controlling bacteria in two hot spring facilities.

In this study, NH4-N, TOC concentrations, and the pH of bathtub water were analyzed at Station
B as chemical pollution indicators. Increases in pH, NH4-N, and TOC concentrations were observed(Table 3 and Fig. 2).
It is presumed that the increase in the NH4-N concentration was due to the addition of
monochloramine, and that the increase in the TOC concentration was due to perspiration anddirt washed off the bath users. In addition, variations of these concentrations significantly
depended on the number of bath users as well as the amount of additional hot spring watersupplied.
However, the most prominent variation factor may be the frequency of bathtub water
replacement. In many case, the concentration of dissolved components (including organic
matter) increase proportionally in the bathtub water unless otherwise vaporized or precipitated(Mori et al., 2010).
The higher the organic matter concentration in the bathtub water, the higher the risk ofbacteria growth, as bacteria may consume that organic matter. Also, as the number of viable
and heterotrophic bacteria increases, the risk of growth of amoeba preying on them may increase.
Additionally, dirt accumulation may lead to an increased risk of Legionella spp. growth on57

森 康則，栁本恵太，山本哲司，永井佑樹，吉村英基，赤地重宏，山上隆也，植松香星，久田美子，西尾正也，八木樹里奈，泉山信司

温泉科学

amoeba.
The “Guidelines for the Management of Environmental Health in Public Bath Facility”(Minister of Health, Labor and Welfare, Deputy Vice-Minister for Public Health and Food Safety,2019), specifies the following : “Change the bathtub water every day and clean the bathtub.
However, even if this is difficult, clean the bathtub by cleaning water completely at least once a
week.” If there is an interval of several days between complete water changes, an increase in
the concentration of chemical components due to bath users is unavoidable. However, it isimportant to understand that this leads to the risk of Legionella spp. growth.
In Station A, it was assumed that the chemical and microbiological contamination returnedto the initial state every time the water was replaced. Therefore, it is necessary to completely
exchange the water, clean the pipes of the circulation filtration system, and clean the bathtub
itself in order to prevent the accumulation of microbial contamination, including biofilms.

4.

Conclusion

In this study, the effects of simple manual addition of monochloramine disinfection were
determined through chemical and microbiological monitoring, including an analysis of Legionella
spp. in bathtub water. Hot spring facilities using hot spring water with a high pH, and thosewith hot spring water containing a significant amount of NH4-N, were selected as target facilities
since these types of spring water are both likely to reduce the disinfection effect of sodium
hypochlorite.
No Legionella spp. was detected in any of the bathtub water samples or samples collected bywiping the inside of the pipes. However, the majority of the samples were positive for viable andheterotrophic bacteria. In particular, the numbers of viable and heterotrophic bacteria increased
day by day at the hot spring facility that did not completely replace the bathtub water daily.
This growth may indicate that bacteria, such as M. phlei., are resistant to monochloramine
disinfection. In addition, we found a growth in bacteria that preyed on the organic matter inbathtub water. This can be inferred from the increase of TOC concentration in the bathtub
water. Notably we were able to verify that TOC concentration is a good chemical indicator forthe contamination of bathtub water and the risk of bacterial growth.
The growth of these bacteria increases the risk of Legionella spp. growth. Therefore, thisstudy determined that proper management by frequent and complete bathtub water
replacement, bathtub cleaning, and pipe cleaning is necessary.
The results of this study suggest that monochloramine disinfection by simple manual
addition can control Legionella spp. Therefore, if a facility using hot spring water with an
inhibitory factor for sodium hypochlorite disinfection would like to consider the introduction of
monochloramine disinfection, it is possible to perform on-site verification using this disinfection
method without incurring upfront costs.
The disinfection method presented in this study aids in the selection of the most appropriate
disinfection for bathtub water with various chemical characteristics. It is likely that thisresearch will contribute to the prevention of legionellosis caused by public baths.

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Acknowledgments
The authors would like to thank the facilities that cooperated with this study. In addition,
the authors gratefully acknowledge anonymous reviewers, whose valuable and helpful comments
improved our manuscript.
This study was supported partially by a Health and Labor Sciences Research Grant (19LA0601)
from the Ministry of Health, Labor and Welfare of Japan.
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温泉科学

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